牡蛎,有待保护的海岸线前哨

huitre sentinelle témoin littoral à préserver

  海洋软体动物中的牡蛎是我们法国沿海的一个重要物种,具有重要的经济与遗传价值。作为独特的物种,牡蛎在沿海生态系统中发挥着多重作用。然而牡蛎正承受着巨大的压力,包括人类活动导致的污染。我们将在本文中详细介绍以下几种污染:化学性污染、生物污染(人类活动导致的天然有毒微藻大量繁殖)以及新的颗粒性化学污染物——微塑料,从而对之前阐述牡蛎生态重要性以及对牡蛎影响极大的全球变暖相关威胁的文章进行补充。(见牡蛎:鲜为人知的沿海环境建筑师)。牡蛎作为反映沿海生态系统健康状况(或退化程度)的前哨种,处于警戒线的位置,因此,需要采取强有力的措施来保护牡蛎沿海栖息地。

1. 牡蛎:一种重要但受威胁的海洋软体动物

图1. 布雷斯特前滨的杯状牡蛎 [来源:© IFREMER / Stéphane Pouvreau]

  牡蛎(图1)在我们的沿海海洋生态系统中一直扮演重要角色,对生态系统正常运转至关重要。同时它们也是我们盘中的美味佳肴。不幸的是,它们受到了人为压力,导致其生态环境被破坏,其生存也遭到威胁。我们希望通过研究两种互补的生物模型,即本地的欧洲牡蛎(Ostrea edulis)及引进的欧洲牡蛎的表亲——长牡蛎(Crassostrea gigas),从而了解大量存在的人为污染物对其繁殖、生长和免疫防御功能的影响。这些主要的功能决定了牡蛎的生态环境,从而影响到其在自然环境下对种群的维持以及在农业中发挥的作用。毕竟牡蛎具有双重角色:它既是生态系统的建设者,又是人类的供养者。

2. 牡蛎是所有恶行的受害者

  过度开发、生境破坏以及部分由人类活动意外引入的疾病或寄生虫对牡蛎来说都是梦魇(见牡蛎:鲜为人知的沿海环境建筑师)。最近的研究表明,沿海城市化、全球变暖及海洋酸化可能会影响牡蛎的繁殖,进而对牡蛎产业造成影响[1]。此外,作为最接近人类活动的区域,沿海地区聚集了大量的污染物,如农药、药物残留、重金属和碳氢化合物。

  比如20世纪80年代初的阿卡雄盆地,长牡蛎的增量(即长牡蛎幼虫的丰度)为零,其天然群体的更新受到威胁。直到一项持续多年的研究计划结束,研究人员才得以证实是防污涂料中的三丁基锡[2][3]引起了年轻幼虫的死亡。

  在诸多影响牡蛎生长发育的因素中,还包括了来自病原菌、病毒以及有毒微藻的生物污染。

2.1. 有毒的微藻

  海洋微藻产生的水华是指这些光合单细胞生物在适宜环境条件下的迅速繁殖(图2)。与城市地区和集约化农业排放关系密切的水体富营养化[4]尤其容易导致水华进一步扩大。在布列塔尼,富营养化因导致绿潮而广为人知(见环境中的硝酸盐,磷与富营养化)。微藻是海洋食物链基础,也能为我们的呼吸提供氧气,对人类而言不可或缺,然而,在数千种微藻中,已知至少有300种在繁殖时具有毒性。这种现象被称为有害藻华(harmful algal blooms,HABs)。

  近几十年来,HAB事件的数量、强度持续增加,地理分布也持续扩大,有一部分是因为全球环境变化和沿海地区的富营养化。其中一些水华因发生过程中产生的大规模效应而产生危害。事实上,2018年至2019年,拓泻湖热浪期间发生了一系列极端环境变化(温度、盐度),这给予了当地某些极小物种繁殖的有利条件,但由于其无法被牡蛎摄取,从而导致浮游生物群落结构发生改变,最终引起了绿水现象。这一现象的起因便是Picochlorum属的一次水华。它是一种几微米大小,能经受巨大环境变化的浮游植物,但牡蛎对它没有食用兴趣。这些微藻大规模占据了其繁殖环境,导致滤食动物的鳃闭塞或剥夺周围物种的氧气,进而使周围生物因缺氧大量死亡。

  此外,还有一百种能够产生藻毒素的有毒微藻。它们中的一部分在人类食用的海洋生物体内积累,从而对人类健康构成威胁。根据它们在人类身上引起的综合征,可将其归纳为以下几种毒素,包括PSP(麻痹)、DSP(腹泻)、ASP(遗忘)、NSP(神经毒性)和CFP(雪卡毒素中毒)。

