Insects and pathogens frequently exploit the same host plant and can potentially impact each other's performance. However, studies on plant–pathogen–insect interactions have mainly focused on a fixed temporal setting or on a single interaction partner. In this study, we assessed the impact of time of attacker arrival on the outcome and symmetry of interactions between aphids (Tuberculatus annulatus), powdery mildew (Erysiphe alphitoides), and caterpillars (Phalera bucephala) feeding on pedunculate oak, Quercus robur, and explored how single versus multiple attackers affect oak performance. We used a multifactorial greenhouse experiment in which oak seedlings were infected with either zero, one, two, or three attackers, with the order of attacker arrival differing among treatments. The performances of all involved organisms were monitored throughout the experiment. Overall, attackers had a weak and inconsistent impact on plant performance. Interactions between attackers, when present, were asymmetric. For example, aphids performed worse, but powdery mildew performed better, when co-occurring. Order of arrival strongly affected the outcome of interactions, and early attackers modified the strength and direction of interactions between later-arriving attackers. Our study shows that interactions between plant attackers can be asymmetric, time-dependent, and species specific. This is likely to shape the ecology and evolution of plant–pathogen–insect interactions.

中文翻译：

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植物-病原体-昆虫相互作用的时间和不对称性

昆虫和病原体经常利用同一个寄主植物，并且可能会影响彼此的性能。然而，关于植物-病原体-昆虫相互作用的研究主要集中在固定的时间环境或单一的相互作用伙伴上。在这项研究中，我们评估了攻击者到达时间对以有蒂橡树、栎属植物为食的蚜虫（Tuberculatus annulatus）、白粉病（Erysiphe alphitoides）和毛虫（Phalera bucephala）之间相互作用的结果和对称性的影响，并进行了探索单个攻击者与多个攻击者如何影响 Oak 性能。我们使用了一个多因素温室实验，其中橡树幼苗被零个、一个、两个或三个攻击者感染，攻击者到达的顺序因处理而异。在整个实验过程中监测所有相关生物的表现。总体而言，攻击者对工厂性能的影响微弱且不一致。攻击者之间的交互（如果存在）是不对称的。例如，当同时发生时，蚜虫表现更差，但白粉病表现更好。到达顺序强烈影响交互的结果，早期攻击者修改了后来到达的攻击者之间交互的强度和方向。我们的研究表明，植物攻击者之间的相互作用可能是不对称的、时间依赖性的和物种特异性的。这可能会影响植物-病原体-昆虫相互作用的生态和进化。例如，当同时发生时，蚜虫表现更差，但白粉病表现更好。到达顺序强烈影响交互的结果，早期攻击者修改了后来到达的攻击者之间交互的强度和方向。我们的研究表明，植物攻击者之间的相互作用可能是不对称的、时间依赖性的和物种特异性的。这可能会影响植物-病原体-昆虫相互作用的生态和进化。例如，当同时发生时，蚜虫表现更差，但白粉病表现更好。到达顺序强烈影响交互的结果，早期攻击者修改了后来到达的攻击者之间交互的强度和方向。我们的研究表明，植物攻击者之间的相互作用可能是不对称的、时间依赖的和物种特异性的。这可能会影响植物-病原体-昆虫相互作用的生态和进化。