长三角地区 化学品污染挑战

Chemical Pollution Challenges in the Yangtze River Delta

长三角地区 化学品污染挑战

Chemical Pollution Challenges in the Yangtze River Delta Chemical Pollution Challenges in the Yangtze River Delta, China A 2017 Sino-Swedish Research Report Editors: Åke Bergman, Anders Bignert, Yanling Qiu, Ge Yin Design: Blomquist & Co Photo: Åke Bergman, Qinghui Huang, Zhiliang Zhu Print: AJ E-print AB ISBN printed: 978-91-87355-31-8 ISBN PDF: 978-91-87355-32-5 ISBN E-pub: 978-91-87355-33-2

4 Chemstrres participants and collaborators

The project involve a large number of professionals from China and Sweden as presented below. The authors of the individual chapters in this book are named without af liations in the chapters.

Chemstrres contractors Prof. Daqiang Yin, Department of environmental Prof. Åke Bergman (Coordinator (PI), editor), science, College of environmental science and Swedish toxicology sciences research center, engineering, Tongji University, Shanghai, and Södertälje, Karolinska Institutet; Department of Department of analytical chemistry and analytical chemistry and environmental sciences, environmental sciences, Stockholm University, Stockholm University, Stockholm, and College of Stockholm environmental science and engineering, Tongji Prof. Jianfu Zhao, Department of environmental University, Shanghai. E-mail: [email protected] science, College of environmental science and Assoc. Prof. Lillemor Asplund, Department of engineering, Tongji University, Shanghai, and analytical chemistry and environmental sciences, Department of analytical chemistry and Stockholm University, Stockholm. environmental sciences, Stockholm University, Prof. Anders Bignert (Editor), Swedish museum of Stockholm natural history, Stockholm, and College of Prof. Zhiliang Zhu, Department of environmental environmental science and engineering, Tongji science, College of environmental science and University, Shanghai. E-mail: [email protected] engineering, Tongji University, Shanghai, and Prof. Magnus Breitholtz, Department of analytical Department of analytical chemistry and chemistry and environmental sciences, Stockholm environmental sciences, Stockholm University, University, Stockholm Stockholm Prof. Elena Gorokhova, Department of analytical chemistry and environmental sciences, Stockholm Contracted researchers within Chemstrres University, Stockholm Prof. Xiangzhou Meng, Department of environmental Dr. Anna Strid, Department of analytical chemistry science, College of environmental science and and environmental sciences, Stockholm University, engineering, Tongji University, Shanghai Stockholm Assoc. Prof. Qinghui Huang, Department of Prof. Yanling Qiu (Co-coordinator, Editor), environmental science, College of environmental Department of environmental science, College of science and engineering, Tongji University, Shanghai environmental science and engineering, Tongji Assoc. Prof. Lingling Wu, Department of University, Shanghai, and Department of analytical environmental science, College of environmental chemistry and environmental sciences, Stockholm science and engineering, Tongji University, Shanghai University, Stockholm. E-mail: [email protected]

5 Dr. Elisabeth Nyberg, Swedish museum of natural Ms. Qianfen Xiao, State Key Laboratory of Pollution history, Stockholm Control and Resource Reuse, College of Dr. Birgit Paulsson, Department of analytical environmental science and engineering, Tongji chemistry and environmental sciences, Stockholm University, Shanghai University, Stockholm Dr. Ge Yin (Editor), Department of analytical Collaborators chemistry and environmental sciences, Stockholm Prof. Ling Chen, Department of environmental University, Stockholm science, College of environmental science and Dr. Zhenyang Yu, Department of environmental engineering, Tongji University, Shanghai science, College of environmental science and Ms. Qiaofeng Chen, Department of environmental engineering, Tongji University, Shanghai science, College of environmental science and Dr. Bo Yuan, Department of analytical chemistry and engineeringTongji University, Shanghai environmental sciences, Stockholm University, Mr. Xinyu Du, Department of environmental science, Stockholm College of environmental science and engineering, Dr. Yihui Zhou, Department of environmental Tongji University, Shanghai science, College of environmental science and Ms. Lei Duan, Department of environmental science, engineering, Tongji University, Shanghai, and College of environmental science and engineering, Department of analytical chemistry and Tongji University, Shanghai environmental sciences, Stockholm University, Ms. Li Li, Department of environmental science, Stockholm College of environmental science and engineering, Mr. Ioannis Athanassiadis, Department of analytical Tongji University, Shanghai chemistry and environmental sciences, Stockholm Ms. Qian Li, Department of environmental science, University, Stockholm College of environmental science and engineering, Ms. Mafalda Castro (Ph.D. student), Department of Tongji University, Shanghai analytical chemistry and environmental sciences, Ms. Vivian Lindberg Chen, Department of analytical Stockholm University, Stockholm chemistry and environmental sciences, Stockholm Ms. Sara Danielsson, Swedish museum of natural University, Stockholm history, Stockholm Mr. Yang Lu, Department of environmental science, Ms. Yajie Sun, State Key Laboratory of Pollution College of environmental science and engineering, Control and Resource Reuse, College of Tongji University, Shanghai environmental science and engineering, Tongji University, Shanghai

6 Ms. Linlin Song, Department of environmental Chemstrres reference group science, College of environmental science and Dr. Anders Glynn, National Food Agency, Sweden, engineering, Tongji University, Shanghai Uppsala Prof. Taowu Ma, College of biology and Ms. Charlotta Järnmark, World Wildlife Fund environmental sciences, Jishou University, Jishou Sweden, Solna Assoc. Prof. Anna Sobek, Department of analytical Dr. Bert-Ove Lund, Swedish Chemicals Agency, chemistry and environmental sciences, Stockholm Sundbyberg University, Stockholm Ms. Tove Lundeberg, Swedish Environmental Dr. Kathryn Stewart, Department of environmental Protection Agency, Stockholm science, College of environmental science and Prof. Chunxia Wang, National Natural Science engineering, Tongji University, Shanghai Foundation of China, Beijing Mr. Meng Wang, Department of environmental Prof. Yongning Wu, China National Centre for Food science, College of environmental science and Safety Risk Assessment, Beijing engineering, Tongji University, Shanghai Prof. Gang Yu, Tsinghua University, Beijing Dr. Rui Wang, Department of environmental science, Prof. Weixian Zhang, State Key Laboratory of College of environmental science and engineering, Pollution Control and Resource Reuse, Tongji Tongji Shanghai University, Shanghai Dr. Jana Weiss, Department of analytical chemistry and environmental sciences, Stockholm University, Stockholm Mr. Nan Xiang, Department of environmental science, College of environmental science and engineering, Tongji University, Shanghai Mr. Ziye Zheng, Department of analytical chemistry and environmental sciences, Stockholm University, Stockholm

7 Acknowledgement

The Chemstrres project (2014-2018), with its full The project has found additional support via the name “Swedish – Chinese chemical pollution stress following Chinese funds: and risks research programme in the Yantze River • Development of an Environmental Specimen Bank Delta region” is funded by the Swedish Research in the Yangtze River Delta and Study on the Council (VR) through their initiative “Sino-Swedish Spatial Distribution of Typical Pollutants. Funded Research Cooperation”, project number: 2013-6913. by the Fundamental Research Funds for Chinese Central Universities (2012-2014) Chemstress is built on the achievements and initial • Running Cost of the State Key Laboratory of efforts (2011-2013) through a project “Development of Pollution Control and Resource Reuse a Yangtze River Delta Monitoring Program, including • 985 College Funding of Tongji University an Environmental Specimen Bank and an Environment • High-end Foreign Experts Program of the China and Health Laboratory” and nancially supported by State Administration of Foreign Experts Affairs the Swedish International Development Cooperation • Innovative Talents Base of Pollution Control and Agency (SIDA) PDC project AKT-2010-015. Resource Reuse (111 Program) • Infrastructure investment from Jiaxing local government

8 Abbreviations

The abbreviations presented below relates to chapter 1 and 2. All abbreviations for chapter 3 and 4 are presented within those chapters.

AQI: Air quality index PACs: Polycyclic aromatic compounds BPA: Bisphenol A PAEs: Phthalate esters CHLs: Chlordanes PAHs: Polycyclic aromatic hydrocarbons CPs: Chlorinated paraf ns PBDEs: Polybrominated diphenyl ethers DBP: Dibutyl phthalate PCBs: Polychlorinated biphenyls DDT: Dichlorodiphenyltrichloroethanes PCDD/Fs: Polychlorinated dibenzo-p-dioxins and DDTs: Sum of DDT ant its major transformation polychlorinated dibenzofurans products, DDE and DDD PFOA: Peruorooctanoic acid

DnOP: Di-n-octyl phthalate PM2.5: Fine particles with a diameter of 2.5 μm DEHP: Di-2-ethylhexyl phthalate and less

DiNP: Diisononyl phthalate PM10: Suspended particulates smaller than 10 DEP: Diethyl phthalate μm in aerodynamic diameter EDCs: Endocrine disrupting chemicals POPs: Persistent Organic Pollutants EDI: Estimated daily intake PPCPs: Pharmaceuticals and personal care GDP: Gross domestic production products HCB: Hexachlorobenzene SCCPs: Short chained chlorinated paraf ns HCHs: Hexachlorocyclohexanes TH: Thyroid hormone MCCPs: Medium chained chlorinated paraf ns YRD: Yangtze River Delta OCPs: Organochlorine pesticides OP: Octylphenols

9 Preface

The strife for improved life conditions has been part The development continued over the years, more and of building civilizations as long as we have been more chemicals were described, and many of those walking on this planet. This is what innovation and came into use over the years: DDT, PCB, brominated development is about. Hence there are many ame retardants, bisphenol A, phthalates and many landmarks on this historical path for mankind, not more. Major application areas are as active ingredients the least by signi cant early achievements in China. in pharmaceuticals, pesticides, additives in chemical Focusing on innovations built on chemistry, it may be products, materials and goods. The development worth mentioning: paper making, printing and continued for long before any concern was raised for gunpowder, all three from China. Other innovations unintentional health and environmental effects of relate to an area discussed in the present book – re chemicals being manufactured and used. The book safety – an area with historical roots in ancient Egypt by Rachel Carson, “Silent spring”, published in 1962, using alum as a ame retardant. became a starting point of intense and continuous developments in the area of chemicals, health and However, the era, renowned as the “Industrial environment, research including monitoring of revolution”, starting in the mid 19th century, is when environmental contaminants. Sweden became one the development of our modern society really takes of the world leading countries in this context. off. Chemists started to discover the world of Swedish researchers performed early work on chemicals by mixing and observing – being mercury in the environment, discovered PCBs in experimentalists. Some of the work was almost wildlife, unintentional production and environmental directly found useful, such as the work by Charles distribution of “dioxins” and performed ground Goodyear who invented the vulcanization process, by breaking work on brominated ame retardants, to mixing natural rubber and sulfur, even though mention some. serendipity seems to have played an important role for him. This is the cradle of rubber manufacturing Over time China became the globally most important today, even though it has been tremendously re ned manufacturer of chemicals and inherited the pollution since then. Another two chemicals addressed in this problems with production and use of chemicals. The book are the pesticide, DDT, and technical product, environmental contamination of chemical pollutants PCB (polychlorinated biphenyls). Both DDT and PCB is of course potentiated by the large production were synthesized in the 1870’s, the former through a volumes required for the large Chinese population, successful synthesis but without any known of food but also of consumer products in general application of the product at the time. The latter, the and a large construction business. The Yangtze River original synthesis of PCBs did not give anything but Delta is very much a central area for the chemical a useless chemical mixture. Still these two chemicals production and for manufacturing of a variety of became bestsellers for ghting vector borne diseases chemical products, materials and goods. and for many electric applications, respectively.

10 A science based cooperation between researchers environment, wildlife and food/water quality. The from Tongji University, Stockholm University and framework integrates: (i) Study design, methods and the Swedish Museum of Natural History started to evaluation; (ii) Environmental exposure assessment and develop in the rst decade of the present century. The (iii) Ecotoxicological effect assessment, surrounding cooperation was aimed to improve the understanding the central issue of (iv) Improved hazard and risk of chemical pollutants and their inuence on wildlife assessments of chemicals and the environment to and humans in the Yangtze River Delta area, to promote enlightened and science based management generate novel data and establish advanced chemical in the Yangtze River Delta. Therefore, Chemstrres is monitoring programs. A modern laboratory facility divided into a number of sub-projects as presented in was created in Jiaxing, under the initial name of chapter 3. The aims, some results and discussions are Sino-Swedish Environment and Health Laboratory. presented therein and with some further highlights in This laboratory with 2000 square meters for research chapter 4. Our work is devoted to both chemical and development activities is designed for both assessments and developing bioindicators of use for national and international cooperation, and now in environmental monitoring of pollution stress. In operation. The plans also included the establishment addition we are also addressing human exposure to of an environmental specimen bank, which is indeed pollutants via studies of mothers’ milk and organic implemented by the Yangtze Environmental pollutants in dust. Specimen Bank (YESB), also located to Jiaxing. Over 5,000 environmental specimens, e.g. sh, birds and We hope Chemstrres will to bring scientists and eggs, snails, soil, sediment, human hair and mother’s decision makers closer together, to enable science milk, have been collected in the recent 5 years. All based management for improved human health and these specimens are available for future studies. environmental prosperity. It is my sincere hope that you will read and learn from what we are sharing The present project, Chemstrres (“Swedish – Chinese with you in this book. chemical pollution stress and risks research program in the Yangtze River Delta region”) is funded by the Swedish Research Council to promote Sino-Swedish Research Cooperation. The background for and start of Chemstrres is addressed in the present book. This includes the more holistic view of the Yangtze River Delta region and the pollution situation, which is described in the rst two chapters. The Chemstrres program as such is intended to integrate interdisciplinary research for assessment of the

11 Contents

1. Introduction to the Yangtze River Delta ...... 14 1.1 Introduction ...... 15 1.2 Yangtze River Delta ...... 16 1.2.1 Administrative Division ...... 16 1.2.2 Province and capital city...... 19 1.3 Natural Resource ...... 22 1.3.1 Water ...... 22 1.3.2 Land ...... 23 1.3.3 Biological ...... 23 1.4 Culture ...... 24 1.5 Economy and Industry ...... 26

2. Highlights of chemicals, health and environment challenges in the Yangtze River Delta ...... 28 2.1 Introduction ...... 29 2.1.1 Environmental concerns and chemical pollution ...... 29 2.1.2 Chemical pollution in the Yangtze River Delta ...... 30 2.2 Origin of Chemical Pollution in the YRD ...... 31 2.2.1 Energy Consumption ...... 32 2.2.2 Chemical Industry ...... 35 2.2.3 Agricultural Chemicals...... 36 2.2.4 Pharmaceutical and Personal Care Products (PPCPs) ...... 37 2.3 Environmental Quality ...... 41 2.3.1 Air quality ...... 41 2.3.2 Water quality ...... 42 2.3.3 Soil quality...... 44 2.3.4 Exposure to wildlife ...... 46 2.3.5 Exposure to humans ...... 47 2.3.6 Conclusions ...... 48

3. Chemstrres research activities ...... 52 3.1 Ecotox project with the pond snail (Bellamya aeruginosa) ...... 53 Background and aim of project ...... 53 Preliminary results and reasoning ...... 55 3.2 Ecotoxicology of chlorinated paraffins ...... 59 Background and aim of project ...... 59 Preliminary results and reasoning ...... 61

12 3.3 Establishment of Bellamya aeruginosa as a research monitoring species in the Yangtze River Delta ...... 64 Background and aim of project ...... 64 Preliminary results and reasoning ...... 66 3.4 Drinking water contaminants – a screening project ...... 69 Background and aim of project ...... 69 Preliminary results and reasoning ...... 71 3.5 Sewage sludge as a mirror of human activities...... 74 Sewage sludge as a suitable matrix to monitor human activities...... 74 Pollutants analyzed in sewage sludge from Shanghai...... 76 Future needs ...... 77 3.6 Assessing persistent and bioaccumulative compounds in wildlife from the Yangtze River Delta ...... 79 Background and aim of project ...... 79 Results and reasoning ...... 80 3.7 Heron eggs and environmental quality in the Yangtze River Delta region ...... 83 Background and aim of project ...... 83 Preliminary results ...... 85 3.8 Mothers’ milk monitoring in the Yangtze River Delta ...... 88 Background and aim of project ...... 88 Preliminary results and reasoning ...... 93 3.9 Establishment of optimal –sh species for research monitoring in the Yangtze River Delta ...... 94 Background and aim of project ...... 94 Preliminary results and reasoning ...... 94 3.10 Chemical pollutants in dust ...... 99 Background and aim of project ...... 99 Results and reasoning ...... 100

4. Highlights of two research projects within Chemstrres ...... 104 4.1 POPs in wildlife from the Yangtze River Delta ...... 105 4.2 POPs in the aquatic ecosystem of the Yangtze River Delta – establishment of a monitoring program ...... 115 4.2.1 Introduction ...... 115 4.2.2 Concentration and congener pattern of pollutants ...... 115 4.2.3 Biota – sediment accumulation ...... 119 4.2.4 Risk assessment ...... 119 4.2.5 Establishment of a monitoring program using snails ...... 120

13 Chapter 1:

Introduction to the Yangtze River Delta

14 Chapter 1: Introduction to the Yangtze River Delta

1.1 Introduction

A delta is known as the river alluvial plain, which is The Yangtze is the cradle of the Chinese civilization. formed of the clays and sands carried by the river Along its banks, there are thousands of archaeological from the upstream accumulation and precipitated in sites. The YRD is rich with myths and legends, and the estuary. There are many well-known deltas in the it has witnessed endless poets and artists such as Bai world, such as of the Nile River, the Mississippi Juyi (772-846), Xin Qiji (1140-1207) and Lu Xun River, the Ganges, the Mekong and of the Yangtze (1881-1936) growing up and living here. These River. They are the cradles of human civilization, the celebrities, together with their immortal poems, most developed and active economic and cultural are forever retained in the long history of Chinese developments in the world. civilization. Also, many important historical events have taken place in this area. In ancient history, Liu Sometimes delta owned the reputation as a golden Bang (247 B.C.-195 B.C.) and Xiang Yu (232 B.C.- triangle. The Yangtze River Delta (YRD) is China’s 202 B.C.) have successively gathered uprising in Golden Triangle, located in the umbilicus of the Peixian (Jiangsu) and Wuzhong (now Suzhou, eastern coast of China, facing the world’s largest Jiangsu), got the victory of the Qin Dynasty war. ocean and backed by the world’s largest land mass, This created the precedent of the peasant uprising in that of Asia and Europe. Through thousands of years, the Chinese history to overthrow the feudal dynasty. it was formed with the contribution of both the In modern history, the Communist Party of China Yangtze River and Qiantang River. With its own was born in 1921 in YRD area. The First National natural and cultural advantages, it has become China’s Congress of the Communist Party of China was held most economically developed, the most densely in Shanghai and the South Lake of Jiaxing City, populated, with the most advanced science and opening a new chapter in Chinese history. education, and one of the most convenient traf c areas.

15 Chapter 1: Introduction to the Yangtze River Delta

1.2 Yangtze River Delta Tongling, Anqing, Chuzhou and Xuancheng) in Anhui Province [1]. This book focuses primarily on 1.2.1 Administrative Division environmental issue in the Small-YRD, with The YRD is located in the east coast of mainland of emphasis on the Taihu Lake Basin and the Yangtze China. It is an alluvial plain formed by sediment River Estuary. which is carried by the Yangtze River before owing into the East China Sea. The development of YRD is This book also refers to some geographic terms in based on the plain of the Yangtze River Estuary. At relation to the YRD as introduced below. present, there are different interpretations of YRD. The rst is the concept of the Small-YRD, which is Taihu Lake Basin includes southern part of Jiangsu including Shanghai, cities in Jiangsu (Suzhou, Wuxi, Province; Jiaxing, Huzhou and part of Hangzhou Changzhou, Zhenjiang, Nanjing, Nantong, Taizhou city of Zhejiang Province; and most of Shanghai, and Yangzhou) and cities in Zhejiang (Jiaxing, with an area of 36900 km2. The main area in the Huzhou, Shaoxing, Hangzhou, Ningbo, Zhoushan Taihu Lake Basin is a plain, accounting for 2/3 of the and Taizhou). The Small-YRD is a geographic total area, followed by water (1/6) and the rest are de nition (Figure 1.1). The second is the concept of hills (1/6). Numerous lakes and rivers are scattered in Large-YRD, including all the administrative region of the area. Among them, Taihu Lake which is located Shanghai, Jiangsu Province and Zhejiang Province. in the center. It is the third largest freshwater lake in The third is the concept of Pan-YRD, even including China, with a water area of 2338 km2 and average some of the cities (Hefei, Wuhu, Maanshan, depth of only 1.9 m.

View from the eastern shore over Taihu Lake. Photo: Åke Bergman

16 Chapter 1: Introduction to the Yangtze River Delta

Figure 1.1. Map of the Small-YRD.

17 Chapter 1: Introduction to the Yangtze River Delta

View over the busy Huangpu River and central Shanghai from the top The three main sky scraps in Shanghai reaching towards heaven. of the Shanghai World Financial Centre in Pudong. Photo: Åke Bergman Photo: Åke Bergman

View of the Bund, once the heart of colonial Shanghai, on the eastern side of Huangpu River. Photo: Åke Bergman

18 Chapter 1: Introduction to the Yangtze River Delta

Yangtze River Estuary is a section of Yangtze River is an epitome of modern China. When it comes to the owing to the East China Sea. It is from Jiangyin E native language, shanghainese belongs to the Wu Bi Zui Reef to the mouth of Ji Gu Reef, with a length dialect and Shanghai’s local avor dishes are called of 232 km. Benbang Cuisine.

Hangzhou Bay is an inlet of the East China Sea Shanghai was the rst free trade zone “China where Qiantang River ows into it. It lies between (Shanghai) Pilot Free Trade Zone” in China. Many south of Shanghai and the city of Hangzhou, large-scale international activities, such as the 2010 containing many small islands collectively called World Expo, Shanghai International Film Festival Zhoushan Islands. have been held successfully in Shanghai, making it a well-known international city. According to the 1.2.2 Province and capital city China’s strategic plan, Shanghai will be built into an Shanghai international economic, nance, trade and shipping Shanghai is called in Chinese ”Hu（沪）” for short center by 2020, adapting to China’s economic and “Shen（申）” as a nickname. According to the strength, international status and global resource legend, Shanghai was once the ef of Huang Xie, allocation capability. who was called Lord Chunshen in Chu State during Spring and Autumn Period Warring States, so Jiangsu (Nanjing) Shanghai is also called “Shen”. In the fourth and fth Jiangsu Province, ”Su (苏)” for short, gets its name centuries of the Jin Dynasty, the residents who from the rst word of the ”Jiangning House” and created the shing for the livelihood of a bamboo ”Suzhou House”. Jiangsu Province covers an area of shing tool called ”Hu（扈）”, but also because the 107200 km2, mainly characterized by plains. The river into the sea called ”ditch”（渎） , so the lower plains area ratio ranks rst in the provinces of China. reaches of the Songjiang area known as ”Hu Du（扈 The resident population of Jiangsu Province reached 渎）”, and later was changed to “Hu（沪）” [2]. 80 million by 2015 [3].

Shanghai is one of the four municipalities in China, Jiangsu Province has booming economy, widespread one of the rst open coastal cities and also the education and prosperous culture. The Beijing- important center of China’s economy, transportation, Hangzhou Grand Canal connects south and north of science and technology, industry, nance, exhibition Jiangsu; the Yangtze River across west and east of and shipping. At the end of 2015, the total resident Jiangsu divides Jiangsu Province into two blocks: population of Shanghai city reached a little more southern and northern Jiangsu, respectively. than 24 million inhabitants. Although the scale of Jiangsu’s industrial economy is Shanghai is a famous national historical and cultural very large, the major industries are mainly city. The integration of traditional Wu (吴) and Yue distributed in Nanjing, Suzhou and few other big (越) culture from Jiangnan area and industrial cities. The proportion of traditional industries, high culture from the West form a unique Shanghai style consumption and high pollution industries in the culture. Now, many modern historic building have entire industry is still very high, so the growth rate of been retained in Shanghai, and the concession history the third industry is lower than some mega-cities like

19 Chapter 1: Introduction to the Yangtze River Delta

Xiaoling Tomb of the Ming Dynasty in Nanjing belongs to the Worlds Cultural Heritage from 2003. Photo: Åke Bergman

20 Chapter 1: Introduction to the Yangtze River Delta

Shanghai, and the speed of the industrial transferring, Zhejiang is one of the most vigorous economic upgrading and restructuring is relatively slow. provinces in China. Hangzhou, Ningbo, Shaoxing and Wenzhou are four major economic pillars of The provincial capital city of Jiangsu Province is Zhejiang Province. Under the premise of giving full Nanjing, which has long been a major center of play to the leading role of state owned economy, culture, education, politics and tourism in China. Zhejiang province uses the development of the private Nanjing served as the capitals of various dynasties, economy to boost the economy, forming a distinctive kingdoms and republican governments dating from characteristic “Zhejiang economy”. In recent years, 229 (state capital of Eastern Wu in Three Kingdoms the economy in Zhejiang retains good development period) until 1949 (capital of Republic of China). tendency and the “Internet +” plays an important Today, Nanjing is the second largest city in the east role. The new emerging internet industry represented China region, with area of 6582 km2 and a by Alibaba and e-commerce industry have brought population of 8.2 million. In the past decades, new energy to promote Zhejiang’s economic Nanjing has been developing its economy, commerce transformation and upgrading. and city construction. According to the plan, Nanjing will focus on the development of modern logistics, The provincial capital city of Zhejiang Province is technology, culture and tourism and other service Hangzhou. A household Chinese saying is “Paradise industries. above, Suzhou and Hangzhou below”, illustrating the beauty of the city. Hangzhou is also famous for its Zhejiang (Hangzhou) historic relics. It is one of the Seven Ancient Capitals Zhejiang Province, “Zhe (浙)” for short, is located in of China. Today, Hangzhou is considered as one of the the coastal area of southeast China. The biggest river most important manufacturing and logistics hub in in Zhejiang is the Qiantang River, which twists and China. The city has developed many industries, turns a lot It was therefore called “（之江）Zhi River” including medicine, information technology, heavy or “（折江）Zhe (twisted) River”. The province is equipment, automotive components, household named after the river’s name. The resident population electrical appliances, electronics, telecommunication, of Zhejiang reached 55 million by 2015. ne chemicals, chemical ber and food processing. In the future, Hangzhou will accelerate the construction Zhejiang is the birthplace of Wu Yue culture and of national innovation demonstration zone and Jiangnan culture. It is also one of the origins of integrated cross-border e-commerce area. In 2016, Chinese ancient civilization. Characterized by G-20 summit was held in Hangzhou, attracting the complicated topography, the proportion of global attention to this modern city with its long mountains and hills, plains and basins, and rivers history. and lakes are 70.4%, 23.2%, 6.4%, respectively, of the total area of the land of Zhejiang. Thus, there is a saying that “seven mountains, one water and two elds” [4].

21 Chapter 1: Introduction to the Yangtze River Delta

1.3 Natural Resource water resource o f about 190 billion cubic meters. The percentages of annual water resource in Shanghai 1.3.1 Water City, Jiangsu Province and Zhejiang Province are There are many lakes and rivers in the YRD. The 2.1%, 25.0%, 72.9%, respectively. Considering the water resource is abundant, with the total annual resident population, the total amount of water resources per capita is about 890 cubic meters in the YRD. Shanghai City has the minimum amount of water resource in YRD, coupled with the largest population density in mainland China, so the per capita water amount is rather small, with 200 cubic meters; the Yangtze River runoff accounts for more than 95% of the average transit water in Jiangsu Province, and plays a very important role in the water resource of Jiangsu province.

Due to its superior geographical position, (i.e. approaching the East China Sea), the subtropical monsoon climate, abundant precipitation, dense river networks, the total annual water resource of Zhejiang Province is the highest in three provinces or municipalities of the YRD. A traditional town and lake in the Yangtze River Delta. Photo: Zhiliang Zhu

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1.3.2 Land about 4%, 67% and 29%, respectively. Although the There are multiple complex ecosystems and arable land area of Shanghai City accounts for 39% complicated surface land cover in the YRD. Six main of the city’s area, it has the smallest arable land area types of land use include cultivated land (including in the YRD, mainly because the area of Shanghai paddy eld and dry land), woodland (including forest City is very small, accounting for about 0.06% of land, shrub land, sparse forest and other forest land), China’s total area. grassland (including grassland with high coverage, moderate coverage and low coverage), water area Jiangsu Province has the largest cultivated area in the (including rivers, lakes, reservoirs, ponds, marshes YRD, the proportion in land area is also the largest, and beaches), construction land (including urban accounting for about 42% of the land area of Jiangsu land, rural residential and transportation Province. At the same time, the coastal open beach construction land) and undeveloped land (including area is also very large, accounting for about a quarter bare land and rock land) [5]. of the total area of the China’s beaches and occupies the rst place in China. The cultivated land area of In the YRD, the southern area of the Yangtze River Zhejiang province is only 19% of the total land area, is called “the land of sh and rice”, according to but the forest land area is relatively large, accounting the Chinese history. However, the process of for about 54% of the total area of all kinds of land industrialization activities resulted in the severe loss [6]. of cultivated land. In recent years, the cultivated land area of the YRD has decreased. Therefore, it is an 1.3.3 Biological urgent concern to protect the limited arable land in Different local dominant species are distributed over the rapid developing urbanization process. Currently, the regions of the YRD. Shanghai City located in the the arable land area of the YRD is about 0.1 million Yangtze River Estuary with extensive biological km2, and the arable land area of Shanghai City, resources, not the least related to the aquatic life. Jiangsu Province and Zhejiang Province account for More than 108 kinds of sh species among which

View of the Yangtze River estuary from the Xisha Wetlands of the West Chongming Island. Photo: Qinghui Huang

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20 species are of signi cant economic interest. At 1.4 Culture the same time, the benthic biota resources including Yangtze River has borne witness to Chinese history spiral shell, clams and mussels are abundant because throughout the ages. It has seen the solemnity of Qin of many natural lakes in Shanghai. The bird migration Dynasty (221 – 206 BC), the grandeur of Han is particularly intensive in the Yangtze River mouth Dynasty (206 BC – 220), the glory of Tang Dynasty at Chongming Island. (618 – 907) and the pomposity of Song Dynasty (960 – 1279). The formation and development of the The wildlife resources in Jiangsu Province are regional culture of the YRD, experienced a long limited, for instance, birds mainly include pheasants historical evolution and cultural integration. The and ducks. However, the plant resources are extensive traditional Wu Yue culture, rooted in the Jiangnan with about 850 species. There are more than 4 000 region, was thought to represent the YRD culture. plant species in Zhejiang Province, of which 45 As a typical culture in the YRD, the traditional species belong to the national key protected wild Wu-Yue culture was originated in the Jiangnan region plants [7]. of China. Nourished by the charming Jiangnan landscape, the Wu-Yue culture is characterized by its delicacy and elegance. It advocates humanity, pragmatism as well as virtues of honesty and trustworthiness. Residents in this area value education and show respect to talented people. Additionally, they are encouraged to challenge themselves and never fear to break the routine.

The Haipai culture, a derivative from Wu-Yue culture, has been widely known for its diversity and inclusiveness. Inuenced by both orientalism and western culture, Haipai represents an ideology which is “rebellious” against conventional thoughts and may be characterized as “bold” in relation to innovation.

The culture covered a diversity of food specialties, life habits, local dialects, buildings, poetry and drama, also in the “the land of sh and rice”. Because of favorable weather conditions, rice was grown and became the main food source. Based on rice, people created some famous local food as e.g. zongzi, rice wine, rice cakes, and rice dumplings. Here, you can taste famous local food, such as Longjing tea, balsamic vinegar, fermented bean curd Lotus near the shore. Photo: Zhiliang Zhu (tofu) and ham are a few among many other dishes.

24 Chapter 1: Introduction to the Yangtze River Delta

Drama performance in a traditional garden. Photo: Zhiliang Zhu

You can use your eyes to enjoy many crafts, such as silk, embroidery, paper cut, teapot and so on. You can use your ear to listen to traditional poetry and drama, for example Yue drama, Hu drama, Kun drama, Huangmei opera and Shaoxing opera.

