Specialized natural enemies have long been used to implement the biological control of invasive insects. Although research tracking populations following biological control introductions has traditionally focused on the impact of the introduced agent, recent studies and reviews have reflected an appreciation of the complex interactions of the introduced specialist agents with native generalist natural enemies. These interactions can be neutral, antagonistic, or complementary. Here we studied the invasive defoliator winter moth (Operophtera brumata) in the Northeast USA to investigate the role of native, generalist pupal predators along with the introduced, host-specific parasitoid Cyzenis albicans. Prior research in Canada has shown that predation of winter moth pupae from native generalists increased after C. albicans was established as a biological control agent. To explain this phenomenon, the following hypotheses were suggested: (H₁) parasitoids suppress the winter moth population to a density that can be maintained by generalist predators, (H₂) unparasitized pupae are preferred by predators and therefore experience higher mortality rates, or (H₃) C. albicans sustains higher predator populations throughout the year more effectively than winter moth alone. We tested these hypotheses by deploying winter moth pupae over 6 years spanning 2005 to 2017 and by modeling pupal predation rates as a function of winter moth density and C. albicans establishment. We also compared predation rates of unparasitized and parasitized pupae and considered additional mortality by a native pupal parasitoid. We found support for the first hypothesis; we detected both temporal and spatial density dependence, but only in the latter years of the study when winter moth densities were low. We found no evidence for the latter two hypotheses. Our findings suggest that pupal predators have a regulatory effect on winter moth populations only after populations have been reduced, presumably by the introduction of the host-specific parasitoid C. albicans.

中文翻译：

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本地通才天敌和引进的专业寄生蜂共同控制入侵的森林昆虫

专门的天敌长期以来一直被用来实施入侵昆虫的生物防治。尽管生物控制引入后跟踪人群的研究传统上侧重于引入代理的影响，但最近的研究和评论反映了对引入的专业代理与本地通才天敌的复杂相互作用的认识。这些相互作用可以是中性的、对立的或互补的。在这里，我们研究了美国东北部的侵入性落叶冬蛾 ( Operophtera brumata )，以调查本地的通才蛹捕食者以及引入的宿主特异性寄生蜂Cyzenis albicans的作用. 加拿大的先前研究表明，在白色念珠菌被确定为生物控制剂后，对本地通才的冬蛾蛹的捕食增加了。为了解释这一现象，提出了以下假设：(H ₁ ) 拟寄生物将冬蛾种群抑制到通才捕食者可以维持的密度，(H ₂ ) 捕食者更喜欢未寄生的蛹，因此死亡率更高，或者(H ₃ )白色念珠菌比单独的冬蛾更有效地维持全年更高的捕食者种群。我们通过在 2005 年至 2017 年的 6 年间部署冬蛾蛹，并将蛹的捕食率建模为冬蛾密度和白色念珠菌的函数来检验这些假设成立。我们还比较了未寄生和寄生蛹的捕食率，并考虑了本地蛹寄生蜂的额外死亡率。我们找到了对第一个假设的支持；我们检测到时间和空间密度依赖性，但仅在研究的后几年冬季飞蛾密度较低时才检测到。我们没有发现后两个假设的证据。我们的研究结果表明，只有在种群数量减少后，蛹捕食者才会对冬蛾种群产生调节作用，这可能是由于引入了宿主特异性寄生蜂C. albicans。