图2. 2017年10月,日本磐城港由有毒的微藻水华引起的赤潮 [来源:melvil, CC BY-SA 4.0, via Wikimedia Commons]
  许多国家已经部署了监测网络以确保对有毒微藻物种和贝类污染进行高频监测。在法国,Ifremer REPHY网络(Réseau d’Observation et de Surveillance du Phytoplancton et de l’Hydrologie dans les Eaux Littorales [5])分析了海岸线上产生ASP、DSP和PSP毒素的微藻浓度以及几种贝类的毒素水平。该网络为地方当局提供了决策工具,即在贝类中毒素含量超过依据欧洲水平建立的健康阈值时,通过地方法令禁止休闲捕鱼,捕捞以及销售贝类。

  20世纪80年代以来,法国常有产生麻痹性毒素的微藻,特别是甲藻中的微小亚历山大藻(Alexandrium minutum)和链状亚历山大藻(Alexandrium catenella)水华的记录。2012年夏天以来,布雷斯特湾发生了数次微小亚历山大藻水华,而在之前从未有过此类水华记录[3]。2012年7月,微小亚历山大藻的浓度甚至达到创纪录水平,导致相应贝类体内健康毒素阈值超过10倍,也让其销售被迫叫停。

图3. 图示暴露于有毒微藻微小亚历山大藻中的牡蛎幼体(右)与未暴露的对照牡蛎幼体(左)相比,其面盘(一种具纤毛的游泳器官,图中由黑色箭头指示)畸形 [来源:©UBO / Justine Castrec]

  除给人类带来健康风险外,有毒的微藻还可以影响沿海物种,并引发多种症状。牡蛎对亚历山大藻属的响应表现为生物节律[6]即心脏瓣膜及滤食行为的紊乱[7]。还可观察到不同器官(鳃、肌肉、消化系统)的病变和感染,甚至对病原体的反应也发生了改变,进而引起免疫系统紊乱。这种广泛的影响一直延续到繁殖并可传递给下一代:在配子形成过程中接触到微小亚历山大藻的牡蛎会产生一部分畸形幼虫(图3),而对于其他一部分幼虫来说,相比父母未接触过微小亚历山大藻的幼虫,这部分幼虫生长得更慢[10]。最近,人们已经发现牡蛎对麻痹性贝类毒素并不像哺乳动物那么敏感,但它们对微小亚历山大藻排泄的化合物更敏感,这可以解释在牡蛎身上观察到的大部分症状。现在的当务之急是确定这些新化合物的化学性质。

2.2. 化学污染

  在法国海洋开发研究院(French Research Institute for Exploitation of the Sea,Ifremer)运作的化学污染观察网(chemical contamination observation network,ROCCH)框架内,牡蛎被用作环境污染的前哨。与贻贝和其它生物一样,这种软体动物具有一大特点,其在受污染环境的暴露程度越高,环境中存在的一些化学污染物在体内富集越多。1974年以来,在ROCCH框架内,每年都会对牡蛎肉中的金属如镉、铜、汞或铅、多环芳烃(PAHs)、多氯联苯(PCBs)、多溴联苯醚(PBDEs)和某些农药如林丹、艾氏剂和DDT的残留物进行一次分析,以得出关于海洋环境质量的信息。

  这种方法并非法国所特有,在世界上的许多国家,牡蛎都在常年监测网络的框架内或在具体的科学研究中被用来评估环境的化学污染。牡蛎还能够帮助寻找新出现的污染物,如最近在葡萄牙海岸开展的一项研究中,除上述污染物外,牡蛎还帮助测定了29种阻燃剂、包括拟除虫菊酯类杀虫剂在内的35种农药,以及麝香和紫外线吸收剂等13种护理产品[8]

  除了作为前哨种的角色,牡蛎也是环境毒理学模式物种,这是一门研究污染物对生物影响的学科:

  • 短期接触植物保护产品(与海洋环境中的浓度相近)会改变牡蛎的DNA结构和修复过程。这些可以影响到生殖细胞并传递给后代[9]
  • 农药也会影响牡蛎的免疫防御和新陈代谢,特别是能量代谢[10]
  • 最后,重金属多环芳烃甚至一些药物都足以改变牡蛎的生理;这些分子的影响与它们的作用机制密切相关。例如,研究已经证明直到幼虫变态之前,抗抑郁药都能够扰乱牡蛎的胚胎发育(胚胎毒性)。

  目前,要证明这些实验结果有效,必须在更复杂的自然环境条件下进行评估。对直接从自然环境采集的生物开展研究,有助于我们建立起环境污染、污染物在动物组织中的生物积累和生物的健康状况之间的联系。一项印度的研究在受多环芳烃和重金属污染的阿拉伯海沿岸的几个地点开展,其结果表明,僧帽牡蛎(Saccostrea cucullata)体内多种多环芳烃的生物累积与DNA完整性损害之间存在相关性;现在已经知道的是,这种损害能够干扰暴露于污染条件下牡蛎的后代[11]。这些结果揭露了一大问题,从观察到的个体效应来看,其对于群体乃至更加广泛的生态系统都产生了不良影响:迄今为止,针对这一领域的研究大部分仍是空白。

2.3. 新的颗粒性污染物:微塑料

图4. 酸奶罐,牡蛎在人类世的新生境? [来源:© IFREMER / Stéphane Pouvreau]