At last, do not miss the following spots. The West Lake, a famous tourism resort located in Hangzhou, attracts visitors from home and abroad. Suzhou has many famous private gardens, such as the Humble Administrator’s Garden, Lingering Garden and Lion Grove Garden, which occupies an important position in the history of Chinese gardens. The ruins of the Ming Dynasty and Nanjing massacre site in Nanjing, witnessed the most glorious and tragic moments of Chinese history, respectively.

Shanghai is renowned for its Lujiazui skyline, museums and historic buildings, such as those along The Bund, as well as the City God Temple and the Yu Garden, and described as the “showpiece” of the booming economy. Shanghai skyline of the Lujiazui area, Pudong. Photo: Åke Bergman

25 Chapter 1: Introduction to the Yangtze River Delta

1.5 Economy and Industry Industry structure refers to the relationship between The YRD has excellent natural conditions and the various industrial sectors in the economy and resources, convenient transportation, and suitable degree of industrial structure related to economic and climate. It is also the economic center in modern social development, as well as people’s material and China. The reform and open policy bring the YRD cultural life. The main economic indicators between an open and wide international and domestic sky. the whole country and the core area of the YRD in With the rapid development of the economy, this 2015 is presented in Table 1.1. The GDP growth rate delta has become the biggest export base and the of YRD is higher than the average of the whole most promising economic circle in China. In 2015, country. The primary industry growth is slow; the YRD contributed with more than 20% of the however, the secondary industry and modern services Chinese GDP, with 1% of the land area and hosted develop quickly, which promote the economic 6% of the population all of China. structure transformed from “2-3-1” to “3-2-1”.

Table 1.1. Comparison of main economic indicators between the China and the core area of the Yangtze River Delta in 2015 [8]. China Yangtze River Delta Key Indicators units Yangtze River Delta/China (%) total growth (%) total growth (%) GDP trillion RMB 67.67 6.9 11.31 8.2 16.7 Value-added of the trillion RMB 6.09 3.9 0.32 1.8 5.2 primary industry Value-added of the trillion RMB 27.43 6.0 4.91 5.7 17.9 secondary industry Industrial added value trillion RMB 22.90 5.9 4.37 5.8 19.1 Value-added of the trillion RMB 34.16 8.3 6.08 10.8 17.8 tertiary industry Gross †xed asset trillion RMB 56.20 9.8 5.82 9.1 10.4 formation Total retail sales of trillion RMB 30.09 10.7 4.40 9.8 14.6 consumer goods Dsbursement of foreign billions dollars 1263 6.4 544 -2.2 43.0 capital Import-export volume billions dollars 39455 -7.0 12401 -3.6 31.4 Value of exports billions dollars 16776 -12.3 7226 -2.6 43.1 Public †nance budget trillion RMB 15.22 5.8 1.45 10.8 9.5 revenues Urban per capita RMB 31195 8.2 43629 8.3 – disposable income Rural residents per capita RMB 11422 8.9 22504 9.0 – disposable income

26 Chapter 1: Introduction to the Yangtze River Delta

The delta promotes economic restructuring and Overall, the YRD actively explores the development industrial optimization, and has achieved quite some of regional integration, with Shanghai as the leader, remarkable results. Agricultural development in the Jiangsu and Zhejiang as the two wings. The industrial YRD is mainly achieved through the development structure in the delta is relatively concordant, and of urban modern agriculture, the implementation forms a virtuous cycle. There are complementary of agricultural science and technology innovation advantages between the cities in the region, showing project and development of agricultural circular a “metropole driven and regional coordination” economy. The rapid development of technology- development pattern. By 2020, the YRD is expected intensive industry, represented by microelectronics to form a world-class city group, with vibrant and information products manufacturing industry, economy, top talent aggregation, innovation, is the driving force for the economic growth in the intensive and ef cient use of space [9]. YRD’s industries, which gradually replace labor- intensive industries. Development of tertiary industry Authors: bene ts from development of nance, security Prof. Jianfu Zhao and Dr. Ge Yin industry, software and IT services industries.

References

1. The State Council of China. The State Council formally approves 6. Department of land and resources of Zhejiang Province. the implementation of "Regional planning for the Yangtze River Changes of land use in Zhejiang Province in 2014 (In Chinese). Delta" (In Chinese). Available from: http://www.gov.cn/zhengce/ Available from: http://www.zjdlr.gov.cn/art/2015/8/17/ content/2014-09/25/content_9092.htm. Accessed April 16th, art_1070690_387190.html. Accessed April 16th, 2017. 2017. 7. Department of land and resources of Zhejiang Province. Natural 2. Shanghai municipal people's government website. The origin of resources (In Chinese). Available from: http://www.zj.gov.cn/col/ “Shen” and “Hu” (In Chinese). Available from: http://www. col924/index.html. Accessed April 16th, 2017. shanghai.gov.cn/nw2/nw2314/nw3766/nw3767/nw3768/ 8. Jiangsu government. Analysis on the economic development of u1aw12.html. Accessed April 16th, 2017. the Yangtze River Delta in 2015 (In Chinese). Available from: 3. National economic and social development statistical bulletin of http://www.jiaxing.gov.cn/stjj/tjxx_6433/tjfx_6436/201604/ Jiangsu Province in 2015 (In Chinese). Available from: http:// t20160401_584644.html. Accessed April 16th, 2017. www.jssb.gov.cn/tjxxgk/tjfx/sjfx/201602/t20160229_278000. 9. The State Council of China. National development and reform html. Accessed April 16th, 2017. commission, Minister of Housing and Urban-Rural 4. Zhejiang government. Geographic pro«le (In Chinese). Available Development’s circular on printing and distributing the from: http://www.zj.gov.cn/col/col922/index.html. Accessed development plan of the Yangtze River Delta city group: April 16th, 2017. “The development plan of the Yangtze River Delta city group” 5. Sun KQ. The Yangtze River Delta Yearbook. Nanjing, 2010. (In Chinese). 2016.

27 Chapter 2:

Highlights of chemicals, health and environment challenges in the Yangtze River Delta

28 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

2.1 Introduction

2.1.1 Environmental concerns and chemical pollution environment, in quantities, and concentrations that Environmental problems generally refer to the exceed the self-puri cation capacity of the phenomenon of environmental degradation, environment, which can affect the ecological balance ecological imbalances or effects caused by human as well as human health and nally lead to an activities, which in turn adversely affects human life. unacceptable poor environmental conditions. However environmental changes can also be caused Chemical pollution has gained signi cant attentions by natural evolution and natural disasters, known as compared to some other kinds of pollution because the primary environmental problems, such as of its ubiquity and seriousness. With the rapid earthquakes, oods and landslides. The other is development of the economy in China, along with a caused by human activities, known as secondary rapid increase of chemical industry and related environmental problems, i.e. including environmental downstream industries’, has led to large volumes of pollution, ecological damage and human health chemicals entering people’s living environment. effects. The main issues that are threatening humans Common sources for chemicals entering our and wildlife include, but are not limited to: global environment include chemical products, materials, warming, ozone depletion, acid rain, freshwater goods, waste and waste incineration. Such chemical resource crisis, smog, energy shortage, sharp drop in pollutants can be classi ed in several ways: according forest resources, land deserti cation, accelerated to the source, they can be divided in natural and extinction of species and chemicals pollution. anthropogenic sources; according to physical- chemical properties, they can be divided into primary Chemical pollution implies that chemical substances pollutants and secondary pollutants; according to the (often stable synthetic chemicals) enter into the environmental compartments affected by pollutants,

29 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

they can be divided into e.g. air, water and soil these chemicals directly to water, releases with pollutants. Still there are other ways of classifying particular harm in fresh water ecosystems. environmental pollution, of course. Moreover, there are over 90 million people living in When pollutants are released, they are distributed in the YRD. Such a huge population discharges the environmental compartments depending on their potential environmental pollutants to the physicochemical properties (e.g. partitioning environment via their waste water, sewage, properties, volatility and adsobtivity). Many transportation, waste from construction activities, pollutants have relatively short half-life in biota but disposal of expired pharmaceuticals, garbage and may form degradation and biotransformation poorly controlled incineration of waste. Still the YRD products of concern, in both humans and wildlife. has many industrial and municipal waste water However, some pollutants may have strong treatment plants, land lls and hazardous waste persistency in the environment, and adsorb into the treatment plants. However, even though these plants compartments with high organic carbon (e.g. are under full operation, they are not suf cient particulate matter, sediment, soil). These pollutants enough to completely degrade, eliminate or control have a potential to accumulate in biota and transfer the pollutants that enter the environment. Moreover, up the food chain and nally be consumed by accidental leaks, illegal use and emissions, and loads humans and other top predators. from upper stream sources further increase the pollutant burden in the YRD. 2.1.2 Chemical pollution in the Yangtze River Delta The Yangtze River Delta (YRD) environment has Accordingly the qualities of air, water and soil are been deteriorating rapidly with the growing economic facing serious challenges. The air quality in YRD is development of the region. Firstly, the YRD receives characterized as light pollution according to the large loads of environmental pollutants through Ambient Air Quality Standards (GB3095-2012), various pathways of their releases, as discussed in while it becomes worse in some cities or regions this chapter. In the YRD, there are at least 15 where industries are clustered. For example, the

state-level economic and technological development forecast of nitrogen oxides (NOx) emissions show zones, and over 240 province-level economic and steady growing loads. By 2030 in Shanghai, Jiangsu technological development zones. The YRD also Province and Zhejiang Province, and the green-house hosts thousands of industrial parks (e.g. over 300 gases emissions in the YRD would be 1.8 times that industrial parks in Shanghai alone) which use and of 2005 in 2030 [1]. produce plenty of raw materials and consumer products, materials and goods. At the same time, The water qualities of larger rivers or lakes in the there are a lot of farmland and rural areas in the YRD are usually better than medium-sized and small YRD that greatly rely on chemical fertilizers and rivers. For example in 2002, the water quality of the pesticides. In both industry and agriculture, Yangtze River and the Qiantang River, remained numerous pollutants are emitted into the air, water very good and reached approximately Category II of and soil via waste gas, efuent, runoff and the National Surface Water Standard (NSWS) of composting. Use of chemicals (antibiotics and China (GB3838-2002), meanwhile city and rural pesticides) in aquaculture releases large quantities of streams of the Jinghang Channel are poor and

30 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta generally below Category V [2]. According to the farmed sh. For example, high concentrations of National survey of soil pollution, the soil quality of chlorinated paraf ns (CPs) ranging between 200 – 340 the YRD is bad due to severe heavy metal pollutions μg/g fat were found in the short-tailed mamushi snake [3]. More details on environmental quality in air, (Gloydius blomhof i) ), peregrine falcon (Falco water and soil are given in 2.3, below. peregrinus) (8-59 μg/g fat) and asiatic toad (Bufo gargarizans) (97 μg/g fat) [11]. In sh from Taihu The environment of the YRD is challenged by Lake, PAHs and organochlorine pesticides (OCPs) well-recognized pollutants (persistent organic could be detected in all samples, with an average total pollutants (POPs) and heavy metals) accompanied by concentration of PAHs and OCPs in each species emerging ones (e.g. pharmaceuticals and personal ranging from 290 to 9500 ng/g fat and from 120 to care products (PPCPs) and per and polyuorinated 900 ng/g fat, respectively [12]. Further, over 30 substances (PFAS)). One example is hexachlorocyclo- endocrine disrupting chemicals were found in drinking hexanes (HCHs) for which concentrations in the water plants in Shanghai, where octylphenols (OPs) sediments in Taihu Lake increased from lower than showed the highest concentration of 23 ng/L and 10.0 ng/g dry weight (dw) before 2000 to over 50 bisphenol A (BPA) ranged from 0.6 to 7.4 ng/L [13]. ng/g dw around 2010 even if lindane (composed of 99% γ-HCH) were banned around 2004 [4]. The concentrations of HCHs have decreased in recent 2.2 Origin of Chemical Pollution in the YRD years [5]. Another example is polycyclic aromatic hydrocarbons (PAHs) which are estimated to have a The YRD area is the largest comprehensive industrial total deposition ux of 152 tones/year in the Yangtze base in China. In 2014, the six key development estuarine-inner shelf, accounting for ~38% of the 16 industries including the automotive manufacturing, USEPA priority PAHs (16 PAHs) into the East China the petrochemical and ne chemical industry, the Sea [6]. equipment manufacturing industry, the biomedical manufacturing, the ne steel-manufacturing industry As emerging pollutants, antibiotics are widely detected and the electronic information manufacturing in Huangpu River with the concentrations ranging industry reached 67% of the gross industrial output from 37 ng/L (tetracycline) to 313 ng/L value in Shanghai. Fertilizers, pesticides and plastic (sulfamethazine) [7]. One more example is phthalate lms for farming play important roles in agricultural esters (PAEs) which were detected in waste water non-point source pollution. Jiangsu and Zhejiang treatment plants in Shanghai and Huangpu River, and provinces have become two large fertilizers and their concentrations ranged from 18 to 346 μg/L [8]. pesticides manufacturers and consumers in China. Several researchers have investigated the sources of The YRD environment poses exposure risks to the environmental chemical pollutants in the YRD area. ecosystem and human health. It was found that PAHs The results indicate that the joint pollution from (e.g., naphthalene, anthracene, uorene, uoranthene, industry, agriculture and transportation, instead of a atrazine and malathion) and organophosphororus single industry, are the main sources of chemical pesticides are likely to pose a ecological risk to pollutants. The pollutants are accordingly making up organisms in the Taihu Lake [9, 10]. Moreover, there very complex mixtures with yet unknown effects on are numerous pollutants reported in both wild and humans and wildlife.

31 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

2.2.1 Energy Consumption China is the largest developing country, with a high

demand and dependence on energy. In 2010, China tons of standard coal surpassed the Unites States and became the world’s biggest energy consumption country. By 2035, China 5x10¹ will still be the world’s largest energy consumer. Total energy consumed According to the public statistics, China’s total 4x10¹ energy consumption is by an equivalent of 43 million

tons of standard coal in 2015, with a 0.9% increase 3x10¹ over 2014. The coal consumption fell by 3.7%, but the consumption of the crude oil, natural gas and electricity increased with 5.6%, 3.3% and 0.5%, 2x10¹ respectively. 1x10¹ More than 90% of carbon emissions in China are

from energy consumption and the unreasonable high 0 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 energy consumption from fossil sources may be the main contribution to air pollution. In the YRD region, the atmospheric environment and the energy Figure 2.1. Total energy consumption in China during 2006 – 2015. consumption structure are highly correlated. A study analyzed the ne particles with a diameter of 2.5 μm The constitution of energy consumption (%) (PM2.5) trends of three major economic zones including the YRD region in the period 2001-2010. It 100

showed that the particulate matter pollution of YRD 90

area remained at a high but stable level. Further, the 80 ne particle pollution is the worst and is exceeding 70 the average level in YRD region by far [14]. 60 By 2015, China’s total energy consumption was 43 50 million tons of equivalent standard coal, and had an 40 increase of 50% compared to 2006 (Figure 2.1). 30

However, the growth of total energy consumption 20 started to slow down from 2011. The general 10 characteristic of China’s energy structure is “rich in 0 coal, oil-poor, less gas”. As can be seen in Figure 2.2, 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 the proportion of China’s oil consumption is stable Others Natural Gas Petroleum Coal from 2006 to 2014, while the ratio of electricity and other energy consumption has increased. Although natural gas is becoming increasingly popular at this Figure 2.2. Energy Consumption structure in China during stage, the dominance of coal is still a fact. 2006 – 2015.

32 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

The major pollutants created by the use of coal for Ningbo accounted for about 60% of the total energy production are sulfur dioxide (SO2), NOx, emissions of the YRD region. It is found that the soot and polycyclic aromatic compounds (PACs) emissions of SO2 and NOx are mainly from the including PAH, which may have a signi cant impact industrial and thermal power sectors. The emissions on the environment when they are emitted to the air. of particulate and carbon monoxide (CO) are mainly The global environmental problems such as ozone from the industrial sector, the motor vehicle have a depletion and the greenhouse effect or the regional large contribution rate of CO emissions. The atmospheric pollutions as acid rain, haze, smog, etc. pollutants emissions of thermal power sector have are closely related to the energy production. In 2014, signi cant characteristics of monthly variation. The the total emissions of SO2, NOx and smoke (powder vehicle’s emissions are affected by the residents’ travel or dust) in the waste gas in China are 20, 21 and 17 patterns, which have the obvious characteristics of million tons, respectively [15]. The proportion of the weekly and daily variation. total energy consumption of Yangtze River Delta region to the whole country remained stable, with The emission trends of SO2, NOx and smoke (powder slight increase during 2005-2010 and slight decrease and dust) in the atmosphere of the YRD region from after 2011 (Table 2.1). 2005 to 2014 are presented in Figure 2.3, based on data from the statistical yearbook of China [15].

A study on energy consumption in 16 cities of the According to the gure, the SO2 emission in the YRD region in 2008 has been published [17]. The region showed a gradually decreasing trend. results show that the total pollutant discharges from Shanghai has the largest reduction compared with

Shanghai, Suzhou, Nanjing, Hangzhou, Wuxi and 2005, of which the SO2 emissions decreased by 63%

Table 2.1. Energy consumption statistics of the Yangtze River Delta region [16].

Year The country’s total energy Energy consumption of Yangtze River Delta region consumption accounted for the proportion of the country’s (10000 ton standard coal) Sum Shanghai Jiangsu Zhejiang 2005 261369 14.3% 3.1% 6.6% 4.6% 2006 286467 14.3% 3.1% 6.5% 4.6% 2007 311442 14.5% 3.1% 6.7% 4.7% 2008 320611 14.8% 3.2% 6.9% 4.7% 2009 336126 14.8% 3.1% 7.1% 4.6% 2010 360648 14.9% 3.1% 7.1% 4.7% 2011 387043 14.6% 2.9% 7.1% 4.6% 2012 402138 14.5% 2.8% 7.2% 4.5% 2013 416913 14.3% 2.8% 7.0% 4.5%

33 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

in 2014. During the same period, the SO2 emission Thermal power industry, as well as other industrial reduction of Jiangsu and Zhejiang were 34% and combustion processes, are important sources of

33%, respectively. In 2011-2014, NOx emissions of atmospheric pollution. According to the data in region showed a slow decreasing trend, while the China Statistical Yearbook in 2014 and 2015 [15], smoke emissions initially decreased and then Nanjing, Hangzhou and Shanghai are the main cities increased. in the YRD region and their industrial smoke

(a) NOX (b) Dust 1.8x106 9x105

1.6x106 8x105

1.4x106 7x105

1.2x106 6x105

1.0x106 5x105

8.0x105 4x105 Emissions (ton) 6.0x105 3x105

4.0x105 2x105

2.0x105 1x105

0 0 2011 2012 2013 2014 2011 2012 2013 2014

(c) SO2 1.6x106

1.4x106

1.2x106

1.0x106

8.0x105

5 Emissions (ton) 6.0x10

4.0x105

2.0x105

0 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014

Jiangsu Zhejiang Shanghai

Figure 2.3. Emissions of major pollutants in the atmosphere of the Yangtze River Delta region [15] showing upper left diagram: nitrogen

oxides (NOx); upper right diagram: dust/smoke and in the lower diagram: sulfur dioxide (SO2).

34 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

(powder and dust) emissions increased by 47%, 75% 2.2.2 Chemical Industry and 96%, respectively in 2014 compared to 2013 China’s chemical industry has experienced a rapid (Table 2.2). As for the domestic emission in 2014, the growth since the beginning of this century and its smoke discharge of Nanjing and Hangzhou were GDP ranked in rst place in the world in 2010. There similar to 2013, but the emissions in Shanghai were are more than 25,000 large chemical enterprises in reduced by 38%. The emission of smoke in the YRD China as a total. The production of pesticides, fuel, region is thus mainly affected by industrial pollution fertilizer and many other chemical products and sources in recent years. additives to materials and goods is the largest in the world. China’s major chemical productions in 2014 is Researchers estimated the major air pollutant shown in Table 2.3. In the next period, China will emissions of the thermal power industry in the YRD still be in the state of rapid industrial development, area in 2012. Their analysis shows that the units and heavy and chemical industries will account for a above 300 MW contributed 85% and 82% of SO2 large proportion of the development. and NOx, respectively, and the units below 100 MW contributed 81% of smoke and dust [18]. The study According to the released twelfth ve year plan of on the emission characteristics of atmospheric “Chemical Environmental Risk Prevention and pollutants in the region also found that power plants Control” by the Ministry of Environmental and other industrial combustion facilities contributed Protection of China in 2013 [20], there are, before greatly to the emission of SO2 and NOx, while cement January 2013, more than 40,000 chemical substances production for the construction business, iron and with a record of production and use in China. steel metallurgy companies have the greater Among these, three thousands chemicals are listed as contribution of emitted particulate matter [19]. hazardous compounds. There are large numbers of

Table 2.2. Emission of smoke in the main cities of the Yangtze River Delta in 2013-2014 [15].

Industrial smoke (powder and dust) Domestic smoke (powder and dust) emissions (tons) emissions (tons) 2013 2014 Growth rate 2013 2014 Growth rate Nanjing 65256 96177 47% 1000 1000 0% Hangzhou 40243 70346 75% 135 135 0% Shanghai 67174 131433 96% 6451 4017 -38%

Table 2.3. China’s major chemical productions in 2014.

Index Raw coal(a) Coke(a) cement(a) Steel synthetic Chemical Chemical(b) products(a) rubber(b) pesticide(b) production 38.74 4.79 24.92 11.25 549.55 374.40 303.40

35 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

chemicals for which their hazardous properties are challenge the safety of farmland, drinking water still insuf ciently known. In the process of chemical sources and other environmentally sensitive objects. production, storage, transportation, usage, waste It was also found that about 52% of the chemical disposal and other sectors, various accidents (such as enterprises are within one kilometer downstream of explosions, spills, poisoning, res and others) leading air environment protection objects, among which to casualties and property losses, as well as a large 15000 enterprises are so close to residential number of chemicals entering the environment. In settlements that there are obvious human health and 2011-2013, there were 569 registered accidents safety risks. After a preliminary assessment, it is related to dangerous chemicals in China. Zhejiang, concluded that about 18% of the surveyed enterprises Jiangsu, Shandong, Hubei and Sichuan are provinces have a major environmental risk, and 22% of the with a high frequency of accidents [21]. enterprises have a large environmental risk. Therefore, the environmental risks from these In 2010, the Ministry of Environmental Protection enterprises are indeed serious. conducted an environmental risk and chemicals inspection, which focused on three Key Industries 2.2.3 Agricultural Chemicals including national petroleum processing and coking China is a large agricultural country, and the industry, chemical raw materials and chemical agricultural diffuse pollution sources have become products manufacturing industry as well as for the one of the biggest environmental problems due to the pharmaceutical manufacturing industry. The results development of the agricultural sector. It mainly showed that about 23% of the enterprises of the derives from irrational use of chemicals, such as surveyed companies are within 5 km downstream of pesticides, fertilizers, plastic lms. The main

theThe water constitution environment of energy consumption protection (%) areas, which may consumption of agrochemicals from 2008 to 2014 is visualized in Figure 2.4. The consumption of 10 000 fertilizer, pesticides, plastic lms and diesel oil 9 000 showed steady growth in the past several years. In 8 000 2014, the consumption of chemical fertilizers was 7 000 about 0.6 billion tons, with an increase of 14.4%

6 000 compared to 2008. From 2008 to 2014, the consumption of plastic lms increased by 28.5%, 5 000 which is mainly due to vegetable production and 4 000 ower cultivation in greenhouses. 3 000 2 000 The wide use of fertilizer is an important factor for 1 000 agricultural diffuse source pollution. After the 0 fertilizer application, most of them stay in the soil, 2008 2009 2010 2011 2012 2013 2014 move into waters or enter the atmosphere by runoff, Agricultural diesel oil Agricultural plastic lm leaching, de-nitri cation, adsorption and erosion. Chemical fertilizer Pesticides The consequences are eutrophication, groundwater Figure 2.4. Consumption of China’s agricultural chemicals in pollution, destruction of soil physical and chemical 2008 – 2014 (10 000 tons). properties, loss of organic matter, heavy metal

36 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta accumulation, etc. It may also threaten the 2006 to 2014, including 151 cases of occupational agricultural product safety and human health [22]. poisoning without fatality and 271 cases of non- Besides, the large consumption volumes of pesticides, occupational poisoning with a fatality rate of 7.4%. especially of the high-toxic pesticide, these chemicals A total of 494 pesticide poisoning cases were can cause residue accumulation in soil, aquatic reported from 2001-2010 in Baoshan District of environments and crops. The pollution of agricultural Shanghai, including 404 abnormal pesticide lms has been linked to causing soil sealing, the poisoning cases and 57 deaths with a mortality rate reduction of soil adaptability and permeability. The of about 14%. The main pesticides leading to concentrations of antibiotics in soil and aquatic abnormal pesticide poisoning in people’s daily life environment derived mainly from the large amount were organic phosphorus pesticides, among which usage in livestock and aquaculture eld. dichlorphos poisonings were responsible for the highest number of intoxications. China is, on a global scale, a country with both high production and consumption of pesticides. According 2.2.4 Pharmaceutical and Personal Care Products to the data published by National Bureau of Statistics (PPCPs) of China, the production of chemical pesticides was PPCPs include pharmaceuticals for all human use, 3.7 million tons in 2015, with an annual increase of veterinary and agricultural use, as well. The personal 2.3%. The national use of pesticides was estimated care products are represented by a vast number of to be around 1.8 million tons. Regarding the ingredients (chemicals) that are widely used in daily Zhejiang Province, the total production of chemical life. China is a large country with a high production raw pharmaceutical in 2015 was estimated to be and consumption of PPCPs because of its economic approximately 220 thousand tons, with an annual development and population growth in recent years. decline of 6%. The production of insecticides, PPCPs, especially antibiotics, have attracted fungicides, herbicides and ethoxyquin were 2015, ca. signi cant concerns in recent years for their potential 28 thousand tons (remaining at), 17 thousand tons threat to the ecological environment and for human (rose 15% from 2014), 170 thousand tons (declined health. The production of antibiotics has an average 8% from 2014) and 3353 tons (rose 1% from 2014) annual growth rate of 8% in the international tons, respectively. The extensive production of market. New antibiotics have continually been pesticides may be exempli ed with the 28 companies introduced on the market. It is reported that China is in the Jiangsu Province, that produced about 450 the world’s largest producer of pharmaceutical thousand tons, 2015. The production of insecticides, products (Figure 2.5), with an annual production of fungicides, herbicides and ethoxyquin were 81260, 28,000 tons penicillin (60% of the world total 94900, 265600 and 5600 tons, respectively, in 2015. production), 10,000 tons of terramycin (65% of world total), and ranked rst amongst nations for Acute poisoning by pesticide happens frequently. In doxycykline hydrochloride and cephalosporins in Shanghai for example, a total of 587 pesticide 2003 [23]. China’s antibiotics production is more poisoning incidents included 12 deaths as reported to than 120 thousand tons in 2013. About 70% of the occur in the Pudong New Area, between 2009 and prescriptions in China are antibiotics, and in 2011. In Jinshan District of Shanghai, a total of 422 contrast, this gure is approximately 30% in western acute pesticide poisoning cases were reported from countries.

37 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

(a) antibiotic (b) non-antibiotic 8 % 18 % 10 % 33 % 50 %

2 % 2 % 9 % Sulfonamides Steroids Quinolones 4 % Anti-inammatory Tetracyclines Antibacterial Macrolides Antilipiemic 10 % β-lactams 11 % Anticonvulsant Others Antihypertensive Others 13 % 30 %

Figure 2.5. Distribution of reported antibiotic and non-antibiotic pharmaceuticals in surface water in China [25].

China also have the largest market for personal care unchanged or as metabolites. The excreted APIs are products in the world, with the total industry value discharged into the municipal waste stream. The exceeding 145 billion Yuan as reported for 2013 [24], disposal of undesirable or out of date medicines, are and the consumption of personal care products are released via household wastewater or solid waste to expected to continue to increase in coming years. end up at waste water treatment plants, land ll sites and the aquatic environment (e.g. rivers and lakes). In the research report of China’s food safety status from the major consulting project organized by Pharmaceuticals released into the environment can Chinese Academy of Engineering, four types of food lead to serious problems such as the development of safety problems are pointed out. Among them, antibiotic resistant bacteria, the enhancement of excessive use of pesticide and abuse of veterinary microbial resistance and the diminishment of drugs are considered as the most important factors animal’s ability to ght diseases. The large quantity impacting the food safety in China. Veterinary drug residues of harmful veterinary drugs can accumulate products used exceedingly in the process of in environment, causing destruction of the ecological aquaculture and drugs for human used in balance and harm human health. aquaculture, can lead to considerable risks to human beings. For the treatment of animal diseases and The sources and pathways of PPCPs in the aquatic promotion of livestock growth, antibiotics are also environment are illustrated in Figure 2.6. The widely used in livestock agriculture. After the personal care products, coming either from domestic intended medical use, about 40-90% of the active sewage or industrial discharges, will reach sewage pharmaceutical ingredients (APIs) can leave the body treatment plants by discharge pipes from hygiene

38 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta activities, including removal of cosmetics after use. groundwater and surface water are the sources of During sewage treatment, most of the lipophilic drinking water, these mobilized compounds may compounds will absorb to solid materials (sludge), ultimately pose a threat to humans well-being. and can enter farmland or forest by sludge application. Due to low concentrations and complex Several publications have reported concentrations of chemical structure of PPCPs, the traditional PPCPs in the YRD and other areas of China [25, 26]. technologies used in sewage and drinking water The ten most frequently reported PPCPs are all treatment plants are not ef cient enough to antibiotics, dominated by sulfonamides antibiotics accomplish complete removal of the PPCPs. such as methoxazole and sulfamethoxazole (cf. Table Untreated products may then be released into aquatic 2.4). Among the non-antibiotic PPCPs, naproxen and systems (such as groundwater and surface water), and diclofenac are the most commonly studied ones. induce ecotoxic effects. Further, considering that

HOSPITAL/INDUSTRY

LIVESTOCK

AQUACULTURE

FARMLAND SEWAGE TREATMENT PLANT LANDFILL SURFACE WATER GROUNDWATER

DOMESTIC SEWAGE SOIL

DRINKING WATER

Figure 2.6. Sources and pathways of PPCPs in the aquatic environment [25].

39 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

Table 2.4. Main reported PPCPs in the surface water environment of China [25].

PPCPs Type of pharma Times reported a) Detection frequency b) (%) Sulfamethoxazole Antibiotics 15 >60 Sulfamerazine Antibiotics 12 30~60 Sulfadiazine Antibiotics 10 >60 Norœoxacin Antibiotics 10 >60 Oœoxacin Antibiotics 10 >60 Erythromycin Antibiotics 10 >60 Ciproœoxacin Antibiotics 8 30~60 Roxithromycin id Antibiotics 8 >60 Tetracycline Antibiotics 8 30~60 Oxytetracycline Antibiotics 8 30~60 Naproxen Anti-inœammatory analgesics 8 30~60 diclofenac Anti-inœammatory analgesics 8 30~60 Ibuprofen Anti-inœammatory analgesics 7 30~60 Clo†bric acid Blood-lipid lowering drug 7 30~60 17α ethinyl estradiol Natural hormone 6 30~60 Diethylstilbestrol Hormone active substance 6 <30 Gem†brozil Blood-lipid lowering drug 6 30~60 Carbamazepine Anticonvulsant 6 30~60 Indometacin Anti-inœammatory analgesics 5 <30 Triclosan Disinfectant 5 >60

a) The reported times of the PPCPs in the current study of China; b) The ratio of the times the PPCPs have been reported times and the detection frequency in each study, is used to calculate an overall detection frequency shown here. For example, if one PPCP is reported in «ve articles (A,B, C, D, E), and the detection frequency in each one is (100%, 90%, 100%, 0,% and 20%), then the ratio is set as (1, 0.5, 1, 0 and 0,5) and the «nal detection frequency is (1+0.5+1+0+0.5)/5=60%.

40 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

Table 2.5. Relationship between AQI (air quality index) and health implication in China (HJ 663-2012).

