中华白海豚生态学研究进展
Research advances on the ecology of Sousa chinensis
通讯作者: * E-mail:wangxianyan@tio.org.cn
编委: 杨光
责任编辑: 李会丽
收稿日期: 2022-12-4 接受日期: 2023-03-8
基金资助: |
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Corresponding authors: * E-mail:wangxianyan@tio.org.cn
Received: 2022-12-4 Accepted: 2023-03-8
中华白海豚(Sousa chinensis)是国家一级重点保护水生野生动物, 处于食物链的顶端, 是近岸海洋生态系统健康状况的指示物种和海洋生物多样性保护的旗舰物种, 具有重要的生态、科学和文化价值。自20世纪90年代开始, 中华白海豚的研究逐渐兴起; 近年来, 随着3S技术、生态模型及分子生物学等技术方法的发展应用, 在中华白海豚种群生态学、行为生态学、分子生态学等领域的研究取得了长足发展。国内外学者利用截线抽样法和标志重捕法, 调查研究了全球范围内已知的中华白海豚种群的分布、数量等生态信息; 在物种保护的背景下, 开展了对中华白海豚栖息地的选择偏好、栖息地质量评价及潜在栖息地的预测研究; 探究了中华白海豚的觅食行为和繁殖行为的规律和其他行为的生态意义; 分子生物技术的应用, 初步揭示了中华白海豚的遗传分化规律, 以及该物种对气候变化表现出的脆弱性; 涉海工程、水下噪声、水体污染、渔业活动等人类活动仍是目前中华白海豚面临的主要威胁。本文在总结已有研究的基础上, 对未来该物种的生态学研究与保护提出了以下展望: (1)建立国家层面的动态基线数据库, 以更好地追踪中华白海豚的种群动态及栖息地环境变化; (2)构建栖息地识别及保护评价体系, 开展对中华白海豚关键栖息地和潜在栖息地的识别以及分级管理; (3)从生态系统层面开展栖息地选择机制研究, 结合生态模型探究当前栖息地对中华白海豚的承载力, 进一步探究栖息地水文要素、生物资源以及人类活动等因素对中华白海豚选择栖息地的影响; (4)构建中华白海豚遗传资源库, 探究自然选择-生态影响-遗传进化之间的联系, 以揭示物种进化、适应与濒危的分子机制; (5)为有效应对全球海洋环境变化对中华白海豚的影响, 建议在中华白海豚分布国家间建立科研合作平台及保护管理网络。
关键词:
Background & Aims: The Indo-Pacific humpback dolphin (Sousa chinensis) has been listed as the Grade 1 National Key Protected Animal in China. As the top predator of the inshore marine food chain, S. chinensis is an indicator species of the health status of the inshore ecosystem. Due to the important ecological, scientific and cultural values, it is also used as the flagship species for marine biodiversity conservation. Since the 1990s, the studies on S. chinensis have gradually risen, and developed to a new period in recent years along with the application of 3S (RS, GPS, GIS), ecological models, and molecular biological techniques. We summarized the studies of S. chinensis from the aspects of population ecology, behavioral ecology, molecular ecology and the threats that the species faced so far, aiming to clarify the advances in the ecological studies and the contributions to conservation of S. chinensis.
Progress: Ecological information such as distribution and abundance of S. chinensis population known globally in the world has been investigated by domestic and foreign scholars using line-transect sampling and capture-mark-recapture methods. In the context of species conservation, studies on habitat selection preference, habitat quality evaluation and potential habitat prediction of S. chinensis were performed. The rules of foraging behavior and reproduction behavior of S. chinensis were preliminarily understood, and the ecological significance of other behaviors were also explored. With the application of molecular biotechnology, the genetic differentiation of S. chinensis and its vulnerability to climate change have been preliminarily revealed. Human activities such as marine construction projects, underwater noise, marine pollution, and fishery activities are still the main threats to S. chinensis.
Perspectives: Based on the summary of existing studies, we propose the following prospects for the future ecological research and conservation of S. chinensis: (1) Establish a dynamic baseline database at the national level to better track the population dynamics and habitat environment changes of S. chinensis. (2) Establish a habitat identification and conservation evaluation system, and carry out identification and hierarchical management of critical and potential habitats of S. chinensis. (3) Study the habitat selection mechanism from the ecosystem level, combined with the ecological model to explore the carrying capacity of the current habitat to the S. chinensis, and further explore the impact of habitat hydrological factors, biological resources and human activities on the habitat selection of S. chinensis. (4) Construct a genetic resource database for S. chinensis, and explore the links among natural selection, ecological impact and genetic evolution, so as to reveal the molecular mechanisms of species evolution, adaptation and endangerment. (5) In order to effectively deal with the impact of global marine environmental changes on the S. chinensis, it is recommended to establish a scientific research cooperation platform and protection management network among the S. chinensis distribution countries.
Keywords:
本文引用格式
雍李明, 张语克, 赵丽媛, 曾千慧, 林龙山, 高旻昊, 程昊, 王先艳 (2023)
Liming Yong, Yuke Zhang, Liyuan Zhao, Qianhui Zeng, Longshan Lin, Minhao Gao, Hao Cheng, Xianyan Wang (2023)
中华白海豚的科学研究最早见于1751年, Peter Osbeck在我国广东省珠江口海域首次记录到中华白海豚(Osbeck, 1771); 1757年Peter Osbeck又对该物种进行了形态学描述, 并将其命名为“Delphinus chinensis”, 隶属于真海豚属(Delphinus) (Jefferson, 2000), 后改为驼海豚属/白海豚属(Sousa) (Scheffer & Rice, 1963)。早期, 分布于南非(Karczmarski et al, 2000)、澳大利亚(Parra et al, 2004)和阿拉伯(Baldwin et al, 2004)等水域的白海豚均被认为是中华白海豚, 后被分为中华白海豚(Sousa chinensis)、大西洋白海豚(S. teuszii)、澳大利亚白海豚(S. sahulensis)和印度洋白海豚(S. plumbea) 4种, 并得到了海洋哺乳动物协会分类委员会的认可(Jefferson & Rosenbaum, 2014)。目前, 学术界认为的中华白海豚全球分布范围包括东印度洋和西太平洋的近岸海域, 北至中国东南沿海, 向南包括整个东南亚, 向西至孟加拉湾及印度半岛南侧海域(Jefferson & Rosenbaum, 2014; Jefferson & Smith, 2016; Parra & Jefferson, 2018)。在我国, 中华白海豚主要栖息于东南沿海的近岸及河口水域(王先艳等, 2012)。
1 种群生态学
国际上常用截线抽样法(line-transect sampling)和基于照相识别的标记重捕法(capture-mark- recapture, CMR)来研究中华白海豚种群动态(Jefferson, 2000; Weinrich et al, 2001)。截线抽样法可以在缺乏基线数据的前提下, 确定动物的分布边界和在不同区域内的相对密度(刘文华和黄宗国, 2000; Jefferson et al, 2002; Zhou et al, 2007)。基于照相识别的标记重捕法对种群数量的估算具有较高的精确度, 而且可以收集行为和其他生态信息, 近年来得到较多应用(Peng et al, 2020; Zeng et al, 2020; Lin et al, 2022)。
1.1 种群数量及分布
全球范围内, 目前已知的中华白海豚数量约5,700头, 且存在下降趋势(Jefferson & Smith, 2016; Chan & Karczmarski, 2017; Li et al, 2019; Araújo-Wang et al, 2022)。国外对该物种的研究较少, 据报道最大种群分布于孟加拉湾北部, 有636头(Smith et al, 2015), 泰国东海岸的Donsak海域(193头)和西海岸的Sarai岛(24头)、Sukon岛(23头) (Cherdsukjai et al, 2013; Jutapruet et al, 2015), 以及马来西亚的Kuching湾(84头) (Poh et al, 2016) (图1)。印度尼西亚西加里曼丹的Kubu Raya海域仅有目击和搁浅记录, 未见详细的种群数量报道(Minton et al, 2016)。
图1
图1
全球范围内中华白海豚主要地理种群分布及数量, 阴影部分代表中华白海豚分布范围(Jefferson & Smith, 2016; IUCN, 2017)。地理位置含义及数据来源: 国内样点(XM: 厦门湾(Zeng et al, 2020); TWC: 台湾西海岸(Araújo-Wang et al, 2022); HK: 香港(Chan & Karczmarski, 2017); PRE: 珠江口(Chen T et al, 2010); MRE: 漠阳江口(Li et al, 2019); LZB: 雷州湾(Xu et al, 2015); SC: 沙田-草潭(Chen BY et al, 2016); BBG: 北部湾(Chen BY et al, 2016; Lin et al, 2022); WSHN: 海南西南海域(Li et al, 2016)); 国外样点(NBB: 北孟加拉湾(Smith et al, 2015); DO: 泰国Donsak (Jutapruet et al, 2015); SU: 泰国Sukon岛, SI: 泰国Sarai Island (Cherdsukjai et al, 2013); KB: 马来西亚Kuching湾(Poh et al, 2016))。
Fig. 1
Distribution and abundance of major geographical populations of Sousa chinensis in the world. The shaded area represents the distribution area (Jefferson & Smith, 2016; IUCN, 2017). Abbreviations and data sources: Sites in China (XM, Xiamen Bay (Zeng et al, 2020); TWC, Taiwan West Coast (Araújo-Wang et al, 2022); HK, Hong Kong (Chan & Karczmarski, 2017); PRE, Pearl River Estuary (Chen T et al, 2010); MRE, Moyang River Estuary (Li et al, 2019); LZB, Leizhou Bay (Xu et al, 2015); SC, Shatian-Caotan (Chen BY et al, 2016); BBG, Beibu Gulf (Chen BY et al, 2016; Lin et al, 2022); WSHN, Southwest Sea Area of Hainan (Li et al, 2016)); Sites in other countries (NBB, Northern Bay of Bengal (Smith et al, 2015); DO, Donsak, Thailand (Jutapruet et al, 2015); SU, Sukon Island, Thailand; SI, Sarai Island, Thailand (Cherdsukjai et al, 2013); KB, Kuching Bay, Malaysia (Poh et al, 2016)).