  微塑料是小于5毫米的塑料颗粒。这种海洋环境污染是1972年于马尾藻海发现的,当时全球塑料年产量还不到500万吨。从那时起,为满足我们的日常需要,塑料产量持续增加。如今塑料年产量已超过3亿吨,而由于报废管理不善,每年有数千吨最终进入海洋(图4)。微塑料造成的污染遍布所有海洋区室(水柱、沉积物、动植物区系)以及海洋各个区域,从沿海地区到海洋流涡,从表层海洋到深层沉积物,从人口密集地区到极地等无人居住的地区都存在微塑料污染(见海上塑料污染:“第七大洲”)。

  平均而言,在海上发现的塑料碎片有80%来自陆地(风、河流、径流、废水),其余来自海事活动(旅游业、划船、捕鱼、水产养殖)。塑料在海上的影响主要表现为两个方面。

图5. 在布雷斯特港收集到的微塑料(颗粒、纤维、细丝、薄膜) [来源: © UBO / Sébastien Hervé]

  首先,它们促进了物种的传播。一旦到了海上,塑料就构成了被称为“塑料圈”的环境,它是有利于微生物(细菌、真菌、原生动物、病毒)定植的生境。其中一些物种具有毒性或致病性,如已知对牡蛎具有致病性的某些科的细菌。接下来出现的问题是,这些散布在塑料表面的病原体是否会传播疾病?

  塑料垃圾对海洋的第二类主要影响仅体现于某些大型海洋动物(鸟类、哺乳动物或海龟)身上,它们或被困于塑料废物中,或是呼吸道或消化道被塑料阻塞。

  然而,这只是冰山一角,因为90%以上的漂浮在海上的塑料垃圾都小于5毫米,即微塑料(图5)。由于其体积小,这些微塑料很容易通过食物链摄入。首先接触微塑料的就是包括牡蛎在内的滤食动物。

图6. 实验性接触后牡蛎消化道内荧光聚苯乙烯微球的检测结果 [来源:© IFREMER]

  一旦被摄入,微塑料或是堵塞消化系统,或是仅通过消化系统,后者是实验室中证实的主要问题(图6)。但微塑料即使仅通过消化系统,也会对摄入它们的动物的生物学特性产生不利影响。我们已经在实验中证明,对于暴露于2和6微米的聚苯乙烯微粒中两个月的牡蛎,其繁殖会受到干扰[12]:产生的卵母细胞更少(减少40%),精子的运动能力更差,与人类一样,这都是精卵质量的指标。事实上,一旦受精,这些配子产生了的幼虫便少了40%,剩下的幼虫生长也会延迟6天。在自然环境中,这多出了6天的幼体期里,幼虫随时可能死亡或被捕食。

  至于最小的纳米塑料,由于缺乏新的检测方法,其在海洋中的数量仍然未知,它们极小的尺寸使其能够与生物膜相互作用。由于牡蛎为体外受精,它们的配子一旦被释放到海洋中,就会受到环境的危害。虽然聚苯乙烯微球对牡蛎配子、胚胎和幼体没有产生影响(在我们的实验条件下),但50纳米的纳米珠会强烈地干扰它们。为什么会这样呢?

图7. 暴露于50纳米聚苯乙烯纳米珠1小时后,牡蛎精子的扫描电镜观察结果。白色箭头指示了纳米塑料在精子头部(红框)和鞭毛(绿框)的黏附情况 [来源:© IFREMER / Kevin Tallec]
  • 通过电镜可以观察到纳米塑料黏附在牡蛎精子的表面(图7),这将削弱其与卵子结合所需的移动能力[13]
  • 暴露于这些纳米珠中24小时后,牡蛎胚胎出现畸形,而在高剂量下其发育完全停止。

  最后,牡蛎以及其他双壳类动物的食物来源也可能受到影响,因为硅藻类微藻的生活史似乎也受到这些纳米塑料的干扰,这表明在生态系统这一复杂尺度上去理解微塑料和纳米塑料的影响非常重要。

3. 应该怎么办?有何解决方案吗?

  已有的解决方案还是很多的,还有不少方案有待发现,从而减少或停止主要人类活动所造成的压力。我们可以以三丁基锡为例。由于它的毒性和环境风险已被证实,1982年三丁基锡在法国被禁用,2001年在世界范围内普遍禁止使用。然而,寻找无毒、环境友好的三丁基锡替代品并不容易,需要研究和技术创新。而当考虑到污染的多样性、替代物的来源和用途时,这一过程就变得更加复杂。还没有单一方案能够解决这些问题。

  科学监测和研究对于了解污染及其在自然界中的影响是非常必要的,对于增强公众和决策者的认识也是如此。在欧洲,它们被特别纳入《海洋战略框架指令》(Marine Strategy Framework Directive,MSFD)[14],其目标是到2020年实现欧洲海洋水域的 “良好生态状态”,在未来几年内,这一目标也会包含更多内容。

