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Urban stormwater and crude oil injury pathways converge on the developing heart of a shore-spawning marine forage fish
Aquatic Toxicology ( IF 4.5 ) Pub Date : 2020-10-11 , DOI: 10.1016/j.aquatox.2020.105654
Louisa B. Harding , Mark Tagal , Gina M. Ylitalo , John P. Incardona , Jay W. Davis , Nathaniel L. Scholz , Jenifer K. McIntyre

Understanding how aquatic organisms respond to complex chemical mixtures remains one of the foremost challenges in modern ecotoxicology. Although oil spills are typically high-profile disasters that release hundreds or thousands of chemicals into the environment, there is growing evidence for a common adverse outcome pathway (AOP) for the vulnerable embryos and larvae of fish species that spawn in oiled habitats. Molecular initiating events involve the disruption of excitation-contraction coupling in individual cardiomyocytes, which then dysregulate the form and function of the embryonic heart. Phenanthrenes and other three-ring (tricyclic) polycyclic aromatic hydrocarbons (PAHs) are key drivers for this developmental cardiotoxicity and are also relatively enriched in land-based urban runoff. Similar to oil spills, stormwater discharged from roadways and other high-traffic impervious surfaces contains myriad contaminants, many of which are uncharacterized in terms of their chemical identity and toxicity to aquatic organisms. Nevertheless, given the exceptional sensitivity of the developing heart to tricyclic PAHs and the ubiquitous presence of these compounds in road runoff, cardiotoxicity may also be a dominant aspect of the stormwater-induced injury phenotype in fish early life stages. Here we assessed the effects of traffic-related runoff on the embryos and early larvae of Pacific herring (Clupea pallasii), a marine forage fish that spawns along the coastline of western North America. We used the well-characterized central features of the oil toxicity AOP for herring embryos as benchmarks for a detailed analysis of embryolarval cardiotoxicity across a dilution gradient ranging from 12 to 50% stormwater diluted in clean seawater. These injury indicators included measures of circulatory function, ventricular area, heart chamber looping, and the contractility of both the atrium and the ventricle. We also determined tissue concentrations of phenanthrenes and other PAHs in herring embryos. We find that tricyclic PAHs are readily bioavailable during cardiogenesis, and that stormwater-induced toxicity is in many respects indistinguishable from canonical crude oil toxicity. Given the chemical complexity of urban runoff, non-tricyclic PAH-mediated mechanisms of developmental toxicity in fish remain likely. However, from the standpoint of managing wild herring populations, our results suggest that stormwater-driven threats to individual survival (both near-term and delayed mortality) can be understood from decades of past research on crude oil toxicity. Moreover, Pacific herring embryos are promising sentinels for water quality monitoring in nearshore marine habitats, as in situand sensitive indicators of both toxic runoff and the effectiveness of pollution reduction efforts such as green stormwater infrastructure.



中文翻译:

城市雨水和原油伤害途径汇聚在海岸产卵海洋饲料鱼的发育中心

了解水生生物如何对复杂的化学混合物做出反应仍然是现代生态毒理学面临的首要挑战之一。尽管溢油事故通常是引人注目的灾难,将数百或数千种化学物质释放到环境中,但越来越多的证据表明,在加油的栖息地中产卵的鱼类的易受害胚胎和幼虫具有常见的不良结局(AOP)。分子引发事件涉及单个心肌细胞中激发-收缩偶联的破坏,然后失调了胚胎心脏的形式和功能。菲和其他三环(三环)多环芳烃(PAHs)是这种发展性心脏毒性的主要驱动力,并且在陆基城市径流中也相对丰富。类似于漏油,从道路和其他高流量不透水表面排放的雨水含有无数的污染物,其中许多污染物的化学特性和对水生生物的毒性均未表征。然而,考虑到发育中的心脏对三环PAHs的特殊敏感性以及道路径流中这些化合物的普遍存在,心脏毒性也可能是鱼生命早期雨水诱导的伤害表型的主要方面。在这里,我们评估了与交通有关的径流对太平洋鲱鱼胚胎和早期幼虫的影响(鉴于发育中的心脏对三环PAHs的异常敏感性以及这些化合物在道路径流中的普遍存在,心脏毒性也可能是鱼生命早期雨水诱导的伤害表型的主要方面。在这里,我们评估了与交通有关的径流对太平洋鲱鱼胚胎和早期幼虫的影响(鉴于发育中的心脏对三环PAHs的异常敏感性以及这些化合物在道路径流中的普遍存在,心脏毒性也可能是鱼生命早期雨水诱导的伤害表型的主要方面。在这里,我们评估了与交通有关的径流对太平洋鲱鱼胚胎和早期幼虫的影响(lu豆),是沿北美西部海岸线产卵的海洋饲料鱼。我们使用鲱鱼胚胎的油毒性AOP的特征明确的中心特征作为基准,对在干净海水中稀释的12%至50%雨水的稀释梯度范围内的幼虫心脏毒性进行详细分析。这些损伤指标包括循环功能,心室面积,心室环回以及心房和心室的收缩性的量度。我们还确定了鲱鱼胚胎中菲和其他多环芳烃的组织浓度。我们发现三环PAHs在心脏发生过程中很容易被生物利用,并且雨水诱导的毒性在许多方面与规范的原油毒性没有区别。考虑到城市径流的化学复杂性,非三环PAH介导的鱼类发育毒性的机制仍然很可能。但是,从管理野生鲱鱼种群的角度来看,我们的结果表明,可以通过几十年来对原油毒性的研究来理解暴雨驱动的个体生存威胁(短期和延迟死亡)。此外,太平洋鲱鱼胚胎有望成为近岸海洋栖息地水质监测的前哨,因为关于有毒径流和减少污染工作(例如绿色雨水基础设施)的有效性的现场和敏感指标。

更新日期:2020-11-06
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