全球约83% (4,730头)的中华白海豚栖息于我国东南沿海(Jefferson & Smith, 2016), 主要有珠江口(含香港和河口西部海域) (Jefferson, 2000; Jefferson et al, 2012)、雷州湾(Zhou et al, 2007; Xu et al, 2015)、北部湾(Chen BY et al, 2016; Wu et al, 2017a)、厦门湾(Chen BY et al, 2008; Wang et al, 2017)、台湾西海岸(Wang et al, 2016a; Araújo-Wang et al, 2022)和海南西南沿海(Li et al, 2016)等6个地方种群(图1), 不同种群数量差异较大, 且有下降趋势。此外, 在福建宁德、泉州湾、东山湾和广东汕头等海域还有少量个体分布(Wu et al, 2014)。最大的珠江口种群现存约2,555头(Chen T et al, 2010), 但该种群个体数量正以每年2.46%的速度下降, 75%的现存个体很可能在未来60年内消失(Huang et al, 2012)。北部湾大风江口种群在2011-2014年间估计为261头(Chen BY et al, 2016), 最近研究显示该种群数量正在快速下降(Lin et al, 2022)。台湾西海岸的种群数量也从2010年的74头下降至2017年的61头, 其中18%的繁殖个体丧失, 这对于小种群而言是极为致命的(Huang et al, 2014; Araújo-Wang et al, 2022)。另外, 其他小种群可能正处于局部灭绝边缘, 生存状况亟待关注(Chen et al, 2018)。
1.2 性别比例
中华白海豚绝大部分时间生活在水下, 且出水呼吸时极少露出腹部生殖裂, 野外调查时很难对其性别进行鉴定。因此, 国内外对中华白海豚种群性别比研究有限。目前主要有3种方法鉴别中华白海豚的性别: 一是野外观察中华白海豚的生殖裂, 但只有跃出水面露出生殖裂时才能鉴定; 二是通过分子生物学方法进行判别(Jefferson et al, 2012; Ming et al, 2022), 但目前活体采样方法应用于中华白海豚较少; 三是行为观察, 如雌性的哺育、抚幼行为, 雄性的弑婴行为等(Zheng et al, 2016), 是目前野外判断中华白海豚性别的主要手段, 但该方法也存在一定局限。例如, 广西北部湾的中华白海豚种群中已知性别的个体有40头(雌:雄 = 35:5), 其中87.5%的个体性别是基于抚幼行为判断得出①(①林啸鹏 (2020) 广西水域中华白海豚(Sousa chinensis)种群数据库的建立及其社会结构和栖息地使用研究. 硕士学位论文, 山东大学, 山东威海.), 对没有表现出抚幼行为的个体难以判断性别, 特别是对雄性个体鉴别较少, 因此该性别数据难以反映种群的真实性比。此外, Zeng等(2021)通过抚幼行为识别出厦门湾种群的13头雌性繁殖个体(2010-2015年), 约占同时期种群数量的20%。
1.3 年龄结构
在国外, 仅有孟加拉湾和泰国海域开展过种群的年龄结构研究。孟加拉湾的种群以青少年和亚成体为主(61%), 其次为成年个体(27%)和幼年个体(12%) (Smith et al, 2015); 泰国Donsak海域种群的成年个体(30.6%)和幼年个体(18.7%)比例略高, 青少年(30.1%)和亚成体(20.7%)比例略低(Jutapruet et al, 2015)。我国珠江口种群老年个体占比高达34.61%, 幼年个体占比22.40% (Guo et al, 2020); 厦门湾种群的幼年个体比例最低, 已从21世纪初的20.08%下降至10%②③(②翟飞飞 (2006) 厦门中华白海豚社会组织结构、行为和栖息地选择的初步研究. 硕士学位论文, 南京师范大学, 南京.③钟铭鼎 (2021) 厦门湾中华白海豚种群生态学研究. 硕士学位论文, 自然资源部第三海洋研究所, 厦门.)。此外, 曾千慧(2021)报道了2013-2019年间广东江门西黄茅海78头雌性中华白海豚的年龄结构, 其中约50%为中年母豚, 11.54%为老年母豚。
2 行为生态学
2.1 栖息地选择与利用
中华白海豚对栖息地的选择受栖息地的底质、理化以及生物等因子的影响。中华白海豚常出没于河口、岩礁等水域(Jefferson & Smith, 2016; Jefferson, 2018)。物理因子如水深、离岸距离、离河口距离和海水透明度等均会影响中华白海豚对栖息地的选择(刘宣, 2007④(④刘宣 (2007) 中华白海豚(Sousa chinensis)的栖息地选择. 硕士学位论文, 华南师范大学, 广州.); 张西阳等, 2015; 王新星等, 2018), 而表层水温、潮流方向对中华白海豚栖息地选择无明显影响(陈炳耀等, 2007; Li SS et al, 2018) (表1)。化学因子如盐度、化学需氧量、活性磷酸盐和无机氮在不同浓度范围对中华白海豚栖息地选择有不同影响。例如中华白海豚对盐度表现出较强的适应性, 可适应0-30‰范围内的盐度变化, 但会回避活性磷酸盐和无机氮浓度高的海域(Jefferson, 2000; 张西阳等, 2015)。生物因子也是影响中华白海豚栖息地选择的重要因素。一般认为河口区域叶绿素a含量高、食物资源更丰富, 因而海豚的利用程度更高(Chen M et al, 2016; Huang et al, 2019)。例如北部湾的中华白海豚在叶绿素a浓度大的海域目击率较高(Wu et al, 2017a)。在珠江口海域, 饵料鱼类密度在38-250 kg/km2时, 中华白海豚目击率随被捕食种密度增加而增加(王新星等, 2018)。Pan等(2016)构建了台湾西部新虎尾溪口的生态通道模型, 从生态系统营养关系和生态功能的视角, 指出饵料是影响中华白海豚分布的主要因素。此外, 不同环境因子也会相互影响, 进而对中华白海豚的栖息地选择起到直接或间接作用。例如, 水深通过影响饵料鱼类的移动, 进而影响中华白海豚的觅食效率和分布(Parra et al, 2004)。
表1 中华白海豚对栖息地环境因子的适宜范围
Table 1
环境因子 Environmental factors | 研究区域 Survey region | |||||
---|---|---|---|---|---|---|
大襟岛海域 Dajin Waters | 厦门湾 Xiamen Bay | 湛江水域 Zhanjiang Waters | 珠江口 Pearl River Estuary | 珠江西部河口 Western Pearl River Estuary | 马来西亚古晋湾 Kuching Bay, Malaysia | |
深度 Bathymetry (m) | 5-20 | 5-20 | 8.46 ± 5.13 | 5-15 | 5-20 | 0-10 |
离岸距离 Distance to the coastline (km) | 0-3 | 0-1 | 2.17 ± 2.14 | - | 0.1-3 | - |
离河口距离 Distance to river mouth (km) | 10-30 | - | - | - | 0-2 | 0-5 |
盐度 Salinity (‰) | 10-30 | - | - | 0-30 | - | - |
底层水温 Bottom water temperature (℃) | 19.3-28.6 | - | - | - | 17-19.5 | - |
表层水温 Sea surface temperature (℃) | 20-35 | - | - | * | - | - |
参考文献 Reference | 刘宣, 2007①(①刘宣 (2007) 中华白海豚(Sousa chinensis)的栖息地选择. 硕士学位论文, 华南师范大学, 广州.) | 陈炳耀等, 2007 | Liu et al, 2021 | 张西阳等, 2015 | 王新星等, 2018 | Kuit et al, 2019 |
数值表示研究给出的范围参考; -表示空缺; *表示该因子对中华白海豚分布无显著影响。
Numerical value represents the range reference given by the study; - for vacant; * indicates that this factor has no significant effect on the distribution of Sousa chinensis.