AQI Air Pollution Health Implications Level 0–50 Excellent No health implications. 51–100 Good Few hypersensitive individuals should reduce outdoor exercise. 101–150 Lightly Polluted Slight irritations may occur, individuals with breathing or heart problems should reduce outdoor exercise. 151–200 Moderately Polluted Slight irritations may occur, individuals with breathing or heart problems should reduce outdoor exercise. 201–300 Heavily Polluted Healthy people will be noticeably affected. People with breathing or heart problems will experience reduced endurance in activities. These individuals and elders should remain indoors and restrict activities. 300+ Severely Polluted Healthy people will experience reduced endurance in activities. There may be strong irritations and symptoms and may trigger other illnesses. Elders and the sick should remain indoors and avoid exercise. Healthy individuals should avoid outdoor activities.

2.3 Environmental Quality human activities. The energy supply in the YRD mainly relies on coal, which is the main source of air 2.3.1 Air quality pollution. Other sources mainly include motor Nowadays, one of the environmental threats of vehicle exhaust and straw burning. Accordingly, the highest concern in China is air pollution. In 2015, main air pollutants in the YRD are inhalable “Under the dome（穹 顶之下）”, a self- nanced particulate (particulate matters smaller than 10 μm, documentary that reects air pollution, has aroused PM10), SO2 and NO2. great repercussions in China. The documentary started with a story that an unborn daughter The air quality index (AQI) was developed for air developed a tumor in the womb and the director quality monitoring and applied by the Chinese openly criticized industrial companies as well as government. The AQI in China includes six showing the inability of authority to act against such atmospheric pollutants: SO2, NO2, PM10, PM2.5, CO, polluters. Indeed, air pollution is a serious issue and ozone (O3). An individual score is assigned to the which has a major impact on human health leading level of each pollutant and the nal AQI is the to a large number of casualties every year. highest of those 6 scores. The relationship between AQI and health implication is presented in Table 2.5. Air pollutants are discharged to the atmosphere due The AQI is monitored in major cities and publically to natural processes and human activities. However available. Taking Shanghai as an example [27] in the air pollution in China is mainly attributed to 2015 there were 258 (90.7%) days when the AQI

41 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

varied in the range between excellent and good. various sources such as coal combustion, traf c For the rest of 107 days, the numbers of the lightly emission, industrial processes and petroleum polluted, moderately polluted, heavily polluted and manufacturing. PAHs are linked to development of severely polluted days were 73, 26, 8 and 0, human cancer [28]. A study concerning the variation

respectively. Among those 107 polluted days, there of PAHs in atmospheric PM2.5, during a winter haze

were 67 days when the primary pollutant was PM2.5, period around the 2014 Chinese Spring Festival, was

33 days for ozone and 7 days for NO2. carried out in Nanjing [29]. The average sum of 18 PAHs for pre-Spring Festival, Spring Festival and In the YRD, acid rain commonly occurs even though after Spring Festival periods were 50.6, 17.2 and it shows a decreasing trend during the past few years. 29 ng/m3, respectively. The results indicated The pH value in precipitation in the YRD is around 5, variations of PAH sources in these three periods, i.e. lower than the standard value (5.6). Sulfur dioxide reduced traf c, industrial and construction activities has proved to be the main contributor to the acid during Spring Festival and gradually re-starting them

rain. The annual trend of emission of SO2 in Jiangsu after the Spring Festival. Fireworks burning and Zhejiang Province is shown in Figure 2.7. contributed 14.0% of PAHs during Spring Festival period, suggesting the necessity of controlling It is noteworthy that the AQI only consider the major reworks burning during Chinese Spring Festival part of air pollutants, and therefore a number of period which has commonly been accompanied with pollutants with adverse effect to human and serious regional haze pollution. In addition to its environment are not reported by the AQI. One of the local sources, the YRD may get PAHs inputs from examples is PAHs. PAHs are released to the air via other regions, e.g. North China plain and Central China.

160 2.3.2 Water quality Surface water: The Yangtze River has been listed as 140 one of the World’s Top 10 Rivers at risk by the World 120 Wildlife Fund (WWF). The water in the estuary has

100 been shown to be signi cantly altered since it is ows downstream of the river containing an accumulation 80 of pollutants discharged from upstream [30]. There 60 are ve categories of the Environmental Quality Standard for Surface water, in China, as shown in 40 Table 2.6. 20 According to the environmental bulletin in Shanghai, 0 2001 2003 2005 2007 2009 2011 2013 2015 Jiangsu and Zhejiang in 2015 [27, 31, 32], the surface Jiangsu Zhejiang water quality is in general below Category III. The composition of surface water quality in these three Figure 2.7. The variation of annual emission (x 10 000 tonnes) of provinces/city is presented in Figure 2.8. Apparently, sulfur dioxide (SO2) in Jiangsu and Zhejiang Province from 2001 to 2015. the surface water quality in Zhejiang Province is the

42 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta best. The Category I-III water contributes to 73% of 2001 to 73% in 2015, and the percentages of waters the total, whereas the Category IV - V are the main belonging to inferior Category V decreased from groups in Shanghai and Jiangsu, contributing to 52% around 20% in 2001 to 7% in 2015. In Jiangsu and 86% of total, respectively. However, considering Province, the percentages of waters belonging to the present temporal trend, the surface water quality Category I to III increased from 32% in 2001 to 48% in the YRD has improved during the past 15 years. in 2015, and the percentages of waters belonging to In Zhejiang Province, the percentages of waters inferior Category V decreased from 28% in 2001 to belonging to Category I to III increased from 52% in 2.4% in 2015.

Table 2.6. Classi« cation and main indicators of the « ve surface water quality (mg/L) according to the Environmental Quality Standard for Surface water (GB 3838-2002). Air quality index) and health implication in China (HJ 663-2012).

Category DO (≥) COD (≤) TP (≤) NH3-N (≤) Description I 7.5 15 0.02 (0.01) 0.15 Describes water sources and national nature reserves II 6 15 0.1 (0.025) 0.5 Describes Class I protection zones for drinking water resources, protection zones for valuable † sh and spawning grounds III 5 20 0.2 (0.05) 1.0 Describes Class II protection zones for drinking water sources, general protection zones for † sh and swimming areas IV 3 30 0.3 (0.1) 1.5 Describes general industrial water zones and water recreation areas where no direct contact with human occurs V 2 40 0.4 (0.2) 2.0 Describes agricultural water zones and scenic water areas

I II III I-III IV V Inferior

Figure 2.8. Composition of surface water quality in Shanghai Jiangsu Zhejiang Shanghai municipal city, Zhejiang Province and Jiangsu Province

43 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

Among the 24 basic indicators of the standard, the investigation on drinking water quality from water main pollutants are ammonia nitrogen, and total plants was conducted by Ministry of Housing and phosphorus. The excess of such pollutants can cause Urban-Rural Development. The investigation resulted the explosive growth of plants and algae, the in an observed pass rate of around 50%. depletion of oxygen in the water body, and nally the deaths of aquatic animals such as sh. Take Taihu Even though boiling water can remove many visible Lake as an example where the algae blooms frequently microbial contaminants causing acute disease, other occurs, the overall state of the lake is characterized invisible contaminants may be overlooked. A as mild eutrophication. The average annual total considerable part of such contaminants are endocrine phosphorus concentration meets the IV class standard, disrupting chemicals, which may reduce may inuence and the average annual total nitrogen concentration reproduction, hormone related cancer, the immune meets V class standard. The government has paid system and interfere with the nervous system. Shi and attention to environmental problems and taken co-workers [33] studied phthalate esters in water measures to prevent further pollution through sources from the YRD, and found di-2-ethylhexyl optimizing the economic structure and promoting phthalate (DEHP), diethyl phthalate (DEP) and transformation of the economic mode. Nevertheless, dibutyl phthalate (DBP) as the major phthalate esters it will be an arduous task and take a long time to in the drinking water being analyzed. Thyroid improve the quality of the water environment in the hormone antagonist potencies were present in most Taihu Lake. of the detected water sources from the YRD. DBP is speculated to be the primary thyroid hormone Drinking water: Drinking water is an exposure receptor antagonist in water sources in the YRD, pathway of a number of pollutants to humans. In the while DEHP, di-n-octyl phthalate (DnOP) and YRD, the main water source for drinking is surface diisononyl phthalate (DiNP) also may contribute. water, including rivers and lakes. In May and June, 2007, the blue algae blooming incident happened in 2.3.3 Soil quality the Taihu Lake, resulting in pollution of drinking Soil is a major reservoir and a sink for organic water for Wuxi city. As a consequence, there was a pollutants because of its adsorption capacity. serious shortage of domestic and drinking water and According to the bulletin of nation soil pollution the bottled water was sold out in the city. survey, China is suffering severely from soil contamination of pollutants. The soil pollution is The National Standard Committee and Ministry of more severe in the south of China than in the north. Health jointly revised and issued the Drinking Water The primary pollutants in soil are heavy metals Health Standards (GB 5749-2006). On the basis of (cadmium, nickel, copper, arsenic, mercury, lead), its rst version which was issued in 1985, the number PAHs and DDTs (DDT and its main metabolites, of indicators was increased from 35 to 106, including DDE and DDD). sensory properties and general physicochemical, toxicological and radioactivity indicators. As one of the main food producing areas in China, Environmental pollutants such as heavy metals, the YRD also suffers from soil contamination. The pesticides, PAHs and phthalate esters have been arable land area (per capita) in YRD is only about included in this standard. In 2009, a national 2/3 of that in the whole country. In addition, it

44 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta decreases over the years, indicating the lack of soil identi ed regional hot spots in the urban and resources in YRD, a decrease becoming increasingly industrial areas of Shanghai, which all suffered from severe. high PAH pollution (Figure 2.9). In another study, Wang et al [35] reported soil concentrations of PAHs Further, the soil in the farmland of the YRD is under (83 to 7220 ng/g for the sum of 16 PAHs) in Shanghai. increasing threats due to contamination. Excessive These concentrations were higher than those in other use of chemical fertilizers and pesticides increased areas around the world. The authors observed that the the residues of heavy metals, nitrates and organic high molecular weight PAHs were the most abundant compounds in the soil. The un-supervised emission components. Both studies pointed out that petrogenic and discharge of various pollutants changed the soil sources, coal combustion, and vehicular emissions as quality and nutrient status, requiring more chemical the main contributors of PAHs contaminating the soil fertilizers and pesticides and forming a vicious circle. in Shanghai. Exposure to PAHs from these soils, through direct contact, may pose a risk to humans. The PAHs spatial distribution in soil from Shanghai The urban soil PAHs pose a potential threat to potable has been well studied. Liu et al. [34] quanti ed 18 groundwater quality due to leaching of carcinogenic PAHs in surface soil samples from Shanghai. They PAH mixtures from soil in the study area.

Figure 2.9. Sampling locations (a) and isopleth map of total concentrations of 18 PAHs (b) in surface soils in the Shanghai area.

45 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

2.3.4 Exposure to wildlife hexachlorobenzene (HCB). This study describes a Wildlife have long been used for monitoring chemical geographical (spatial) pollution pattern among contamination from POPs since these pollutants are species, where high levels of DDTs and HCHs were persistent, bioaccumulative and toxic. Available data observed in mussels from China while PCBs and suggested that industrialization and urbanization CHLs level in China are relatively low (Figure 2.10). have caused elevated pollutants burden in wildlife Regarding the spatial distribution of POPs in mussel from China. However, there is still very little within mainland China, ten sites were selected and information on pollutants levels in wildlife from the three of them (Chongming Island, Shengsi Island and YRD. The existing studies from the YRD mainly Lianyungang) are located in the YRD. The results focused on aquatic biota, i.e. mussel and sh. indicate medium to low contamination of POPs in However, the Chemstrres research project is focused the YRD in general compared to other sites (e.g. on POPs and related compounds in wildlife as Xiamen, Jiaozhou Bay) in China. However, the level further discussed in Chapter 3.6 and 4.1. of DDTs (13000 ng/g fat) and HCHs (96 ng/g fat) in Chongming Island, Shanghai was one of the highest In a systematic study, mussels were used to compare contamination levels among sites in China, even in the POPs level in the coastal waters of several Asian Asia, according to this study (Figure 2.11). countries [36]. It showed that the analyzed POPs occurred in the general descending order of China is the one of main e-waste recycling countries concentrations: DDTs > polychlorinated biphenyls in the world. Some of the e-waste recycling sites are (PCBs) > chlordanes (CHLs) > HCHs > located in the YRD (e.g. Taizhou) and pollutants in

Concentrations of DDTs (ng g-1 lw) Concentrations of HCHs (ng g-1 lw)

100 000 240 x x 220 10 000 200 180 160 1000 x x x 140 x 120 100 x x 100 x x x x 80 x 10 60 40 1 20 0 China India Japan Korea Malaysia Philippines China India Japan Korea Malaysia Philippines

Figure 2.10. Spatial distribution of DDTs and HCHs in mussels from Asian countries.

46 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta electronic devices, such as brominated  ame tissues from the same area ranged from 15 to 3140 retardants are released to the environment and some ng/g fat, which was 2–3 orders of magnitude higher of which accumulate in the wildlife. Jiang et al. [37] than those reported in the literature. Risk assessment measured PBDEs congeners in the muscle tissue of on dietary intake is required. seven sh and shell sh species that were collected downstream of e-waste recycling plants in Taizhou, 2.3.5 Exposure to humans Zhejiang. The concentration sum PBDEs ranged from In some cases, human samples are directly used to 545 to 1690 ng/kg wet weight (ww), and the mean assess the internal exposures for persistent and concentration was 1382 ng/kg ww in sh and 858 bioaccumulative chemicals. Human milk, blood and ng/kg ww in shell sh, respectively. These levels are hair are convenient matrices for analysis of much higher than other studies in sh from non- contaminants in humans. Human milk is commonly hotspots areas [38]. In addition, PBDEs in chicken applied for monitoring of POPs since readily

ng/g fat PBDEs PCBs CHLs HCHs DDTs

500

400

300

200

100

0 Cheng Si Dao Chong Ming Dao, ShanghaiLian Yun Gang Xiamen (Haichang) Qingzhou Fuzhou (Ming Jian) Beihai Dalian Jiao Zhou Wan, QingdaoShantau (Lauping)

Figure 2.11. Level of POPs (ng/g fat) in pooled mussels from China (Please observe that the concentration of DDTs has been divided by 100 in the « gure to make it visible among the other POPs in this diagram).

47 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

accessible and allowing relatively large volumes to be However, PCBs and PCDD/Fs concentrations in collected noninvasively. Human exposures are human milk from the urban area of Shanghai were elaborated on in the Chemstrres project as assessment the highest among the 12 provinces/cities of POPs and related compounds are carried out in investigated. Moreover, high concentrations of mothers’ milk as presented in Chapter 3.8. Further, peruorooctanoic acid (PFOA) (814 pg/ml) for the human exposure to these pollutants, via household rural samples and 616 pg/ml for the urban samples, dust, is researched in Chemstrres as well (Chapter were found in human milk from Shanghai, higher 3.10). than the average value in any of the other of the 11 provinces [41]. The estimated daily intake (EDI) for A series of national survey on several groups of POPs PFOA (88.4 ng/kg and day) for Shanghai was close to in human milk from China has been carried out since the tolerable daily intake of 100 ng/(kg and day) as 2007 [39-42]. A total number of 1237 human milk proposed by the German Federal Institute for Risk samples collected from 12 provinces in China and Assessment and the Drinking Water Commission. It divided into 24 pools, have been assessed. Shanghai should be pointed out that pooled samples were used was included and the only place representing the in the national survey even if they are divided into YRD area. The results showed DDTs as the most urban and rural areas. In this case, the extreme value abundant pesticide in human milk, followed by can inuence the results to some extent. HCHs [39]. Levels of chlordanes, “drins” and mirex were lower. The concentrations of PCBs, PBDEs and 2.3.6 Conclusions PCDD/Fs are in general in the moderate to low range As one of the rapidly developing areas in China, or in global perspective. However, PFAS showed higher even in the world, the YRD area suffers from exposure level compared with many other countries complex matrix of environmental problems. A large [41]. In a recent published paper, CPs levels in these proportion of these are attributed to the direct and human milk samples were reported with median indirect chemical pollution. For the public, the main

concentrations of 681 and 60 ng/g fat for short concern would be air pollution (PM2.5) and drinking chained chlorinated paraf ns (SCCPs) and medium water quality, which might suggest the authority to chained chlorinated paraf ns (MCCPs), respectively take priority to handle these issues. However, other [42]. In addition, an increasing trend over time was non-intuitive environmental issues must not be indicated for the CPs from 2007 to 2011. This neglected. They can cause chronic and irreversible increase is consistent with the increasing production adverse effect in humans and wildlife. Taken together volumes of CPs in China. this implies a need for a structured framework (including study plan, method development, chemical A large variation was indicated for the levels of POPs analysis, and ecotoxicology effects) for assessment of and related compounds depending on the environmental pollutants and their possible risks in geographical locations of the mothers’ milk samples the YRD area. [39-42]. With regard to the POPs level in Shanghai’s human milk, PBDEs and OCPs showed a low or Authors median level. The study found that from 1997 to Professors Daqiang Yin, Zhiliang Zhu, Yanling Qiu, 2007, HCHs and DDTs levels in human milk from Åke Bergman and Dr. Ge Yin Shanghai decreased by 80% and 45%, respectively.

48 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

References

1. Zheng JJ, Jiang P, Qiao W, Zhu Y, Kennedy E. Analysis of air 13. Zhang H, Yu X, Yang W, Peng J, Xu T, Yin D, Hu X. MCX based pollution reduction and climate change mitigation in the solid phase extraction combined with liquid chromatography industry sector of Yangtze River Delta in China. Journal of tandem mass spectrometry for the simultaneous Cleaner Production 2016, 114:314-322. determination of 31 endocrine-disrupting compounds in 2. Chen Z, Xu S, Xu Q, Hu X, Yu L. Surface water pollution in the surface water of Shanghai. Journal of Chromatography B 2011, Yangtze River Delta: Patterns and Countermeasures. 879:2998-3004. Pedosphere 2002, 12:111-120. 14. Ma LM, Zhang X. Space effect of smog pollution in China and 3. Ministry of Environmental Protection and Ministry of Land and impact on economic and energy structure. China Industrial Resources. Bulletin of the national soil pollution survey (In Economics 2014, 4:19-31 (In Chinese). Chinese). 2014. 15. National Bureau of Statistics of China. China Statistical 4. Liu GQ, Zhang G, Jin ZD, Li J. Sedimentary record of hydrophobic Yearbook 2014. Available from: http://www.stats.gov.cn/tjsj/ th organic compounds in relation to regional economic ndsj/. Accessed April 16 , 2017. development: A study of Taihu Lake, East China. Environmental 16. China Energy Bureau of China Statistical Division. China Energy Pollution 2009, 157:2994-3000. Statistical Yearbook 2014. Beijing: Statistics Press, 2015, 5. Xu Y, Zhou Y, Chen X, Miao S, Honwah L M, Qin Q. Chemical pp54-55. characterization and risk assessment of organochlorine 17. Zhai YR, Wang QG, Song YY. Air pollutant emissions from pesticides in sediments and biota from Meiliang Bay of Taihu energy consumptions in the Yangtze River Delta region. China Lake. Journal of Southesat University 2015, 45:328-335 (In Environmental Science 2012, 32:1574-1582 (In Chinese). Chinese). 18. Ding QQ, Chen CH, Li L. The estimates of main air pollutant 6. Lin T, Hu L, Guo Z, Zhang G, Yang Z. Deposition µuxes and fate emission about the thermal power industry in Yangtze River of polycyclic aromatic hydrocarbons in the Yangtze River Delta Region. China Environmental Science 2015, 7:2389-2394 estuarine-inner shelf in the East China Sea. Global (In Chinese). Biogeochemical Cycles 2013, 27:77-87. 19. Huang C, Chen CH, Li L. Anthropogenic air pollutant emission 7. Jiang L, Hu X, Yin D, Zhang H, Yu Z. Occurrence, distribution and characteristics in the Yangtze River Delta region,China. Acta seasonal variation of antibiotics in the Huangpu River, Scientiae Circumstantiae 2011, 9: 1858-1871 (In Chinese). Shanghai, China. Chemosphere 2011, 82:822-828. 20. Ministry of Environmental Protection (MEP). Chemical risk th 8. Wu M, Wang F, Yang X, Shi M, Xu G. Concentration levels and prevention 12 «ve-year plan. 2013. distribution features of PAEs in water environment in Shanghai. 21. Li J, Bai XJ, Ren ZJ. 2011-2013 Statistics analysis and Journal of Shanghai University (Natureal Science) 2016, countermeasures of dangerous chemical accidents in our 22:105-113 (In Chinese). country. Journal of Safety Science and Technology 2014, 9. Jiang D, Yue L, Ma D, Zhu Y, Yin D. Ecological risk assessment of 6:142-147. water in Taihu Lake and Tianmu Lake using species sensitivity 22. Yu Y. The trend of fertilizer pollution and countermeasures. distribution model. Environmental Chemistry 2012, 31:296-301 China forum on sustainable development and China society for (In Chinese). sustainable development annual conference.Beijing, China. 10. Jiang D, Hu X, Yin D. Ecological risk assessment of polycylic 2009. aromatic hydrocarbons of sediment in Taihu Lake using species 23. Richardson BJ, Larn PKS, Martin M. Emerging chemicals of sensitivity distributions. Asian Journal of Ecotoxicology 2011, concern: Pharmaceuticals and personal care products (PPCPs) in 6:60-66. Asia, with particular reference to Southern China. Marine 11. Zhou Y, Asplund L, Yin G, Athanassiadis I, Wideqvist U, Bignert Pollution Bulletin 2005, 50:913-920. A, Qiu Y, Zhu Z, Zhao J, Bergman Å. Extensive organohalogen 24. Kantar K. An overview of the consumption trend of personal contamination in wildlife from a site in the Yangtze River Delta. care products in China. Sales and marketing 2016, 32-34. Science of the Total Environment 2016, 554-555:320-328. 25. Wang D, Sui Q, Zhao WT, Lv SG, Qiu ZF, Yu G. Pharmaceutical 12. Wang D. Polycyclic aromatic hydrocarbons and organochlorine and personal care products in the surface water of China: A pesticides in «sh from Taihu Lake: their levels, distribution and review. Chinese Science Bulletin 2014, 59:743-751 (In Chinese). human health risk assessment. Shanghai University Doctoral Thesis 2013, (In Chinese).

49 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

26. Zhang Q, Xin Q, Zhu JM, Cheng JP. The antibiotic 36. Ramu K, Kajiwara N, Sudaryanto A, Isobe T, Takahashi S, contaminations in the main water bodies in China and the Subramanian A. Ueno D, Zheng G, Lam P, Takada H, Zakaria M, associated environmental and human health impacts. Viet P, Prudente M, Tana T, Tanabe S. Asian mussel watch Environmental Chemistry 2014, 33:1075-1083 (In Chinese). program: Contamination status of polyhrominated diphenyl 27. Shanghai Environmental Protection Bureau (SEPB). Annual ethers and organochlorines in coastal waters of Asian environmental bulletin in Shanghai in 2015 (In Chinese). countries. Environmental Science & Technology 2007, 41:4580- Available from: http://www.sepb.gov.cn/fa/cms/shhj// 4586. shhj2143/shhj2144/2016/03/92097.htm. Accessed April 16th, 37. Jiang J, Shi S, Chen T. Occurrence of polybrominated diphenyl 2017. ethers in «sh and shell«sh downstream from electronic-waste 28. Bostrom CE, Gerde P, Hanberg A, Jernstrom B, Johansson C, recycling plants. Journal of Environmental Science 2010, Kyrklund T, Rannug A, Törnqvist M, Victorin K, Westerholm R. 22:723-730. Cancer risk assessment, indicators, and guidelines for polycyclic 38. Qiu YL, Strid A, Bignert A, Zhu ZL, Zhao JF, Athanasiadou M, aromatic hydrocarbons in the ambient air. Environmental Athanassiadis I, Bergman Å. Chlorinated and brominated Health Perspectives 2002, 110:451-488. organic contaminants in «sh from Shanghai markets: A case 29. Kong SF, Li XX, Li L, Yin Y, Chen K, Yuan L, Zhang Y, Shan Y, Ji Y. study of human exposure. Chemosphere 2012, 89:458-466. Variation of polycyclic aromatic hydrocarbons in atmospheric 39. Zhou PP, Wu YN, Yin SA, Li JG, Zhao Y, Zhang L, Chen H, Liu Y, PM2.5 during winter haze period around 2014 Chinese Spring Yang X, Li X. National survey of the levels of persistent Festival at Nanjing: Insights of source changes, air mass organochlorine pesticides in the breast milk of mothers in direction and «rework particle injection. Science of the Total China. Environmental Pollution 2011, 159:524-531. Environment 2015, 520:59-72. 40. Zhang L, Li JG, Zhao YF, Li XW, Wen S, Shen HT, Wu YN. 30. Dai ZJ, Du JZ, Zhang XL, Su N, Li JF. Variation of riverine material Polybrominated diphenyl ethers (PBDEs) and indicator loads and environmental consequences on the Changjiang polychlorinated biphenyls (PCBs) in foods from China: Levels, (Yangtze) Estuary in recent decades (1955-2008). Environmental dietary intake, and risk assessment. Journal of Agricultural and Science & Technology 2011, 45:223-227. Food Chemistry 2013, 61:6544-6551. 31. Environmental Protection Department of Jiangsu Province 41. Liu JY, Li JG, Zhao YF, Wang YX, Zhang L, Wu YN. The occurrence (JSHB). Annual environmental bulletin in Jiangsu Province in of perµuorinated alkyl compounds in human milk from 2015 (In Chinese). Available from: http://www.jshb.gov.cn/ different regions of China. Environment International 2010, hbzl/hjjb/201606/t20160603_352565.html. Accessed April 16th, 36:433-438. 2017. 42. Xia D, Gao LR, Zheng MH, Li JG, Zhang L, Wu YN, Tian QC, Huang 32. Zhejiang Environmental Protection Bureau (ZJEPB). Annual HT, Qiao L. Human exposure to short- and medium-chain environmental bulletin in Zhejiang Province in 2015 (In chlorinated paraffins via mothers' milk in Chinese urban Chinese). Available from: http://www.zjepb.gov.cn/root14/ population. Environmental Science & Technology 2017, xxgk/hjzl/hjzkgb/201606/t20160602_414196.html. Accessed 51:608-615. April 16th, 2017. 33. Shi W, Zhang FX, Hu GJ, Hao YQ, Zhang XW, Liu HL, Wei S, Wnag XR, Giesy JP, Yu HX. Thyroid hormone disrupting activities associated with phthalate esters in water sources from Yangtze River Delta. Environment International 2012, 42:117-123. 34. Liu Y, Chen L, Zhao JF, Wei YP, Pan ZY, Meng XZ, Huang QH, Li WY. Polycyclic aromatic hydrocarbons in the surface soil of Shanghai, China: Concentrations, distribution and sources. Organic Geochemistry 2010, 41:355-362. 35. Wang XT, Miao Y, Zhang Y, Li YC, Wu MH, Yu G. Polycyclic aromatic hydrocarbons (PAHs) in urban soils of the megacity Shanghai: Occurrence, source apportionment and potential human health risk. Science of the Total Environment 2013, 447:80-89.

50 Chapter 2: Highlights of chemicals, health and environment challenges in the Yangtze River Delta

51 Chapter 3:

Chemstrres research activities

52 Chapter 3: Chemstrres research activities

3.1 Ecotox project with the pond snail (Bellamya aeruginosa)

As sinks and secondary sources of heavy metals and Chemstrres is focused on assessment of the sediment organic pollutants in the aquatic environment, quality of the eastern part of Taihu Lake using caged sediments may pose direct threats to benthic biota pond snails. and organisms. As a dominant community member of freshwater aquatic systems in China, Bellamya Background and aim of project aeruginosa (Gastropoda, Prosobranchia, Valvatidae) Aquatic contamination has been of environmental has been found to accumulate contaminants and to concern for quite some time. Sediments are well- be sensitive to sediment-borne pollutants at the known sinks and long-term sources of xenobiotics. A biochemical level. This species is used for human large variety of contaminants (e.g. synthetic organic consumption and a primary food item of the black chemicals, polycyclic aromatic hydrocarbons, trace carp (Mylopharyngodon piceus). Therefore, the pond metals, pharmaceuticals) from industries, agricultural, snail represents a key organism involved with the urban and maritime activities can accumulate in this transfer of contaminants through the food web in matrix and reach concentrations higher than those Chinese surface waters, and plays a key role in the detected in the water column [1]. In the sediment- assessment of contaminant risks to the aquatic water interface, these compounds may be ecosystems in China. Taihu Lake located in the delta resuspended, transported and redeposited far from region of the Yangtze River, is the third largest their origin source, producing negative effects to the freshwater lake in China and an important drinking benthic biota and biomagni cation events along the water source for surrounding cities. With rapid food chain. Thus, characterizing sediment economic development and population increase, the contamination is viewed as an important goal in pollution of Taihu Lake has been getting worse over environmental monitoring. the past few decades. The present project under

53 Chapter 3: Chemstrres research activities

The assessment of sediment quality can be carried the black carp (Mylopharyngodon piceus) and also out through several tools, including routine chemical consumed by Chinese people and visitors to China. analyses and sediment toxicity protocols. One of the Therefore, pollutants may be transferred from this most ef cient methods for understanding the species to higher trophic levels through the food linkages between chemical exposure and potential chain. Furthermore, B. aeruginosa has been reported health outcomes in contaminated environments is in to be relatively sensitive to different sorts of situ toxicity test using caged organisms. In the anthropogenic pollutants [6], which makes it useful beginning, sh and bivalves were used more as a test species for sediment toxicity assessments. frequently owing to technology transfer from aquaculture. Later this approach was extended to Biomarkers are de ned as biochemical, cellular, macroinvertebrates such as cladocerans, amphipods, physiological or behavioral variations that can be and midges [2]. For the sediment compartment, measured in biological samples and used as tools Nebeker et al. [3] rst proposed the idea of in situ for the assessment of adverse biological effects of sediment test chambers for macroinvertebrates. In pollutants. A multiple biomarker approach combined situ tests are more relevant in ecological terms than with chemical analysis could provide better laboratory toxicity tests, since interactions among evaluation of the environmental hazard [7]. biological variables (such as multi-species interactions), physical variables (such as light In this project, the caged snails were employed to intensity and water  ow rate) and chemical variables assess the sediment quality of the eastern part of (mixtures of toxic substances) have been considered Taihu Lake (Figure 3.1.1). The objectives were as [4]. Further, there are some other advantages in using follows: caged organisms, such as the precise knowledge of – to determine the suitability of a battery of the location, the exact duration of exposure and the biochemical biomarkers analyzed in the caged selection of species with speci c biology and B. aeruginosa after exposure to contaminated developmental stages. Besides, using transplanted sediments under eld conditions as a tool for the animals from the same source also reduces inter- assessment of sediments. The battery of biomarkers individual variability among exposed organisms and consisted of activities of phase I biotransformation minimizes the in uence of adaptive mechanisms. In enzymes ethoxyresoru n-O-deethylase (EROD), this way, results from different sites can be validly antioxidant enzymes including superoxide compared. dismutase (SOD) and catalase (CAT), reactive oxygen species (ROS), the protein carbonyl content Benthic gastropods are important members of (PCO) and lipid peroxidation (LPO); aquatic environment, and relatively sensitive to – to evaluate the sediment quality of Taihu Lake contaminants [5]. B. aeruginosa is a freshwater involving both chemical analysis and toxic effects. gastropod that is quite common and abundant throughout Chinese freshwater ecosystems. As deposit-feeders, they are closely associated with surface sediments where they burrow in the upper layer and ingest particulate matter, algae and bacteria. The pond snail is a primary food item of

54 Chapter 3: Chemstrres research activities

WATER

NYLON AND POLYPROPYLENE SNAILS (B. AERUGINOSA) CAGES CONTAINING SNAILS

SEDIMENT

Figure 3.1.1. System used for in situ transplants of caged pond snails in Taihu Lake.