  因此,为了从源头上减少和控制污染,有必要沿整个价值链同时施行各种解决方案。这包括:

  • 从原材料开采、生产到使用都要保持节制(例如塑料,见法国议会报告[15]),因此需要改变工业、农业和公民的行为;
  • 更好地管理报废的产品和废物;
  • 工业技术的开发,特别是新工艺、新产品以及生物来源和/或生物降解的新材料,确保在任何情况下都不影响环境和人类健康(设计安全的理念)
  • 制定旨在保护环境的相关立法,特别是环保法。保护我们极其珍贵的沿海区域,能够进一步加强海洋系统完整性,这也符合人类的共同利益。

4. 结论

  • 许多污染物、农药、药物残留、重金属、微塑料,对牡蛎的整个生活史都有影响。
  • 一些毒性影响可以传递到下一代的幼龄牡蛎(造成胚胎毒性、内分泌紊乱)。
  • 这些污染物的 “综合“效应(以及更进一步的暴露组)仍有待研究,以了解牡蛎种群的演化。
  • 牡蛎在我们的海岸线上存在了数百万年,而现在它向我们发出警告,呼吁我们采取强有力的措施来保护沿海生境。

 


参考文献和说明

封面图片。在实验室实验中摄取绿色微塑料的牡蛎幼体[来源:© IFREMER / Rossana Sussarellu]

[1] Thomas, Y. (2018). Oysters as sentinels of climate variability and climate change in coastal ecosystems. Environmental Research Letters 13, 104009. Publisher’s official version : https://doi.org/10.1088/1748-9326/aae254, Open Access version : https://archimer.ifremer.fr/doc/00461/57255/

[2] https://perturbateursendocrinienssite.wordpress.com/2017/05/04/tributyletain/

[3] https://fr.wikipedia.org/wiki/Antifouling

[4] Chapelle, A. (2016). Modélisation du phytoplancton dans les écosystèmes côtiers. Application à l’eutrophisation et aux proliférations d’algues toxiques. https://archimer.ifremer.fr/doc/00360/47141/

[5] https://wwz.ifremer.fr/envlit/Surveillance-du-littoral/Phytoplancton-et-phycotoxines

[6] Payton, L. (2017). Chronobiologie moléculaire et comportementale des huîtres Crassostrea gigas diploïdes et triploïdes exposées à l’algue toxique Alexandrium minutum. Thèse de l’Université de Bordeaux. https://tel.archives-ouvertes.fr/tel-01579783/document

[7] Castrec, J (2018). Impacts des efflorescences du dinoflagellé toxique Alexandrium minutum sur la reproduction et le développement de l’huître Crassostrea gigas. Thèse de l’Université de Bretagne occidentale. https://tel.archives-ouvertes.fr/tel-03035012/document

[8] Gadelha, J.R. (2019). Persistent and emerging pollutants assessment on aquaculture oysters (Crassostrea gigas) from NW Portuguese coast. Science of the Total Environment, 666, 731-742.

[9] Bachere, E. (2017). Parental diuron-exposure alters offspring transcriptome and fitness in Pacific oyster Crassostrea gigas. Ecotoxicology and Environmental Safety, 142, 51-58. https://doi.org/10.1016/j.ecoenv.2017.03.030

[10] Epelboin, Y. (2015). Energy and Antioxidant Responses of Pacific Oyster Exposed to Trace Levels of Pesticides. Chemical Research In Toxicology, 28, 1831-1841. Publisher’s official version : https://doi.org/10.1021/acs.chemrestox.5b00269, Open Access version : https://archimer.ifremer.fr/doc/00284/39490/

[11] Melwani, A.R. (2016). PAHs and heavy metals at each sampling location along the west coast of India around Goa, India. Aquatic Toxicology, 173, 53-62.

[12] Sussarellu, R. (2016). Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. USA, 113, 2430-2435. Open Access version: https: //archimer.ifremer.fr/doc/00311/42233/

[13] Tallec, K. (2019). Impacts des nanoplastiques et microplastiques sur les premiers stades de vie (gamètes, embryons, larves) de l’huître creuse Crassostrea gigas. Thèse de l’Université de Bretagne occidentale. https://tel.archives-ouvertes.fr/tel-02996550/document

[14] https://wwz.ifremer.fr/Expertise/Eau-Biodiversite/Directive-Cadre-Strategie-pour-le-Milieu-Marin

[15] http://www.senat.fr/fileadmin/Fichiers/Images/redaction_multimedia/2020/2020-Documents_pdf/20201512_Conf_presse_OPECST/Rapport_final.pdf


环境百科全书由环境和能源百科全书协会出版 (www.a3e.fr),该协会与格勒诺布尔阿尔卑斯大学和格勒诺布尔INP有合同关系,并由法国科学院赞助。

引用这篇文章: HUVET Arnaud, SANCHEZ Wilfried, POUVREAU Stéphane, FABIOUX Caroline (2024年2月23日), 牡蛎,有待保护的海岸线前哨, 环境百科全书,咨询于 2024年10月8日 [在线ISSN 2555-0950]网址: https://www.encyclopedie-environnement.org/zh/vivant-zh/oyster-sentinel-of-coastline-to-be-preserved/.