中华白海豚的栖息地利用模式存在时空差异(Jefferson, 2000; 刘明明, 2020)。由于中华白海豚喜好在半封闭海湾内活动, 雨水的丰枯和退涨潮使得湾内水文条件及食物分布发生短暂变动, 进而影响了白海豚对栖息地的利用模式(Kimura et al, 2012)。旱季与雨季相比, 厦门湾、台湾西海岸和雷州湾种群更偏好在近岸水域活动(Lin et al, 2014; 王先艳, 2016; Liu et al, 2021); 珠江口和北部湾种群则在远离岸边的深水区活动(Chen T et al, 2010; Li et al, 2018); 而大襟岛海域的中华白海豚在旱季和雨季没有显著的分布差异①。此外, 潮汐状况对中华白海豚的栖息地利用影响存在地理差异。如北部湾和台湾西海岸的中华白海豚在涨潮时对近岸海域利用较多(Lin et al, 2013; Li SS et al, 2018); 香港海域的中华白海豚在退潮期出现率更高(Parsons, 1998); 而厦门湾中华白海豚对潮汐变化没有表现出明显的响应(陈炳耀等, 2007)。
2.2 栖息地预测
了解和掌握动物的栖息地是就地保护与管理的基础。中华白海豚的栖息地预测主要使用了最大熵模型(maximum entropy models, MaxEnt)和人工神经网络(artificial neural network, ANN)模型(Chen et al, 2020; Lin ML et al, 2021)。Chen M等(2016)利用MaxEnt研究了北部湾中华白海豚的潜在栖息地, 预测北仑河口是潜在栖息地。Huang等(2019)也利用MaxEnt模型预测了北部湾的潜在栖息地, 推测雷州半岛西部到北部湾北部、红河河口到越南中部的东京湾西北部和海南岛西南海域均为潜在栖息地。Wu等(2021b)最近利用MaxEnt模型预测北部湾北仑河口、越南清化和荣市海域存在448.1 km2的潜在栖息地, 且潜在栖息地范围在旱季比雨季略有增加。Bao等(2019)通过MaxEnt模型预测了福建和广东沿海中华白海豚的关键栖息地和潜在分布区, 认为初级生产力和水深是影响中华白海豚分布的主要环境因子。Chen等(2020)利用MaxEnt模型预测出福建沿海存在约2,043.96 km2的潜在栖息地, 除莆田海域, 其余4个预测区域均已被证实存在中华白海豚分布。除被用于确定中华白海豚及其他物种的栖息地外, MaxEnt模型也为海洋保护规划提供依据(Wang et al, 2021)。例如, Wu等(2021a)利用MaxEnt模型估算出广东海域有90%以上的适宜栖息地尚未得到有效保护, 并提出了调整和扩建海洋自然保护区的建议。此外, Lin ML等(2021)通过构建人工反向传播神经网络模型(artificial back-propagation neural network, BP-ANN), 预测雷州半岛东部水域为潜在栖息地; 并通过实地调查证实了中华白海豚的存在, 显示了模型的应用潜力。无论是利用MaxEnt还是ANN, 预测结果准确性和可靠性均受到调查设计(Bao et al, 2019; Wang et al, 2021)和环境变量选择的影响(Chen M et al, 2016; Lin ML et al, 2021), 而野外的目击数据常被用于验证预测结果的可靠性。值得注意的是, 目击数据大多采集于观察条件良好的白天, 而海豚夜间分布模式可能与白天不同(Pine et al, 2017, 2018), 夜间数据的缺乏可能会造成验证结果的偏差(Lin ML et al, 2021)。
2.3 个体/社群行为
个体行为方面, 香港海域中华白海豚经常跟随拖网渔船伺机觅食, 因此对船只的躲避行为没有其他海豚明显(Parsons, 1998; Jefferson, 2000); 但相较于非育幼期, 雌性在育幼期间对船只的躲避行为更为频繁(Jefferson et al, 2012)。游戏行为是贯穿海豚整个生活史的重要行为, 对于海豚的捕食能力、认知能力、社会联系以及适应环境等具有重要促进作用(Kuczaj & Eskelinen, 2014)。翟飞飞(2006)①(①翟飞飞 (2006) 厦门中华白海豚社会组织结构、行为和栖息地选择的初步研究. 硕士学位论文, 南京师范大学, 南京.)通过联系度指数(association index, AI)发现厦门湾中华白海豚的游戏行为与旅行、抚幼及捕食行为之间联系密切。郑锐强(2014)构建了珠江口中华白海豚的行为谱, 定义了8大类共123种行为; 并解析了空中行为的生态学意义和接触幼豚行为的成因。李怡婷(2017)②(②李怡婷 (2017) 广东省江门市海域中华白海豚(Sousa chinensis Osbeck, 1765)行为谱的构建和行为模式的初步研究. 硕士学位论文, 山东大学, 山东威海.)依据中华白海豚的行为姿势、动作和环境3个要素, 构建了广东江门海域中华白海豚的PAE行为谱; 并统计了该海域中华白海豚行为的时间分配模式: 觅食是主要行为(60.49%), 其次是玩耍(17.87%)和休息(9.65%)。此外, 中华白海豚的一些特殊行为, 例如母豚对死亡幼豚的超常守护行为(Hung & Jefferson, 2004; Cheng et al, 2018); 对江豚(Neophocaena phocaenoides sunameri)幼仔的救助行为(Wang et al, 2013); 雄性个体的弑婴行为等(Zheng et al, 2016)也值得关注。
中华白海豚的社会行为是种群内部社会网络关系形成的重要因素, 包括交配行为、集体捕食及共同育幼等行为。交配行为有助于增强种群的基因交流; 集体捕食有助于提高捕食效率; 母豚之间的共同育幼行为则有助于提高幼仔的存活率和生存技能(Dungan et al, 2016; Würsig et al, 2016; 曾千慧, 2021)。集群是其社会行为的直接表现, 且存在季节变化。例如香港海域的中华白海豚集群多见于雨季(3-6月) (Jefferson et al, 2012)。此外, 幼豚对于种群内部的社会行为及社会关系网络维系至关重要(Dungan et al, 2012)。相较于非育幼群体, 育幼群体的集群规模显著增大, 种群个体之间联系也更紧密(Dungan et al, 2016; 刘明明, 2020)。中华白海豚种群内部的社会结构及行为会受到地理隔离和人为活动的影响。例如厦门湾、北部湾和珠江口的种群内部均存在社群分离现象, 并且社群之间交流较少(Dungan et al, 2012; Wang et al, 2015, 2016; 李闪闪, 2017③(③李闪闪 (2017) 厦门与北部湾海域中华白海豚社会网络结构研究. 硕士学位论文, 南京师范大学, 南京.))。
2.4 觅食行为
目前, 关于中华白海豚的觅食生态研究主要包括食性和觅食策略等方面。早期对中华白海豚食性研究, 多通过胃肠内含物中鱼类耳石形态辨别饵料物种。对厦门湾、北部湾、珠江口及香港海域搁浅中华白海豚胃含物的研究, 发现其食性复杂, 捕食鱼类至少包括鲈形目、鲱形目和鲽形目等在内的9目19科45种, 以及部分头足类(黄文几等, 1978; 贾晓平等, 2000; Barros et al, 2004; 王丕烈, 2012)。中华白海豚的饵料种类和组成存在地理差异, 主要与栖息地的饵料资源状况有关。例如在北部湾喜食斑鰶(Konosirus punctatus) (王丕烈, 2012); 在厦门湾喜食鲻鱼(Mugil sp.) (黄文几等, 1978); 在香港和珠江口水域喜食叫姑鱼(Johnius sp.)、棘头梅童鱼(Collichthys lucidus)、凤鲚(Coilia mystus)等(Barros et al, 2004)。值得关注的是, 近海渔业资源的衰退可能导致中华白海豚食物短缺, 进而影响到中华白海豚的食物结构(Brownell et al, 2019; Wang et al, 2020)。研究发现珠江口的中华白海豚胃含物中低营养级的鱼种增多, 食物多样性明显少于早期的研究结果, 表明其食物结构已发生变化(Lin WZ et al, 2021)。
中华白海豚的觅食策略受到饵料的营养能量、体型大小、栖息水层和饵料资源状况的影响。例如三娘湾的中华白海豚选择能量密度较高的鲱科和鳀科鱼类①(①余敏航 (2019) 三娘湾中华白海豚潜在饵料鱼能量密度研究. 硕士学位论文, 广西大学, 南宁.), 这可能与高能量密度的鱼类更能满足中华白海豚的能量需求有关。这种觅食策略与飞旋海豚(Stenella longirostris)和真海豚(Delphinus delphis)相似(Benoitbird, 2004; Spitz et al, 2010)。饵料体型大小对其觅食选择的影响主要跟中华白海豚吞咽的进食方式有关②(②王晓晓 (2018) 中华白海豚摄食生态学研究. 硕士学位论文, 汕头大学, 广东汕头.)。此外, 中华白海豚喜食表层、中上层和中下层的鱼类, 较少选择栖息在底层和岩礁等难以进入或觅食风险较大区域的鱼类(Lin WZ et al, 2021)。中华白海豚的觅食策略也有一定的灵活性。当饵料丰度降低时, 中华白海豚可能会扩大饵料种类范围或选择较大风险的海域捕食。例如进入浅滩、养殖区或者跟随渔船觅食, 这会增加其搁浅或被渔网缠绕的风险(Würsig et al, 2016)。
2.5 繁殖行为
中华白海豚的交配方式为混交制, 雌性大约9-10岁达到性成熟, 雄性稍晚1-2年, 身体完全发育成熟晚于性成熟时间(Jefferson, 2000; Jefferson et al, 2012)。雌性妊娠期约11个月, 每胎一仔, 哺乳期可受孕。繁殖间隔一般为2-3年, 存在地理差异, 香港海域最长(Jefferson et al, 2012), 其后依次为厦门湾(Zeng et al, 2021)、江门海域(曾千慧, 2021)和台湾西海岸(Chang et al, 2016), 这可能与不同地理种群面临的环境压力以及雌性年龄和幼仔存活率不同等有关(Robinson et al, 2017) (表2)。中华白海豚全年可交配, 全年有幼仔出生, 但春、夏两季高于秋、冬两季; 其中, 珠江口东部海域出生高峰期偏早(3-6月) (Jefferson et al, 2012), 而雷州湾偏晚(8-10月) (Xu et al, 2015)。幼仔存活率同样存在地理差异: 江门海域幼仔(0-1岁)存活率高达0.879 (曾千慧, 2021), 而台湾西海岸、香港和厦门湾幼仔存活率较低, 分别为0.667、0.61和0.6。
表2 中华白海豚不同地理种群的繁殖参数对比
Table 2
种群 Population | 研究时期 Research period | 繁殖间隔(年) Calving interval (year) | 出生高峰(月) Calving seasonality (month) | 粗出生率 Crude birth rate | 年补充率 Annual recruitment rate | 幼仔存活率(0-1岁) Calf survival (0-1 year) | 参考文献 Reference |
---|---|---|---|---|---|---|---|
厦门湾 Xiamen Bay | 2010-2015 | 4.27 ± 1.06 | 3-8 | 0.053 ± 0.025 | 0.028 ± 0.024 | 0.6 ± 0.392 | Zeng et al, 2021 |
珠江口/香港海域 Pearl River Estuary/Hong Kong | 1995-2009 | 5.21 ± 3.98 | 3-6 | - | - | 0.61 | Jefferson et al, 2012 |
江门海域 Jiangmen Sea | 2013-2019 | 3.50 ± 0.96 | 4-9 | 0.057 ± 0.01 | - | 0.879 ± 0.070 | 曾千慧, 2021 |
台湾西海岸 Taiwan West Coast | 2007-2011 | 3.26 ± 1.23 | 5-10 | 0.046 ± 0.02 | 0.041 ± 0.014 | 0.667 | Chang et al, 2016 |
雷州湾 Leizhou Bay | 2005-2012 | - | 8-10 | - | - | - | Xu et al, 2015 |
-表示空缺。
- for vacant.