Preliminary results and reasoning Two experimental sites in Taihu Lake were selected, samples were collected from both sites. Analyses including site A (31°13'51" N-120°22'7" E) and site of contaminations in the sediment of Taihu Lake B (31°6'2" N-120°13'55" E) (c.f. Figure 3.1.2). The in showed that heavy metals (Cr, Cu, Pb, Ni, Zn, Cd, situ exposure tests were conducted for 21 days during As), organochlorine pesticides (OCPs), PCBs and the summer (August 2015). Three cages were placed PBDEs existed in both sites. Further, the results at each site and 120 snails were contained in each showed that the concentrations of heavy metals, cage. A cage in each site was sampled on the 7th, 14th, OCPs and PCBs analyzed in the sediment from site 21st day and the number of surviving snails were A were higher than at site B. The survival rate of the counted. A number of them were immediately frozen snails caged at site A was lower than site B. Thus, it in liquid nitrogen for biochemical and chemical can be indicated that B. aeruginosa was a relatively analysis, and others were transferred for sensitive species for biomonitoring in freshwater histopathological examination. Surface sediment lakes.

55 Chapter 3: Chemstrres research activities

CHANGZHOU

WUXI

YIXING

SUZHOU

SITE A TAIHU LAKE

SITE B XISHAN ISLAND

DONGSHAN ISLAND

HUZHOU

Figure 3.1.2. The location of the two sampling sites in Taihu Lake, site A and site B. The locations of the two cities, Suzhou and Wuxi, are given as well.

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Biochemical parameters, including EROD, SOD, In conclusion, the in situ exposure tests using caged CAT, ROS, PCO and LPO were evaluated in the pond snails can be recommended as indicated as an hepatopancreas of snails, as well as histapothological ef cient biomonitoring species in evaluating sediment effects. The methodology of the Integrated Biomarker quality. Response (IBRv2) [8] was used to integrate the responses of different biomarkers into a single value Authors and sub-project researchers or graph. On the 7th day of the caging exposure, the Corresponding author: Assoc. Prof. Lingling Wu* IBR values for site A and site B were 10.2 and 10.8, ([email protected]) respectively. On the 14th day of the caging exposure, Profs. Magnus Breitholtz, Ling Chen, Markus the site A and site B showed the highest IBR values, Hecker, Taowu Ma, Yanling Qiu, Jianfu Zhao; namely 18.2 and 17.0, respectively. After exposure Ms. Lei Duan, Ms. Qian Li, Mr. Meng Wang for 21 days, the IBR value for site B decreased to 14.1. There is no IBR value for the site A since the cage unexpectedly disappeared during the last phase of the experiment. The IBR value for the site A was higher than site B, indicating that site A was a more stressful place for the Pond snails. References

From the results of chemical analysis, higher 1. Hartwell SI, Hameedi MJ, Pait AS. Empirical assessment of contamination levels of heavy metals, OCPs and incorporating sediment quality triad data into a single index to distinguish dominant stressors between sites. Environmental PCBs were detected in the sediments collected at site Monitoring and Assessment 2011, 174:605-623. A. Thus, it can be assumed that the IBR index was in 2. Chappie DJ, Burton GA. Applications of aquatic and sediment agreement with the contamination levels in sediments toxicity testing in situ. Soil & Sediment Contamination 2000, from Taihu Lake. The integration of multiple 9:219-245. biomarker responses found in caged snails could thus 3. Nebeker AV, Cairns MA, Gakstatter JH, Malueg KW, Schuytema GS, Krawczyk DF. Biological methods for determining toxicity of be used to reect the contamination levels detected at contaminated fresh-water sediments to invertebrates. different sites and considered as an ef cient Environmental Toxicology and Chemistry 1984, 3:617-630. biomonitoring approach. 4. Bonnineau C, Moeller A, Barata C, Proia L, Sans-Piché F, Schmitt-Jansen M, Guasch H, Segner H. Advances in the In gastropods, hepatopancreas is the main organ multibiomarker approach for risk assessment in aquatic ecosystems. The Hand- book of Environmental Chemistry v.19 involved in the detoxi cation of organic and — Emergency and Priority Pollutants in Rivers. Edited by inorganic toxic substances and histopathological Guasch H, Ginebreda A, Geiszinger A. Berlin: Springer, 2012, pp responses are important indicators of the effects of 147-179. environmental threats [9, 10]. Enlarged tubular 5. Oetken M, Nentwig G, Loffler D, Ternes T, Oehlmann J. Effects lumina (T) and dilated hemolymph spaces (HS) of pharmaceuticals on aquatic invertebrates. Part I. The antiepileptic drug carbamazepine. Archives of Environmental between tubules and physiological damages in the Contamination and Toxicology 2005, 49:353-361. form of loss of tissue integrity were observed in the 6. Ma TW, Gong SJ, Zhou K, Zhu C, Deng KD, Luo QH, Wang ZJ. hepatopancreas of snails. The histopathological Laboratory culture of the freshwater benthic gastropod effects might have been induced by the Bellamya aeruginosa (Reeve) and its utility as a test species for contaminations in sediments. sediment toxicity. Journal of Environmental Sciences 2010, 22:304-313.

57 Chapter 3: Chemstrres research activities

7. Galloway TS, Sanger RC, Smith KL, Fillmann G, Readman JW, Ford TE, Depledge MH. Rapid assessment of marine pollution using multiple biomarkers and chemical immunoassays. Environmental Science & Technology 2002, 36:2219-2226. 8. Sanchez W, Burgeot T, Porcher JM. A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environmental Science and Pollution Research 2013, 20:2721-2725. 9. Osterauer R, Kohler HR, Triebskorn R. Histopathological alterations and induction of hsp70 in ramshorn snail (Marisa cornuarietis) and zebra«sh (Danio rerio) embryos after

exposure to PtCl2. Aquatic Toxicology 2010, 99:100-107. 10. Tanhan P, Sretarugsa P, Pokethitiyook P, Kruatrachue M, Upatham ES. Histopathological alterations in the edible snail, Babylonia areolata (Spotted babylon), in acute and subchronic cadmium poisoning. Environmental Toxicology 2005, 20:142-149.

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3.2 Ecotoxicology of chlorinated paraffins Directive (76/679/EEC). However, medium chain CPs and long chain CPs are still used in some industries Chlorinated paraf ns (CPs) are widely used in Europe as substitutes for the SCCPs and other industrial chemicals with China as the largest CP additives, as well. In contrast, in China, none of the producer in the world. The largest contributors for classes have any use restrictions. CPs release to the environment are the metal working industry, being used as a ame retardant and Production, storage, transportation, industrial use, application as plasticizers and sealants/adhesives, release from incorporated items and leaching are contributing greatly to high emissions into air, routes of CPs release to the environment, via runoff, surface water and soil. Short chain chlorinated or volatilization from land lls, sewage sludge or paraf ns (SCCPs) are under consideration to be waste disposal sites [1]. The improper disposal of included in the Stockholm Convention on Persistent used metal working items and land lling of products Organic Pollutants (POPs) list, due to their POP as PVC, textiles and painted items may also result in characteristics. Still ecotoxicological data are scarce an increased leaching of CP into the environment and which may be due to the dif culties in testing this further be a major source of CPs in the environment class of chemicals. This can possibly be due to their [2]. strongly hydrophobic properties and mixture complexity. Therefore, there is an urgent need to CPs have found widespread distribution among develop new tools to promote understanding of any almost all environmental matrices, including air [3, underlying ecotoxicological effects of this group of 4], water [5, 6], soil [7], sediment [8] and wildlife [5, contaminants in the environment. 9, 10], but also in other matrices as sewage sludge, The main goal of this project under Chemstrres is to e-waste[11], household dust [12] and human mothers’ validate a new tool for the accurate testing of CPs milk [13]. In fact, SCCP concentrations found in and to provide fundamental understanding and human breast milk in the UK ranged from 49 to 820 relevant ecotoxicological data concerning the effects ng/g fat [13], which is 3 times the PCB levels of the CPs in biota. previously found in mothers’ milk in Japan [14]. CPs are globally spread, found in both urban areas of Background and aim of project Europe and North America, but also in remote areas Chlorinated paraf ns, also known as polychlorinated i.e. the Arctic [15]. Hence, it is hypothesized that air alkanes, are a group of chlorinated derivatives of transportation might be a signi cant route of the high molecular weight n-alkanes, divided in groups propagation worldwide [16]. depending on their carbon number in the aliphatic chain: short chain (C10-C13, SCCPs), medium chain In highly industrialized countries as China, the

(C14-C17, MCCPs), and long chain (C18-C30, LCCPs) production and, by consequence, release into the chlorinated paraf ns. They are considered both environment of CPs is expected to continue PBT- (i.e. persistent, bioaccumulative and toxic) and increasing. China began its production of CPs in the vPvB (i.e. very persistent, very bioaccumulative) end of the 1950s. Due to the high demand from the substances, being now under restricted use in eleven metal manufacturing and plastics industry, CPs’ EU member states in metal working and leather annual production in China increased from less than nishing, under the amended Marketing and Use 10 thousand tons in the 1980s up to more than one

59 Chapter 3: Chemstrres research activities

million tons per year as of 2009, making China The lack of data concerning this group of currently the largest producer of CPs in the world. contaminants is due to their inherent high molecular SCCPs are estimated to account for about 46% of the complexity: they present dif culties in, not only whole CPs production and release (China Chemical testing due to their high hydrophobicity, but also Industry News, 2010). In comparison, until 2006, concerning analytical detection. The work within the the European production volume ranged from 1,500 Chemstrres project is aimed at validating equilibrium to 2,500 tons per year, whereas the estimated passive dosing as a controlled and stable exposure production for the USA ranged from 6,000 to 8,800 system to CPs, anticipated to overcome losses due to tons per year. sorption and/or volatilization. In passive dosing experiments, silicone is loaded with the hydrophobic CPs’ high usage and production are actively chemical (in this case, CPs) and brought into contact contributing to the increased environmental with a medium (e.g. water, culture medium). Once deterioration of the Yangtze River Delta (YRD) and we have validated the passive dosing as an adequate this has been shown in the scienti c literature that test system for CP, with the aid of state of the art CP describes increasing levels of these contaminants in detection and quanti cation methods (APCI-QTOF- both biotic and abiotic compartments of the YRD. MS and GC-MS based), we aim to strengthen passive Previous studies have demonstrated that SCCPs do dosing as a method to understand and test these bioaccumulate and biomagnify: a trophic hydrophobic contaminants in an ecotoxicological magni cation factor of 2.39 was calculated in a context. zooplankton-shrimp- sh food web from the Bohai Sea, China [17]. Air samples in Chinese cities showed We therefore intend to use this system to: mean total CPs concentrations of 137 and 200 ng/m3, • Generate new ecotoxicological data on growth 30 and 50 times higher than the concentrations in and survival in Daphnia magna Zurich, a highly industrialized city in Switzerland • Compare the risk and hazards between SCCPs [4]. In 2012, the highest SCCP concentrations among and MCCPs through their bioaccumulative wildlife samples were found in mollusk samples of potential in a two trophic level system 2.83 mg/g dw in Tianjin, China [11]. These are two important challenges, not only for the Even though these are alarming numbers, most scienti c community, but also to ll current gaps in articles describing CP concentrations and effects in the regulatory eld. CPs have the potential to severely biota are still scarce, in particular when compared to harm exposed biota (both aquatic and terrestrial) and other classic POPs, SCCPs seem to be of higher given their persistence, as mentioned before, there is concern in the environment. Even though SCCPs a need to generate ecotoxicological data. Recently, it have been proposed to be less persistent and was demonstrated that exposure to SCCPs can affect bioaccumulative than MCCPs and LCCPs [15], they development of zebra sh embryos, as malformation are found in higher levels. SCCPs have been shown to and survival rates at 96 hours post fertilization [24]. have relatively higher toxicity towards aquatic and The potential effect of SCCPs on gene expression in mammalian animals than the higher molecular mass the hypothalamic-pituitary-thyroid axis and thyroid CPs [18-23]. hormone levels was also demonstrated [25, 26]. This agrees with previous studies that have pointed out

60 Chapter 3: Chemstrres research activities

liver, thyroid and kidney are target organs of PCA toxicity in mammals[23]. Developmental toxicity and teratogenicity of SCCPs have been reported in e.g. zebra sh, sheephead minnow and Japanese medaka embryos exposed to SCCPs [22, 24].

Preliminary results and reasoning Passive dosing experiments have been performed with 5 different CP mixtures: one SCCP with low chlorine content, one SCCP with high chlorine content, one MCCP with medium chlorine content, one LCCP with medium chlorine content and the commercially available CP-52.

Analytical analysis showed that we are able to achieve a stable silicone/water equilibrium after 48h. Silicone/water partition coef cients (log Ksilicone/ water) were determined to be (mean±SD) 3.40±0.66, 4.27±0.24 and 4.12±0.66 for Cereclor 50LV, Hüels 70C and Cereclor S45, respectively. Ecotoxicological testing using the passive dosing system will follow,

namely Daphnia magna immobilization (EC50, LC50) and bioaccumulation studies (Figure 3.2.1.). CI CI CI CI

CH3 Authors and sub-project researchers H3C CI CI Corresponding author: Ms Mafalda Castro* ([email protected]) Profs. Magnus Breitholtz, Elena Gorokhova; Assoc. Prof. Lillemor Asplund; Drs. Anna Sobek, Bo Yuan, Mr. Ioannis Athanassiadis.

CI CI CI CI

CH3 H3C CI CI

Figure 3.2.1. Illustration of the passive dosing system.

61 Chapter 3: Chemstrres research activities

References

1. Wei GL, Liang XL, Li DQ, Zhuo MN, Zhang SY, Huang QX, Liao YS, 10. Ma XD, Zhang HJ, Wang Z, Yao ZW, Chen JW, Chen JP. Xie ZY, Guo TL, Yuan ZJ. Occurrence, fate and ecological risk of Bioaccumulation and trophic transfer of short chain chlorinated paraffins in Asia: A review. Environment chlorinated paraffins in a marine food web from Liaodong Bay, International 2016, 92-93:373-387. North China. Environmental Science & Technology 2014, 2. Nost TH, Halse AK, Randall S, Borgen AR, Schlabach M, Paul A, 48:5964-5971. Rahman A, Breivik K. High concentrations of organic 11. Yuan B, Fu JJ, Wang YW, Jiang GB. Short-chain chlorinated contaminants in air from ship breaking activities in Chittagong, paraffins in soil, paddy seeds (Oryza sativa) and snails Bangladesh. Environmental Science & Technology 2015, (Ampullariidae) in an e-waste dismantling area in China: 49:11372-11380. Homologue group pattern, spatial distribution and risk 3. Wang XT, Zhou J, Lei BL, Zhou JM, Xu SY, Hu BP, Wang DQ, assessment. Environmental Pollution 2017, 220:608-615. Zhang DP, Wu MH. Atmospheric occurrence, homologue 12. Hilger B, Fromme H, Volkel W, Coelhan M. Occurrence of patterns and source apportionment of short- and medium- chlorinated paraffins in house dust samples from Bavaria, chain chlorinated paraffins in Shanghai, China: Biomonitoring Germany. Environmental Pollution 2013, 175:16-21. with Masson pine (Pinus massoniana L.) needles. Science of the 13. Thomas GO, Farrar D, Braekevelt E, Stern G, Kalantzi OI, Martin Total Environment 2016, 560:92-100. FL, Jones KC. Short and medium chain length chlorinated 4. Diefenbacher PS, Bogdal C, Gerecke AC, Gluge J, Schmid P, paraffins in UK human milk fat. Environment International Scheringer M, Hungerbuhler K. Short-chain chlorinated 2006, 32:34-40. paraffins in Zurich, Switzerland-atmospheric concentrations 14. Todaka T, Hirakawa H, Kajiwara J, Onozuka D, Sasaki S, and emissions. Environmental Science & Technology 2015, Miyashita C, Yoshioka E, Yuasa M, Kishi R, Iida T, Uchi H, Furue 49:9778-9786. M. Concentrations of polychlorinated dibenzo-p-dioxins, 5. Sun RX, Luo XJ, Tang B, Li ZR, Huang LQ, Wang T, Mai BX. polychlorinated dibenzofurans, and polychlorinated biphenyls Short-chain chlorinated paraffins in marine organisms from the in blood and breast milk collected from pregnant women in Pearl River Estuary in South China: Residue levels and Sapporo City, Japan. Chemosphere 2011, 85:1694-1700. interspecies differences. Science of the Total Environment 2016, 15. Feo ML, Eljarrat E, Barcelo D. Occurrence, fate and analysis of 553:196-203. polychlorinated n-alkanes in the environment. Trac-Trends in 6. Pribylova P, Klanova J, Holoubek I. Screening of short- and Analytical Chemistry 2009, 28:778-791. medium-chain chlorinated paraffins in selected riverine 16. Li QL, Li J, Wang Y, Xu Y, Pan XH, Zhang G, Luo CL, Kobara Y, Nam sediments and sludge from the Czech Republic. Environmental JJ, Jones KC. Atmospheric short-chain chlorinated paraffins in Pollution 2006, 144:248-254. China, Japan, and South Korea. Environmental Science & 7. Wang XT, Zhang Y, Miao Y, Ma LL, Li YC, Chang YY, Wu MH. Technology 2012, 46:11948-11954. Short-chain chlorinated paraffins (SCCPs) in surface soil from a 17. Ma XD, Chen C, Zhang HJ, Gao Y, Wang Z, Yao ZW, Chen JP, Chen background area in China: occurrence, distribution, and JW. Congener-speci«c distribution and bioaccumulation of congener pro«les. Environmental Science and Pollution Research short-chain chlorinated paraffins in sediments and bivalves of 2013, 20:4742-4749. the Bohai Sea, China. Marine Pollution Bulletin 2014, 79:299- 8. Huttig J, Oehme M. Presence of chlorinated paraffins in 304. sediments from the North and Baltic Seas. Archives of 18. Warnasuriya GD, Elcombe BM, Foster JR, Elcombe CR. A Environmental Contamination and Toxicology 2005, Mechanism for the induction of renal tumours in male Fischer 49:449-456. 344 rats by short-chain chlorinated paraffins. Archives of 9. Reth M, Ciric A, Christensen GN, Heimstad ES, Oehme M. Toxicology 2010, 84:233-243. Short- and medium-chain chlorinated paraffins in biota from 19. Tomy GT, Fisk AT, Westmore JB, Muir DCG. Environmental the European Arctic – differences in homologue group patterns. chemistry and toxicology of polychlorinated n-alkanes. Reviews Science of the Total Environment 2006, 367:252-260. of Environmental Contamination and Toxicology 1998, 158:53-128.

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20. Madeley JR, Birtley RDN. Chlorinated paraffins and the environment. 2. Aquatic and avian toxicology. Environmental Science & Technology 1980, 14:1215-1221. 21. Geng NB, Zhang HJ, Zhang BQ, Wu P, Wang FD, Yu ZK, Chen JP. Effects of short-chain chlorinated paraffins exposure on the viability and metabolism of human hepatoma HepG2 cells. Environmental Science & Technology 2015, 49:3076-3083.

22. Fisk AT, Tomy GT, Muir DCG. Toxicity of C10-, C11-, C12-, and

C14-polychlorinated alkanes to Japanese medaka (Oryzias latipes) embryos. Environmental Toxicology and Chemistry 1999, 18:2894-2902. 23. Duncan R, Birtley N, Conning DM, Daniel JW, Ferguson DM, Longstaff E, Swan AAB. The toxicological effects of chlorinated paraffins in mammals. Toxicology and Applied Pharmacology 1980, 54:514-525. 24. Liu LH, Li YF, Coelhan M, Chan HM, Ma WL, Liu LY. Relative developmental toxicity of short-chain chlorinated paraffins in Zebra«sh (Danio rerio) embryos. Environmental Pollution 2016, 219:1122-1130. 25. Zhang Q, Wang JH, Zhu JQ, Liu J, Zhang JY, Zhao MR. Assessment of the endocrine-disrupting effects of short-chain chlorinated paraffins in in vitro models. Environment International 2016, 94:43-50. 26. Hallgren S, Darnerud PO. Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats – testing interactions and mechanisms for thyroid hormone effects. Toxicology 2002, 177:227-243.

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3.3 Establishment of Bellamya aeruginosa as strategies inuence the results. Further, we aim to a research monitoring species in the Yangtze investigate spatial distribution and temporal trends of River Delta selected POPs in the YRD environment by using the pond snail as an indicator. Environmental biomonitoring includes processes and activities to assess the quality of the environment by Background and aim of project using biological samples as indicators. It commonly Historically, YRD is famous for agriculture and refers to the chemicals with high persistency and aquaculture in China, termed “a land of rice and toxicity, i.e. including the persistent organic sh”. YRD area is also rich in resources of aquatic pollutants (POPs). A number of wildlife species, species, such as algae, snail, mussels and sh. Lower covering a wide range of trophic levels, including blue trophic level organisms are often selected to assess mussel, perch, seal and guillemot egg, have been used the contamination situation of pollutants in local in Swedish biomonitoring programs since the 1960’s. areas as well as to evaluate the risk of top-predators It should be stressed that the design of environmental being exposed to environmental contaminants. Their biomonitoring programs is highly important. Given relatively small home ranges makes them that the budget is a limiting factor, it has to be representative of well-de ned areas. Their low emphasized that the programs must enable us to biotransformation capacity makes them suitable as observe changes in the burden of environmental indicators for substances degraded by species at a pollutants or biomarker responses. Hence it is higher trophic levels with a potentially higher important to use proper species and sampling metabolic capacity (e.g. for PAHs). For instance, the strategies. “Mussel Watch” program was established in United State 1986 to monitor the concentration of In the Chemstrres project, we introduce the pond contaminants (e.g. DDT, PAHs and PCBs) in mussels, snail (Bellamya aeruginosa) as a monitoring species oyster and sediments. Table 3.3.1 lists a number of and we can illustrate how different sampling Mussel Watch program in the world.

Table 3.3.1. Examples of Mussel Watch programs in the world.

Region Program Starting year Species Analytes USA U.S. Mussel Watch 1986 M. edulis OCPs, Program M. californianus Trace metals, PBDEs C. virginica France Reseau National 1974 M. edulis Metals, PAHs, OCPs, d’Observation M. galloprovincialis Radiochemicals Mediterranean Mediterranean Mussel 2002 M. galloprovincialis Radiochemicals, Watch Program Trace metals Asia Asia-Paci†c Mussel 1994 M. galloprovincialis OCPs, PBDEs Watch Program P. viridis C. grayamus

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Apart from fresh water mussels, the pond snail is an power (1 – β) is de ned as the probability to detect abundant aquatic organism in YRD, used for human an effect, and if the effect actually exists. This is consumption. Considering that mussels have been essential in designing and evaluating monitoring widely cultivated in YRD to produce pearls, it might programs. Compared with the Type I error which is be better to choose snail as a biomonitoring species. set, prior to any statistical analyses, at a level more or There are a few studies showing the environmental less commonly agreed upon (usually α = 0.05 or exposure and bioaccumulation of contaminants in 0.01), the Type II error is more dif cult to calculate snails in aquatic ecosystems [1, 2]. The pond snail depending on several factors [5]. However, the has also been selected for sediment toxicity testing ignorance of Type II errors may result in serious [3]. However, to the best of our knowledge, there is consequences for monitoring programs (e.g. loss of no program using snail for environmental monitoring. future revenue), making the refund cost even higher This motivates us to start this project as pioneers. [6]. To solve this, statistical power is introduced as a priori analysis, to determine optimal sample size, at a A number of factors need to be carefully considered xed Type I, II error, and effect size. More when we establish a new monitoring program. introduction on statistical power is described Choosing tissue type is important because of the elsewhere [7]. composition difference. For example, POPs tend to accumulate in lipids, whereas phenolic compounds In this project, we are aiming to establish a new tend to accumulate in blood. However, for snail environmental biomonitoring program by applying samples, the whole soft tissue is the only practical the pond snail as an indicator species. The project option for chemical analysis. Another important can be separated in four steps: issue is whether to use pooled samples or individual 1. To design the program by taking advantage of samples for analyses. In general, individual analysis is statistical power. Several sampling strategies were preferred when the budget is suf ciently large. compared in combination with chemical analysis Advantages of individual analyses are e.g. to assess and computer simulation. relationships between the studied contaminant and 2. To investigate spatial distribution of POPs in snails potential confounding variables like age and lipid and sediment in YRD and to assess if content and to trace extreme values [4]. On the other bioaccumulation of certain POPs occurs. hand, pooling is necessary if individual samples 3. From a long term monitoring perspective, to cannot provide enough sample material for chemical monitor temporal trend of selected POPs in the analysis. Given that good knowledge on properties of YRD environment. pollutants and species is available, pooling might be 4. To expand the experience to Sweden by the best choice. Pooling can also save cost for introducing another species of snail (Viviparus chemical analyses that can be used to expand the viviparous) in Swedish lakes, as a new monitoring number of sampling sites and increase the species. geographical coverage. It is notable that the project can be more integrated To ensure highest possible quality of monitoring and linked to other parallel projects within programs, it is important to consider Type I (α) and Chemstrres, e.g., the sh project (c.f. Chapter 3.9) to Type II (β) errors in statistical analysis. Statistical explore the biomagni cation in the food web, and

65 Chapter 3: Chemstrres research activities

snail toxicity (c.f. Chapter 3.1) to have a complete Taihu Lake area. Meanwhile, sampling activities dataset in terms of using snail as a monitoring species have been carried out for a Swedish snail species in the YRD. Viviparus viviparous in Lake Tärnan (Figure 3.3.1).

Preliminary results and reasoning In the rst step, chemical analyses were performed on Snails and sediments were collected from three lakes individual snail from Tianmu Lake, China and Lake (Tianmu Lake, Taihu Lake and Dianshan Lake) in Tärnan, Sweden. For both lakes, each of ten YRD in 2014. Initially, Tianmu Lake was chosen as a individual snails from ve sites were analyzed. The reference site as it is located far from any truly urban chromatography showed a general low level of the areas. However, chlorinated paraf ns (CPs) were industrial POPs, e.g. PBDEs and PCBs. Lake Tärnan detected in the pond snails, indicating an in uence is considered as a reference lake under the Swedish from anthropogenic sources. Still, the sampling monitoring program. activities continue but currently with a focus on

Box Plot of DDE ng/g lw grouped by Station 24 Median 25%–75% 22 Non-Outlier Range Outliers

20

18

16 DDE ng/g lw DDE ng/g 14

12

10

8 1 2 3 4 5

Station

Figure 3.3.1. Sampling of the snail, Viviparus viviparous, was performed at « ve sites in Lake Tärnan (photo), 30 km Northwest of Stockholm. Chemical analysis of DDE was performed of the individual snail samples from the lake. The diagram shows DDE concentrations in the snails from the diff erent sampling sites in Lake Tärnan. Photos by Sara Danielsson (upper) and Anna-Karin Dahlberg (lower).

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High concentrations of DDE and pentachloroanisole were detected in the Tianmu Lake pond snails, as 4,4´-DDE indicated in the chromatogram shown in Figure 3.3.2. DDE is a metabolite of DDT, whereas pentachloroanisole is a methylated form of pentachlorophenol (PCP). The occurrences of these

Pentachloroanisole chemicals indicate previous or present use in the area.

Concentration of the ame retardant compound, BDE-47, in Tianmu Lake snails were selected for computer simulation. The variance of BDE-47 in the snails represents other polybrominated diphenyl ether

4,4´-DDT (PBDE) congeners quite well. By simulation, it is Dec603 (IS) veri ed that convenient sampling should be avoided, and sampling should be spread to a wide range area, to promote best quality monitoring of temporal 201918171615141312111098 trends of pollutants. The results from this subproject Figure 3.3.2. Chromatogram of a pond snail sample from Tianmu are discussed in some further details in Chapter 4.2. Lake. The chromatogram indicate the presence of both the DDE precursor, DDT, and DDE itself. The pentachloroanisole is an In the second step, pooled samples were collected abundant contaminant in the pond snails from Tianmu Lake. The analytical methodology requires addition of an internal standard from seven sites in Taihu Lake area together with (IS), i.e. Dec603, to the sample.

Figure 3.3.3. Spatial distribution of PCBs and PBDEs in the pond snail (left) and sediments (right) at the following sampling sites in Taihu Lake: L1: East Taihu Lake, L2: Xiaomeikou, L3: Dapukou, L4: Zhushan Lake, L5: Meiliang bay, L6: Gong Lake: and in Dianshan Lake L7. The concentrations of PBDEs and PCBs are shown at the individual sampling sites.

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sediments for PCB and PBDE analyses. The results References showed that the northern part of Taihu Lake (Zhushan Lake) has a higher level of such 1. Kobayashi J, Imuta Y, Komorita T, Yamada K, Ishibashi H, contaminants than the eastern part (East Taihu Lake) Ishihara F, Nakashima N, Sakai J, Arizono K, Koga M. Trophic magni«cation of polychlorinated biphenyls and (Figure 3.3.3). This spatial distribution pattern is polybrominated diphenyl ethers in an estuarine food web of consistent with studies on PAH and heavy metal [8, the Ariake Sea, Japan. Chemosphere 2015, 118:201-206. 9], implying that the northern part of Taihu Lake is 2. She YZ, Wu JP, Zhang Y, Peng Y, Mo L, Luo XJ, Mai BX. highly impacted by human activities. Bioaccumulation of polybrominated diphenyl ethers and several alternative halogenated µame retardants in a small herbivorous food chain. Environmental Pollution 2013, Authors and sub-project researchers 174:164-170. Corresponding author: Dr. Ge Yin* (ge.yin@aces. 3. Ma TW, Gong SJ, Zhou K, Zhu C, Deng KD, Luo QH, Wang ZJ. su.se) Laboratory culture of the freshwater benthic gastropod Profs. Yanling Qiu, Anders Bignert, Taowu Ma, Åke Bellamya aeruginosa (Reeve) and its utility as a test species for Bergman; Drs. Yihui Zhou, Elisabeth Nyberg and sediment toxicity. Journal of Environmental Sciences 2010, 22:304-313. Mr. Ioannis Athanassiadis, Ms. Sara Danielsson 4. Bignert A, Eriksson U, Nyberg E, Miller A, Danielsson S. Consequences of using pooled versus individual samples for designing environmental monitoring sampling strategies. Chemosphere 2014, 94:177-182. 5. Gewurtz SB, Backus SM, Bhavsar SP, McGoldrick DJ, de Solla SR, Murphy EW. Contaminant biomonitoring programs in the Great Lakes region: Review of approaches and critical factors. Environmental Reviews 2011, 19:162-184. 6. Peterman RM. Statistical Power Analysis Can Improve Fisheries Research and Management. Canadian Journal of Fisheries and Aquatic Sciences 1990, 47:2-15. 7. Cohen J. Statistical Power Analysis for the Behavioural Sciences. New York: Academic Press, 1977. 8. He XJ, Lu GH, Ding JN, Xie ZX. Distribution, sources and risk assessment of PAHs, PBDEs and PCBs in surfaces sediment from northern Taihu lake. Journal of Environ Health (China) 2013, 30:699-702 (In Chinese). 9. Hu LF, Wang YH, Wang QY, Lu GH, Xie ZX, Zhang ZH. Distribution and ecological risk assessment of mercury in water, sediments and typical aquatic organisms from Northern Taihu Lake. Journal of Agro-Environment Science 2014, 33:1183-1188 (In Chinese).

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3.4 Drinking water contaminants water products on the market include: bottled and – a screening project barreled water products. These products are manufactured distilled water, reversed osmosis (RO) Drinking water is an important pathway for human pure water, mineralized water, natural mineral water, exposure to chemicals. The types of drinking water deep lake water, well water and mountain spring are so diverse, including tap water, bottled water, water. barreled water and all kinds of beverages. Persistent organic pollutants (POPs) and endocrine disrupting In North America and Europe, tap water can be used compounds (EDCs) are, with an increasing for direct drinking, and most of the residents never frequency, reported worldwide in tap water which is doubt that their water is safe to drink. However, high commonly used for drinking and cooking. Indeed levels of perchlorate, originating from rocket/ numerous contaminants are also found, including spacecraft launch activities in tap water were several emerging ones. Nowadays, more and more reported in United States [1]. Other drinking water people in the big cities located in the Yangtze River contaminants are disinfection by-products, per- and Delta prefer to drink bottled water or freshly puri ed polyuorinated compounds (PFAS) from PFAS water instead of drinking tap water, directly. applied to re- ghting foams, organophosphate ame However, the contamination of commercial drinking retardants and many other emerging contaminants water products and locally and/or privately produced were also found in tap water in United States, China, water, is not well understood. Further, the risks of Japan and many other countries [2-5]. Most of the consuming contaminated drinking water, to human emerging contaminants, such as phthalate esters and health is yet linked to uncertainty due to the lack of organotin, found in drinking water are still not data. The present project under Chemstrres, is focused regulated. Accordingly, human health is challenged on screening of contaminants in drinking water being due to the emerging contamination of drinking consumed by the inhabitants of the YRD. water.