环境百科全书中的文章是根据知识共享BY-NC-SA许可条款提供的,该许可授权复制的条件是:引用来源,不作商业使用,共享相同的初始条件,并且在每次重复使用或分发时复制知识共享BY-NC-SA许可声明。

The oyster, the sentinel of a coastline to be preserved

huitre sentinelle témoin littoral à préserver

In the category of marine molluscs, the oyster is an essential species of our French coasts and has strong economic and heritage stakes. An ingenious species, it provides many services in coastal ecosystems. However, oysters undergo strong pressures, including pollution of human origin. Among these pollutions, we will detail in this article, chemical pollutions, biological pollutions such as natural toxic microalgae whose proliferation can have an anthropic origin, and new chemical and particulate contaminants, microplastics, thus completing the previous article showing the ecological importance of oysters and the threats related to global warming which weigh on them (See Oysters: these unknown architects of coastal environments). The oyster, as a sentinel species indicating the state of health (or degradation) of the coastal ecosystem, is therefore in the position of an alarm bellwether requiring strong measures to protect coastal habitats.

1. The oyster: an essential and threatened marine mollusc

oysters-holy-earth-brest
Figure 1. Cupped oysters on the foreshore of Brest [Source: © IFREMER / Stéphane Pouvreau]
Oysters (Figure 1) have always played an important role in our coastal marine ecosystems and are essential to their functioning. They are also a delicacy on our plates. Unfortunately, they are subject to anthropogenic pressures that disrupt their ecology and threaten their existence. By working on two complementary biological models, the native oyster Ostrea edulis and its introduced closed taxa Crassostrea gigas, we aim to understand the effects of anthropogenic contaminants – and there are many of them – on their functioning, reproduction, growth and defence. These major functions determine their ecology and thus the maintenance of populations in natural environment as well as their performance in farming, the oyster having this double role, species engineer of the ecosystem, and feeder of humans.

2. Oysters are victims of all the evils

Overexploitation, habitat destruction, and the presence of diseases or parasites, some of them being accidentally introduced by human activity, are real scourges for oysters (See Oysters : the unknown architects of coastal environments). Recent studies show that changes linked to coastal urbanization, global warming and ocean acidification could affect oyster reproduction with consequences for the oyster industry [1]. Moreover, coastal areas, which are the closest to human activities, gather a quantity of pollutants such as pesticides, drug residues, heavy metals and hydrocarbons.

For example, in the Arcachon basin at the beginning of the 1980s, recruitment (i.e. the abundance of Crassostrea gigas oyster larvae) had become null and the renewal of natural stocks was threatened. It was only at the end of a multi-year research program that researchers demonstrated the responsibility of tributyltin [2] in antifouling paints [3] in the mortality of young larvae.

To this long list, we should add biological pollution from pathogenic bacteria and viruses, or toxic micro-algae.

2.1. Toxic micro-algae

A bloom of marine micro-algae is defined by the very rapid multiplication of these photosynthetic unicellular organisms, favoured by environmental conditions (Figure 2). It is particularly favoured and amplified by eutrophication [4] linked to discharges from urban areas and intensive agriculture, known in Brittany to stimulate green tides (see Nitrates in the environment & Phosphorus and eutrophication). However, among the thousands of species of microalgae, which are essential because they are at the base of the marine food chain and produce part of the oxygen we breathe, at least 300 are known to be toxic when they proliferate. These are known as Harmful Algal Blooms (HABs).

In recent decades, the number, intensity and geographical distribution of HAB events have been increasing, partly due to global change and eutrophication of coastal areas. Some of them are harmful because of the mass effect produced during blooms. Indeed, extreme variations (temperature, salinity) during the 2018 and 2019 heat waves in the Thau lagoon modified the planktonic communities by favouring very small species that are not

assimilated by the oyster, which generated a green water phenomenon. The origin was a bloom of Picochlorum, a phytoplankton of a few micrometres that tolerates great environmental variations but has no food interest for the oyster. These micro-algae literally suffocate the environment where they proliferate. This can lead, for example, to occlusion of the gills in filter-feeder animals or deprive surrounding species of oxygen and cause massive deaths by anoxia.