中华白海豚幼仔死亡高峰期在其出生一年之内, 这可能与幼仔的健康状况、母豚的育幼经验、种内关系, 以及栖息地环境压力等内外因素有关(Jefferson et al, 2006; Robinson et al, 2017)。探究幼仔高死亡率的原因对该物种保护而言极为紧迫(Huang et al, 2012)。水体污染、繁忙航运及水下噪音等是已知幼仔高死亡率的主要外因, 例如珠江口和香港海域的死亡幼仔体内含有高浓度的重金属和有机污染物(Jefferson et al, 2006; Sun et al, 2022)。此外, 小种群的近亲繁殖和雄性的弑婴行为也可能是幼仔高死亡率的原因之一(Zheng et al, 2016)。
3 分子生态学
中华白海豚的分子生态学研究从微观层面揭示了该物种进化历史和遗传分化等宏观现象的本质。国内主要针对厦门湾、珠江口、北部湾和雷州湾海域的中华白海豚种群开展了分子遗传学研究, 不同的分析方法和样品数量导致研究结果也有所差异。Chen HS等(2008)通过对珠江口和厦门湾中华白海豚线粒体DNA (mitochondrial DNA, mtDNA)序列分析, 推测这两地中华白海豚种群可能存在基因交流。Chen LA等(2010)的研究则认为珠江口和厦门湾的中华白海豚种群已产生了显著的遗传分化。Lin等(2012)利用mtDNA和微卫星遗传标记, 进一步分析了厦门湾、珠江口和北部湾3地中华白海豚种群的遗传结构, 认为中华白海豚的整体遗传多样性水平较低, 种群间不存在基因交流。近年来, 国际合作进一步补充了国外中华白海豚的样品, 开展了更大分布范围内中华白海豚种群的遗传学研究。Dai等(2022)利用微卫星遗传标记, 发现中国厦门湾、泰国湾西部以及安达曼海3个地方的中华白海豚种群存在高水平的遗传分化, 地理隔离可能是造成这一现象的主要原因。Zhao等(2021)利用mtDNA标记, 对西太平洋至东印度洋的7个中华白海豚地理种群开展了种群遗传学研究, 结果表明西太平洋和东印度洋的中华白海豚达到种的分化水平, 西太平洋一侧的泰国湾和中国水域的中华白海豚达到亚种水平的分化, 该区域中华白海豚的准确分类有待进一步研究。
基因组研究也为中华白海豚适应近岸水生环境提供了新的视角。Gui等(2013)首次对中华白海豚的白细胞转录组进行组装, 鉴定出大量与免疫反应和适应进化相关的基因家族。Ming等(2019a)绘制了中华白海豚首个基因组草图, 分析了中华白海豚可能适应近岸水生环境的物种特异基因家族, 为今后在基因组水平上探究该物种的生态适应机制提供了基础数据库。此后, Ming等(2019b)进一步对中华白海豚的基因组序列进行组装, 获得了高质量的基因组信息, 促进了在基因组水平上对该物种的遗传、进化以及生态保护研究。另外, 中华白海豚的全基因组研究也为开发治疗人类心血管疾病药物提供了重要参考(Jia et al, 2019)。Zhang等(2020)基于全基因组测序和群体重测序, 对中华白海豚的染色体进化和种群环境适应性演化进行了探讨, 揭示了该物种对气候变化的高度敏感性及种群的脆弱性。
4 面临的威胁与保护现状
4.1 涉海工程
近几十年来, 各类涉海工程(如围填海、桥梁、海上风电场等)累计蚕食了大量的沿岸水域, 导致全球中华白海豚栖息地面临不同程度的丧失和破碎化的威胁(Karczmarski et al, 2017; Wu et al, 2017b)。涉海工程可能会导致自然海岸线减少、栖息地生态系统功能衰退以及饵料生物改变等, 进而对中华白海豚的栖息地产生长期或永久性影响(Marcotte et al, 2015; Huang et al, 2022)。自20世纪70年代开始, 台湾西海岸、厦门湾、北部湾和珠江口伶仃洋因围填海, 分别丧失了222、119.95、129.6和344.1 km2中华白海豚的自然栖息地(Karczmarski et al, 2017; Wang et al, 2017; Wu et al, 2017b; 王新星等, 2022)。此外, 跨海大桥、海上风电场、清淤等涉海工程也会加速中华白海豚栖息地破碎化的进程(Pine et al, 2017; Wang et al, 2019)。
4.2 水下噪声
中华白海豚听觉系统灵敏, 其求偶、繁殖、捕食及个体交流等活动高度依赖水下声信号, 因此需特别关注水下噪声对中华白海豚的影响(Li et al, 2015)。航运、水下爆破、工程打桩等产生的水下噪声, 以及工程运营期的噪声都可能会影响到中华白海豚的行为, 甚至导致死亡。有研究显示, 中华白海豚会回避噪声污染严重的栖息地(Wang et al, 2014; Li SH et al, 2018)。香港海域的中华白海豚也很少出现在施工密集的水域(Piwetz et al, 2021)。此外, 水下噪声也会掩盖栖息地内中华白海豚饵料生物的声信号, 进而导致中华白海豚对栖息地的利用模式发生变化。广西三娘湾的观豚旅游快艇产生的水下噪声影响了中华白海豚对栖息地的利用(Li et al, 2015); 台湾西海岸海上风电场建设和运营后, 该海域中华白海豚遇见率显著下降(Huang, 2022)。
4.3 水体污染
不同于一般物理伤害, 水体污染很难及时发现并快速改善, 对中华白海豚具有长期累积性影响(Jefferson et al, 2016; 王先艳等, 2021)。水体污染一方面会引起中华白海豚的栖息地质量下降。例如有机污染物、塑料垃圾和重金属污染, 以及近岸水域富营养化等水体污染问题, 在厦门湾、珠江口和北部湾等中华白海豚重要的栖息水域均有报道(马玉等, 2011; 张典等, 2020; Xie et al, 2021)。生活污水也是影响泰国Donsak海域和马来西亚Matang海域中华白海豚栖息地质量的重要原因之一(Jutapruet et al, 2015; Kuit et al, 2019)。另一方面, 由于食物链传递和生物富集作用, 高浓度的污染物会诱发多种疾病, 甚至对中华白海豚的生殖和发育造成威胁。有研究发现, 重金属汞(Hg)对中华白海豚的潜在威胁很大(Barros et al, 2004; Gui et al, 2017)。多环芳烃和多氯联苯能通过胎盘转移, 对中华白海豚的生殖和胎儿发育具有潜在影响(Zhu et al, 2014; Yu et al, 2020; Zhang et al, 2021)。
4.4 渔业活动
4.5 保护现状
目前, 加强立法和设立海洋保护区是保护中华白海豚及其栖息地的重要方式。中华白海豚于1988年被列为我国国家一级重点保护野生动物, 1991年被《濒危野生动植物物种国际贸易公约》(the Convention on International Trade in Endangered Species of Wild Fauna and Flora, CITES)列为附录I物种。孟加拉国于2014年设立了Swatch of No-Ground (SoNG)海洋保护区以保护中华白海豚及其他物种(Smith et al, 2015)。我国大陆先后设立了厦门和珠江口2个国家级自然保护区, 以及江门、汕头、湛江、潮州、饶平等5个省级或市级保护区, 广西合浦儒艮国家级自然保护区也将中华白海豚列为主要保护对象, 以上保护区总面积约11,304 km2; 香港特别行政区则通过设立海洋公园的形式来划定保护范围。此外, 我国于2014年成立了“中华白海豚保护联盟”, 初步构建了我国中华白海豚协同保护网络, 并发布了《中华白海豚保护行动计划(2017-2026)》, 这是我国中华白海豚保护工作的指导性文件。各地方政府也越来越重视中华白海豚的保护, 如厦门市、漳州市和泉州市建立了“厦-漳-泉中华白海豚保护工作联动机制”, 加强三地的协同保护和管理, 还研究制定了相应措施(如加强涉海工程监管、涉海工程施工期的声学驱赶、饵料资源的增殖放流等)来减轻上述威胁对中华白海豚及其栖息地的影响(Wang et al, 2015; 王先艳等, 2021)。
5 研究展望
5.1 建立统一的动态基线数据库
目前, 全球范围内中华白海豚的种群动态尚有一些问题亟待解决: (1)国内外尚有一些种群基础数据不足, 没有对同时期全球范围内的中华白海豚采用统一方法进行调查和统计(Jefferson & Smith, 2016), 不同团队的调查方法、调查范围和努力量有差异, 导致难以对调查结果进行比较。(2)缺乏长期连续的种群动态监测, 短期监测对生活史较长的中华白海豚种群动态和保护成效评估有限。(3)个体识别主要依靠人工识别, 大种群(如珠江口种群)开展个体识别工作量非常大。上述问题会影响该物种现状的准确评估和有效保护。因此, 有必要总结和提出针对中华白海豚的统一调查方法或标准, 加强地区间合作, 开展长期的连续监测, 并建立统一的种群动态基线数据库; 结合人工智能技术开发中华白海豚个体自动识别程序, 以提高个体识别效率。此外, 建立一个国家层面的中华白海豚数据共享平台, 包括个体识别、种群数量与分布、栖息地的水文与地形, 以及栖息地内航运、渔业、涉海工程等数据, 并制定相应的数据收集、审核、管理与使用规范, 可为国家层面中华白海豚的保护决策提供科学依据(Huang et al, 2022)。
5.2 构建栖息地识别及保护评价体系
识别关键栖息地和潜在栖息地有助于掌握中华白海豚分布现状和未来变化趋势。目前主要是针对中华白海豚出现的“热点”区域的监测, 而没有被调查的海域也许会弥补当前已知生境退化的需求, 基线信息的缺乏可能导致对这些栖息地识别存在偏差。因此有必要依据栖息地选择机制, 参照各地种群的历史分布信息, 结合遥感技术, 构建完善的栖息地识别和评价体系, 对当前的关键栖息地和潜在栖息地进行识别和分级管理。
一些已设立保护区的种群数量仍然呈现下降趋势(Zeng et al, 2020), 建议对现有的中华白海豚保护区的管理成效进行评估, 对海豚分布有明显变化的保护区进行优化调整。例如, 厦门湾、珠江口和北部湾海洋保护区和中华白海豚现有和潜在分布范围重叠度较低, 早年规划的保护区难以起到有效保护作用(Wang et al, 2015; Huang et al, 2019; Wu et al, 2021a)。此外, 随着更多的水域重新发现中华白海豚, 如在海南水域的种群(Li et al, 2016), 因此有必要在全国范围内对中华白海豚保护区域进行系统规划, 将更多的种群及关键栖息地纳入保护范围, 并构建生态廊道, 保障种群在“热点”区域间的连通性。
5.3 从生态系统层面开展栖息地选择机制研究
其次, 在沿海经济高速发展的背景下, 上述各种威胁因子将会长期存在, 但目前的栖息地选择研究多关注自然因素的影响, 渔业活动、涉海工程、航运、海洋污染等人为因素很少被纳入研究, 各类人为活动对中华白海豚的长期累积性影响仍不清楚(Marcotte et al, 2015)。
最后, 栖息地选择的影响因子之间的相互作用及其相对重要性仍不清楚, 各类因子(如潮汐、洋流、水质、地形地貌、其他生物及人为活动等)如何直接或间接影响中华白海豚的栖息地选择尚待深入研究。因此, 有必要对栖息地内的水文要素、饵料资源、水下噪声等影响因素进行长期监测, 进而评估栖息地生态系统的健康状况。在了解和掌握中华白海豚栖息地选择机制的基础上, 对中华白海豚的受损栖息地开展生态修复, 拓展生存空间, 这对一些栖息地范围狭小的中华白海豚种群的保护尤为重要。
5.4 揭示物种进化、适应与濒危的分子机制
