Parasites can alter the traits or densities of mutualistic partners, potentially destabilizing mutualistic associations that underpin the structure, functioning, and stability of entire ecosystems. Despite the potentially wide-ranging consequences of such disruptions, no studies have directly manipulated parasite prevalence and/or intensity in a mutualistic partner, nor quantified the resulting community-level effects. Here, we investigated the effects of a common trematode parasite (Cercaria opaca) on the strength of a keystone facultative mutualism in western Atlantic salt marshes between the foundational marsh cordgrass, Spartina alterniflora, and the ribbed mussel, Geukensia demissa. Cordgrass increases mussel survivorship and growth through shading, while mussels enhance cordgrass growth by producing nutrient-rich biodeposits. This mutualistic association also creates conditions that enhance biodiversity and ecosystem functioning, and mediates the ability of foundational plants to resist and recover from extreme drought. We used lab and field assays to show how increasing infection with trematode metacercariae negatively influenced mussel biodeposit production, as well as the strength of mussel shells and byssal attachments. By conducting a field manipulation using experimentally infected mussels, we demonstrated that the mutualistic benefits of mussels to cordgrass growth decreased with increasing trematode infection intensity—a pattern likely generated by reduced mussel biodeposition and enhanced mortality. Additionally, increasing parasite loads in mussels led to predictable decreases in the abundances of benthic invertebrates, as well as in key ecosystem characteristics and process rates (i.e., redox potential and sediment accretion). Finally, a survey of five North Carolina salt marshes demonstrated that infection with C. opaca was most common in mussels in areas experiencing cordgrass die-off due to drought, and that infection intensity decreased with distance from die-off areas. Because the mussel–cordgrass mutualism underpins marsh ecosystem resilience to drought-associated die-off, our results suggest that parasitism may depress recovery from these disturbances. Although this is the first experimental demonstration of parasites indirectly altering community structure and functioning by undermining an ecologically influential mutualism, this type of relationship could be common in nature, given that parasites frequently infect influential mutualists.

中文翻译：

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寄生虫破坏了支撑沿海生态系统结构、功能和复原力的关键共生关系


寄生虫可以改变互惠伙伴的特征或密度，可能会破坏支撑整个生态系统的结构、功能和稳定性的互惠关系的稳定性。尽管这种破坏可能产生广泛的后果，但没有研究直接操纵互惠伙伴的寄生虫流行率和/或强度，也没有量化由此产生的社区层面的影响。在这里，我们研究了常见的吸虫寄生虫 （Cercaria opaca） 对西大西洋盐沼中基础沼泽草 Spartina alterniflora 和罗纹贻贝 Geukensia demissa 之间的基石兼性共生强度的影响。Cordgrass 通过遮荫提高贻贝的存活率和生长能力，而贻贝通过产生营养丰富的生物沉积物来促进 Cordgrass 的生长。这种互惠互利的联系还创造了增强生物多样性和生态系统功能的条件，并介导了基础植物抵抗极端干旱并从中恢复的能力。我们使用实验室和现场分析来显示吸虫 metacercariae 感染的增加如何对贻贝生物沉积物的产生以及贻贝壳和贻贝附着体的强度产生负面影响。通过使用实验感染的贻贝进行田间操作，我们证明贻贝对绳索草生长的互惠益处随着吸虫感染强度的增加而降低——这种模式可能是由贻贝生物沉积减少和死亡率增加引起的。此外，贻贝中寄生虫负荷的增加导致底栖无脊椎动物的丰度以及关键的生态系统特征和加工速率（即、氧化还原电位和沉积物增加）。最后，对北卡罗来纳州五个盐沼的调查表明，在因干旱导致灯芯草死亡的地区的贻贝中，羊苔藓感染最为常见，并且感染强度随着与死亡地区的距离而降低。由于贻贝-绳索草共生关系支撑着沼泽生态系统对干旱相关死亡的恢复力，我们的结果表明，寄生可能会抑制从这些干扰中恢复。虽然这是寄生虫通过破坏具有生态影响力的共生主义来间接改变群落结构和功能的首次实验证明，但鉴于寄生虫经常感染有影响力的互惠论者，这种类型的关系在自然界中可能很常见。