There are, moreover, a hundred of toxic micro-algae that produce phycotoxins. Some of them present a danger for human health by their accumulation in marine organisms consumed by humans. Several types of toxins are listed and classified according to the syndromes they cause in humans, including PSP (paralytic), DSP (diarrheic), ASP (amnesic), NSP (neurotoxic), and CFP (Ciguatera).

red seaweed toxic micro-algae
Figure 2. red tide in October 2017 in the port of Iwaki, Japan, caused by a toxic microalgae bloom. [Source: melvil, CC BY-SA 4.0, via Wikimedia Commons]
Monitoring networks have been deployed in many countries to ensure high frequency monitoring of toxic microalgae species and shellfish contamination. In France, the Ifremer REPHY network (Réseau d’Observation et de Surveillance du Phytoplancton et de l’Hydrologie dans les Eaux Littorales [5])

analyses the concentration of ASP, DSP and PSP toxin-producing microalgae and the level of toxins in several shellfish species along the coastline. This network provides local authorities with a decision-making tool, namely the prohibition by prefectural decree of the recreational fishing, and the fishing and sale of shellfish when the toxin content in the shellfish exceeds the health threshold established at the European level.

In France, blooms of paralytic toxin-producing micro-algae, in particular the dinoflagellates Alexandrium minutum and Alexandrium catenella, have been regularly recorded since the 1980s. In the Bay of Brest, several A. minutum blooms have occurred since the summer of 2012, whereas they had never been recorded before [3]. In July 2012, the concentration of A. minutum even reached record levels, causing the closure of the sale of shellfish exceededing the health toxin threshold by 10 times.

malformation larva oyster micro algae toxic
Figure 3. Illustration of a malformation of the velum, a ciliated swimming organ (black arrow), in an oyster larva exposed to the toxic microalga Alexandrium minutum (right) compared to an unexposed control oyster larva (left) [Source: © UBO / Justine Castrec]
In addition to human health risks, toxic microalgae can affect coastal species causing multiple symptoms. In response to the Alexandrium genus, oysters show disruptions in their biological rhythm [6], in their valve and filtration behaviour [7]. Lesions and inflammations of different organs (gills, muscle, digestive system) are observed up to a disturbance of the immune system modifying their response to pathogens. This broad spectrum of effects extends to reproduction and can be transmitted to the next generation: oysters exposed to Alexandrium minutum during gamete formation produce young larvae, some of which are malformed (Figure 3), while others grow more slowly than those whose parents were not exposed [10]. Recently, it has been discovered that oysters are not so sensitive to paralytic shellfish toxins as mammals, but that they are much more sensitive to compounds excreted by Alexandrium minutum, which would explain most of the symptoms observed in oysters. It is urgent to identify the chemical nature of these new compounds.

2.2. Chemical pollution

The oyster is used as a sentinel of environmental contamination in the framework of the chemical contamination observation network (ROCCH) operated by the French Research Institute for Exploitation of the Sea (Ifremer). Like mussels and other organisms, this mollusc has the property of concentrating some of the chemical pollutants present in its environment in proportion to its exposure. Since 1974, within the framework of the ROCCH, metals such as cadmium, copper, mercury or lead, polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and certain pesticides such as lindane, aldrin and DDT residues have been analysed once a year in the flesh of oysters in order to provide information on the quality of the marine environment.

This approach is not specific to France and in many countries of the world, oysters are used to evaluate the chemical contamination of the environment either within the framework of perennial monitoring networks or during specific scientific studies. The latter allow the search for emerging pollutants, as in a recent study carried out on the Portuguese coast in which, in addition to the pollutants described above, 29 flame retardants, 35 pesticides including pyrethroid insecticides and 13 care products such as musks and UV filters were measured [8].

Beyond its role as a sentinel species, the oyster is also a model species in environmental toxicology, a discipline that studies the effects of pollutants on organisms:

  • Short-term exposures to plant protection products (at concentrations similar to those found in the marine environment) alter their DNA structure and repair processes. These effects can reach the germ cells and be transmitted to the offspring [9].
  • Pesticides also affect the oyster’s immune defences and metabolism, especially energy metabolism [10].
  • Finally, heavy metals, PAHs or even some drugs have the capacity to alter the physiology of the oyster; the effects of these molecules being closely linked to their mechanism of action. For example, it has been demonstrated that antidepressants have the capacity to disrupt the embryonic development of oysters (embryotoxicity) until the metamorphosis of the larvae.

The validity of these laboratory results must now be evaluated in the more complex conditions of the natural environment.  Work carried out on organisms taken directly from the natural environment makes it possible to establish the link between environmental contamination, the bioaccumulation of pollutants in animal’s tissues and the state of health of the organisms. An Indian study, carried out on several sites of the Arabian Sea coast, characterized by a contamination by PAHs and heavy metals, highlighted a correlation between the bioaccumulation of various PAHs and the damage to the DNA integrity in Saccostrea cucullata oysters; damage whose capacity to disturb the progeny of exposed organisms in oysters is now known [11]. These results raise the question of the repercussion of the individual effects observed on populations and, more broadly, on ecosystems: a field of research that remains largely unexplored to this day…

2.3. New particulate contaminants: microplastics

yoghurt pot habitat oyster
Figure 4. The yoghurt pot, a new habitat for the oyster in the Anthropocene period? [Source: © IFREMER / Stéphane Pouvreau]
Microplastics are plastic particles smaller than 5 mm. This pollution of the marine environment was detected in 1972 in the Sargasso Sea, when annual global plastic production was less than 5 million tonnes. Since then, this production of plastics has continued to increase to meet our daily needs. It now exceeds 300 million tonnes per year and several thousand tonnes end up in the oceans each year due to poor end-of-life management (Figure 4). Microplastics constitute a pollution found in all marine compartments (water column, sediment, fauna and flora) and in every zones of the Ocean, from coastal areas to ocean gyres, from the surface ocean to deep sediments, from populated areas to uninhabited areas such as the poles (See Plastic pollution at sea: the seventh continent).