鲸目动物是研究生物从陆地环境向水生环境适应进化的模式动物, 中华白海豚独特的进化历史和重要的生态功能, 为理解水生生物对近岸水生环境的生态适应的遗传基础提供了可能(Ming et al, 2019a)。开展中华白海豚分子生态学研究, 可为该物种的分类、种质资源评价、进化及濒危机制提供科学依据(Zhang et al 2020; Zhao et al, 2021)。目前, 中华白海豚的分子生态学研究尚不充分。例如, 中华白海豚体色变化与近岸分布的分子机制尚不清楚; 不同种群间的隔离程度和灭绝风险也未被详细评估。因此, 有必要协调现有研究力量, 建立一套完整的样品收集与共享机制, 构建中华白海豚遗传资源库, 结合其进化历史和栖息地环境变化, 探究自然选择-生态影响-遗传进化之间的联系, 可为保护中华白海豚的遗传多样性提供科学参考。
5.5 全球海洋环境变化背景下的研究前瞻
海洋变暖的速度、强度和持续时间预计在未来将继续增加, 鲸类动物的丰度和分布极易受到全球气候变化的影响(Kershaw et al, 2021)。例如, 加那利群岛(Canary)和马德拉群岛(Madeira)海域的短肢领航鲸(Globicephala macrorhynchus)、瓶鼻海豚(Tursiops truncatus)和灰海豚(Grampus griseus)均已表现出对气候变化的高度脆弱性(Sousa et al, 2021)。另一方面, 过去几十年, 沿海城市加速发展, 导致人类与海洋生物竞争生存空间(Marcotte et al, 2015)。但中华白海豚在气候变化、沿海城市发展及人口增加等全球变化情景下的脆弱性研究较少(Lu et al, 2023), 种群未来的变化趋势尚不清楚。为有效应对全球海洋环境变化的影响, 有必要在中华白海豚分布国家间建立科研合作平台及保护管理网络。
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Distribution and habitat characteristics of three sympatric cetacean species in the coastal waters of Matang, Perak, Peninsular Malaysia
DOI:10.1002/aqc.v29.10 URL [本文引用: 2]
Indo-Pacific humpback dolphins (Sousa chinensis) in the Moyang River Estuary: The western part of the world’s largest population of humpback dolphins
DOI:10.1002/aqc.v29.5 URL [本文引用: 3]
First record of the Indo-Pacific humpback dolphins (Sousa chinensis) southwest of Hainan Island, China
DOI:10.1186/s41200-016-0005-x URL [本文引用: 4]
Potential impacts of shipping noise on Indo-Pacific humpback dolphins and implications for regulation and mitigation: A review
DOI:10.1111/1749-4877.12304
PMID:29316222
[本文引用: 2]
Shipping noise is a widespread and relatively loud sound source among human-induced underwater sounds. The impacts of shipping noise are of special concern for Indo-Pacific humpback dolphins (Sousa chinensis), as they inhabit shallow and nearshore habitats and are highly dependent on sound for survival. This study synthesizes our current understanding of the potential impacts of shipping noise on Indo-Pacific humpback dolphins combined with knowledge on sound production and hearing of these animals and the impacts of noise on other whales and dolphins. For further protection and management of Indo-Pacific humpback dolphins and their habitats, shipping noise should be regulated and mitigated to modify sound from ships, to reduce overall noise levels, and to set more marine protected areas (MPAs) covering most Indo-Pacific humpback dolphin habitats with seasonal and geographical restrictions to avoid ensonification of shipping noise. The emphasis for future research should be on obtaining more baseline information about the population distribution, sound production, hearing capabilities at the population level, behavior, and stress hormones of the humpback dolphins under different noise conditions or under different noise-producing activities, and/or in high-noise areas compared with relatively quiet areas, and the noise characteristics of ships of different types, sizes and speeds.© 2018 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.
Mid- to high-frequency noise from high-speed boats and its potential impacts on humpback dolphins
DOI:10.1121/1.4927416
PMID:26328710
[本文引用: 2]
The impact of noise made by vessels on marine animals has come under increased concern. However, most measurements on noise from vessels have only taken into account the low-frequency components. For cetaceans operating in the mid- and high-frequencies, such as the Indo-Pacific humpback dolphin (Sousa chinensis), mid- to high-frequency noise components may be of more concern, in terms of their potential impacts. In this study, noise made by a small high-speed boat was recorded using a broadband recording system in a dolphin watching area focusing on the effects on humpback dolphins in Sanniang Bay, China. The high-speed boat produced substantial mid- to high-frequency noise components with frequencies to >100 kHz, measured at three speeds: ∼40, 30, and 15 km/h. The noise from the boat raised the ambient noise levels from ∼5 to 47 decibels (dB) root-mean-square (rms) across frequency bands ranging from 1 to 125 kHz at a distance of 20 to 85 m, with louder levels recorded at higher speeds and at closer distances. To conclude, the noise produced by the small high-speed boat could be heard by Sousa chinensis and therefore potentially had adverse effects on the dolphins.
Seasonal, lunar and tidal influences on habitat use of Indo-Pacific humpback dolphins in Beibu Gulf, China
Modelling habitat suitability of the Indo-Pacific humpback dolphin using artificial neural network: The influence of shipping
DOI:10.1016/j.ecoinf.2021.101274 URL [本文引用: 4]
Tidal influences on the habitat use of Indo-Pacific humpback dolphins in an estuary
DOI:10.1007/s00227-013-2187-7 URL [本文引用: 1]
Seasonal distribution of Indo-Pacific humpback dolphins at an estuarine habitat: Influences of upstream rainfall
DOI:10.1007/s12237-014-9886-2 URL [本文引用: 1]
Differentiated or not? An assessment of current knowledge of genetic structure of Sousa chinensis in China
Prey decline leads to diet shift in the largest population of Indo-Pacific humpback dolphins?