With attention to drinking water quality, Chinese Background and aim of project urban residents have a diversity of drinking water Generally, drinking water could be divided into two habits. The type of drinking water has shifted from main types: tap water and bottled water products single source of tap water into different bottled (Figure3.4.1). Tap water from public water supply water, barreled water, freshly puri ed water and all system can be directly used for drinking in most kinds of beverages, which were increasingly developed countries. However, people in China are consumed. The commonly used bottles and barrels used to drink tap water after boiled, and they also are made of polycarbonates (PC) or polyethylene use tap water for cooking rice and soup, and making terephthalate (PET) plastics, which may release tea or coffee. Freshly puri ed tap water from 24 h bisphenols (e.g. BPA) from PC and phthalate esters water vending machines in some residential from PET, to drinking water. Recently, there are communities is increasingly consumed in large cities, some report on the contamination of bottled water. like Shanghai. Compared to tap water, the First, 69 organic compounds were investigated in consumption of bottled and barreled water, is less PET bottled water in 22 countries and plasticizers common but is increasing in China. The re ned (e.g. dimethyl phthalate 0.005-0.125 μg/L) were

69 Chapter 3: Chemstrres research activities

RAW TAP WATER

DIRECTLY DRINKING

ª«H WATER BOILING MACHINE

BOILEDTAP WATER FOR COOKING

©ªH WATER VENDING MACHINE

MAKE TEA OR COFFEE PURIFIED TAP WATER

NATURAL WATER PURIFIED WATER DISTILED WATER MINERALIZED WATER

DIRECTLY DRINKING BOTTLED & BARRELED WATER Figure 3.4.1. Major types of drinking water in Chinese cities . (Photos: Qinghui Huang).

70 Chapter 3: Chemstrres research activities detected from 77% of these bottled water samples Table 3.4.1. Selected identi«ed organic contaminants in drinking [6]. Some other studies also reported estrogenic-like water from Shanghai with high instrumental signals by GCxGC/MS, substances and DNA damage active compounds (e.g. (Huang and coworkers, unpublished data 2016). diethylhexyl phthalate, DEHP) in PET bottled water Compound Names CAS No. [7, 8]. At present, the investigation data on phthalates in bottled and barreled water are very limited. 1. 1,3,5-Triazine-2,4,6(1H,3H,5H)- 827-16-7 trione, 1,3,5-trimethyl- Instead of dimethyl phthalate (DMP) in other countries, dibutyl phthalate (DBP) and DEHP are 2. 1-methylnaphthalene 90-12-0 two of most commonly detected phthalates in 3. 2-methylnaphthalene 91-57-6 Shanghai and some other Chinese cities. Disinfection 4. 9H-Fluoren-9-one 486-25-9 by-products compounds, such as trihalomethanes (THMs) and haloacetic acids (HAAs), could also be 5. Acetophenone 98-86-2 detected at low concentrations in bottled waters [9]. 6. Anthracene 120-12-7 7. Atrazine 1912-24-9 However, there is less knowledge on contaminants in 8. 2,4-Di-tertbutyl-6-nitrophenol 728-40-5 other types of drinking water than tap water. This sub-project will therefore include tap water, boiled 9. Benzaldehyde 100-52-7 tap water, and commercially available water products 10. Benzophenone 119-61-9 (e.g. bottled water, barreled water and station water) 11. Benzothiazole 95-16-9 in the YRD. The main objectives are: 12. Benzyl Benzoate 120-51-4 • to establish a research monitoring framework for human exposure to drinking water 13. Caffeine 58-08-2 • to bank water samples in the Yangtze 14. Diisobutyl phthalate; 84-69-5 Environmental Specimen Bank (ESB) 1,2-Benzenedicarboxylic acid; • to identify and quantify major organic pollutants bis(2-methylpropyl) ester (POPs and related compounds, semi-persistent 15. Dibutyl phthalate 84-74-2 chemicals and endocrine disruptors, in drinking 16. Diethyl Phthalate 84-66-2 water from the YRD area. The research will initially focus on the occurrence of phthalates, 17. Dimethyl phthalate 131-11-3 organotin compounds and organophosphate ame 18. Ethanedione, diphenyl- 134-81-6 retardants. 19. Isophorone 78-59-1 20. Naphthalene 91-20-3 Preliminary results and reasoning Based on a non-targeted analysis on two drinking 21. Phenol 108-95-2 water samples by using a GC×GC-MS, at least 25 22. Biphenol A 80-05-7 organic contaminants were identi ed. The numbers and signals of the compounds identi ed in boiled tap 23. Pyrene 129-00-0 water from Water Boiling Machine in Tongji campus 24. Quinoline 91-22-5 were mostly higher than those in freshly-puri ed tap 25. Tris(2-chloroethyl) phosphate 115-96-8 water (also called Station water) from Water Vending

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Machine in the neighborhood. Most of the identi ed detection frequency of 63% and median compounds with higher signals were the common concentration of 1.1 ng/L. The contamination semi-volatile organic compounds (SVOCs), including pattern of phthalates in different types of water polycyclic aromatic hydrocarbons (PAHs), samples were quite different. phthalates, pesticides and phenols. Based on the non-target screening, Phthalate esters were Organotin compounds in drinking water, were rst dominated by diisobutyl phthalate (DIBP), DBP, reported in Shanghai. Organotins including diethyl phthalate (DEP) and DMP while Tri(2- methyltin and butyltin compounds were detected at chloroethyl) phosphate (TCEP) was found to be a levels of 8 to 36 ng Sn/L in raw tap water, which may major organophosphate ame retardant identi ed in be mainly derived from the release of the organotin drinking water produced by different types of stabilizer in PVC pipes or water storage devices. Less commercial water machines. The compounds organotin (methyltin ≤19.4 ng Sn/L; butyltin: ≤11.4 identi ed are listed in Table 3.4.1. ng Sn/L) were found in most of the boiled tap water samples for inef cient removal of organotin by the A total of 157 drinking water samples including 20 24-h water boiling machines. Freshly puri ed tap raw tap water, 71 puri ed tap water, 28 boiled tap water samples from the 24-h water vending machine water and 38 bottled or barreled water were taken were also contaminated with organotin compounds from Shanghai in 2016-2017. The result showed that (e.g. monomethyltin, dimethyltin and dibutyltin) with 19 of 22 phthalate esters were detected in 97% of the an average of 50 ng Sn/L in samples taken in the drinking water in Shanghai. The detection summer. These levels are higher than in raw tap frequencies of seven phthalate esters (DIBP, DBP, water going into the machine. Biological methylation DEP, DMP, DEHP, DMEP, DNP) were all above and the release of organotin stabilizer may happen in 50%, indicating that these plasticizers are ubiquitous purifying water by 24-h water vending machines. in drinking water in Shanghai. DIBP and DBP exhibited high contamination levels and detection Six different organophosphate ame retardants were frequencies with median concentrations of 21 ng/L investigated in different types of water samples (range from

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Table 3.4.2. Organophosphorus µame retardants concentrations (ng/L) in drinking water and surface water in Shanghai.

TIBP TNBP TCEP TCIPP TDCIPP TPHP Tap water Tongji 7.1 3.3 63 25 1.3 0.17 Pudong 5.1 2.6 57 15 0.67 0.13 Station Water Tongji 1.4 0.8 83 10 0.38 0.37 Pudong

Notes: TIBP, TNBP, TDCIPP and TPHP are close to the LOQ in most cases; there is one major peak appearing in almost all chromatograms, not identi«ed yet.

Authors and sub-project researchers Corresponding author: Assoc. Prof. Qinghui Huang* Åke Bergman, YanlingQiu; Ms. Linlin Song, ([email protected]), Profs. Zhiliang Zhu, Mr. Ziye Zheng, Mr. Yang Lu

References

1. Urbansky ET, Schock MR. Issues in managing the risks 6. Guart A, Calabuig I, Lacorte S, Borrell A. Continental bottled associated with perchlorate in drinking water. Journal of water assessment by stir bar sorptive extraction followed Environmental Management 1999, 56:79-95. by gas chromatography-tandem mass spectrometry 2. Li J, Yu NY, Zhang BB, Jin L, Li MY, Hu MY, Zhang XW, Wei S, Yu (SBSE-GC-MS/MS). Environmental Science and Pollution HX. Occurrence of organophosphate µame retardants in Research 2014, 21:2846-2855. drinking water from China. Water Research 2014, 54:53-61. 7. Biscardi D, Monarca S, De Fusco R, Senatore F, Poli P, Buschini A, 3. Lien NPH, Fujii, S., Tanaka, S., Nozoe, M., Wirojanagud, W., Rossi C, Zani C. Evaluation of the migration of mutagens/ Anton, A., Lindstrom, G. Perµuorinated substances in tap water carcinogens from PET bottles into mineral water by of Japan and several countries and their relationship to surface Tradescantia/micronuclei test, Comet assay on leukocytes and water contamination. Environmental Engineering Research GC/MS. Science of the Total Environment 2003, 302:101-108. 2006, 43:611-618. 8. Pinto B, Reali D. Screening of estrogen-like activity of mineral 4. Mak YL, Taniyasu S, Yeung LWY, Lu GH, Jin L, Yang YL, Lam PKS, water stored in PET bottles. International Journal of Hygiene Kannan K, Yamashita N. Perµuorinated compounds in tap and Environmental Health 2009,212:228-232. water from China and several other countries. Environmental 9. Leivadara SV, Nikolaou AD, Lekkas TD. Determination of organic Science & Technology 2009, 43:4824-4829. compounds in bottled waters. Food Chemistry 2008, 108:277- 5. Quinones O, Snyder SA. Occurrence of perµuoroalkyl 286. carboxylates and sulfonates in drinking water utilities and related waters from the United States. Environmental Science & Technology 2009, 43:9089-9095.

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3.5 Sewage sludge as a mirror of human generated in the YRD, most of which were disposed activities in land ll sites.

Sewage sludge is a by-product produced during the Sewage sludge as a suitable matrix to monitor human treatment of municipal wastewater. Fresh sewage activities sludge is mainly from primary and secondary settling After released from consumer products, organic tanks, in which liquids and solids are separated by contaminants are transported to outdoor sedimentation technologies, and often contains environment via air exchange, or be adsorbed onto 0.25-12% solids by weight [1]. To maximally reduce particulate matters and accumulate in domestic dust its production, sludge is thickened rstly using particles, and along with those in atmospheric technologies like gravity thickening, otation and deposition, they can reach WWTPs via municipal mechanical thickening followed by chemical sewage collection systems, as shown in Figure 3.5.1. conditioning to improve the ef ciencies of dewatering Organic contaminants present in urban wastewater processes, such as belt dewatering, centrifugal are predominantly lipophilic in nature, and during dewatering, and plate-frame dewatering. The sedimentation processes, they will be largely removed moisture content of sewage sludge is often reduced to to sewage sludge with suspended solids. Therefore, lower than 40% before nal disposal in some large various anthropogenic contaminants from human wastewater treatment plants (WWTPs), and activities in municipal environment can be traced in anaerobic digestion is used for sludge stabilization. sewage sludge in levels up to mg/g dry weight (dw) [5].

Sewage sludge contains nutrients such as nitrogen, In recent years, with the development of instrumental phosphorous and organic matter, which makes it analysis technologies, increasing numbers of potentially suitable as a land fertilizer or an organic emerging organic contaminants have been identi ed soil improver. However, contaminants such as heavy and quanti ed in sewage sludge samples worldwide metals and persistent organic pollutants or related [6]. Since indoor air and dust are important sources compounds will jeopardize its use in such a context. for organic contaminants in sewage sludge, their Sewage sludge is known as a sink for harmful heavy occurrence in indoor environment is closely related to metals like cadmium, mercury, lead and arsenic, human activities and use of materials and goods. By potentially pathogenic bacteria and viruses, and measuring pollutant concentrations in sewage sludge, various organic contaminants barely biodegradable, we can acquire valuable information on regional therefore safe disposal of sewage sludge is population exposure status. Simply with air or dust challenging. Currently, common sludge disposal samples collected from individual homes, assessments strategies include sanitary land ll, incineration, and of regional pollution situation of certain organic land application. In the United States and several contaminants are often inconvincible, while in European countries, over half of sewage sludge contrast, sewage sludge can be viewed as an epitome annually generated is applied onto agricultural and of the entire service area of a WWTP. Moreover, other lands [2, 3]. In 2013, the production of levels of organic contaminants in sewage sludge may dewatered sewage sludge reached 6.25 million tons in be used to retrieve historic application information. China, 84% of which was improperly disposed [4]. For example, in the study by Hale, La Guardia [7], More than 2 million tons of dewatered sludge was the concentrations of penta-BDE increased from 1975

74 Chapter 3: Chemstrres research activities to 2000 and then gradually plateaued in archived sewage sludge samples from Chicago. This result is perfectly matched with the application of commercial PentaBDE products in the United States. WASTEWATER TREATMENT PLANT

During disposal processes, organic contaminants in sewage sludge may be re-introduced to the environment. Among several sludge disposal strategies, land application as agricultural fertilizers is commonly recommended, considering its low energy and space cost, as well as the recycling of nutrients. However, during sludge application, organic contaminants will be released from organic fractions of the sludge particles, and further transport into the soil ecosystems, which is leading to contamination of what is grown in the elds. The long-term accumulation effects of organic WASTEWATER contaminants in sludge-amended soils have been observed in several studies [3, 8-10], which raises concerns over potential plant uptake and SEWAGE SLUDGE translocation processes. Besides, organic contaminants in soils introduced by sludge application, may volatilize and re-engage in long- range atmospheric transport. Therefore, sewage sludge should hardly be seen as the nal fate of various organic contaminants, since they are likely to continue to transport to other environmental Hg compartments such as soil, air, and groundwater. The detection of organic contaminants in sewage Pb sludge often suggests their strong recalcitrance to various biological treatments in WWTPs, or long half-lives in the environment. The contaminants are likely to reach threshold levels in the environment and pose threats to human health after years of application. Overall, if sewage sludge is considered as concentrated pollution sources of organic contaminants in a certain region, continuous monitoring of their levels in sewage sludge can Figure 3.5.1. Flow of various contaminants from domestic and provide essential information on their regional industrial environment to sewage sludge in wastewater treatment emission  ux. plants (WWTPs).

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Pollutants analyzed in sewage sludge from Shanghai (mean: 452 ng/g dw; range: 126–809 ng/g dw), DPs In 2010, 28 sewage sludge samples were collected (mean: 18 ng/g dw; range: 0.2–135 ng/g dw), and from Shanghai, and the concentrations of ve groups HBCDDs (mean: 4.7 ng/g dw; range: 0.1–37.2 ng/g of organic contaminants were analyzed, including dw). polybrominated diphenyl ethers (PBDEs), hexabromocyclododecanes (HBCDDs), dechlorane Polybrominated diphenyl ethers (PBDEs): All PBDE plus (DPs), per- and polyuorinated chemicals congeners can be found in sewage sludge from (PFAS), and phthalate esters (PAEs). All targets were Shanghai but with different detection frequencies detected in the sewage sludge, indicating their wide [11]. BDE-28, 33, 47, 66, 99, 183, 203, 206, 207, usage and ubiquity in the studied area. 208, and BDE-209 were detectable in all sludge samples; other congeners can be detected in over The concentrations of ve groups of contaminants 70% of the samples. BDE-209 was the most varied in a large range, as shown in Figure 3.5.2. abundant PBDE congener with a mean contribution Based on dry weight, phthalate esters have the of 85% (range: 35–99%) of the total PBDEs in the highest levels with a mean concentration of 123 µg/g sludge. The levels of BDE-209 in sludge varied dw (range: 23–1,350 µg/g dw), followed by PBDEs largely, from 30 to almost 35000 ng/g dw (mean: (mean: 2.4 µg/g dw; range: 0.03–35 µg/g dw). The 2370 ng/g dw), which are, in a global perspective, the following compounds are reported in another scale, highest concentrations reported in sludge/biosolids, i.e nanogram (ng) instead of microgram (µg) showing so far. The abundance of BDE-209 in sludge from their lower abundance in the sewage sludge: PFAS Shanghai indicate that the commercial product of

7 Outlier 90th percentile 6 75th percentile Mean 5 Median 4 25th percentile 10th percentile 3

2

1 Concentrations (ng/g dw) (ng/g Concentrations 10 0 Log Log Figure 3.5.2. Concentrations (ng/g dry -1 weight) of PBDEs, HBCDDs, DPs, PFAS, and PAEs in sewage sludge from -2 Shanghai [11-14]. PBDEs HBCDs DPs PFCs PAEs

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DecaBDE was commonly used in the studied area, PFOS were in the range of 0.46–6.8. In addition, compared to PentaBDE and OctaBDE. Currently, the PFOA levels in sewage sludge from different European Union and North America, have restricted wastewater treatment plants varied widely, whereas also the usage of DecaBDE, signi cantly, whereas no PFOS levels show a relatively small variation. similar action has been taken in China. Compared to other countries/regions, PFOA levels were generally higher, while PFOS concentrations Hexabromocyclododecane (HBCDDs): HBCDDs were lower, suggesting that PFOA-based chemicals were detected in all sludge samples from Shanghai are heavily applied in the YRD. [12]. The sum of three HBCDD diastereoisomers (∑HBCDDs) varied from 0.10 to 37 ng/g dw with a Phthalate esters (PAEs): The highest concentration of mean concentrations of 4.7 ng/g dw. Two of the phthalates was 1,350,000 ng/g dw, i.e. 1.35 mg/g dw highest ∑HBCDDs were found in sludge from two which was detected in a WWTP near the Shanghai WWTPs which mainly treated wastewater from Chemical Industry Park, one of the largest chemical automobile and motorcycle industries. Of the three industry bases in the world [14]. DEHP and DnBP HBCDD diastereoisomers, γ-HBCDD was the most were two abundant PAEs in the sludge with mean abundant isomer in 17 sludge samples, with a large concentrations of 97 µg/g dw and 22 µg/g dw, variation of ratios ranging from 5.6% to 76% (mean: respectively, placing these contamination levels at the 48%). α-HBCDD dominated in the other 10 sludge high end of data reported on a global range. samples (mean: 48%). Especially for DEHP, its mean concentration was close to the maximum limit that is permitted in Dechlorane Plus (DPs): Currently, very few data of sludge for agricultural application according to DPs are available from sewage sludge analysis. guidelines by the European Union. For other Hence, de la Torre and coworkers [15] reported DPs phthalates, their mean concentrations varied from in Spanish sewage sludge with a mean concentration 0.4 to 1200 ng/g, one to ve orders of magnitude of 32 ng/g dw. By comparison, our data were slightly lower than those of DEHP and DnBP. lower with a mean of 18 ng/g dw. Two isomers of DP, syn- and anti-DP, were detected in all sludge samples Future needs from Shanghai with mean of 12 ng/g dw and 5.7 ng/g As reviewed by Meng, et al. [16], a total of 35 classes dw, respectively. The average fanti (anti-DP/(anti-DP of chemicals consisting of 749 individual compounds + syn-DP)) was 0.69, which is slightly higher than and one mixture have been detected in sewage sludge that in technical DP mixture (fanti = 0.65), samples since 1987, in China. Recently, the number suggesting syn-DP could be slightly more vulnerable of organic contaminants found in sewage sludge has to degradation during wastewater treatment been increasing, as well as the concentrations of some processes. emerging contaminants, which is causing serious concern over the safety disposal of sewage sludge. A Per- and poly uorinated substances (PFAS): Among national sewage sludge survey with well-designed all chemicals in this group, PFOA and PFOS are by sampling strategies is necessary in China. During this far the dominating compounds in sewage sludge from survey, the representativeness of sewage sludge Shanghai, with concentration ranges of 130-810 ng/g samples should be given prioritized consideration, dw and 23-300 ng/g dw [13]. The ratios of PFOA to meaning that not only sewage sludge samples should

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be collected from different regions across China, they 5. Harrison EZ, Oakes SR, Hysell M, Hay A. Organic chemicals in should also be from WWTPs with varied scales and sewage sludges. Science of the Total Environment 2006, treatment technologies. 367:481-497. 6. Clarke BO, Smith SR. Review of ‘emerging’ organic contaminants in biosolids and assessment of international Moreover, among organic contaminants which have research priorities for the agricultural use of biosolids. been detected in sewage sludge, those required to be Environment International 2011, 37:226-247. continuously monitored should be identi ed, based 7. Hale RC, La Guardia MJ, Harvey E, Chen D, Mainor TM, Luellen on comprehensive evaluation criterions, including the DR, Hundal LS. Polybrominated diphenyl ethers in U.S. sewage sludges and biosolids: temporal and geographical trends and occurrence in sewage sludge, persistence in the uptake by corn following land application. Environmental environment, and human exposure potentials. Science & Technology 2012, 46:2055-2063. 8. Sellström U, de Wit CA, Lundgren N, Tysklind M. Effect of Finally, with advanced analysis technologies like sewage-sludge application on concentrations of higher- non-targeted screening strategy using high resolution brominated diphenyl ethers in soils and earthworms. Environmental Science & Technology 2005, 39:9064-9070. mass spectrometry, certain suspected but unknown 9. Wilson S, Alcock RE, Sewart A, Jones KC. Persistence of organic organic contaminants may be identi ed in sewage contaminants in sewage sludge-amended soil: a «eld sludge, which can provide valuable information on experiment. Journal of Environmental Quality 1997, human activities and for risk assessments of sewage 26:1467-1477. sludge in the environment. 10. Wild S, Berrow M, Jones K. The persistence of polynuclear aromatic hydrocarbons (PAHs) in sewage sludge amended agricultural soils. Environmental Pollution 1991, 72:141-157. Authors and sub-project researchers 11. Yang C, Meng XZ, Chen L, Xia SQ. Polybrominated diphenyl Corresponding author: Prof. Xiang-Zhou Meng ethers in sewage sludge from Shanghai, China: Possible ([email protected]) ecological risk applied to agricultural land. Chemosphere 2011, Mr. Nan Xiang and Prof. Åke Bergman 85:418-423. 12. Xiang N, Chen L, Meng XZ, Dai XH. Occurrence of hexabromocyclododecane (HBCD) in sewage sludge from Shanghai: Implications for source and environmental burden. Chemosphere 2015, 118:207-212. 13. Yan H, Zhang CJ, Zhou Q, Chen L, Meng XZ. Short-and long- chain perµuorinated acids in sewage sludge from Shanghai, References China. Chemosphere 2012, 88:1300-1305. 14. Meng XZ, Wang Y, Xiang N, Chen L, Liu ZG, Wu B, Dai X, Zhang 1. Metcalf E. Wastewater engineering—treatment, disposal and YH, Xie ZY, Ebinghaus R. Flow of sewage sludge-borne phthalate reuse (3rd edition). New York: McGraw Hill, 1991. esters (PAEs) from human release to human intake: implication 2. Hale RC, Alaee M, Manchester-Neesvig JB, Stapleton HM, for risk assessment of sludge applied to soil. Science of the Total Ikonomou MG. Polybrominated diphenyl ether µame Environment 2014, 476:242-249. retardants in the North American environment. Environment 15. de la Torre A, Sverko E, Alaee M, Martínez MÁ. Concentrations International 2003, 29:771-779. and sources of Dechlorane Plus in sewage sludge. Chemosphere 3. Eljarrat E, Marsh G, Labandeira A, Barceló D. Effect of sewage 2011, 82:692-697. sludges contaminated with polybrominated diphenyl ethers on 16. Meng XZ, Venkatesan AK, Ni YL, Steele JC, Wu LL, Bignert A, agricultural soils. Chemosphere 2008, 71:1079-1086. Bergman Å, Halden RU. Organic contaminants in Chinese 4. Yang G, Zhang GM, Wang HC. Current state of sludge sewage sludge: a meta-analysis of the literature of the past 30 production, management, treatment and disposal in China. years. Environmental Science & Technology 2016, 50:5454-5466. Water Research 2015, 78:60-73.

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3.6 Assessing persistent and bioaccumulative may be distinguished from contamination of compounds in wildlife from the Yangtze domesticated animals, e.g. sh farming and meat River Delta production that today apply large quantities of chemicals, including antibiotics. With the evolution of human society, the living space for wildlife has been squeezed. Man has exploited the Based on the living habit, wildlife can be classi ed as land for various purposes and are inuencing the aquatic, amphibian and terrestrial species. In an ideal survival of wildlife in various ways. In addition, ecosystem, there are food chains starting from chemicals, products of industrialization, some of primary producers (algae, grass), to primary consumer which are known to cause adverse effect to wildlife, and ending at a variety of predator species. Each level i.e. lead to e.g. reproductive insuf ciency, of a food web stands for a trophic level. With increasing neurotoxicity and feminization of male sh, trophic levels, the energy transfers but reduces by hermaphroditism among snails (UNEP/WHO 2013). 90%, which is termed as the energy pyramid. In The damage of ecosystem may inuence human contrast, some environmental contaminants transfer health in turn. For instance, persistent organic via the food chain and accumulate in the high trophic pollutants (POPs) are bioaccumulated in wildlife and level species with increasing concentrations, i.e. the domesticized animals. This is accordingly a pathway pollutants undergo biomagni cation. for how humans are exposed to POPs. Wildlife is important for environmental exposure Given that the landscape in the YRD is diverse, assessment of pollutants. Compared with abiotic dominated by plains and surrounded by hills; it is matrices, i.e. air, water, soil, they are, if persistent, dotted with many lakes and rivers. The biological integrating the exposure, reecting the pollution level diversity in the YRD is rich. Paddy elds are complex and may display adverse impact of the pollutants. ecosystem, which is functionally between aquatic and Wildlife at different trophic levels may play different terrestrial environment. The present project began roles in terms of monitoring. On one hand, high level with screening persistent and bioaccumulting species have a great potential for screening studies of compounds in a number of wildlife species from POPs and related compounds [1]. On the other hand, paddy eld sites (c.f. below). The research has so far stationary species, e.g. invertebrates, may imply that focused on certain selected prioritized compounds, a certain indicator species integrates the contaminant including some method development for chemical situation in a smaller or greater geographical area. analysis, migration and transformation of pollutants However, as described previously (c.f. Chapter 3.4), in the environment. The present project is further by an appropriate sample design, stationary species highlighted in chapter 4.1. may represent large areas, e.g. as the mussel-watch programs. At a lower trophic level we can expect a Background and aim of project less developed metabolic capacity, hence making Wildlife traditionally refers to those undomesticated these animal more suitable as indicator species for animal species that grow and live in areas without more rapidly metabolized environmental being introduced by humans. However, since the contaminants, such as the combustion byproducts, human activities are ubiquitous, scientists agree that polycyclic aromatic hydrocarbons (PAHs), most of wildlife is affected by humans. Still, wildlife plasticizers and phthalate esters.

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An increasing interest to study environmental The aims of the present project are: exposure of POPs and related compounds in Chinese • to screen for persistent and bioaccumulative wildlife has developed during the past two decades [2, environmental pollutants in wildlife from the 3]. However, this is still a non-dominant research area YRD compared to analysis of abiotic samples (e.g. air and • to determine concentrations and congener pro les soil). The current wildlife studies are so far dominated of persistent and bioaccumulative environmental by studies in the Pearl River Delta and the North part pollutants in the species of China. It may be summarized that the knowledge • to search for, and potentially identify sources of on POPs and related compounds in wildlife in the indicated pollutants YRD is still poor. Even if wildlife studies are mainly • to select species of preference for research focused on aquatic system in the YRD, using mussel monitoring of persistent and bioaccumulative and sh [4, 5], information about such contaminants environmental pollutants in wildlife in terrestrial species are rarely reported. Results and reasoning Paddy elds represent a typical ecosystem in the A scienti c article, by us, about screening for YRD as rice is the staple food for South of China. persistent and bioaccumulative environmental Paddy elds are a mixture of aquatic and terrestrial pollutants in wildlife in a paddy eld and quantifying environments, making the biological diversity selected pollutants was published in 2016 [7]. CPs extensive. The levels of persistent contaminants in have been shown as the major group of contaminants wildlife from paddy eld reect the contamination in several species, especially terrestrial species e.g. situation, and give a rsthand estimation of intake of snakes. Some hitherto non-identi ed contaminants such pollutants via staple food. were detected, but require structural con rmation for unambitious identi cation. The results from this Among the persistent contaminants, one of the subproject and the article are further described and examples, are the short-chained chlorinated paraf ns discussed in Chapter 4.1. (SCCPs). These chemicals are bioaccumulated in wildlife, transported globally in the environment On-going researches focuses on CPs in wildlife, and are toxic to aquatic species at low concentrations including two snake species and yellow weasel. (UNEP 2016; see also Chapter 3.2). At the 2011 Among them, yellow weasel (Mustela sibirica) POPs conference, SCCPs did not manage to be listed showed highest level of SCCPs and MCCPs, followed as a new POP by only one vote ticket. The SCCPs by the two snake species. Compared with other have been restricted in EU since 2008. In China, the studies, our results showed comparable annual production of CPs is reported 2013 to reach concentrations with other data reported from China, such a high volume as one million tons annually [6]. but higher than from other countries [8, 9]. The Due to reasons of production cost, the CPs are not congener pattern of SCCPs and MCCPs were well fractionated in the manufacturing process, analyzed and compared with two commercial resulting in products containing complex product CP-42 and CP-52 (Figure 3.6.1). The nger composition. For instance, the predominant product print pattern showed that CPs in wildlife resemble sold on the market, CP-52, is a mixture of short and CP-52, which accounts for 80% of the domestic medium chained CPs. production. However, the pattern in wildlife slightly

80 Chapter 3: Chemstrres research activities

10% C| 14% CP-42 commercial product CP-52 commercial product Red-backed rat snake 5 8% C|6 C| 12% 8% 7 C|8

10% 6% C|9

6% C|10 8% 4% 6% 4%

4% 2% 2% 2%

0% 0% 0% C17C16C15C14C13C12C11C10 C17C16C15C14C13C12C11C10 C17C16C15C14C13C12C11C10

8% 10% Pond loach Rice eld eel Short-tailed mamushi snake 8% 8% 6% 6% 6% 4% 4% 4%

2% 2% 2%

0% 0% 0% C17C16C15C14C13C12C11C10 C17C16C15C14C13C12C11C10 C17C16C15C14C13C12C11C10

10% 10% 12% Yellow weasel Chinese pond heron Cuckoo 10% 8% 8%

8% 6% 6% 6% 4% 4% 4%

2% 2% 2%

0% 0% 0% C17C16C15C14C13C12C11C10 C17C16C15C14C13C12C11C10 C17C16C15C14C13C12C11C10

Figure 3.6.1. Chlorinated paraffins in two commercial products, CP-42 and CP-52, upper left and in the middle column, respectively. The CP patterns as determined in seven wildlife species are shown as well: upper right: red-backed rat snake (Elaphe rufodorsata); middle row left: pond loach (Misgurnus anguillicaudatus); middle: rice «eld eel (Monopterus albus); right: short-tailed mamushi snake (Gloydius brevicaudus); bottom row left: yellow weasel (Mustela sibirica); middle: Chinese pond heron (Ardeola bacchus); and right: cuckoo (Cuculus canorus). CP concentrations have not yet been determined in the species indicated in the study.