On average, 80% of plastic debris found at sea comes from land (wind, rivers,  runoff, wastewater) and the rest from maritime activities (tourism, boating, fishing, aquaculture). The impacts of plastics at sea can be presented in two main areas.

Firstly, they promote the transport of species. Once at sea, plastics constitute a habitat favourable to the colonisation of micro-organisms (bacteria, fungi, protozoa, viruses) called the “plastisphere”. Some of these species are toxic or pathogen, such as families of bacteria known to be pathogen to oysters. The question then arises as to whether these pathogen species disseminated on the surface of plastics can transmit diseases?

The second major category of impacts of plastic waste at sea is only visible on large marine animals (birds, mammals or turtles) trapped in plastic waste or obstructing their respiratory or digestive tracts. However, this is only the tip of the iceberg as more than 90% of plastic waste floating at sea is smaller than 5 mm, known as microplastics (Figure 5). Because of their small size, these microplastics are easily ingested through the food chain. The first to be exposed are filter feeders, including oysters.

fluorescent-polystyrene-microspheres-oyster
Figure 5 et 6. Detection of fluorescent polystyrene microspheres in the digestive tract of oyster after experimental exposure [Source: © IFREMER]
Once ingested, these microplastics can either clog the digestive system or simply transit through it, this latter being the main issues demonstrated in laboratory (Figure 6). But even a simple transit of microplastics in the digestive tract causes disturbances on the biology of the animal that ingested them. We have shown that oysters exposed experimentally to 2 and 6 µm polystyrene microparticles for two months had a disrupted reproduction [12] : fewer oocytes were produced (40% reduction) and spermatozoa were less mobile, which is an indicator of their quality as in humans. And indeed, once fertilized, these gametes produced 40% fewer young larvae, with the remaining larvae showing a 6-day growth delay. This means 6 more days of larval life during which mortality or predation can occur when in the natural environment.

As for the smallest ones, the nanoplastics, whose quantities in Ocean are still unknown due to the lack of innovative methods, their small size allows them to interact with the biological membranes. Since oysters fertilize externally, their gametes, once released into the sea, are subject to environmental hazards. While polystyrene microbeads have no effect (under our experimental conditions) on oyster gametes, embryos and larvae, the 50 nanometer nanobeads strongly disturb them. How do you tell me?

spermatozoa oysters nanoplastics
Figure 7. Oyster spermatozoa observed by scanning electron microscopy after 1 h of exposure to 50 nm polystyrene nanobeads. The white arrows indicate the adhesion of nanoplastics on the head (red frame) and flagellum (green frame) of the spermatozoon [Source: © IFREMER / Kevin Tallec]
  • Nanoplastics have been observed by electron microscopy stuck to the surface of oyster spermatozoa (Figure 7), which would prevent their mobility necessary for their fertilizing ability [13].
  • Exposed for 24 hours to these nanobeads, oyster embryos show malformations up to complete  developmental arrest at high doses.

Finally, the diet of oysters, and more broadly of bivalves, may also be impacted since the life cycle of diatom micro-algae also appeared to be disrupted by these nanoplastics, showing the importance of understanding the effects of micro- and nano-plastics at the complex scale of ecosystems.

3. What can be done? Are there any solutions?

Many solutions exist or are to be discovered to decrease or stop the main anthropogenic pressures. We can cite the example of tributyltin, which was banned in France in 1982 and then generalized worldwide in 2001 due to its proven toxicity and environmental risks. However, finding alternatives to tributyltin, which are non-toxic and therefore without risk to the environment, is a complex issue requiring research and technological innovation. And this reasoning becomes more complex when considering the diversity of pollution, its sources and uses. No single solution can solve the problems.

Scientific monitoring and research are necessary to understand pollution and its effects in nature, and just as much to raise awareness among the general public and decision-makers. They are notably framed at the European level in the Marine Strategy Framework Directive (MSFD) [14], the objective of which is to achieve a “good ecological status” of European marine waters by 2020, a goal that will be extended in the years to come.

A juxtaposition of solutions along the entire value chain is and will therefore be necessary to limit and stem pollution at source. This involves :

  • Sobriety from the extraction of raw materials and production to their use (for example, for plastics, see the French parliamentary report [15]), and therefore changes in our industrial, agricultural and citizen behaviour;
  • A much better management of the end-of-life of products and waste;
  • Technological developments in industry, especially for new processes, products, materials such as bio-sourced and/or biodegradable, in any case without impacting the environment and human health (concept of safe-by-desing);
  • Legislation, in particular environmental law, for the development of legal rules aimed at protecting the environment. Protecting our coastal marine areas, so precious, is a way to strengthen the integrity of the ocean system, a common good of humanity.