DOI:10.1111/1749-4877.12548
PMID:33880881
[本文引用: 3]
The Pearl River Delta (PRD) region on the southeast coast of China has long been known as a highly productive fishing ground. Since the late 1980s, fishing pressure in the PRD has been intense, which warrants concerns of potential fishery-related impacts on the food resources and foraging ecology of apex marine predators in this region, such as the Indo-Pacific humpback dolphin (Sousa chinensis). In this study, we examined 54 stomachs with food remains, collected from beached carcasses of humpback dolphins recovered during fifteen years between 2003 and 2017. The 6043 identified prey items represent 62 teleost taxa, primarily small estuarine fish, but also larger reef fish. The dolphins appear to be opportunistic foragers, hunting across the water-column, with preference for shoaling and meaty fishes (e.g. Chrysochir aureus IRI% = 38.6%, Johnius belangerii IRI% = 23.1%, Mugil cephalus IRI% = 14.0%). Our findings suggest a dietary shift in recent years, from primarily demersal (as previously reported) to greater intake of neritic and pelagic fish. Dolphin foraging group size has decreased in recent years, which corresponds with declining size and numbers of prey items retrieved from dolphin stomachs. We suggest that these are indicators of declining food resources. Faced with a shortage of preferred prey, humpback dolphins may have broadened their dietary spectrum to maintain their daily energy intake, while their foraging group size decreased in response to the altered tradeoff between the costs and benefits of group foraging. This article is protected by copyright. All rights reserved.This article is protected by copyright. All rights reserved.
Low survivals and rapid demographic decline of a threatened estuarine delphinid
DOI:10.3389/fmars.2022.782680
URL
[本文引用: 4]
Beibu Gulf’s (BBG) Indo-Pacific humpback dolphins present both a genetic differentiation and phenotypical differences from conspecifics from other areas of the South China Sea. Given the recent urbanization and industrialization in southern China, humpback dolphins from the BBG warrant conservation attention. However, this population’s demographic trend is unclear, making it hard to take conservation measures. To assess the population status of humpback dolphins in the BBG, photo-identification surveys were conducted between 2015 and 2019 in the inshore region surrounding the Dafeng River Estuary, which represents the most urbanized and industrialized coastal area of the BBG region. Robust design modeling suggested a constant survival for the female adults (0.89, 95% CI: 0.83–0.94). In comparison, the survival of the juvenile and sex-undetermined adults dropped from 0.92 (95% CI: 0.75–0.98) in 2015 to 0.86 (95% CI: 0.71–0.94) in 2016 and bounced back to 0.89 (95% CI: 0.80–0.94) in 2018. The low level of survival may justify the rapid decline in the annual population size from 156 (95% CI: 133–184) in 2015 to 102 (95% CI: 98–107) in 2019. We found little impact of emigration on the dolphin demographic process. Instead, the low and fluctuating survivals, although with overlapping confidence intervals, seemingly suggested a presence of strong marine stressor(s). Our study highlighted that obtaining high-resolution data is essential to improving our understanding of the demographic dynamics. Moreover, the anthropogenic stress in the BBG region should be quantitatively studied in both temporal and spatial perspectives, to help depict the ecological response of the dolphins to anthropogenic activities.
Studies on Grouping Behavior and Habitat Protection of Indo-Pacific Humpback Dolphins (Sousa chinensis)
中华白海豚集群行为和栖息地保护研究
Spatiotemporal variations in fine-scale habitat use of the world’s second largest population of humpback dolphins
DOI:10.1093/jmammal/gyab001
URL
[本文引用: 2]
We assessed habitat use by the population of Indo-Pacific humpback dolphin, Sousa chinensis, in the waters off Zhanjiang, China, by performing boat-based surveys between 2013 and 2018. In total, we gathered 253 sightings of humpback dolphins. To assess habitat use of humpback dolphins within the study area, we measured two spatial metrics at each sighting site: WDT (tide-calibrated water-depth) and DS (distance to the nearest shore). Results showed that dolphins mainly were observed in shallow (WDT: 8.46 ± 5.13 m, mean ± SD) and inshore (DS: 2.17 ± 2.14 km) waters. Their preference of inhabiting shallow waters was more apparent during the wet season (April–September) than during the dry season (October–March); however, they were encountered in waters much closer to shore during the dry season than the wet season. By weighting survey effort, our sighting density maps further confirmed that humpback dolphins changed their habitat use between wet and dry seasons. Such spatiotemporal variations in dolphin habitat use might be associated with spatiotemporal movements of their prey. Our findings provide insights into variations in fine-scale habitat use of inshore apex predators, and also assist to designate proper conservation measures for these vulnerable animals.
Distribution and abundance of Chinese white dolphins (Sousa chinensis) in Xiamen
厦门中华白海豚的分布和数量
Anthropogenic footprints are invading global habitats of Indo-Pacific humpback dolphins
DOI:10.1016/j.geosus.2022.12.001 URL [本文引用: 1]
Water quality assessment and influencing factors analysis of Chinese White Dolphin Reserve in Dajin Island of Pearl River Estuary
珠江口大襟岛中华白海豚保护区水质评价及影响因素分析
Mapping cumulative impacts on Hong Kong’s pink dolphin population
Molecular footprints of inshore aquatic adaptation in Indo-Pacific humpback dolphin (Sousa chinensis)
DOI:10.1016/j.ygeno.2018.07.015 URL [本文引用: 2]
The genome resources for conservation of Indo-Pacific humpback dolphin, Sousa chinensis
DOI:10.1038/s41597-019-0078-6
[本文引用: 1]
The Indo-Pacific humpback dolphin (Sousa chinensis), is a threatened marine mammal and belongs to the First Order of the National Key Protected Wild Aquatic Animals List in China. However, limited genomic information is available for studies of its population genetics and biological conservation. Here, we have assembled a genomic sequence of this species using a whole genome shotgun (WGS) sequencing strategy after a pilot low coverage genome survey. The total assembled genome size was 2.34 Gb: with a contig N50 of 67 kb and a scaffold N50 of 9 Mb (107.6-fold sequencing coverage). The S. chinensis genome contained 24,640 predicted protein-coding genes and had approximately 37% repeated sequences. The completeness of the genome assembly was evaluated by benchmarking universal single copy orthologous genes (BUSCOs): 94.3% of a total 4,104 expected mammalian genes were identified as complete, and 2.3% were identified as fragmented. This newly produced high-quality assembly and annotation of the genome will greatly promote the future studies of the genetic diversity, conservation and evolution.
The landscape of genome-wide and gender-specific microsatellites in Indo-Pacific humpback dolphin and potential applications in cetacean resource investigation
DOI:10.3390/jmse10060834
URL
[本文引用: 1]
Microsatellites are one of the important genome characterizations that can be a valuable resource for variety identification, genetic diversity, phylogenetic analysis, as well as comparative and conservation genomics research. Here, we developed comprehensive microsatellites through genome-wide mining for the threatened cetacean Indo-Pacific humpback dolphin (Sousa chinensis). We found 87,757 microsatellites with 2–6 bp nucleotide motifs, showing that about 32.5 microsatellites per megabase comprises microsatellites sequences. Approximately 97.8% of the markers developed in this study were consistent with the published identified markers. About 75.3% microsatellites were with dinucleotide motifs, followed by tetranucleotide motifs (17.4%), sharing the same composition pattern as other cetaceans. The microsatellites were not evenly distributed in the S. chinensis genome, mainly in non-coding regions, with only about 0.5% of the markers located in coding regions. The microsatellite-containing genes were mainly functionally enriched in the methylation process, probably demonstrating the potential impacts of microsatellites on biological functions. Polymorphic microsatellites were developed between different genders of S. chinensis, which was expected to lay the foundation for genetic diversity investigation in cetaceans. The specific markers for a male Indo-Pacific humpback dolphin will provide comprehensive and representative male candidate markers for sex identification, providing a potential biomolecular tool for further analysis of population structure and social behavior of wild populations, population trend evaluation, and species conservation management.
The trophic significance of the Indo-Pacific humpback dolphin, Sousa chinensis, in Western Taiwan
DOI:10.1371/journal.pone.0165283 URL [本文引用: 2]
The Indo-Pacific humpback dolphin, Sousa chinensis (Osbeck, 1765), in Australian waters: A summary of current knowledge
DOI:10.1578/AM.30.1.2004.197 URL [本文引用: 3]
The behaviour of Hong Kong’s resident cetaceans the Indo-Pacific humpback dolphin and the finless porpoise
Abundance and residency dynamics of the Indo-Pacific humpback dolphin, Sousa chinensis, in the Dafengjiang River Estuary, China
DOI:10.1111/mms.v36.2 URL [本文引用: 1]
Investigating the spatiotemporal variation of fish choruses to help identify important foraging habitat for Indo-Pacific humpback dolphins, Sousa chinensis
DOI:10.1093/icesjms/fsx197
URL
[本文引用: 1]
Given the common physical overlapping between coastal developments and important marine mammal habitats, there is a need to identify potentially important foraging grounds for dolphins when informing marine spatial planning and management of underwater noise. Hydrophones were deployed at four locations either side of the mainland China–Hong Kong Special Administrative Region border to monitor the presence of soniferous fishes; a key prey item for Indo-Pacific humpback dolphins. Five distinct chorus-types were identified; each showing spatiotemporal variability. Each chorus-type was assumed to represent a separate species. Chorus-type diversity also differed between sites, with SP4 and SP5 types only being detected within Hong Kong waters where bottom trawling is illegal. Chorus-type SP1 was only detected at the recording sites in mainland Chinese waters. Call rates and chorus duration were highest during the spring and summer months. Given these dolphins show a predator-prey relationship, these data provide new information on the local fish communities at a much finer-scale than fish landing records and a baseline of fish activity in an environment that is challenging to explore. Overlaid with acoustic detections of foraging dolphins, these data form a basis for identifying potentially important foraging habitats that should be afforded the highest priority for protection.
