Department of Forestry and Natural Resources, Purdue University, West Lafayette, Indiana, 47907, USA.
Department of Entomology, University of Minnesota, Saint Paul, Minnesota, 55108, USA.
Ecology. 2020 Nov;101(11):e03156. doi: 10.1002/ecy.3156. Epub 2020 Sep 2.
Changes in thermal regimes that disparately affect hosts and parasitoids could release hosts from biological control. When multiple natural enemy species share a host, shifts in host-parasitoid dynamics could depend on whether natural enemies interact antagonistically vs. synergistically. We investigated how biotic and abiotic factors influence the population ecology of larch casebearer (Coleophora laricella), a nonnative pest, and two imported parasitoids, Agathis pumila and Chrysocharis laricinellae, by analyzing (1) temporal dynamics in defoliation from 1962 to 2018, and (2) historical, branch-level data on densities of larch casebearer and parasitism rates by the two imported natural enemies from 1972 to 1995. Analyses of defoliation indicated that, prior to the widespread establishment of parasitoids (1962 to ~1980), larch casebearer outbreaks occurred in 2-6 yr cycles. This pattern was followed by a >15-yr period during which populations were at low, apparently stable densities undetectable via aerial surveys, presumably under control from parasitoids. However, since the late 1990s and despite the persistence of both parasitoids, outbreaks exhibiting unstable dynamics have occurred. Analyses of branch-level data indicated that growth of casebearer populations, A. pumila populations, and within-casebearer densities of C. laricinellae-a generalist whose population dynamics are likely also influenced by use of alternative hosts-were inhibited by density dependence, with high intraspecific densities in one year slowing growth into the next. Casebearer population growth was also inhibited by parasitism from A. pumila, but not C. laricinellae, and increased with warmer autumnal temperatures. Growth of A. pumila populations and within-casebearer densities of C. laricinellae increased with casebearer densities but decreased with warmer annual maximum temperatures. Moreover, parasitism by A. pumila was associated with increased growth of within-casebearer densities of C. laricinellae without adverse effects on its own demographics, indicating a synergistic interaction between these parasitoids. Our results indicate that warming can be associated with opposing effects between trophic levels, with deleterious effects of warming on one natural enemy species potentially being exacerbated by similar impacts on another. Coupling of such parasitoid responses with positive responses of hosts to warming might have contributed to the return of casebearer outbreaks to North America.
热环境的变化对寄主和寄生生物的影响各不相同，可能会使寄主摆脱生物控制。当多种天敌物种共享一个寄主时，寄主-寄生生物动态的变化可能取决于天敌是相互拮抗还是协同作用。我们通过分析（1）1962 年至 2018 年期间的落叶时间动态，以及（2）1972 年至 1995 年期间历史上、树枝级别的有关舞毒蛾幼虫（Coleophora laricella）、两种进口寄生生物（Agathis pumila 和 Chrysocharis laricinellae）密度和寄生率的数据，来研究生物和非生物因素如何影响非本地害虫舞毒蛾幼虫及其两种进口寄生生物的种群生态学。分析落叶表明，在寄生生物广泛建立之前（1962 年至~1980 年），舞毒蛾幼虫每隔 2-6 年爆发一次。在接下来的 15 年多时间里，种群密度处于低水平，显然处于稳定状态，通过航空调查无法检测到，可能是受到寄生生物的控制。然而，自 20 世纪 90 年代末以来，尽管两种寄生生物仍然存在，但不稳定的爆发已经发生。树枝级数据的分析表明，舞毒蛾幼虫种群、A. pumila 种群以及舞毒蛾幼虫内 C. laricinellae 的密度——一种可能还受到替代寄主利用影响的广食性种——受到密度依赖性的抑制，当年的高种内密度会减缓下一年的生长。舞毒蛾幼虫的种群增长也受到 A. pumila 的寄生抑制，但不受 C. laricinellae 的影响，并且随着秋季温度的升高而增加。A. pumila 种群的生长和舞毒蛾幼虫内 C. laricinellae 的密度随着舞毒蛾幼虫密度的增加而增加，但随着年最高温度的升高而减少。此外，A. pumila 的寄生作用与舞毒蛾幼虫内 C. laricinellae 密度的增加有关，而对其自身的种群动态没有不利影响，表明这两种寄生生物之间存在协同作用。我们的研究结果表明，变暖可能与营养级之间存在相反的影响有关，一种天敌物种受到变暖的不利影响可能会因类似的影响而加剧另一种天敌物种的影响。这种寄生生物反应与寄主对变暖的积极反应的结合，可能促成了舞毒蛾幼虫在美国的再次爆发。