4. Messages to remember

  • Many pollutants, pesticides, drug residues, heavy metals, microplastics, have effects on the entire life cycle of the oyster.
  • Some toxic effects can be propagated to the next generation of young oysters (embryotoxicity, endocrine disruption).
  • The “cocktail” effect of these pollutants (and more broadly the exposome) remains to be studied for the understanding of the evolution of oyster populations.
  • Oysters, present on our coasts for millions of years, are now alerting us to the need for strong measures to protect coastal habitats.

Notes and references

Cover image. Oyster larvae that ingested green microplastics during a laboratory experiment [Source: © IFREMER / Rossana Sussarellu]

[1] Thomas, Y. (2018). Oysters as sentinels of climate variability and climate change in coastal ecosystems. Environmental Research Letters 13, 104009. Publisher’s official version : https://doi.org/10.1088/1748-9326/aae254, Open Access version : https://archimer.ifremer.fr/doc/00461/57255/

[2] https://perturbateursendocrinienssite.wordpress.com/2017/05/04/tributyletain/

[3] https://fr.wikipedia.org/wiki/Antifouling

[4] Chapelle, A. (2016). Modélisation du phytoplancton dans les écosystèmes côtiers. Application à l’eutrophisation et aux proliférations d’algues toxiques. https://archimer.ifremer.fr/doc/00360/47141/

[5] https://wwz.ifremer.fr/envlit/Surveillance-du-littoral/Phytoplancton-et-phycotoxines

[6] Payton, L. (2017). Chronobiologie moléculaire et comportementale des huîtres Crassostrea gigas diploïdes et triploïdes exposées à l’algue toxique Alexandrium minutum. Thèse de l’Université de Bordeaux. https://tel.archives-ouvertes.fr/tel-01579783/document

[7] Castrec, J (2018). Impacts des efflorescences du dinoflagellé toxique Alexandrium minutum sur la reproduction et le développement de l’huître Crassostrea gigas. Thèse de l’Université de Bretagne occidentale. https://tel.archives-ouvertes.fr/tel-03035012/document

[8] Gadelha, J.R. (2019). Persistent and emerging pollutants assessment on aquaculture oysters (Crassostrea gigas) from NW Portuguese coast. Science of the Total Environment, 666, 731-742.

[9] Bachere, E. (2017). Parental diuron-exposure alters offspring transcriptome and fitness in Pacific oyster Crassostrea gigas. Ecotoxicology and Environmental Safety, 142, 51-58. https://doi.org/10.1016/j.ecoenv.2017.03.030

[10] Epelboin, Y. (2015). Energy and Antioxidant Responses of Pacific Oyster Exposed to Trace Levels of Pesticides. Chemical Research In Toxicology, 28, 1831-1841. Publisher’s official version : https://doi.org/10.1021/acs.chemrestox.5b00269, Open Access version : https://archimer.ifremer.fr/doc/00284/39490/

[11] Melwani, A.R. (2016). PAHs and heavy metals at each sampling location along the west coast of India around Goa, India. Aquatic Toxicology, 173, 53-62.

[12] Sussarellu, R. (2016). Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. USA, 113, 2430-2435. Open Access version: https: //archimer.ifremer.fr/doc/00311/42233/

[13] Tallec, K. (2019). Impacts des nanoplastiques et microplastiques sur les premiers stades de vie (gamètes, embryons, larves) de l’huître creuse Crassostrea gigas. Thèse de l’Université de Bretagne occidentale. https://tel.archives-ouvertes.fr/tel-02996550/document

[14] https://wwz.ifremer.fr/Expertise/Eau-Biodiversite/Directive-Cadre-Strategie-pour-le-Milieu-Marin

[15] http://www.senat.fr/fileadmin/Fichiers/Images/redaction_multimedia/2020/2020-Documents_pdf/20201512_Conf_presse_OPECST/Rapport_final.pdf


环境百科全书由环境和能源百科全书协会出版 (www.a3e.fr),该协会与格勒诺布尔阿尔卑斯大学和格勒诺布尔INP有合同关系,并由法国科学院赞助。

引用这篇文章: HUVET Arnaud, SANCHEZ Wilfried, POUVREAU Stéphane, FABIOUX Caroline (2021年12月10日), The oyster, the sentinel of a coastline to be preserved, 环境百科全书,咨询于 2024年10月8日 [在线ISSN 2555-0950]网址: https://www.encyclopedie-environnement.org/en/life/oyster-sentinel-of-coastline-to-be-preserved/.

环境百科全书中的文章是根据知识共享BY-NC-SA许可条款提供的,该许可授权复制的条件是:引用来源,不作商业使用,共享相同的初始条件,并且在每次重复使用或分发时复制知识共享BY-NC-SA许可声明。