Fine-scale habitat use in Indo-Pacific humpback dolphins, Sousa chinensis, may be more influenced by fish rather than vessels in the Pearl River Estuary, China
DOI:10.1111/mms.2017.33.issue-1 URL [本文引用: 2]
Effects of coastal construction on Indo-Pacific humpback dolphin (Sousa chinensis) behavior and habitat-use off Hong Kong
DOI:10.3389/fmars.2021.572535
URL
[本文引用: 1]
Construction-related loss of habitat, degradation of existing habitat, noise pollution, and vessel activity are growing issues for Indo-Pacific humpback dolphins (Sousa chinensis) that occur in the shallow, near-shore, highly industrialized waters off Lantau Island, Hong Kong. We studied the occurrence of dolphins in discrete locations, fine-scale movement patterns, and dolphin behavioral activity states. Potential explanatory variables varied and included year, season, time of day, dolphin group size and behavioral activity state, proximity to construction activity, and vessel type and number. Land-based observations and theodolite tracking of dolphins and vessels were conducted from seven locations to the north of Lantau Island, Hong Kong, and marine construction activities near survey sites were identified. A total of 636 groups of dolphins were recorded, totaling 150.91 h of tracking, from 405 days of observation effort. Hurdle models were used to analyze dolphin occurrence, multivariate generalized additive models were used to analyze fine-scale movement patterns, and log-likelihood ratio and binomial z score post hoc tests were used to analyze behavioral activity states. Dolphin occurrence was lower in historically important areas near long-term, low-intensity construction activity, and dolphin swimming speed was higher in response to vessel presence. Overall, foraging and traveling were the most frequently observed behavioral activity states and resting behavior was observed off only one location that was not in proximity to construction activities. Temporal overlap in adjacent marine construction areas may displace animals for extended periods and nearby ecologically similar habitats should be identified and designated as marine protected areas to mitigate effects of such disturbance.
Abundance estimates of Indo-Pacific humpback dolphins (Sousa chinensis) in Kuching Bay, East Malaysia
DOI:10.1578/AM.42.4.2016.462 URL [本文引用: 3]
Female reproductive success and calf survival in a North Sea coastal bottlenose dolphin (Tursiops truncatus) population
DOI:10.1371/journal.pone.0185000 URL [本文引用: 2]
A List of the Marine Mammals of the World
Climate change vulnerability of cetaceans in Macaronesia: Insights from a trait-based assessment
DOI:10.1016/j.scitotenv.2021.148652 URL [本文引用: 1]
Prey selection by the common dolphin: Fulfilling high energy requirements with high quality food
DOI:10.1016/j.jembe.2010.05.010 URL [本文引用: 1]
Long-term increase in mortality of Indo-Pacific humpback dolphins (Sousa chinensis) in the Pearl River Estuary following anthropic activities: Evidence from the stranded dolphin mortality analysis from 2003 to 2017
DOI:10.1016/j.envpol.2022.119526 URL [本文引用: 1]
Fine-scale habitat modeling of a top marine predator: Do prey data improve predictive capacity?
DOI:10.1890/07-1455.1 URL [本文引用: 1]
Mark-recapture analysis of the critically endangered eastern Taiwan Strait population of Indo-Pacific humpback dolphins (Sousa chinensis): Implications for conservation
Preliminary observation on the living habits of Chinese white dolphin in Xiamen Harbor
厦门港中华白海豚生活习性初步观察
Relationships between environmental factors and the distribution of Indo-Pacific humpback dolphins (Sousa chinensis) in the western Pearl River Estuary, China
珠江西部河口中华白海豚分布与环境因子的关系
Long-term changes in habitat use of Indo-Pacific humpback dolphins (Sousa chinensis) in response to anthropogenic coastline shift in Lingding Bay of Pearl River Estuary, China
珠江口伶仃洋中华白海豚栖息地利用对海岸线等变迁的响应
Study on selection and utilization of Chinese white dolphin in Xiamen West Port
中华白海豚对厦门西港的选择利用研究
Mapping habitat protection priority over a marine ecoregion under information gaps
DOI:10.1111/ddi.v27.2 URL [本文引用: 2]
Assessment of fishery resources using environmental DNA: Small yellow croaker (Larimichthys polyactis) in East China Sea
DOI:10.1371/journal.pone.0244495
URL
[本文引用: 2]
Species distribution monitoring and biomass assessment are crucial for fishery management and resource conservation. However, traditional methods such as motor trawling are costly and less effective than the novel environmental DNA (eDNA) approach. This study employs eDNA approach to investigate horizontal and vertical distributions of small yellow croaker (Larimichthys polyactis), an economically important species, in the East China Sea. The analysis of 171 eDNA samples collected from 44 stations using the species-specific primers and Taqman probe suggests a presence of small yellow croaker at 28 sampling layers in 44 stations. Significant differences in croaker eDNA concentrations were revealed among sampling stations and layers, consistent with previous findings through motor-trawl capture offshore and nearshore ichthyoplakton surveys, indicating small yellow croaker exhibits strong regional distribution and layer preference. In addition, we found a high eDNA concentration of small yellow croaker in the surface waters beyond the motor-trawl prohibition line, which confirms spawning grounds have been expanded from nearshore to offshore areas. Such expansion of spawning grounds could be a response by small yellow croaker to stressors such as overfishing, climate change, and nearshore environment contamination. To identify environmental variables potentially associated with small yellow croaker presence and absence, we conducted a correlation analysis between eDNA concentration and environmental variables, and the results provide a guideline for further investigation of fishery resources in the future. In conclusion, this study demonstrates the power of the eDNA approach in monitoring small yellow croaker at extensive geographic scales. The developed protocols and the findings are expected to assist in long-term monitoring and protection programs and benefit sustainable fishery in small yellow croaker.
Investigation on the distribution of Sousa chinensis in the coastal waters between Xiamen and the Pearl River Estuary
厦门至珠江口间沿岸海域中华白海豚分布的调查研究
Two separated populations of the Indo-Pacific humpback dolphin (Sousa chinensis) on opposite sides of the Taiwan Strait: Evidence from a larger-scale photo-identification comparison
DOI:10.1111/mms.12257 URL [本文引用: 2]
Indo-Pacific humpback dolphins (Sousa chinensis) assist a finless porpoise (Neophocaena phocaenoides sunameri) calf: Evidence from Xiamen waters in China
DOI:10.1644/13-MAMM-A-064.1 URL [本文引用: 1]
Social organization and distribution patterns inform conservation management of a threatened Indo-Pacific humpback dolphin population
DOI:10.1093/jmammal/gyv097 URL [本文引用: 3]
Seasonal group characteristics and occurrence patterns of Indo-Pacific humpback dolphins (Sousa chinensis) in Xiamen Bay, Fujian Province, China
DOI:10.1093/jmammal/gyw002
URL
Monthly field surveys were conducted between August 2010 and July 2015 to explore seasonal group characteristics and occurrence patterns of Indo-Pacific humpback dolphins (Sousa chinensis) in Xiamen Bay, China. Dolphins formed larger groups in winter and spring (dry seasons) than in summer and autumn (wet seasons; U = 1,564.00, P < 0.001). Sighting encounter rates were higher during the wet season than during the dry season (U = 181.00, P < 0.001), while individual encounter rates were not significantly different between seasons (F = 0.494, d.f. = 3, P = 0.688). Dolphin sightings and the foraging events were mainly found in inner harbors (Western Harbour and Tongan Bay) during the dry seasons and in peripheral areas (Jiulong River Estuary, Wuyu, and Dadeng-Xiaodeng) during the wet seasons. Seasonal occurrence patterns may be associated with the seasonal prey shifts between these different environments.
Long-term changes in the distribution and core habitat use of a coastal delphinid in response to anthropogenic coastal alterations
DOI:10.1002/aqc.v27.3 URL [本文引用: 3]
Indo-Pacific humpback dolphins (Sousa chinensis) in Xiamen Bay: Threats and conservation
厦门湾中华白海豚: 面临的威胁与保护对策
Soundscape of an Indo-Pacific humpback dolphin (Sousa chinensis) hotspot before windfarm construction in the Pearl River Estuary, China: Do dolphin engage in noise avoidance and passive eavesdropping behavior?