81 Chapter 3: Chemstrres research activities

shifts towards lower homologous group (C12-C14), Authors and sub-project researchers indicating a higher bioaccumulation potency of these Corresponding author: Dr. Yihui Zhou*(capitalzyh@ CP congeners. yahoo.com) Profs. Yanling Qiu, Åke Bergman, Anders Bignert; Considering the mass disturbance in analysis, a Assoc. Prof. Lillemor Asplund, Dr. Ge Yin, Mr. pre-separation method is tested to separate CPs from Xinyu Du and Mr. Ioannis Athanassiadis other chlorinated persistent organic pollutants. Samples were applied to the deactivated silica column References (3% water). Analytes were eluted with solvents with an increasing polarity gradient. Non-polar 1. Bignert A, Eriksson U, Nyberg E, Miller A, Danielsson S. contaminants such as PCBs are eluted in the rst Consequences of using pooled versus individual samples for designing environmental monitoring sampling strategies. fraction. CPs are eluted in the second fraction Chemosphere 2014, 94:177-182. together with polybrominated diphenyl ethers 2. Ma J, Qiu XH, Zhang JL, Duan XL, Zhu T. State of polybrominated (PBDEs) and hexachlorocyclohexanes (HCHs). In the diphenyl ethers in China: An overview. Chemosphere 2012, next step, we plan to further improve the method for 88:769-778. clean-up and separation of CPs from other slightly 3. Zheng GJ, Leung AOW, Jiao LP, Wong MH. Polychlorinated dibenzo-p-dioxins and dibenzofurans pollution in China: polar compounds. Sources, environmental levels and potential human health impacts. Environment International 2008, 34:1050-1061. 4. Yin G, Asplund LM, Qiu YL, Zhou YH, Wang H, Yao ZL, Jiang JB, Bergman A. Chlorinated and brominated organic pollutants in shell«sh from the Yellow Sea and East China Sea. Environmental Science and Pollution Research 2015, 22:1713-1722. 5. Zhou YH, Chen QF, Du XY, Yin G, Qiu YL, Ye L, Zhu ZL, Zhao JF. Occurrence and trophic magni«cation of polybrominated diphenyl ethers (PBDEs) and their methoxylated derivatives in freshwater «sh from Dianshan Lake, Shanghai, China. Environmental Pollution 2016, 219:932-938. 6. International Chlorinated Alkanes Industry Association (ICAIA), Newsletter No. 3, 2014. Available from: http://www.eurochlor. org/media/88258/20140908_icaia_newsletter_03_«nal.pdf. 7. Zhou YH, Asplund L, Yin G, Athanassiadis I, Wideqvist U, Bignert A, Qiu YL, Zhu ZL, Zhao JF, Bergman A. Extensive organohalogen contamination in wildlife from a site in the Yangtze River Delta. Science of the Total Environment 2016, 554:320-328. 8. Strid A, Bruhn C, Sverko E, Svavarsson J, Tomy G, Bergman A. Brominated and chlorinated µame retardants in liver of Greenland shark (Somniosus microcephalus). Chemosphere 2013, 91:222-228. 9. Bayen S, Obbard JP, Thomas GO. Chlorinated paraffins: A review of analysis and environmental occurrence. Environment International 2006, 32:915-929.

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3.7 Heron eggs and environmental quality in The monitoring of bird eggs is giving information the Yangtze River Delta region relevant for environmental risk assessments but may likewise be important for assessment of human risk. Bird egg is a valuable matrix for biomonitoring of Differences between among- and within-clutch environmental quality. Persistent and toxic substances variation and also sampling without considering the are potentially accumulated and magni ed along the egg laying sequence from species that lay several eggs food chain. In exposed birds, eggs can be expected to may cause bias when sampling bird eggs, but in contain elevated levels of these substances. general we nd bird egg relatively homogenous Consequently, screening for these contaminants in compared to other sample matrices. Also migrating bird eggs is a tool for detection and identi cation of birds may cause a problem as to what region novel contaminants, determination of contaminant measured contaminant concentrations represent. concentrations and trends over time and to show Hence migrating species should therefore generally be geographical differences between contaminated and avoided in monitoring program. The eggs size relative non-contaminant areas. It can also give information to the parent female size varies considerably among relevant for environmental and human risk species. This can also effect the variation in measured assessments. The present subproject under Chemstrres concentrations and their suitability as a sample focuses on screening of emerging contaminants in bird matrix has to be evaluated for each new bird species eggs within the Yangtze River Delta (YRD) area. candidate. Standardizing the collection and preservation of eggs can further reduce unnecessary Background and aim of project variation [12]. If sampling is carried out in a Eggs of various bird species are proved ef cient consistent way there are reasons to expect lower indicators for temporal trend monitoring and random variation in the measured concentrations screening of Persistent Organic Pollutants (POPs) and compared to e.g. sh [13]. Based on the eld related contaminants in North American and investigation and statistical analysis, guillemot European countries as well as in China [1-6]. Fish egg from Baltic Sea was considered to be a good consuming birds are assumed to show elevated bioindicator for a number of persistent and toxic concentration of biomagnifying compounds like, contaminants [9]. Therefore, sampling strategy is DDT including its transformation products (DDE important to develop a long-term biomonitoring and DDD), PCBs and PBDEs, HCB and HCH program with bird eggs. isomers, organic phosphate ame retardants (PFRs) among others. These organic pollutants may have too Recently, the population of some sh consuming low concentration to be detected in samples at lower birds including black-crowned night heron trophic levels, can be identi ed and quantitated in (Nycticorax nycticorax) and little egret (Egretta bird eggs [7-9]. Some endocrine disrupting garzetta) has increased considerably during breeding compounds like the DDT metabolite, DDE, in birds season in the Yangtze River Delta because there are will interfere with their calcium phosphorus ample and reliable sources of food for birds in the metabolism, which is the cause of eggshell thinning "land of sh and rice" of China. They will and hatching failure [10]. It has shown that the bird accumulate the contaminants from the feeding area of prey populations declined continuously until DDT through their food web and also release the was banned [11]. contaminants by excretion to the breeding area. The

83 Chapter 3: Chemstrres research activities

Figure 3.7.2. A representative black-crowned night heron colony in metasequoia woods in Chongming Islands (Photo: Qinghui Huang).

Figure 3.7.1. Heron eggs in its nest in Chongming Island, in the YRD. Figure 3.7.3. Sampling sites for heron eggs monitoring in the (Photo: Qinghui Huang). Yangtze River Delta.

84 Chapter 3: Chemstrres research activities eggs of black-crowned night heron (Figure 3.7.1), Preliminary results which is a medium-sized heron found throughout a Field work has been conducted in Tianmu Lake, large part of the world and one of the common Taihu Lake, Dianshan Lake and Chongming Island summer resident and migrant birds in the Yangtze (Figure 3.7.3) from 2014 to 2016. Thirty night heron River Delta, is a candidate as a bioindicator for eggs and 24 small white heron eggs were collected environmental contamination. together with 50 eggs of other birds (e.g. whiskered tern, Chlidonias hybrida) from the nests and the The aims of the present study are to focus on heron grass in the woodlands. Unfortunately, we could not egg contamination of persistent, bioaccumulative and obtain black-crowned night heron eggs at each site toxic substances from the YRD. The speci c aims are: every year. • to identify suitable species for long term monitoring of chemical contaminants and to Screening work has been done for some contaminants collect material for the environmental specimen of concern in heron eggs. We have analyzed some bank. One suggested species is the black-crowned legacy POPs such as organiochlorine pesticides night heron. The night heron is abundant and (OCPs), PCDD/Fs, PCBs and PBDEs as well as some fairly wide spread in the YRD area emerging contaminants including chlorinated • to assess trends and status of known chemicals as paraf ns (CPs), polychlorinated diphenyl ethers well as novel emerging environmental (PCDEs), and hydroxylated PCDEs. The relevant contaminants in bird eggs data are reported in the chapter 4.1. Here only the • to identify suitable sample sites for a long-term preliminary results on organic PFRs assessed in biomonitoring program with bird eggs. heron eggs, are shown.

Table 3.7.1. The contamination of organophosphate µame retardants in bird eggs (ng/g ww) as reported from a few sites around the globe. The table is summarizing literature data with references given in the table.

Samples Great-black-backed Herring gull egg Guillemot egg Glaucous gull egg Gull egg, European Shag egg Sites Great Lakes basin Svalbard Svalbard TCEP < 0.33 – 6.1 N.D. -- < 13.6 < 0.06–0.07 1.1 TCPP < 6.7

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With the phase-out and regulation of PBDEs, organic References PFRs have been increasingly used in different applications, such as ame retardants and 1. Chen D, Mai BX, Song J, Sun QH, Luo Y, Luo XJ, Zeng EY, Hale RC. plasticizers. Some of these contaminants have been Polybrominated diphenyl ethers in birds of prey from Northern China. Environmental Science & Technology 2007, 41:1828-1833. detected in various bird eggs from North America 2. Crosse JD, Shore RF, Wadsworth RA, Jones KC, Pereira MG. and Europe according to a few articles in the Long-term trends in PBDEs in sparrowhawk (Accipiter nisus) scienti c literature as shown in Table 3.7.1. eggs indicate sustained contamination of UK terrestrial According to Table 3.7.1, tris(2-chloroethyl) ecosystems. Environmental Science & Technology 2012, phosphate (TCEP), tris(2-chloroisopropyl) phosphate 46:13504-13511. 3. Gauthier LT, Hebert CE, Weseloh DVC, Letcher RJ. Dramatic isomers (TCPP), and tris(2-butoxyethyl)phosphate changes in the temporal trends of polybrominated diphenyl (TBOEP) were the most abundant PFRs in bird eggs, ethers (PBDEs) in herring gull eggs from the Laurentian Great but also some other PFRs were found. Lakes: 1982-2006. Environmental Science & Technology 2008, 42:1524-1530. We have attempted different extraction and cleanup 4. Rudel H, Muller J, Jurling H, Bartel-Steinbach M, Koschorreck J. Survey of patterns, levels, and trends of perµuorinated methods for the PFR analysis in chicken eggs by EI compounds in aquatic organisms and bird eggs from and SIM mode of GC-MS. The method detection representative German ecosystems. Environmental Science and limits for most of PFRs in the egg matrix ranged Pollution Research 2011, 18:1457-1470. from 0.9 to 14 ng/g ww, which were close to the 5. Verreault J, Berger U, Gabrielsen GW. Trends of perµuorinated reported detection limits in references, except for alkyl substances in herring gull eggs from two coastal colonies in northern Norway: 1983-2003. Environmental Science & TBOEP that was above 200 ng/g ww. We found Technology 2007, 41:6671-6677. signals of tris(isobutyl)phosphate (TIBP), TCPP, 6. Vorkamp K, Thomsen M, Falk K, Leslie H, Moller S, Sorensen PB. tris(1,3-dichloroisopropyl)-phosphate (TDCIPP), Temporal development of brominated µame retardants in tris(2-ethylhexyl)phosphate (TEHP) and tri-n-butyl peregrine falcon (Falco peregrinus) eggs from South Greenland phosphate (TNBP), which were identi ed and (1986-2003). Environmental Science & Technology 2005, 39:8199-8206. quanti ed in heron eggs collected from Chongming 7. Chen D, Letcher RJ, Chu SG. Determination of non-halogenated, Island in 2016. However, TBOEP and TCPs were chlorinated and brominated organophosphate µame below the limit of quanti cation in these eggs. We retardants in herring gull eggs based on liquid also identi ed two common phthalate esters (DBP chromatography-tandem quadrupole mass spectrometry. and DEP) and one bisphenol (BPA) in the heron eggs. Journal of Chromatography A 2012, 1220:169-174. 8. Dittmann T, Becker PH, Bakker J, Bignert A, Nyberg E, Pereira The optimization of analytical methods for PFRs in MG, Pijanowska U, Shore RF, Stienen E, Toft GO, Marencic H. bird eggs is still ongoing, and it will be applied to Large-scale spatial pollution patterns around the North Sea more heron egg samples soon. indicated by coastal bird eggs within an EcoQO programme. Environmental Science and Pollution Research 2012, 19:4060- Authors and sub-project researchers 4072. 9. Jorundsdottir H, Bignert A, Svavarsson J, Nygard T, Weihe P, Corresponding author: Assoc. Prof. Qinghui Huang* Bergman A. Assessment of emerging and traditional ([email protected]) halogenated contaminants in guillemot (Uria aalge) egg from Prof. Anders Bignert, Assoc. Prof. Lillemor Asplund, North-Western Europe and the Baltic Sea. Science of the Total Drs. Kathryn Stewart, Yihui Zhou, Ge Yin and Mr. Environment 2009, 407:4174-4183. Ioannis Athanassiadis.

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10. Bignert A, Helander BO. Monitoring of contaminants and their effects on the common guillemot and the white-tailed sea eagle. Journal of Ornithology 2015, 156:S173-S185. 11. Grier JW. Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 1982, 218:1232-1235. 12. Klein R, Bartel-Steinbach M, Koschorreck J, Paulus M, Tarricone K, Teubner D, Wagner G, Weimann T, Veith M. Standardization of Egg Collection from Aquatic Birds for Biomonitoring – A Critical Review. Environmental Science & Technology 2012, 46:5273-5284. 13. Miller A, Nyberg E, Danielsson S, Faxneld S, Haglund P, Bignert A. Comparing temporal trends of organochlorines in guillemot eggs and Baltic herring: Advantages and disadvantage for selecting sentinel species for environmental monitoring. Marine Environmental Research 2014, 100:38-47. 14. Leonards P SE, van der Veen I, Berg V, Ove Bustnes J, van Leeuwen S. Screening of organophosphorus µame retardants 2010. SPFO-report 1091/2011. Available from: http://www. miljodirektoratet.no/old/klif/publikasjoner/2786/ta2786.pdf. 15. Chu SG, Letcher RJ. Determination of organophosphate µame retardants and plasticizers in lipid-rich matrices using dispersive solid-phase extraction as a sample cleanup step and ultra-high performance liquid chromatography with atmospheric pressure chemical ionization mass spectrometry. Analytica Chimica Acta 2015, 885:183-190. 16. Greaves AK, Letcher RJ, Chen D, McGoldrick DJ, Gauthier LT, Backus SM. Retrospective analysis of organophosphate µame retardants in herring gull eggs and relation to the aquatic food web in the Laurentian Great Lakes of North America. Environmental Research 2016, 150:255-263. 17. Hallanger IG, Sagerup K, Evenset A, Kovacs KM, Leonards P, Fuglei E, Routti H, Aars J, Strom H, Lydersen C, Gabrielsen GW. Organophosphorous µame retardants in biota from Svalbard, Norway. Marine Pollution Bulletin 2015, 101:442-447.

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3.8 Mothers’ milk monitoring in the Yangtze higher relative lipid content (3-5%) [2] promoting the River Delta monitoring effort of lipid soluble bioaccumulative compounds. Chemicals binding to proteins, as for Mothers’ milk is a valuable matrix for environmental example many of fully uorinated or polyuorinated monitoring of heavy metals and all stable and chemicals, require rsthand measurements in serum bioaccumulating organic chemicals, i.e. persistent or plasma. In the present project, mothers’ milk is organic pollutants (POPs) and alike. Accordingly, used for screening of persistent and bioaccumulative chemical analysis of these contaminants in mothers’ organic contaminants. milk is a tool for assessing risks for nursing children. It is also a tool for detection and identi cation of Since our offspring is highly vulnerable to exposure novel contaminants, determination of contaminant to anthropogenic chemicals, we want to protect the concentrations and trends over time and space. growing fetus and child from exposure to hazardous Hence WHO is running a mothers’ milk monitoring chemicals. It is important that women of childbearing program since 1976 and in 2005 WHO published an ages are protected from exposure. Still, it is valid international protocol for monitoring of mothers’ with recommendations to men, to limit exposures to milk [1]. Sweden started monitoring mothers’ milk in environmental pollutants. It is beyond doubt that the late 1960’s, while China began in 2007 their alcohol, tobacco smoke and drugs inuence the national biomonitoring of mothers’ milk. health of the growing fetus and accordingly recommendations are given to the pregnant women The present project, as part of Chemstrres, is focused to minimize the exposure to such hazardous on screening chemical pollutants in mothers’ milk substances. The same goes for exposure to in the Yangtze River Delta (YRD) and also to anthropogenic chemicals present in fatty food (e.g. investigate differences in contaminant concentrations lipid rich sh and chicken or wildlife eggs) and food and pro les in mothers’ milk from Sweden and that may contain elevated levels of heavy metals. China. While women may lower some of the contaminants Background and aim of project more rapidly than others, like mercury, most of the Human biomonitoring of general populations are contaminant levels are built up over a long time commonly carried out by analysis of blood, urine, through bioaccumulation. It is important to prevent hair or mothers’ milk. Urine, readily accessible, is females to be exposed to these chemicals in general used for chemicals with short half-lives, i.e. the to minimize both trans-placental transfer and exposure is indirectly measured by analysis of thereafter transfer of the persistent and metabolites of the parent compound in the urine. bioaccumulative compounds via the mothers’ milk. It Hair, also readily accessible, is the common matrix is well-known that fetal exposures may lead to for analysis of heavy metals, but may be used also for adverse health outcome. This is discussed in some organic pollutants. Blood plasma or serum is a detail in the UNEP/WHO report from 2013 [3], but convenient matrix for analysis of both heavy metals also elsewhere. While exposure of some chemicals in and persistent and bioaccumulative chemicals of men may lead to infertility or reduced fertility other anthropogenic origin. While the average lipid content chemicals seem to inuence the sex ratio as reported in blood is on average 0.7%, mothers’ milk holds a for the most toxic dioxin, 2,3,7,8-TCDD.

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800 1 000

600

400 500

200 HCHs (ng/g l.w.) HCHs (ng/g DDTs (ng/g l.w.) (ng/g DDTs 0 SwedenNingxiaHeilongjiangGuanxiShangxiSichuanLiaoningHebeiHenanFujianTianjinJiangxiShandongShanghaiZhejiangBeijingHubei 0 SwedenShangxiGuanxiJiangxiSichuanNingxiaFujianHeilongjiangHebeiTianjinZhejiangHenanLiaoningShanghaiHubeiBeijingShandongHongkong

60 80

50 60 40

30 40

20 20 10 CB-153 (ng/g l.w.) CB-153 (ng/g 0 l.w.) HCB (ng/g NingxiaShangxiSichuanHenanHeilongjiangJiangxiGuanxiHubeiShandongHebeiFujianLiaoningZhejiangBeijingShanghaiSweden 0 SwedenShandongJiangxiGuanxiHongkongSichuanFujianShanghaiNingxiaShangxiHebeiHeilongjiangHenanTianjinLiaoningHubeiBeijing

2

1

Figure 3.8.1. Concentrations of sum of DDTs, hexachlorocyclohexanes (HCHs), the PCB exposure marker, CB-153, BDE-47 (ng/g l.w.) BDE-47 (ng/g 0 HeilongjiangHenanNingxiaSichuanHebeiZhejiangBeijingHubeiJiangxiFujianLiaoningShangxiTianjinJiangsuGuanxiShanghaiTaiwanSwedenHongkongGuangdongShandong and further, hexachlorobenzene (HCB) and the brominated µame retardant exposure marker, BDE-47, from various provinces in China compared to mean concentrations found in mothers' milk in Sweden, ordered from low to high.

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Accordingly chemical analysis of mothers’ milk is an In China, mothers’ milk data have recently been important way for monitoring the contamination reported on chlorinated paraf ns (CPs) [6], levels among fertile women. Information from contributing with data to a hitherto very limited mothers’ milk trend studies may also be extrapolated global dataset. These data are discussed further to the general human population in the studied areas. below. Several of the POPs were regulated in many countries already in the 1970’s, e.g. DDT and PCBs Exposures to the POPs included in the Stockholm due to their dramatic effects on wildlife reproduction Convention [4] via mothers’ milk was recently (c.f. Chapter 3.6). The levels of these organochlorine reviewed [5] indicating extensive data on a smaller pesticides and PCBs have all declined signi cantly selection of the POPs and few data on others (e.g. since the restrictions were implemented. The short chained chlorinated paraf ns (SCCPs) and concentrations in the Swedish mothers’ milk follow Chlordecone). Temporal trend data are scarce for all the same trend as the levels in bird of prey and the POPs investigated in the review. However, it is marine mammals [5, 7-9]. Diagrams of declining clear that there is knowledge gathered on mothers’ concentrations of DDT, PCB (represented by CB-153) milk contaminant concentrations in many countries and HCB in Swedish mothers’ milk are shown in around the globe. Data on concentrations of some of Figure 3.8.2. the POPs reported in Chinese and Swedish mothers’ milk are presented in Figure 3.8.1., respectively [6].

DDT CB-153 HCB 800 400 200

700 350

600 300 150

500 250

400 200 100

300 150

200 100 50

100 50

0 0 0 70 75 80 85 90 95 00 05 10 70 75 80 85 90 95 00 05 10 70 75 80 85 90 95 00 05 10 Figure 3.8.2. Temporal trend concentrations (ng/g fat) trends of DDT, CB-153 and HCB (1972-2010) in mothers’ milk from Stockholm, Sweden.

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Table 3.8.1. Primary halogenated compounds identi«ed in Chinese and Swedish mothers’ milk samples.

Sweden Shaoxing, China Jiaxing, China Shanghai, China 2004 2010 2015-2016 2015-2016 Chlorinated HCB ++ ++ ++ ++ β-HCH ++ ++ ++ ++ DDE + ++ ++ ++ DDT + ++ ++ ++ DDD + + Oxychlordane + + Cis-/trans-heptachlorepoxide + + Cis-chlordane + + CB-101 + + CB-138 ++ ++ + + CB-153 ++ ++ + + CB-180 ++ + + CB-194 + Metoxychlor + Mirex + + + SCCPs + ++ ++ MCCPs + ++ ++

Brominated BDE-28 + + + + BDE-47 + + + + BDE-99 + BDE-100 + BDE-153 + + + + BDE-154 + HBCDD + + +

++ high + medium/low

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Shanghai and Jiaxing, 2015

Shaoxing 2010

Figure 3.8.3. presents the homologous pattern of CPs among diff erent sites in China. Milk from Shanghai and Jiaxing contains CPs with

lower carbon lengths e.g. C10, C11 whereas samples from Shaoxing is dominated by C14. More research work is on-going.

Rather high concentrations of dioxins were observed The present study focus on mothers’ milk contamination in Swedish mothers’ milk in the early 1970’s but over of persistent and bioaccumulative compounds among time, the levels have decreased signi cantly [5]. The women from the YRD with the following objectives: dioxin toxic equivalent concentrations have declined • to establish a research monitoring procedure for approx. one order of magnitude up to 2012 in the sampling mothers’ milk for the Yangtze Swedish milk. There is doubtless a link between the Environmental Specimen Bank management of the chemicals, through regulations • to identify and quantify major persistent and and reducing the emissions, that have led to reduced bioaccumulative compounds in mothers’ milk concentrations in both wildlife and mothers’ milk [5, from the YRD area, with an initial focus on the 10-11]. Hence nursing children are nowadays occurrence of chlorinated paraf ns exposed to lower levels of these POPs than a few • to evaluate differences in contaminant patterns decades ago. and concentrations in human milk from China and Sweden

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Preliminary results and reasoning References Several samples have been collected from Shanghai and Jiaxing recently and stored in the Yangtze ESB. 1. WHO. Fourth WHO-Coordinated Survey of Human Milk for Samples from Shaoxing were collected in 2010. For Persistent Organic Pollutants – A Protocol for Collection, Handling and Analysis of Samples at the Country Level. Geneva, comparison purpose, mothers’ milk from Sweden in Switzerland. 2005. 2004 was analyzed in the pilot study. 2. Jensen RG. The lipids in human milk. Progress in Lipid Research 1996, 35:53-92. Table 3.8.1 shows the preliminary results of 3. UNEP/WHO. State of the science of endocrine disrupting persistent contaminants in human milk samples from chemicals – 2012. Edited by Bergman Å, Heindel JJ, Jobling S, Kidd KA, Zoeller RT. 2013. four sites. The Swedish milk contains higher level of 4. UNEP. Overview of Stockholm Convention. Available from: PCBs and PBDEs than observed in Chinese milk. On http://chm.pops.int/TheConvention/Overview/tabid/3351/. the contrary, CPs, DDTs and Mirex (a pesticide) Accessed April 16th, 2017. show higher concentrations in the Chinese milk than 5. Fang J, Nyberg E, Winnberg U, Bignert A, Bergman A. Spatial those in the Swedish milk. This might re ect the and temporal trends of the Stockholm Convention POPs in mothers’ milk – a global review. Environmental Science and different pollution prerequisites for Sweden and Pollution Research 2015, 22:8989-9041. China. Sweden is one of the developed countries in 6. Xia D, Gao LR, Zheng MH, Li JG, Zhang L, Wu YN, Tian QC, Huang the world where chemical products such as PCBs and HT, Qiao L. Human exposure to short- and medium-chain PBDEs were widely used and consumed which may chlorinated paraffi ns via mothers' milk in Chinese urban explain higher pollution levels of these chemicals, population. Environmental Science & Technology 2017, 51:608-615. compared with samples from China. In contrast, 7. Bignert A, Helander BO. Monitoring of contaminants and their China is the biggest developing country in the world eff ects on the common guillemot and the white-tailed sea with a huge industrial production of chemicals, eagle. Journal of Ornithology 2015, 156:S173-S185. materials and goods, are handling large production 8. Helander B, Bignert A, Asplund L. Using raptors as volumes of emerging chemicals, e.g. CPs. Further, environmental sentinels: Monitoring the white-tailed sea eagle Haliaeetus albicilla in Sweden. Ambio 2008, 37:425-431. YRD is also one of the most important agriculture 9. Helander B, Olsson A, Bignert A, Asplund L, Litzen K. The role of area in China and contaminated with various DDE, PCB, coplanar PCB and eggshell parameters for pesticides. reproduction in the white-tailed sea eagle (Haliaeetus albicilla) in Sweden. Ambio 2002, 31:386-403. Authors and sub-project researchers 10. Miller A, Hedman JE, Nyberg E, Haglund P, Cousins IT, Wiberg K, Bignert A. Temporal trends in dioxins (polychlorinated Corresponding authors: Prof. Jianfu Zhao dibenzo-p-dioxin and dibenzofurans) and dioxin-like ([email protected] ) and Elisabeth Nyberg polychlorinated biphenyls in Baltic herring (Clupea harengus). ([email protected]) Marine Pollution Bulletin 2013, 73:220-230. Profs. Åke Bergman, Anders Bignert, Yanling Qiu, 11. Miller A, Nyberg E, Danielsson S, Faxneld S, Haglund P, Bignert Zhiliang Zhu; Drs. Yihui Zhou, Qianfen Xiao; Ms. A. Comparing temporal trends of organochlorines in guillemot eggs and Baltic herring: Advantages and disadvantage for Yajie Sun selecting sentinel species for environmental monitoring. Marine Environmental Research 2014, 100:38-47.

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3.9 Establishment of optimal ®sh species for monitoring, revealed that exposure of pollutants and research monitoring in the Yangtze River effects on the morphological, hematological, Delta biochemical and oxidative stress, and histopathological biomarkers were linearly correlated, Various wild living organisms are used in chemical and that the biomarkers response could be linked to and biological monitoring around the world. Among the detected metal bioaccumulation [3]. the most employed ones, sh earn attention due to its role in the aquatic food-web and direct connection Accordingly, the application of sh in both chemical and with human beings. The former reason makes shes biological monitoring is considered in various countries. advantageous for studies of bioconcentrations, For example, a novel German guideline, VDI 4230, Part -accumulation and -magni cation of pollutants along 4, has adopted a standardized protocol for the sampling the life-cycle and trophic levels. The latter one makes of freshwater sh for passive biomonitoring with sh as them feasible to show potential adverse effects on accumulation indicators [4]. China is also making such human health based on sometimes similar efforts. For example, sh are widely employed to metabolism among vertebrates, but also differences monitor POPs including PCBs, polybrominated diphenyl must be considered as they do occur. The present ethers (PBDEs), organochlorine pesticides (OCPs), project under Chemstrres is focused on establishment decabromodiphenyl ethane (DBDPE) and chlorinated of an optimal sh species for research monitoring in paraf ns (CPs) in the YRD [5]. the Yangtze River Delta (YRD). The aims of the present study in the YRD are: Background and aim of project • Establishment of optimal sh species for chemical Fish can be found virtually everywhere in the aquatic monitoring environment and they play a major ecological role in • Establishment of optimal biomarkers for aquatic food-webs because of their function as carrier biomonitoring of energy from lower to higher trophic levels. • Facilitate temporal trend data report for both Moreover, sh is an important food source for chemical and biological monitoring humans. Due to close connections with both the environment and human consumption, some sh Preliminary results and reasoning species are quite well studied organisms in evaluating Dr. Yihui Zhou and Mr. Xinyu Du from Tongji the chemical exposure and environmental burden of University collected more than 700 individual sh pollutants. specimens (ten different species) since 2013 in Taihu Lake and in Dianshan Lake in the YRD. The On the one hand of chemical monitoring, sh bile was sampling was done in cooperation with local used to monitor endocrine disrupting compounds shermen to ensure the sh were wild and not (EDCs), and results indicated a relationship between farmed. The chemical analyses done so far indicate the EDC concentration in the water samples with the that various target chemicals were found in common number of intersex sh [1]. Fish liver was employed to carp (Cyprinus carpio), yellow cat sh (Pelteobagrus monitor heavy metals, and the results demonstrated fulvidraco) and snakehead (Ophiocephalus argus signi cant correlations with metal concentrations in Cantor). These sh species may be suitable species to sediments [2]. On the other hand, biological use for research monitoring purposes.

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FISH IN AERATED TISSUE SNAP-FREEZE IN HOMOGENIZED ORIGINAL WATER SEPARATION LIQUID NITROGEN AND ALIQUOTED

Figure 3.9.1. Transport and preparation of «sh samples. The «shes were transported in aerated local water to the laboratories, where different tissues were separately collected, snap-freezed in liquid nitrogen and stored at -80°C. The «sh tissues were homogenized and aliquoted before assayed for different biomarkers. (Photo: Shuang Liang).

For biomonitoring purposes, we focused on the -magni cation. Also, yellow cat sh has no scales and yellow cat sh in eld studies. The yellow cat sh was therefore directly contacts with pollutants in the chosen due to their relative long lifespan and high water besides their gills and food uptake. Moreover, level in the food-web, which make them one model sh are used as human food, making them applicable organism for bioconcentration, -accumulation and to indicate direct exposure and health risk for

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humans. In addition, the selected sh species are wild genotoxicity. Antioxidant indicators, including in the YRD, and hence feasible to indicate superoxide dismutase (SOD) and catalase (CAT), and environmental health status. also oxidative damage indicator, malondialdehyde (MDA) were measured to indicate antioxidant In our preliminary studies, the cat sh was sampled by responses. Glutathione S-transferase (GST) was local sherman in Xukou Bay, Gonghu Bay, Meiliang measured to indicate phase II detoxi cation. Also, Bay, and east, south and west parts of the Taihu Lake, PAHs metabolites in the biles were measured to and also in Yangtze River. As demonstrated in Figure indicate PAHs exposures. 3.9.1, the sh were transported back to the laboratories in aerated local water. Then, different AChE was signi cantly inhibited in sh from the tissues were separately collected, snap-freezed in liquid sampling site 7 (S7) where there were farmlands nitrogen and then stored at -80°C. Before assayed, the polluted by pesticides and heavy metals. Moreover, sh tissues were homogenized and aliquoted. the differences of AChE among sampling sites were related to the pesticide concentrations in the Acetylcholine esterase (AChE) is identi ed as a sediments from earlier studies [6]. When the pesticide biomarker, the changes of which may lead to concentrations increased, the AChE showed a clear behavioral effects. It was chosen to indicate potential decreasing trend (Figure 3.9.2). neurotoxicity. Comet assay was chosen to indicate

20

1.01

0.672 0.761 10

AChE (nmo1/min mg) (nmo1/min AChE 0.354 0.375 Pesticeides in sediments (ng/g) in sediments Pesticeides

0 S7S6S5S4S3S2S1

Figure 3.9.2. Negative correlation between acetylcholine esterase (column with left y-axis) and pesticide concentration (poly-line with right y-axis). In S2 to S7, the «sh AChE showed increasing inhibition with increased pesticide concentration in the sediments (data from Liu and coworkers [6].).

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The antioxidant responses, superoxide dismutase caused oxidative damages when the antioxidant (SOD) and catalase (CAT) showed similar results responses were not strong enough to ght against the among samples, and they generally showed an reactive oxygen species (ROS). Notably, the oxidative reversed response to malondialdehyde (MDA) (Figure damages (indicated by MDA) were generally greater 3.7.3). Such results indicated that pollutants at the at S2 to S4 (Figure 3.7.3) than at other sites. sampling sites provoked antioxidant responses, and

300 2.0 1.8 250 30 1.6 200 1.4 1.2 20 150 1.0 0.8 100 10 0.6 50 0.4 0.2

SOD (U/mgprot) CAT (U/mgprot) CAT 0 0 (nmol/mgprot) MDA 0.0 S9S8S7S6S5S4S3S2S1 S9S8S7S6S5S4S3S2S1 S9S8S7S6S5S4S3S2S1

Figure 3.9.3. Antioxidant response changes with sampling sites. The changes of superoxide dismutase (SOD) and catalase (CAT) in «sh over sampling sites were generally reversed to those of malondialdehyde (MDA) (red lines), indicating their roles in antioxidant responses and oxidative stress.