DOI:10.1016/j.marpolbul.2019.02.013 URL [本文引用: 1]
Assessing the underwater acoustics of the world’s largest vibration hammer (OCTA-KONG) and its potential effects on the Indo-Pacific humpbacked dolphin (Sousa chinensis)
DOI:10.1371/journal.pone.0110590 URL [本文引用: 1]
Cetacean societies: Field studies of dolphins and whales
DOI:10.2307/3802917 URL [本文引用: 1]
Suitable habitat predition for the Indo-Pacific humpback dolphin in Guangdong, China
Prediction of suitable habitats for the Indo-Pacific humpback dolphin (Sousa chinensis) in the Beibu Gulf of China and Vietnam
DOI:10.5343/bms.2019.0116
URL
[本文引用: 1]
The Indo-Pacific humpback dolphin (Sousa chinensis) is a threatened coastal flagship species in Asian marine ecosystems, but the distribution of its suitable habitat remains unclear. In the present study, we characterized habitat relationships and predicted potential suitable\n habitats for humpback dolphins in the Beibu Gulf of China and Vietnam. Maximum entropy modeling identified six discontinuous areas in the Beibu Gulf, with a total area of 4396.8 km2, as suitable habitats for humpback dolphins. Of these, three suitable habitats covering 3948.7 km2\n were known habitats, and three others covering an area of 448.1 km 2 at the border of China and Vietnam or in Vietnamese waters (Beilun River Estuary, Qinghua, and Rongshi) were newly identified. Exploratory line-transect surveys are strongly recommended to determine whether dolphins are present\n in these three areas. The predicted suitable habitat showed seasonal variation, which increased slightly in the dry season compared with that in the wet season. Bathymetry is the most important predictor for habitat suitability, in line with the known coastal distribution of humpback dolphins.\n Our research predicted specific suitable habitat distributions which can be used to develop practical protection measures, such as the establishment of marine protected areas for this species to monitor, mitigate, or prohibit harmful anthropogenic activities.
Distribution pattern of Indo-Pacific humpback dolphins (Sousa chinensis) along coastal waters of Fujian Province, China
DOI:10.1578/AM.40.4.2014.341 URL [本文引用: 1]
Distribution and habitat characteristics of the Indo-Pacific humpback dolphin (Sousa chinensis) in the Northern Beibu Gulf, China
DOI:10.1578/AM.43.2.2017.219 URL [本文引用: 3]
Bycatch mitigation requires livelihood solutions, not just fishing bans: A case study of the trammel-net fishery in the northern Beibu Gulf, China
DOI:10.1016/j.marpol.2022.105018 URL [本文引用: 1]
Long-term habitat loss in a lightly-disturbed population of the Indo-Pacific humpback dolphin, Sousa chinensis
DOI:10.1002/aqc.v27.6 URL [本文引用: 2]
The behavioural ecology of Indo-Pacific humpback dolphins in Hong Kong
DOI:10.1016/bs.amb.2015.08.008
PMID:26790888
[本文引用: 2]
Fewer than 200 Indo-Pacific humpback dolphins (Sousa chinensis) occur in Hong Kong waters (though these are part of a much larger population in the Pearl River Estuary), with a decrease in the past about 10 years. They have partially overlapping individual ranges (mean = 100 km(2)), and two partially overlapping communities. Seasonal occurrence is higher in June-November than December-May, approximate wet and dry monsoon seasons, respectively. Group sizes tend to average three dolphins, a decrease from the past decade. Feeding often occurs in abruptly changing water depths and off rocky natural shores. The area immediately north of Hong Kong International Airport is largely used for travelling between locations to the west, east and further north. The area around Lung Kwu Chau Island in northwest Hong Kong is a "hot spot" for foraging and socializing. The area off Fan Lau, southwest Lantau Island, is largely used for foraging. A former foraging "hot spot" was located around the Brothers Islands east of the airport, now reduced, possibly due to increases in high-speed ferries (HSFs) and other activities. Sound recordings of dolphins from bottom-mounted hydrophones suggest that northwestern Hong Kong waters are used more at night than in daytime. Sexual activity and calving occur throughout the year, with a peak in late spring to autumn (wet monsoon season). Humpback dolphins communicate acoustically with each other and probably passively listen to prey in murky waters, and anthropogenic noises may be masking communication and affecting prey location. Increasing sounds of shipping, HSFs and industrial activities are likely to alter dolphin habitat use patterns and overall behaviours beyond the present already affected status.
Historic changes of polychlorinated biphenyls (PCBs) in juvenile and adult cetaceans from the Pearl River Estuary from 2003 to 2020
DOI:10.1016/j.scitotenv.2021.149512 URL [本文引用: 1]
The world’s second largest population of humpback dolphins in the waters of Zhanjiang deserves the highest conservation priority
DOI:10.1038/srep08147 [本文引用: 5]
Chlorinated organic contaminants in fish from the South China Sea: Assessing risk to Indo-Pacific humpback dolphin
DOI:10.1016/j.envpol.2020.114346 URL [本文引用: 1]
Studies on the Spatial Use, Community Dynamics, and Reproductive Ecology of Indo-Pacific Humpback Dolphins (Sousa chinensis) in Jiangmen Waters
江门水域中华白海豚空间利用、社群动态及繁殖生态的研究
Modeling demographic parameters of an edge-of-range population of Indo-Pacific humpback dolphin in Xiamen Bay, China
DOI:10.1016/j.rsma.2020.101462 URL [本文引用: 4]
Preliminary study on the reproductive ecology of a threatened Indo-Pacific humpback dolphin (Sousa chinensis) population in Xiamen Bay, China
DOI:10.1578/AM.47.1.2021.43 URL [本文引用: 3]
Risk assessment for marine plastic debris ingestion by Indo-Pacific humpback dolphins (Sousa chinensis) in Xiamen Bay, China
厦门湾海洋塑料垃圾对中华白海豚的摄食风险评价
An Indo-Pacific humpback dolphin genome reveals insights into chromosome evolution and the demography of a vulnerable species
DOI:10.1016/j.isci.2020.101640 URL [本文引用: 2]
A study on the habitat preference of Sousa chinensis in Pearl River Estuary based on the generalized additive models
基于广义可加模型的珠江口中华白海豚栖息地偏向性研究
Bioaccumulation of legacy organic contaminants in pregnant Indo-Pacific humpback dolphins (Sousa chinensis): Unique features on the transplacental transfer
DOI:10.1016/j.scitotenv.2021.147287 URL [本文引用: 1]
Early divergence and differential population histories of the Indo-Pacific humpback dolphin in the Pacific and Indian Oceans
DOI:10.1111/1749-4877.12527
PMID:33560551
[本文引用: 3]
The currently recognized Indo-Pacific humpback dolphin occurs in estuaries and surrounding shallow waters from the South China Sea to the Asian coast of the Indian Ocean. However, a recent study suggested that the humpback dolphin from the Bay of Bengal may represent a distinct phylogenetic species. In this study, we sequenced 915-bp mtDNA segments from five geographic populations in both Chinese and Thai waters; together with previously published sequences, these data revealed that the ancestral Indo-Pacific humpback dolphin might have split during the transition from the Oligocene to Miocene (23.45 Mya, 95% HPD: 16.65-26.55 Mya), and then dispersed along the Pacific and Indian Ocean coasts of Asia. Genetic differentiation was detected between most of the examined populations, except for only a few pairwise populations in the northern South China Sea. Genetic differentiation/distance between the humpback dolphins from the northern and southern South China Sea met the sub-species threshold value proposed for marine mammals, whereas that between the humpback dolphins in the Pacific and the Indian Ocean was above the species threshold. Bayesian inference of historic gene flow indicated low but constant northward gene flow along the Indian Ocean coast; however, there was a recent abrupt increase in gene flow in the Pacific region, likely due to the shortening coastline at the low stand of sea level. Our results revealed that the current taxonomic classification of Indo-Pacific humpback dolphins may not reflect their phylogeography.© 2021 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.
Studies on Behavior and Conservation Biology of Sousa chinensis in Pearl River Estuary
珠江口中华白海豚的行为学及保护生物学研究
Infanticide in the Indo-Pacific humpback dolphin (Sousa chinensis)
DOI:10.1007/s10164-016-0475-7 URL [本文引用: 3]
Distribution and abundance of Indo-Pacific humpback dolphins in Leizhou Bay, China
DOI:10.1080/03014220709510061 URL [本文引用: 2]
Changes of accumulation profiles from PBDEs to brominated and chlorinated alternatives in marine mammals from the South China Sea
DOI:10.1016/j.envint.2014.01.023
PMID:24530800
[本文引用: 1]
The present study investigated the composition profiles and levels of polybrominated diphenyl ethers (PBDEs) and five PBDE alternatives in the blubber of two species of marine mammals, Indo-Pacific humpback dolphins (Sousa chinensis) and finless porpoises (Neophocaena phocaenoides) from the South China Sea. Despite the fact that PBDEs were the most predominant brominated flame retardants in the samples analyzed, decabromodiphenyl ethane (DBDPE), 1,2-bis (2,4,6-tribromophenoxy) ethane (BTBPE), bis- (2-ethylhexyl) -tetrabromophthalate (TBPH), 2-ethylhexyl 2,3,4,5-tetrabromobenzoate (TBB) and Dechlorane Plus (DP) were all detected in both cetacean species. In addition, significantly increasing temporal shifting trends of Deca-BDE to DBDPE, Octa-BDE to BTBPE, and Deca-BDE to DP were observed in porpoise samples between 2003 and 2012 and dolphin samples between 2003 and 2011. These patterns may be attributed to the replacement of PBDEs by alternative halogenated flame retardants (HFRs) and the increasing usage of these alternatives following the restriction/voluntary withdrawal of the production and use of PBDE commercial mixtures. Our findings suggest that the study region may be a source of contamination by PBDE alternative flame retardants due to the high detection frequencies and levels of these compounds in marine mammals. Copyright © 2014 Elsevier Ltd. All rights reserved.
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