S9 > S6 > S8 > S2 > S5 > S7 > S1 > S3 > S4 S1 > S9 > S2 > S8 > S7 > S6 > S5 > S4 > S2 S1 > S3 > S9 > S8 > S7 > S5 > S4 > S6 > S2 10 3.0

20 2.5

2.0 5 1.5 10 1.0

0.5

FF341:383 FF380:430 FF290:335 0 0 0.0 S9S8S7S6S5S4S3S2S1 S9S8S7S6S5S4S3S2S1 S9S8S7S6S5S4S3S2S1

Figure 3.9.4.PAHs metabolites among different sampling sites. FF 290:335 reµects naphthalene derived type of metabolites, FF 341:383 reµects benzo[a]pyrene type of metabolites and FF 380:430 reµects pyrene derived type of metabolites.

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In analyzing the PAHs metabolites in sh bile, xed Authors and sub-project researchers wavelength uorescence (FF) was chosen to reect Corresponding author: Prof. Daqiang Yin* (yindq@ biliary PAHs metabolites levels. Results showed that tongji.edu.cn) the sh samples from various sampling sites had Dr. Zhenyang Yu and Dr. Yihui Zhou different levels of PAHs metabolites (Figure 3.7.4). Notably, S2 and S4 showed generally lower levels than other sites, which was different from the earlier References ndings that S2 to S4 suffered from more oxidative stress (Figure 3.7.3). Such conicts should be 1. Ros O, Izaguirre JK, Olivares M, Bizarro C, Ortiz-Zarrogoitia M, Cajaraville MP, Etxebarria N, Prieto A, Vallejo A. Determination considered in future studies. of endocrine disrupting compounds and their metabolites in «sh bile. Science of the Total Environment 2015, 536:261-267. No signi cant results were observed in the comet 2. Rahmanpour S, Ashtiyani SM, Ghorghani NF. Biomonitoring of assays, which showed that the toxic pollutants did heavy metals using bottom «sh and crab as bioindicator likely not exhibit genotoxicity at their current species, the Arvand River. Toxicology and Industrial Health 2016, 32:1208-1214. concentration levels. The contents of GST ranged 3. Saleh YS, Marie MA. Use of Arius thalassinus «sh in a pollution from 59 - 137.5 U/mg•protein in the samples without biomonitoring study, applying combined oxidative stress, particular patterns among sampling sites, indicating hematology, biochemical and histopathological biomarkers: that phase II detoxi cation was not signi cantly A baseline «eld study. Marine Pollution Bulletin 2016, different among samples. 106:308-322. 4. Klein R, Gercken J, Löffler H, von der Trenck T, Braunbeck T. A novel German guideline for the sampling procedures for In conclusion, the preliminary studies have passive biomonitoring with «sh as accumulation indicators: demonstrated the feasibility to test biomarkers from VDI 4230, Part 4. Environmental Sciences Europe 2016, 28:15. wild yellow cat sh, and also showed good 5. Chen QF, Zhou YH, Qiu YL, Zhu ZL, Zhao JF. Research progress of agreements between AChE and pesticide analysis «sh as bioindicators for halogenated persistent organic pollutants. Environmental Science & Technology (China) 2016, results. Such conclusion promotes further utilization 2016:99-110 (In Chinese). of yellow cat sh in the biomonitoring in the YRD. 6. Liu NN, Chen P, Zhu SZ, Zhu LY. Distribution characteristics of Yet, an improved design should be considered in PAHs and OCPs in sediments of Liaohe River and Taihu Lake and future studies to better understand the mechanisms their risk evaluation based on sediment quality criteria. China underlying the observed effects on the biomarkers. Environmental Science 2011, 31:293-300.

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3.10 Chemical pollutants in dust after ignition. Organic ame retardants have been It is obvious that people are exposed to airborne used in polymer-based materials and consumer particulate matter with adsorbed contaminants both products for more than 50 years. In the 1970’s, the from outdoors and indoors. Globally, people are additive organic ame retardant, polybrominated spending an increasing amount of time in many diphenyl ethers (PBDEs), became widely used in different indoor surroundings which are often household and of ce products. Due to their proved referred to as microenvironments such as homes, persistent organic pollutant (POP) characteristics, the work places, public buildings, vehicles etc. commercial products, PentaBDE and OctaBDEs were Contaminants in the indoor environment are banned within the European Union from 2004. primarily from additives in materials, goods and DecaBDE use have been restricted within EU and chemical products used indoor and mobilized. North America and DecaBDE is currently on the Similarly pollutants may come in via the ventilation candidate list under the Stockholm Convention. systems and/or heat exchangers. Selected pollutants Hexabromobiphenyl (HBB) and in WHO Guidelines for Indoor Air Quality (2010) hexabromocyclododecane (HBCDD) are listed for are benzene, carbon monoxide, formaldehyde, elimination under the convention Annex A (http:// naphthalene, nitrogen dioxide, polycyclic aromatic chm.pops.int/). Consequently, organophosphorus hydrocarbons (especially benzo[a]pyrene), ame retardants (PFRs), as one group of chemicals to trichloroethylene, tetrachloroethylene and radon. be applied for substitution of the brominated ame Besides these contaminants, a recent study reported retardants, have increased in production and use that 485 individual chemicals to appear in indoor around the globe. dust [1]. Among these contaminants, ame retardants and plasticizers were listed. These emerging Studies have shown that levels of organophosphates persistent and toxic organic contaminants also have in indoor environment are generally higher than in indoor sources and are often detected in various outdoor environments, and concentrations and indoor environments in concentrations of concern. patterns varies a lot in oor dust from different The present project focuses on phosphorous countries and home environment [5]. A report containing ame retardants and plasticizers in the estimated the daily intake of organophosphates via dust from home environment in the Yangtze River drinking water consumption was 20 times lower than Delta (YRD). Comparisons are made to Swedish that calculated for dust ingestion [6]. Besides, homes as part of another ongoing project applying different pro les of organophosphates found in cats as mirrors of human, especially small children’s human hair and in various food samples supported exposure to indoor pollutants (http://www.aces.su.se/ that the diet was probably not the major source of misse/about-misse). Relevant reports from the intake for these compounds for humans [7]. “MiSSE” project have been published by a group of Therefore, indoor dust ingestion and inhalation are scientists at Stockholm University ([2-4]). possibly the major routes of exposure for humans to these phosphorus-containing compounds. This is Background and aim of project reasonable considering their wide use as additives in Flame retardants are chemicals added to materials to materials and goods in indoor environments. prevent combustion and to delay the spread of re

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Several organophosphate manufacturers are located highest concentrations of the phthalate esters. in the YRD, and two of them are reported to be the Di(2-ethylhexyl) phthalate (DEHP) and di(2- leading enterprises among the manufacturers [8]. propylheptyl) phthalate (DPHP) were quanti ed in Shanghai is characterized by its large population 100% of the samples. density (ca. 25 million inhabitants), high industrialization, active residential decoration, and As the concern rouse regarding endocrine properties no ban on application of organophosphates at of plasticizes, phthalate esters, the European present. Therefore, it is of signi cance to investigate Commission has gradually banned several of the the characteristics of these compounds in dust from phthalates, especially in products easily in contact home environment and to estimate the exposure risk with small children. Listed phthalates in Annex XIV through dust ingestion for Shanghai residents. of REACH are DEHP, benzyl butyl phthalate (BBP) and dibutyl phthalate (DBP) (Regulation (EU) No Among organophosphate compounds, tris(2- 143/2011). DPHP has substituted the use of DEHP chloroethyl) phosphate (TCEP), tris(2-chloroisopropyl) but concentrations of DEHP (mean 243 mikrogram/g phosphate (TCIPP) and tris(2-butoxyethyl) phosphate dust) was still 10 times higher than for the other (TBOEP) have been suspected to be carcinogenic [9, phthalates in the Swedish dust. 10], and triphenyl phosphate (TPP) has been shown to alter hormone levels and decrease the sperm Concentrations of DEHP were determined in indoor concentration [11]. dust from China and was twice as high (557 mikrogram/g dust) compared to the Swedish dust, The aims of the present study are: DBP levels were four times higher (100 mikrogram/g • to report concentrations and compositional pro les of organophosphates in dust from home environment in the Shanghai and Sweden; 1 0000 000 • to investigate seasonal variance in exposures to

organophosphates over the year; 100 000 • to explore main sources of organophosphates in

the home environments 10 000 • to explore human health risks in association with

dust ingestion for Shanghai residents. 1 000

Results and reasoning 100 MiSSE project have been investigating dust content for numerous pollutants in Swedish homes, i.e. 10 brominated and organophosphorus FR, chlorinated persistent organic pollutants, phenolic compounds, dust ng/g 1 DEHP DPHP TCIPP TDCIPP TBOEP BDE-47 BDE-99 BDE-209 DBDPE phthalates and per-and polyuorinated alkyl substances (PFAS). A summary diagram (Figure Figure 3.10.1. Average concentration (ng/g dust, error bars max/ min) of phthalate esters (DEHP and DPHP), PFRs (TCIPP, TDCIPP and 3.10.1) of the phthalates, phosphorus containing TBOEP) and BFRs (BDE-47, BDE-99, BDE209 and DBDPE) analyzed in ame retardants (PFRs) and BFRs in dust indicate Swedish household dust (n=17).

100 Chapter 3: Chemstrres research activities dust) while BBP concentrations were 1/10th of that PFRs are not banned in China except certain found (0,8 mikrogram/g dust) in Sweden [12]. chemicals prohibited or of concern in two or three industries, for example tris(2,3-dibromopropyl) Nine PFRs were quanti ed in the dust samples, of phosphate (TDBPP) prohibited in ecological textiles, which TBOEP and TCIPP dominated the pro le in and TDBPP, TCEP, TPP and trimethyl phosphate the majority of the individual samples (Figure 3.10.2) (TMP) are of concern in the automobile industry. [13]. This pro le is in accordance with dust samples Therefore, PFRs pro les in dust from Chinese homes from other parts of Europe [14]. TBOEP is used in are different compared to Swedish dust. Until now, oor polishes and as a plasticizer in rubber and only a handful of studies concerning PFRs in dust plastics (WHO 2000) whereas TCIPP is used in rigid from Chinese homes have appeared. TCEP (median and exible polyurethane foams used for example in 3.8 mikrogram/g dust) is dominated in dust from furniture upholstery (WHO 1998). The PFR pro le eleven Guangzhou urban homes, and median in dust from Chinese homes are reported to be concentrations of all other eleven PFRs in the dust dominated by the chlorinated PFRs, TCEP and samples are below 1 μg/g dust, for example TCIPP TCIPP [12]. (median 0.75 mikrogram/g dust), TBOEP (median

ng/g dust 35 000 TEHP

DPEHP

30 000 TPP TBOEP

25 000 TDCIPP TCIPP

TCEP 20 000 TBP

TiBP 15 000

10 000

5 000

0 Home 1 Home 2 Home 3 Home 4 Home 5 Home 6 Home 6 Home 7 Home 8 Home 9 Home 10 Home 11 Home 12 Home 13 Home 14 Home 15 Home 16 Home 17

Figure 3.10.2. Individual PFR concentration (ng/g dust) pro«les in dust from Swedish households (n=17) [13].

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0.32 mikrogram/g dust) and TDCIPP (median 0.13 References mikrogram/g dust) [15]. Similar results are also found in dust samples from six homes in Nanjing, 1. Zhang J, Kamstra JH, Ghorbbanzadeh M, Weiss JM, Hamers T, with median concentrations of TCEP, TCIPP, TPhP Andersson PL. In silico approach to identify potential thyroid hormone disruptors among currently known dust and TDCIPP 2.1 mikrogram/g dust, 0.7 mikrogram/g contaminants and their metabolites. Environmental Science & dust, 0.6 mikrogram/g dust, and 0.1 mikrogram/g Technology 2015, 49:10099-10107. dust, respectively [16]. 2. Norrgran J, Jones B, Lindquist NG, Bergman A. Decabromobiphenyl, polybrominated diphenyl ethers, and In our study, dust samples from twenty ve homes in brominated phenolic compounds in serum of cats diagnosed with the endocrine disease feline hyperthyroidism. Archives of Shanghai were collected and PFRs mean Environmental Contamination and Toxicology 2012, 63:161-168. concentrations determined. The concentrations are at 3. Norrgran J, Jones B, Bignert A, Athanassiadis I, Bergman A. the same levels as previously reported from Higher PBDE serum concentrations may be associated with Guangzhou and Nanjing. Composition pro les is feline hyperthyroidism in Swedish cats. Environmental Science also similar, showing that TCEP and TCIPP are most & Technology 2015, 49:5107-5114. 4. Norrgran Engdahl J, Bignert A, Jones B, Athanassiadis I, abundant, followed by TBOEP, TPP, TDCIPP, and Bergman A, Weiss JM. Cats' internal exposure to selected tricresyl phosphate (TCrP), tri(n-butyl) phosphate brominated µame retardants and organochlorines correlated to (TnBP) and tripropyl phosphate (TPrP) are in low house dust and cat food. Environmental Science & Technology proportions. 2017, 51:3012-3020. 5. Van den Eede N, Dirtu AC, Neels H, Covaci A. Analytical developments and preliminary assessment of human exposure The BFRs are a magnitude lower in concentration to organophosphate µame retardants from indoor dust. and the pro le is dominated by DecaBDE. Environment International 2011, 37:454-461. Decabromodiphenylethane (DBDPE) is substituting 6. Lee S, Jeong W, Kannan K, Moon HB. Occurrence and exposure the DecaBDE (BDE-209) and both are found at assessment of organophosphate µame retardants (OPFRs) similar levels in household dust. All these compounds through the consumption of drinking water in Korea. Water Research 2016, 103:182-188. were quanti ed in 100% of the samples (17 families) 7. Zhang X, Zou W, Mu L, Chen Y, Ren C, Hu X, Zhou Q. Rice in the Stockholm area. ingestion is a major pathway for human exposure to organophosphate µame retardants (OPFRs) in China. Journal of Authors and sub-project researchers Hazardous Materials 2016, 318:686-693. Corresponding author: Prof. Yanling Qiu* (ylqiu@ 8. Ou Y. Developments of organic phosphorus µame retardant industry in China. Chemical Industry and Engineering Progress tongji.edu.cn) 2011, 30:210-215 (In Chinese). Prof. Åke Bergman, Dr. Jana Weiss and Ms. Li Li 9. WHO. International Programme on Chemical Safety, Environmental Health Criteria 209, Flame Retardants: Tris(chloropropyl) Phosphate and Tris(2-chloroethyl) Phosphate. Geneva, Switzerland. 1998. 10. WHO. International Programme on Chemical Safety, Environmental Health Criteria 218, Flame Retardants: Tris(2-butoxyethyl) Phosphate, Tris(2-ethylhexyl) Phosphate and Tetrakis(hydroxymethyl) Phosphonium Salts. Geneva, Switzerland. 2000.

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11. Meeker JD, Stapleton HM. House dust concentrations of organophosphate µame retardants in relation to hormone levels and semen quality parameters. Environmental Health Perspectives 2010, 118:318-323. 12. He R, Li Y, Xiang P, Li C, Zhou C, Zhang S, Cui X, Ma LQ. Organophosphorus µame retardants and phthalate esters in indoor dust from different microenvironments: Bioaccessibility and risk assessment. Chemosphere 2016, 150:528-535. 13. Dahlberg AK, Weiss JM. Organophosphorus µame retardants in Swedish house dust. Organohalogen Compounds 2016, 78:1174-1177. 14. Van den Eede N, Dirtu AC, Ali N, Neels H, Covaci A. Multi- residue method for the determination of brominated and organophosphate µame retardants in indoor dust. Talanta 2012, 89:293-300. 15. He CT, Zheng J, Qiao L, Chen SJ, Yang JZ, Yuan JG, Yang ZY, Mai BX. Occurrence of organophosphorus µame retardants in indoor dust in multiple microenvironments of southern China and implications for human exposure. Chemosphere 2015, 133:47-52. 16. He RW, Li YZ, Xiang P, Li C, Zhou CY, Zhang SJ, Cui XY, Ma LQ. Organophosphorus µame retardants and phthalate esters in indoor dust from different microenvironments: Bioaccessibility and risk assessment. Chemosphere 2016, 150:528-535.

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Highlights of two research projects within Chemstrres Chapter 4: Highlights of two research projects within Chemstrres

4.1 POPs in wildlife from the Yangtze River Delta

Introduction Once the POPs are released into the environment, these hydrophobic chemicals tend to adsorb on A cluster of chemicals are de ned as Persistent particulate matter and distribute to lipophilic Organic Pollutants (POPs) according to the compartments in biota. Hence adipose tissue and Stockholm Convention, but the characteristics lipid rich tissues are main targets for their stretches beyond these legacy POPs to also include accumulation in wildlife as well as in humans. POPs other anthropogenic chemicals with similar do biomagnify through the food webs resulting in properties. They are highly stable chemicals under sometimes very high concentration in animals of environmental conditions, they can undergo long prey. These chemicals are hazardous to humans and range transport, bioaccumulate and are toxic [1]. The a risk due to exposure via food, inhalation/ingestion, Stockholm Convention is in place for protection of skin contact and occasionally via water. POPs are humans and wildlife from exposure to POPs. It has ubiquitous. been signed and rati ed by over 180 parties since 2001. Originally, twelve classes of organochlorine The present highlights refer to chemical analysis of chemical were listed as POPs and at the time termed POPs and related compounds in several common “the dirty dozen”. POPs are classi ed in three species in the YRD (see Figure 4.1.1). Based on the categories: organochlorine pesticides, industrial living habits, rice eld eel (Monopterus albus, RFE), chemicals and byproducts from human activities, dark-spotted frog (Pelophylax nigromaculatus, DSF) respectively. With the expanding knowledge on other and chinese pond-heron (Ardeola bacchus, CPH) are chemicals with POP characteristics, the number of considered as aquatic species whereas Asiatic toad pollutants under the Stockholm Convention has (Bufo gargarizans, AT), short-tailed mamushi snake increased to 26, by now [1]. (Gloydius brevicaudus, STM) and peregrine falcon

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Figure 4.1.1. Wildlife species sampled for chemical analysis of pollutants in the Yangtze River Delta at the sampling sites indicated in the map.

(Falco peregrinus, PF) are regarded as terrestrial contamination of CPs in several of the wildlife species. Due to the biomagni cation pattern of POPs, species assessed. For example, concentration of up to we have speci cally focused on high trophic level 340 µg/g fat was found in the snake as reported by species such as snake, pound-heron and falcon. In Zhou and coworkers, 2016 [2]. addition, we also analyzed eggs of black-crowned night-heron (Nycticorax nycticorax) and whiskered CPs are used in metal cutting  uids, as plasticizers tern (Chlidonia hybrid) collected from Tianmu Lake and  ame retardants with China as the by far main and East Taihu Lake in the YRD. The most producer of CPs in the world. The annual production interesting results ordered by pollutants are described of CPs has increased from 0.15 million tons in 2003 below. The full reports of these studies have been to one million tons in 2013 [5]. CPs consists of very published in the scienti c literature [2-4]. complex mixtures of alkanes with numerous chlorine atoms bound to them. The length of the carbon chain Chlorinated paraf ns (CPs): From this work, the de ne the three CP categories: short chain CPs with most important nding is the observation of severe 10-13 carbons (SCCPs); medium chain CPs with

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Paddy «eld used for sampling of wildlife in the YRD.

14-17 carbons in the chain (MCCPs) and long chain Results from our own studies show apparent content CPs that consists of carbon chain lengths of more of CPs in the YRD wildlife [2]. The CPs are than 18 carbon atoms (LCCPs). The CPs are also highlighted in Figure 4.1.2. Except for dark spotted de ned by different degrees of chlorine in the products, frog, CPs were detected in all of the other species. i.e. from 40% up to 70%. The concentration of CPs varies from 0.8 µg/g fat in Chinese-pond heron to 340 µg/g fat in the snake SCCPs are known to cause acute toxicity to fresh (STM). These contamination concentrations are water and marine mollusks [6]. Zeng and coworkers comparable to levels reported in invertebrates (4.8-54 studied SCCPs in an aquatic food chain and observed µg/g fat) and sh (9.7-33 µg/g fat) in Liaodong Bay, the compounds to undergo biomagni cation [7]. The China [8]. The concentrations reported as part of the properties of SCCPs have led to the proposal of Chemstrres project are far higher than other studies including them among the POPs in the Stockholm from the globe as a whole. It is interestingly to Convention. observe that CP concentrations in terrestrial species, as we have de ned them, are much higher than the

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Figure 4.1.2. Chromatograms of persistent pollutants isolated from: (a) Chinese pond-heron; (b) peregrine falcon; (c) short-tailed mamushi snake; (d) rice « eld eel; (e) asiatic toad and (f) dark-spotted frog. The obvious occurrences of CPs are pointed out with “square boxes” in the chromatograms b, c and e.

108 Chapter 4: Highlights of two research projects within Chemstrres levels in the aquatic related species. It is still unclear In 2014, ten eggs of night heron and whiskered how to explain this phenomenon but it is in line with tern were sampled and analyzed for persistent previous observations. It is clear that the terrestrial contaminants. High levels of dioxins were observed, species we have analyzed are relevant for monitoring dominated by the fully chlorinated dibenzo-p-dioxin, of CPs in the environment. octachlorodioxin (OCDD) [4]. Still the toxicity was dominated by the occurrence of the most toxic Dioxins and related compounds: The common name dioxins, i.e. 1,2,3,7,8-PeCDD and 2,3,7,8-TCDD. “dioxins” is used to describe a number of different The calculated mean (with range) toxic equivalents chemicals, including polychlorinated dibenzo-p-dioxins (TEQs) of dioxins were 300 (90-1500) and 520 (PCDDs), dibenzofurans (PCDFs) and dioxin-like (220-1100) pg TEQ/g fat in night heron and polychlorinated biphenyls (PCBs). The toxicity of whiskered tern, respectively. The TEQ levels in our dioxins depends on the chlorine substitution pasttern study are comparable to the previous study in and number. In general, 2,3,7,8-substituted dioxins, peregrine falcon (Falco peregrinus) eggs from including 7 PCDDs and 10 PCDFs are the most toxic Germany [10] and thick-billed murre (Uria lomvia) dioxins. Some of the dioxins are showing very high from Canada [11]. However, such levels are higher toxicity on several end-points [9]. than bird eggs previously reported from Dongting

1000 1000

100 100

10.0

10.0 1.00 sPCDD-TEQ lg(10) pg/g l.w. lg(10) pg/g sPCDD-TEQ l.w. lg(10) pg/g sPCDF-TEQ .100 Ch_NP_2004Ch_AM_2004Ch_M_2004Ch_GE_2004Jp_BT_1998Ca_IG_2004Ca_TM_1994Gr_WS_2000Ge_PF_2002Ca_NF_1984Ca_BK_1993Ch_NH_2014Ch_WT_2014Sw_WS_1996Fi_BG_1985 1.00 Ch_M_2004Ch_NP_2004Ch_AM_2004Ch_GE_2004Jp_BT_1998Ca_IG_2004Ch_WT_2014Ge_PF_2002Ch_NH_2014Ca_NH_2014Gr_WS_2000Fi_BG_1985Ca_NF_1984Ca_BK_1993Sw_WS_1996

Figure 4.1.3. Logarithm TEQ level of PCDD (left) and PCDF (right) in bird eggs from the literatures. The year of sampling is indicated on the x-axis. Light blue bars refer to data from China (Ch) and blue bars from other counties/regions (i.e. Jp: Japan; Ca: Canada; Ge: Germany; Gr: Greenland; Fi: Finland and Sw: Sweden). The species analyzed include from China: mallard (2004), nothern pintail (2004), azure-winged magpie (2004), great egret (2004), whiskered tern (2014), night heron (2014) and from Japan: black-tailed gills (1998); from Canada: ivory gulls (2004), black-legged kittiwakes (1993), northern fulmars (1975-1994), thick-billed murre (1975-1994); from Germany: peregrine falcons (2000-2003), from Greenland and Sweden: white-tailed sea eagle (2000 and 1992-2001, respectively) and from Finland: black guillemot (1985). Further data on the samples analyzed and the relevant full references for the data applied to prepare the diagrams are available from Table 1 in [4].

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Lake in China [12], where pentachlorophenol (PCP) Dioxins sources are e.g. forest res, volcanic eruptions, is the suspected main source [4]. The diagrams in chlorine bleaching of pulp, waste incineration, vehicle Figure 4.1.3 are visualizing in summary, data on exhaust emission and production of chemicals (e.g. TEQ concentrations of PCDDs and PCDFs, chlorinated phenols). Such diverse sources make the respectively, from the globe as presented in the full source interpretation complicated. However, the scienti c report from us on this matter [4]. difference between sources may generate different patterns of dioxins. For instance, the Importantly, wild bird eggs are commonly consumed pentachlorophenol source, as part of this study, is by people in the YRD. Compared to hen and duck predominated by OCDD and heptaCDD whereas eggs, it is likely that environmental pollutants are the waste incineration source is dominated by PCDFs bioaccumulated to higher concentrations in eggs [15]. Based on such pattern differences, multivariate from wild birds unless contaminated feed is used for analysis by principal component analysis is the domesticized birds. Dioxin exposures via food commonly applied [16]. Result from principal are regulated within European Union and therefore component analysis is shown in Figure 4.1.4 and it we performed risk assessment on human dietary is implied that the dioxins in the bird eggs is mainly intake. The results showed that TEQs of PCDD/Fs from the two bird species are at median TEQ levels of 300 and 520 pg TEQ/g, respectively. This is two orders of magnitude higher than EU limit in hen eggs (2.5 pg TEQ/g) [13].

In addition, we have estimated number of eggs for consumption by children and adults based on the tolerable weekly intake of PCDD/Fs suggested by the Scienti c Committee on Food, with the results recently published elsewhere [14]. Based on our assessment children must be careful with eating wild bird eggs regularly if the data presented here are valid throughout a larger span of wild bird eggs, due to the safety of the children. However, bird eggs are traditionally considered to containing more nutrients and to be healthy and accordingly Chinese families are more likely to give them to their children/ Figure 4.1.4. Biplot of principal component analysis to identify the PCDD/Fs sources in eggs of night heron (NH) and whiskered tern grandchildren and to pregnant women. This (WT). The data of speci«c sources were summarized by Yin [17] underscores the importance for additional exposure and include: (1) Household use of coal burning (CB); (2) data for dioxins in bird eggs, including dioxin Pentachlorophenol (PCP); (3) Sodium pentachlorophenol (Na-PCP); concentrations in common chicken and duck eggs. (4) Gaseous emission from secondary Al metallurgy (GE(Al)); (5) The latter is of particular importance since these Gaseous emission from secondary Cu metallurgy (GE(Cu)); (6) Gaseous emission from iron ore sintering plant (IOS) (GE(Fe)); (7) are the eggs consumed on a daily basis year around. Waste water from pulp mill (WPM); (8) Agricultural straw open burning (SOB); Gaseous emission from cement plant (CP).

110 Chapter 4: Highlights of two research projects within Chemstrres related to pentachlorophenol production, bioaccumulate in birds of prey. The high transportation and/or use. However, several sources concentrations of DDE has been linked to eggshell may have similar patterns, which can confound thinning in birds of prey, a serious effect that caused prediction of sources [17]. severe declines in several predator bird species in both Europe and North America. DDT is a POP Interestingly, hydroxylated nonachlorinated diphenyl according to the Stockholm Convention and still ethers (OH-nonaCDEs), i.e. dimerization products of commonly the major POP in environmental, wildlife pentachlorophenol, and the precursor of OCDD, and human samples. were identi ed and quanti ed in the bird egg samples [4]. Mean concentrations of ∑OH-nonaCDEs (sum of Concentrations of DDTs were much higher than any three OH-nonaCDE congeners) were 15 and 98 ng/g of the other organochlorine pesticides in our study fat in eggs of night heron and whiskered tern, of wildlife from the YRD (Figure 4.1.1) with respectively. Further, OH-nonaCDE are methylated concentrations in this group of wildlife presented in to form MeO-nonaCDE [18] and we have been able Table 4.1.1. Our results are comparable or much to identify and quantitate three MeO-nonaCDEs lower than those from Xiamen and Wuxi, China with 2’-MeO-CDE-206 as the main congener. [21, 22]. The results con rm that the DDTs are still Assessing OH-PCDEs may be applied for indicating present at high levels in China, also when compared potential dioxin contamination in wildlife or the to the global contamination situation. The DDT environment in general. contamination in China has been suggested to have been inuenced by production of the organochlorine In addition, also polychlorinated diphenyl ethers pesticide, dicofol [23]. Another potential source of (PCDEs) were detected in the eggs from the two bird DDT released to the Chinese environment is its use species in the study with mean concentrations of 64 as an anti-fouling agents for boats [24]. and 160 ng/g fat for night heron and whiskered tern, respectively. Decachlorinated diphenyl ether (CDE- Contamination levels of an additional number of 209) and the nonachlorinated diphenyl ether, CDE- organochlorine pesticides, a hexachlorocyclohexane 206, are the most abundant PCDEs in both species. isomer (β-HCH), Mirex and hexachlorobenzene The PCDE pattern is different in these eggs compared (HCB) are presented in Table 4.1.1. the pattern reported some Baltic Sea species [15, 19]. The difference is linked to different polychlorophenol Industrial POPs: polychlorinated biphenyls (PCBs) sources in the YRD and Baltic Sea areas. and polybrominated diphenyl ethers (PBDEs)are two classes of industrial chemicals used with the intention DDT and its related chemicals: DDT, with the full to be useful chemicals for mankind in a number of name of dichlorodiphenyltrichloroethane, is one of applications, the PCBs as a chemical product in e.g. the most well-known and most extensively researched transformers, capacitors and as a heat exchanger, and chlorinated pesticides. It was rst time synthesized in the PBDEs as ame retardants in e.g. electric and 1874 [20] and widely used during the Second World electronic devices. Neither the PCBs nor the PBDEs War to protect soldier from vector transferred were intentionally produced to reach and diseases. DDT and its particularly persistent contaminate our environment. Still, both these metabolite, DDE, were identi ed and found to classes of industrial chemicals are abundant and

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Table 4.1.1. Concentrations organochlorine pesticides (HCH, DDTs, Mirex, HCB), polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) (ng/g fat) in muscle of wildlife from the Yangtze River Delta, China. The species are: Chinese pond heron (Ardeola bacchus, CPH), peregrine falcon (Falco peregrinus, PF), short-tailed mamushi snake (Gloydius brevicaudus, STM), Asiatic toad (Bufo gargarizans, AT), dark-spotted frog (Pelophylax nigromaculatus, DSF), rice «eld eel (Monopterus albus, RFE), black crowned night heron (Nycticorax nycticorax, NH) and whiskered tern (Chlidonias hybrid, WT). Data from [2, 3]

CPH PF STM AT DSF RFE NH WT n 3 a 3 a 3 a 1b (8) c 1 b (5) c 1 b (5) c 10 a 10 a median range median range median range median range median range β-HCH 3.4 0.53-93 7.3 5.7-48 91 53-270 69 160 29 190 150-850 56 30-270 4,4'-DDT 28 25-130 8.1 4.7-14 31 27-55 68 29 37 6.1 1.8-110 2.7 2.0-90 4,4'-DDD 6.8 6.3-79 5.8 2.8-11 7.0 3.8-11 15 8.5 140 24 2.4-150 3.3 1.3-11 4,4'-DDE 1600 390- 180 130- 330 210-430 590 23 760 460 280-650 290 240-480 17000 1200 Mirex 120 29-420 35 21-77 20 9.4-32 12 0.35 3.4 49 17-340 28 9.3-160 HCB 0.09 0.02-3.2 0.19 0.08-3.0 3.4 0.90-9.0 9.9 1.1 0.05 170 94-380 120 93-160

CB-118 47 11-280 25 9.9-32 7.1 3.0-18 5.7 0.75 2.9 43 20-180 25 9.9-230 CB-138 190 38-790 71 36-120 15 4.9-29 8.4 1.4 6.1 43 17-150 28 14-220 CB-153 80 31-480 63 36-83 18 7.6-36 15 1.9 7.8 74 39-280 59 32-330 CB-180 71 20-340 32 24-60 4.2 1.7-12 6.1 0.71 2.1 29 7.7-110 9.2 4.2-190 CB-202 48 13-230 21 13-27 4.6 2.7-13 4.1 0.38 2.7 1.0 0.38-2.2 0.36 n.d.-4.7 CB-206 6.8 4.4-26 6.1 5.4-7.2 0.69 n.d.-2.7 1.2 nd nd 3.7 1.9-11 1.1 0.68-5.6 CB-209 6.4 4.2-26 4.8 4.1-9.7 1.1 0.99-5.2 2.2 0.64 0.59 5.6 3.5-16 3.8 1.3-15

BDE-47 0.77 0.57-2.1 1.7 1.1-4.7 0.12 0.12-0.28 0.38 0.22 1.9 3.9 1.2-15 11 6.8-2.6 BDE-99 0.99 0.80-1.0 2.5 2.4-5.2 0.32 0.30-0.44 0.44 0.29 1.28 1.7 0.65-19 5.0 2.1-200 BDE-154 10 5.3-40 2.1 2.0-2.8 1.8 0.47-2.4 1.9 0.10 2.1 10 6.7-47 3.9 2.3-21 BDE-153 16 6.1-60 5.9 5.8-7.9 2.9 1.5-4.6 2.3 0.20 1.2 6.7 4.6-41 2.3 0.58-29 BDE-209 0.83 0.48-1.0 0.64 0.25-1.7 4.0 2.5-12 6.3 5.1 5.0 a Individual sample; b Pool sample; c Number of individual sample in one pool.

globally distributed pollutants with implications for PCB and PBDE occurrence and congener patterns in wildlife and humans. The PCBs belong to the POPs wildlife from YRD are presented in detail elsewhere rst included in the Stockholm Convention, while a [2, 3] but concentrations are shown also herein for a subset of the PBDEs, referred to as PentaBDE and number of marker compounds (Table 4.1.1). For OctaBDE, were listed as POPs in 2009. DecaBDE is example, the tern has median concentration of CB-153 registered as a POP candidate under Stockholm and BDE-47 of 59 and 11 ng/g fat, respectively. It is Convention [25]. much lower than Caspian tern from San Francisco Bay, U.S.A [26] and even slightly lower than Arctic

112 Chapter 4: Highlights of two research projects within Chemstrres tern from Iceland [27, 28]. This might indicate the References contamination of industrial POPs in YRD, in general, is in the medium or low range compared to 1. UNEP. Overview of Stockholm Convention. Available from: the contamination elsewhere in the world. However a http://chm.pops.int/TheConvention/Overview/tabid/3351/. Accessed April 16th, 2017. novel pattern of PCBs, with high numbers of chlorine 2. Zhou YH, Asplund L, Yin G, Athanassiadis I, Wideqvist U, Bignert substituents, were identi ed in falcon from the paddy A, Qiu YL, Zhu ZL, Zhao JF, Bergman A. Extensive organohalogen eld [3]. This observation is remarkable and indicate contamination in wildlife from a site in the Yangtze River Delta. the occurrence of still unknown sources of PCBs in Science of the Total Environment 2016, 554:320-328. China. 3. Zhou YH, Yin G, Asplund L, Qiu YL, Bignert A, Zhu ZL, Zhao JF, Bergman A. A novel pollution pattern: Highly chlorinated biphenyls retained in black-crowned night heron (Nycticorax The highly chlorinated biphenyls were further nycticorax) and whiskered tern (Chlidonias hybrida) from the quanti ed in the bird eggs of night heron and Yangtze River Delta. Chemosphere 2016, 150:491-498. whiskered tern [3]. The median concentrations of 4. Zhou Y, Yin G, Asplund L, Stewart K, Rantakokko P, Bignert A, 16 PCBs (composed of twelve octa-, three nona- and Ruokojärvi P, Kiviranta H, Qiu Y, Ma Z, Bergman Å. Human exposure to PCDDs and their precursors from heron and tern one decachlorinated biphenyls) were 44 and 16 ng/g eggs in the Yangtze River Delta indicate PCP origin. fat in eggs from night herons and whiskered terns, Environmental Pollution 2017, 225:184-192. respectively. These highly chlorinated biphenyls 5. International Chlorinated Alkanes Industry Association (ICAIA), contributed with 10% to total PCBs. According to Newsletter No. 3, 2014. Available from: http://www.eurochlor. the scienti c literature, highly chlorinated biphenyls org/media/88258/20140908_icaia_newsletter_03_«nal.pdf. 6. Friden UE. Sources, emissions, and occurance of chlorinated are present in commercial PCB products with high paraffins in Stockholm, Sweden. Stockholm Univeristy Doctoral chlorine contents (e.g. Arochlor 1270). Another Thesis 2010. potential source is related to pigment production. 7. Zeng LX, Wang T, Wang P, Liu Q, Han SL, Yuan B, Zhu NL, Wang Highly chlorinated biphenyls have been detected in YW, Jiang GB. Distribution and trophic transfer of short-chain phthalocyanine green pigment sold in USA and on chlorinated paraffins in an aquatic ecosystem receiving effluents from a sewage treatment plant. Environmental the Japanese market [29] and [30]. However, there Science & Technology 2011, 45:5529-5535. is still a lack of knowledge on PCB being formed in 8. Ma XD, Zhang HJ, Wang Z, Yao ZW, Chen JW, Chen JP. pigment production on Chinese market. Bioaccumulation and trophic transfer of short chain chlorinated paraffins in a marine food web from Liaodong Bay, Authors and sub-project researchers North China. Environmental Science & Technology 2014, 48:5964-5971. Dr. Yihui Zhou, Prof. Åke Bergman, Prof. Anders 9. Van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland Bignert and Dr. Ge Yin W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, Rose M, Safe S, Schrenk D, Tohyama C, Tritscher A, Tuomisto J, Tysklind M, Walker N, Peterson RE. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicological Sciences 2006, 93:223-241. 10. Malisch R, Baum F. PCDD/Fs, dioxin-like PCBs and marker PCBs in eggs of peregrine falcons from Germany. Chemosphere 2007, 67:S1-S15. 11. Braune BM, Simon M. Dioxins, furans, and non-ortho PCBs in Canadian Arctic seabirds. Environmental Science & Technology 2003, 37:3071-3077.

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12. Fang LP, Zheng MH, Zhang B, Gao LR, Liu WB, Zhao XR. 24. Guo Y, Yu H-Y, Zeng EY. Occurrence, source diagnosis, and Polychlorinated dibenzo-p-dioxins and dibenzofurans in eggs of biological effect assessment of DDT and its metabolites in eight avian species from Dongting Lake, China. Chemosphere various environmental compartments of the Pearl River Delta, 2007, 69:411-421. South China: A review. Environmental Pollution 2009, 157:1753- 13. EUR-Lex. Commission Regulation (eu) No 2015/628 Amending 1763. Annex xvii to Regulation (ec) No 1907/2006 of the European 25. UNEP. The new POPs under the Stockholm Convention. Parliament and of the Council on the Registration, Evalutaion, Available from: http://chm.pops.int/TheConvention/ThePOPs/ Authorisation and Restriction of Chemicals (Reach) as Regards TheNewPOPs/tabid/2511/Default.aspx. Accessed April 16th, Lead and its Compounds. 2015. Available from: http://eur-lex. 2017. europa.eu/legal-content/EN/TXT/?uri=uriserv%3AOJ.L_. 26. She JW, Holden A, Adelsbach TL, Tanner M, Schwarzbach SE, Yee 2015.104.01.0002.01.ENG. Accessed April 16th, 2017. JL, Hooper K. Concentrations and time trends of 14. European Food Safety Authority (EFSA). Update of the polybrominated diphenyl ethers (PBDEs) and polychlorinated monitoring of levels of dioxins and PCBs in food and feed. 2012. biphenyls (PCBs) in aquatic bird eggs from San Francisco Bay, Available from: https://www.efsa.europa.eu/en/efsajournal/ CA 2000-2003. Chemosphere 2008, 73:S201-S209. pub/2832. Accessed April 16th, 2017. 27. Jorundsdottir H, Lofstrand K, Svavarsson J, Bignert A, Bergman 15. Koistinen J, Koivusaari J, Nuuja I, Paasivirta J. PCDEs, PCBs, A. Organochlorine compounds and their metabolites in seven PCDDs and PCDFs in black guillemots and white-tailed sea icelandic seabird species – a comparative study. Environmental eagles from the Baltic Sea. Chemosphere 1995, 30:1671-1684. Science & Technology 2010, 44:3252-3259. 16. Sundqvist K. Sources of dioxin and other POPs to the marine 28. Jorundsdottir H, Lofstrand K, Svavarsson J, Bignert A, Bergman environment-Identi«cation and apportionment using pattern A. Polybrominated diphenyl ethers (PBDEs) and analysis and receptor modeling. Umeå University Doctoral hexabromocyclododecane (HBCD) in seven different marine Thesis 2009. bird species from Iceland. Chemosphere 2013, 93:1526-1532. 17. Yin G. Organohalogen contaminants in wildlife from the 29. Hu DF, Hornbuckle KC. Inadvertent polychlorinated biphenyls in Yangtze River Delta. Stockholm University Doctoral Thesis 2016. commercial paint pigments. Environmental Science & 18. Humppi T. Observation of polychlorinated phenoxyanisoles in a Technology 2010, 44:2822-2827. technical chlorophenol formulation and in sawmill 30. Anezaki K, Nakano T. Concentration levels and congener environment. Chemosphere 1985, 14:523-528. pro«les of polychlorinated biphenyls, pentachlorobenzene, and 19. Koistinen J, Herve S, Paukku R, Lahtipera M, Paasivirta J. hexachlorobenzene in commercial pigments. Environmental Chloroaromatic pollutants in mussels incubated in two Finnish Science and Pollution Research 2014, 21:998-1009. watercourses polluted by industry. Chemosphere 1997, 34:2553-2569. 20. Zeidler OL. Verbindungen von Chloral mit Brom-und Chlorbenzol. Berichte der deutschen chemischen Gesellschaft 1874, 7:1180-1181 (in German). 21. Wang Y, Lam JCW, So MK, Yeung LWY, Cai ZW, Hung CLH, Lam PKS. Polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), dioxin-like polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in waterbird eggs of Hong Kong, China. Chemosphere 2012, 86:242-247. 22. Lam JCW, Kajiwara N, Ramu K, Tanabe S, Lam PKS. Assessment of polybrominated diphenyl ethers in eggs of waterbirds from South China. Environmental Pollution 2007, 148:258-267. 23. Qiu XH, Zhu T, Yao B, Hu JX, Hu SW. Contribution of dicofol to the current DDT pollution in China. Environmental Science & Technology 2005, 39:4385-4390.

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4.2 POPs in the aquatic ecosystem of the addition, sediments were collected in the Taihu Lake Yangtze River Delta – establishment of a area together with the snails at each sampling site. monitoring program The aims of this work include (1) assessing 4.2.1 Introduction contamination of POPs in invertebrates from Invertebrates have been utilized for environmental different water systems in the YRD area; (2) monitoring as they have a wide geographic distribution, evaluating risk for local citizens from exposure of low mobility and high ltration capacity. During the contaminants and (3) working towards establishment past years, suspension-feeding invertebrates, e.g. blue of a monitoring program with an appropriate study mussels have been selected to monitor and assess the design, for future spatial and temporal monitoring of pollution of the aquatic environment from POPs, environmental pollutants and possible effects on heavy metal and radioactive compounds [1]. Many wildlife. invertebrates such as seawater and freshwater mussel and snail species are commercially important food in 4.2.2 Concentration and congener pattern of the YRD, and therefore analyses of contamination pollutants from pollutants are of interest from a public health Mussels were analyzed for POPs from the coast of perspective. China in the summer of 2011. For each location, mussels were homogenized as a pool and analyzed In this work, several invertebrate species were collected with triplicate samples. DDTs is the predominant from the seawater and freshwater environment in the group of contaminants of POPs in invertebrates YRD (see Figure 4.1.1 in chapter 4.1, above). In regardless of species or sites (Figure 4.1.1 in chapter

3 500 8 2,4’-DDD ε-HCH 3 000 7 2,4’-DDE δ-HCH 6 2 500 γ 2,4’-DDT 5 -HCH 2 000 4,4’-DDD 4 β-HCH 1 500 4,4’-DDE 3 α-HCH 1 000 2 4,4’-DDT 500 1

0 0 WH (ME) ZS (ME) NT (CS) NT (RP) NT (SC) WH (ME) ZS (ME) NT (CS) NT (RP) NT (SC)

Figure 4.2.1. DDTs concentration (ng/g fat) and pattern in the Figure 4.2.2. HCH concentrations (ng/g fat) and pattern in the mussel species: Mytilus edulis (ME), Cyclina sinensis (CS), Ruditapes mussel species: Mytilus edulis (ME), Cyclina sinensis (CS), Ruditapes philippinarum (RP) and Sinonovacula constricta (SC) from Weihai philippinarum (RP) and Sinonovacula constricta (SC) from Weihai (WH), Zhoushan (ZS) and Nantong (NT). (WH), Zhoushan (ZS) and Nantong (NT).

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4.1). The results indicated ongoing or at least recent HBCDD in this study were higher than blue mussel input of DDT. Concentration of ∑DDTs (sum of in Sweden [6] but lower than oyster in coastal area of 4,4’-DDT, 4,4’-DDE, 4,4’-DDD, 2,4’-DDT, 2,4’-DDE Japan [7]. One sample was run on HPLC/MS and it and 2,4’-DDD) ranging from 370 ng/g fat in the East was found that α-HBCDD was the predominant China Sea (Zhoushan city) to 1200 ng/g fat in the congener, contributing to 85% of the total amount. South Yellow Sea (Nantong city) [2]. Such level is comparable to other areas in the YRD, e.g. green In general, industrial POPs such as PCBs and PBDEs mussel from Shengsi island [3]. A different DDTs were in the lower end of envioronmental levels pattern was observed among sampling sites. 4,4’- reported when compared to other studies. This is in DDD showed comparable levels with 4,4’-DDE, accordance with the results from wildlife and bird which is unexpected compared with previous studies egg samples (See chapter 4.1). [4]. It might be explained by species-speci c differences. In a later study, snails were collected in the Taihu Lake area together with sediments in 2014, for PCBs Hexachlorocyclohexanes (HCHs) is the second most and PBDEs analyses [8]. Seven sites (East Taihu Lake, important group of organochlorine pesticides in Xiaomeikou, Dapukou, Zhushan Lake, Meiliang bay, mussels. Concentration of sum of all isomers Gong Lake, and Dianshan Lake) covering typical (∑HCHs) varied from 4.0 to 7.6 ng/g fat (Figure areas of the Taihu Lake were selected for sampling. 4.2.2). It is clearly shown that β-HCH is the major For each site, soft tissue of snails were picked out and HCH isomer at all sites which is to expect since this homogenized as pools for chemical analysis. In is the most persistent HCH isomer. The persistency parallel, sediment from ve subsites was mixed to of β-HCH is explained by its chemical structure, all represent one site. Concentrations of PCBs (sum of chlorine are equatorial in the molecule. The ratio 22 PCB congeners) ranged between 90 and 680 ng/g between α-HCH and γ-HCH is between 1.0 and fat in the snails (Figure 4.2.3) and between 0.018 and 2.5, lower than technical HCHs (commonly between 0.82 ng/g dw in the sediments. CB-153 was the 4 and 7) [5]. This may be explained by a primary use predominant PCB congener in both matrices. Highly of lindane, the commercial HCH product that chlorinated PCBs were also detected in both the contains basically only γ-HCH, and not technical snails and sediments. HCH. Concentrations of the sum of 24 PBDE congeners Regarding the ame retardants, HBCDD was varied from 25 to 200 ng/g fat in the snails (Figure detected at relatively high levels, with a range of 4.2.4) and from 0.62 to 67 ng/g dw in the sediments. 21-42 ng/g fat. This level is comparable to the sum of Lower PBDE congener e.g. BDE-47 and BDE-99 are PBDEs in the samples. HBCDD is a cyclic aliphatic the major PBDEs in snail whereas higher brominated compound with six bromines that is applied as a congeners, e.g. BDE-209, are the major ones in ame retardant in polystyrene foam. HBCDD was sediments. It is presumed that highly brominated listed as a POP in 2015. It has in total 16 possible congeners, particularly BDE-209, are less bioavailable stereoisomers; the most abundant ones are to aquatic organisms, due to their large molecule size α-HBCDD (10-13%), β-HBCDD (1-12%) and [9]. This may in part explain the difference in PBDE γ-HBCDD (75-89%). The concentrations of congener patterns between snails and sediments.

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Professional help for sampling of pond snails and a close-up of the snails harvested. Photo: Åke Bergman

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CB-209 L1 CB-206 700 ∑PCBs (ng/g fat) in snail CB-205 606 L2 CB-194 600 CB-207 CB-195+208 500 L3 CB-196+203 CB-199 CB-198 400 L4 CB-197 CB-204+201 293 272 CB-202 300 L5 CB-180 CB-138 200 177 150 141 L6 CB-153 126 CB-118 100 CB-101 L7 CB-52 CB-28 0 L1 L2 L3 L4 L5 L6 L7 0 10 20 30 40 50 60 70 80 90 100

Figure 4.2.3. Concentration (left) and congener pro«le (right) of PCBs in snails from Taihu Lake area. The sites are: L1: East Taihu Lake; L2: Dapukou; L3: Xiaomeikou; L4: Zhushan Lake; L5: Meiliang Bay: L6: Gong Lake and L7: Dianshan Lake.

BDE 209 L1 BDE 206 250 ∑PBDEs (ng/g fat) in snail BDE 207 207 L2 BDE 208 BDE 196 200 183 BDE 198,199,200,203 L3 BDE 197 BDE 201 150 140 BDE 202 L4 BDE 183 BDE 153 BDE 154 L5 100 86 BDE 99 78 BDE 100 L6 BDE 66 50 41 37 BDE 47 BDE 28 L7

0 L1 L2 L3 L4 L5 L6 L7 0 10 20 30 40 50 60 70 80 90 100

Figure 4.2.4. Concentration (left) and congener pro«le (right) of PBDEs in snails from Taihu Lake area. The sites are: L1: East Taihu Lake; L2: Dapukou; L3: Xiaomeikou; L4: Zhushan Lake; L5: Meiliang Bay: L6: Gong Lake and L7: Dianshan Lake.

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Again, the concentrations of PCBs and PBDEs observed between BSAF values and number halogen observed were in the medium to low range compared atoms for PBDEs whereas a parabola trend was noted with other studies worldwide. for PCBs (Figure 4.2.5). In our previous study in Dianshan Lake, Wu [10] found highest calculable 4.2.3 Biota – sediment accumulation BSAFs for BDE-28, BDE-99, BDE-153, BDE-47 and The biota – sediment accumulation factor (BSAF) is CB-209 but not for BDE-209, BDE-208 or BDE-207. used to assess whether pollutants can transfer from This is consistent with other studies. She and sediment and accumulate in biota. The coauthors [11] studied halogenated ame retardants in concentrations of a compound (pollutant) in sediment herbivorous food and found that the bioaccumulation is normalized by total organic carbon and compared factors between apple snail and rice plant increased with lipid weight concentration in biota. Normally for compounds with partitioning factors between BSAF over 1 indicates that bioaccumulation occurs. octanol and water (log Kow) and up to seven halogen It is noteworthy that the pollutants may further substituents, and then decreased for higher biomagnify throughout the food web and cause substituted PCBs. Likewise, Zhu and co-workers [12] higher concentrations in human consumers. found that bioaccumulation factors of PCBs start to decline from hepta-CBs in aquatic species investigated. We analyzed BSAF for PCBs and PBDEs between These phenomena can be be explained by lower snails and sediments collected from the Taihu Lake bioavailability of the pollutants due to increasing area. It is shown that biota - sediment accumulation molecular size (molecular mass and volume), even occur for PCBs and lower brominated diphenyl though the log Kow still increases. ethers, but not for PBDE congeners with high number of bromines. Interestingly, a negative correlation was 4.2.4 Risk assessment Food has been considered as the main exposure pathway of POPs to humans. As mentioned, aquatic food plays an important role in food intake in the 10 YRD. It was reported that the annual consumption 2 Br R =0,561 of seafood is approximately 20 kg in Eastern China 9 Cl R2=0,5858 8 [13]. Consequently, it is necessary to investigate the dietary intake of POPs via aquatic species used as 7 food. The estimation is calculated via the equation 6 EDIs= DC*C/BW 5 BASF 4 Herein, EDI is the estimated daily intake (ng/g and 3 day), DC is daily consumption (g/d), C is the

2 concentration of pollutants (ng/g ww) and BW is body weight (kg) assuming 35 kg and 65 kg for 1 children and adults, respectively. 0 0 2 4 6 8 10 12 Number of Halogens Figure 4.2.5. Regression relationship between biota-sediment The calculated EDI is compared with criteria such as bioaccumulation factors (BSAF) and the number of halogen atoms. Acceptable Daily Intakes (ADIs) recommended by Food Organization and World Health Organization

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(FAO/WHO) and minimal risk levels (MRLs) serve as an indicator out of human hazards, indeed. proposed by the Agency for Toxic Substances and Many developed countries have established such Disease Registry, (ATSDR) USA [14]. programs. For instance, Swedish monitoring program, coordinated by the Swedish Museum of Estimated daily intake of POPs from consumption of Natural History (NRM), has been ongoing since the invertebrates, mussels, clams and snails, is shown in early 1970’s. Mussels, perch, and guillemot egg have Table 4.2.1. Apparently, EDIs of POPs are far lower been used as bioindicators and the results showed than ADIs and MRLs, indicating no or very low risk signi cant decline of several POPs (e.g. PCBs, DDTs) of accumulating POPs via seafood intake. However, after prohibition and restriction during the past few the results may underestimate ADIs of POPs, as sh decades, whereas increasing trends are found for are not taken into consideration. POPs may accumulate others, e.g. HBCDD. Hence it is important to more in sh if they are on a higher trophic level, introduce an advanced research based monitoring while less if it is vegetarian sh. Certain parts of the of environmental pollutants also in China. It may be population may pay more attention such as shermen motivated by (1) the rapid industrialization leading families as they consume these kinds of food more to chemical discharges into the Chinese environment; frequently than other groups. (2) there is lack of well-designed monitoring program in China and (3) the need of advanced specimen 4.2.5 Establishment of a monitoring program using banking for future use in environmental assessments. snails Environmental monitoring serves as a base for In this project, we started with mussel as it has been monitoring environmental quality and also for commonly used for monitoring purposes. However, exposure and risk assessments. Biomonitoring is a natural mussel is not readily available in fresh water valuable tool as it reects how animals are impacted lakes in the YRD, while cultivated mussels are widely by environmental pollution in various geographical used in pearl production. Therefore, it is necessary to regions and over time. The monitoring of wildlife can select an alternative species for monitoring.

Table 4.2.1. Estimated daily intake of POPs from consumption of invertebrates. Acceptable Daily Intakes (ADIs) as recommended by Food Organization and World Health Organization (FAO/WHO) and minimal risk levels (MRLs) are proposed by the Agency for Toxic Substances and Disease Registry, USA (ATSDR). The results are summarized from publications [2, 8].

Mussel Mussel Snail ADIs/PTDIs MRLs (Zhoushan) (Nantong) (Taihu Lake) (FAO/WHO) (ATSDR) Child Adult Child Adult Child Adult DDTs 130 68 41 22 10000 500 HCHs 0.15 0.080 0.11 0.062 5000 600 PCBs 0.38 0.20 0.22 0.12 5.6 3.0 20 PBDEs 0.35 0.19 0.16 0.084 1.6 0.85 HCB 0.060 0.032 0.12 0.067 100

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Considering that snails share similar habitats as differences of three sampling strategies to detect mussels, we sampled both snails, mussels and increasing temporal trends of a selected sediments from small lakes in Jiaxing. The chemical environmental pollutant (BDE-47) by means of the analytical results showed similar patterns of pollutants concept of statistical power. in the two species (Figure 4.2.6). The contaminant pattern in the sediments was different as visualized in Three sampling strategies are: Figure 4.2.6. Hence, we move our interest to snail as 1. Sampling at the same sampling spot from year to a monitoring species. year 2. Sampling takes place at one arbitrarily selected Sampling is the rst important step in any monitoring sub-site program. To enable fair comparison over time or 3. Samples collected randomly from all available between geographical regions, samples should be sites each year independent and representative. However, since sampling is costly, time and labor consuming, it is Statistical power is the probability to detect a trend not always done by neither researchers themselves or when it actually occurs. It could be applied to a nor other experienced persons. There is always a risk priori analysis, which means to determine the sample of so called convenient sampling, to collect sample size necessary to generate acceptably high power (i.e. from easy accessible sites. That may lead to biased 0.8 or 0.9). The simulation data was from chemical results. Another risk is to take samples from the same analysis of BDE-47 in snails. Ten individual snails site each time leaving us with the question of how from each spot were collected from 5 spots in representative results we then will get. In a study, Tianmu Lake. Based on the mean value and variation we use computer simulation to demonstrate the within each group, simulation was performed 5000 times for each of several sample sizes. These three 450 Sediment (ng/g d.w.) Mussel and Snail (ng/g l.w.) sampling strategies were evaluated by the estimation of requiredaDBDPE sample size, to reach a detection of an 400 annual change of 5% with a statistical power of 80% ∑PBDE 350 and 90% with a signi cance level of 5%. 300 ∑PCBs

250 The simulation results are shown in Figure 4.2.7. For the rstHCB strategy, to achieve 80% of power, we need 200 to analyze 8-13 individual snails each year from each 150 site, ∑DDTsif we increase the power to 90%, then 11-18

100 snails∑HCHs are required. Strategy 2 shows that it needs 30 50 snails from an arbitrary selected site and to increase the power to 90 %, it requires over one hundred 0 Sediment Mussel Snail snails, which will be costly. Using the second strategy

aDBDPE ∑PBDE ∑PCBs HCB ∑DDTs ∑HCHs will also increase the risk of overestimated trends considerably compared to strategy 1 and 2. This Figure 4.2.6. Contaminants pattern in sediment, mussel and snail phenomenon is termed magnitude error (M error). from West Qianmudang, Jiaxing [15]. Hence, the second strategy is de nitely not to

121 Chapter 4: Highlights of two research projects within Chemstrres

A) S1 B) S2 C) S3 D) S4 E) S5 X(80.0)=9.37 X(80.0)=9.18 X(80.0)=8.11 X(80.0)=13.2 X(80.0)=13.5 X(90.0)=13.5 X(90.0)=12.7 X(90.0)=10.8 X(90.0)=17.5 X(90.0)=18.5 100 100 100 100 100

80 80 80 80 80

Approach 1: Sampling at the same sampling spot from year 60 60 60 60 60 to year (individual sample) Power 40 40 40 40 40

20 20 20 20 20

0 0 0 0 0 10 20 30 40 10 20 30 40 10 20 30 40 10 20 30 40 10 20 30 40 Sample size Sample size Sample size Sample size Sample size

A) X(80.0)=30.1 X(80.0)=16.3 X(90.0)=100 X(90.0)=22.4 100 100

80 80

Approach 2: Sampling takes Approach 3: Samples place at one arbitrarily collected randomly from 60 60 selected sub-site all available sites each year Power 40 40

20 20

0 0 50 100 150 20 40 60 Sample size Sample size

Figure 4.2.7. Simulation results of statistical power and for various sample sizes and required sample sizes for 80 and 90% power, respectively, for the three selected sampling strategies.

122 Chapter 4: Highlights of two research projects within Chemstrres recommend. The third strategy requires slightly References larger sample sizes than the rst strategy. It requires 16 samples to achieve power of 80%. Considering 1. O'Connor TP. National distribution of chemical concentrations that a xed site is sensitive to future changes of in mussels and oysters in the USA. Marine Environmental Research 2002, 53:117-143. conditions (exploitation, destruction, or that repeated 2. Yin G, Asplund LM, Qiu YL, Zhou YH, Wang H, Yao ZL, Jiang JB, sampling itself will affect the local population of Bergman A. Chlorinated and brominated organic pollutants in snails at a speci c site) and the limited representatives shell«sh from the Yellow Sea and East China Sea. Environmental of such a site for the whole lake (or the selected study Science and Pollution Research 2015, 22:1713-1722. area), we recommend the third strategy for sampling. 3. Ramu K, Kajiwara N, Sudaryanto A, Isobe T, Takahashi S, Subramanian A, Ueno D, Zheng GJ, Lam PKS, Takada H, Zakaria MP, Viet PH, Prudente M, Tana TS, Tanabe S. Asian mussel The analytical results in snail from Tianmu Lake watch program: Contamination status of polyhrominated showed high concentration of pentachloroanisole and diphenyl ethers and organochlorines in coastal waters of DDE. Chlorinated paraf ns were identi ed in some Asian countries. Environmental Science & Technology 2007, of the sites. Preferably, reference lakes with less 41:4580-4586. 4. So MK, Zhang X, Giesy JP, Fung CN, Fong HW, Zheng J, Kramer human impact, located upstream from massive MJ, Yoo H, Lam PK. Organochlorines and dioxin-like compounds agriculture activities should be included in the in green-lipped mussels Perna viridis from Hong Kong monitoring program in the future. The monitoring mariculture zones. Marine Pollution Bulletin 2005, 51:677-687. program has been performed in Taihu Lake where 5. Walker K, Vallero DA, Lewis RG. Factors inµuencing the snails and sediments were collected at a number of distribution of lindane and other hexachlorocyclohexanes in the environment. Environmental Science & Technology 1999, selected sites. Snails were pooled for chemical 33:4373-4378. analysis. We have published an article about spatial 6. Bignert A, Danielsson S, Suzanne F, Elisbeth N. Övervakning av distribution of PCBs and PBDEs [8]. Future studies metaller och organiska miljögifter i marin biota, 2012 (in are required to assess temporal trends of pollutants Swedish). Available from: http://www.diva-portal.org/smash/ of interest. record.jsf?pid=diva2%3A717178&dswid=7047. Accessed April 16th, 2017. 7. Ueno D, Isobe T, Ramu K, Tanabe S, Alaee M, Marvin C, Inoue K, Authors Someya T, Miyajima T, Kodama H, Nakata H. Spatial distribution Dr. Ge Yin, Prof. Anders Bignert and Dr. Yihui Zhou of hexabromocyclododecanes (HBCDs), polybrominated diphenyl ethers (PBDEs) and organochlorines in bivalves from Japanese coastal waters. Chemosphere 2010, 78:1213-1219. 8. Yin G, Zhou YH, Strid A, Zheng ZY, Bignert A, Ma TW, Athanassiadis I, Qiu YL. Spatial distribution and bioaccumulation of polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in snails (Bellamya aeruginosa) and sediments from Taihu lake, China. Environmental Science and Pollution Research 2017, 24:7740- 7751. 9. Van Ael E, Covaci A, Blust R, Bervoets L. Persistent organic pollutants in the Scheldt estuary: Environmental distribution and bioaccumulation (vol 48, pg 17, 2012). Environment International 2014, 63:246-251.

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10. Wu Y. Organohalogen contaminants and metals in sediments and snails from Dianshan Lake, Yangtze River Delta. Stockholm University Master Thesis 2013. 11. She YZ, Wu JP, Zhang Y, Peng Y, Mo L, Luo XJ, Mai BX. Bioaccumulation of polybrominated diphenyl ethers and several alternative halogenated µame retardants in a small herbivorous food chain. Environmental Pollution 2013, 174:164-170. 12. Zhu CF, Wang P, Li YM, Chen ZJ, Li WJ, Ssebugere P, Zhang QH, Jiang GB. Bioconcentration and trophic transfer of polychlorinated biphenyls and polychlorinated dibenzo-p- dioxins and dibenzofurans in aquatic animals from an e-waste dismantling area in East China. Environmental Science-Processes & Impacts 2015, 17:693-699. 13. Chinese Academy of Argricultural Sciences (CAAS). China Agricultural Outlook Report (2015-2024). 2014 (in Chinese). 14. Agency for Toxic Substances and Disease Registry (ATSDR). Minimal Risk Levels for Hazardous Substances. 2016. Available from: https://www.atsdr.cdc.gov/mrls/pdfs/atsdr_mrls.pdf. 15. Chen Q. Organohalogen contaminants in sediments, snails and mussels from the Yangtze River Delta. Stockholm University Master Thesis 2012.

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长三角地区 化学品污染挑战

A 2017 Sino-Swedish Research Report