Data from: Nontarget herbivory by a weed biocontrol insect is limited to spillover, reducing the chance of population-level impacts

Insects approved for classical biocontrol of weeds are often capable of using close relatives of their target weed for feeding, oviposition, or larval development, with reduced preference and performance. When nontarget herbivory occurs and is suspected to reduce survival, growth, or fecundity of individual plants, and insects are capable of reproducing on their nontarget host, characterization of spatial and temporal patterns of the occurrence and intensity of herbivory is valuable for predicting potential population-level effects. Here, we perform a novel post-release manipulative field experiment with a root-feeding biocontrol weevil, Mogulones crucifer, released in Canada to control the rangeland weed Cynoglossum officinale, to test for its ability to establish on the nontarget plant Hackelia micrantha. After Cynoglossum, M. crucifer exhibits its highest preference for and performance on Hackelia spp. We released M. crucifer on Canadian rangeland sites with naturally occurring populations of H. micrantha growing interspersed with the target weed or in the near absence of the target weed. Adult weevil feeding on surrounding plants was monitored for three summers after release (years 0, 1, and 2), and, subsequently, subsets of plants were destructively sampled to determine M. crucifer oviposition levels. Additional oviposition and larval development data were obtained from seven non-experimental sites where weevils were released zero, three, or four years earlier. M. crucifer was not detected on experimental sites without C. officinale after two years, and nontarget herbivory was restricted to rare, low-level spillover. Visible evidence of adult herbivory (i.e., scars on shoots) was associated with oviposition in 90% of targets but only 30% of nontarget plants. We infer, through ecological refuge theory, that nontarget population-level impacts from M. crucifer spillover are unlikely because of temporal, spatial, and probabilistic refuges from herbivory, and make recommendations for monitoring and management of biocontrol systems with similar attributes, such as removing target plants around nontarget populations of interest. Because M. crucifer is among the least host-specific of the modern weed biocontrol agents, and H. micrantha is likely one of its most highly preferred nontargets, these conclusions are, arguably, generally applicable to other nontarget plants and biocontrol systems.

获批用于杂草经典生物防治（classical biocontrol of weeds）的昆虫，通常可利用靶标杂草的近缘物种完成取食、产卵或幼虫发育，但其对这类近缘物种的偏好性与适合度表现会有所降低。当发生非靶标植食作用（nontarget herbivory）且推测其会降低单株植物的存活率、生长速率或繁殖力，同时昆虫可在非靶标寄主上完成繁殖时，明确植食作用发生的时空格局与强度，对预测其潜在的种群水平影响具有重要价值。本研究针对在加拿大用于防治牧场杂草普通牛舌草（Cynoglossum officinale）的取食根系生物防治象鼻虫Mogulones crucifer，开展了一项新颖的释后操控性田间试验，以验证其能否在非靶标植物小花鹤虱（Hackelia micrantha）上定殖。相较于普通牛舌草，M. crucifer对鹤虱属（Hackelia spp.）植物展现出最高的偏好性与适合度表现。我们将M. crucifer释放至加拿大的多个牧场样地，这些样地中自然分布有小花鹤虱种群，且要么与靶标杂草伴生，要么几乎无靶标杂草生长。在释放后的三个夏季（第0、1、2年），我们对取食周边植物的成虫象鼻虫进行监测；随后通过破坏性采样部分植株，以确定M. crucifer的产卵量。此外，我们从7个非试验样地获取了额外的产卵与幼虫发育数据，这些样地分别在0年、3年或4年前释放了该象鼻虫。释放两年后，在无普通牛舌草的试验样地中未检测到M. crucifer，且非靶标植食作用仅局限于罕见的低水平溢出效应。成虫植食作用的可见证据（即枝条上的取食伤痕）在90%的靶标植株中与产卵相关联，但在非靶标植株中仅占30%。基于生态避难理论（ecological refuge theory），我们推断：由于存在时间、空间与概率层面的植食避难所，M. crucifer的溢出效应不太可能对非靶标种群造成种群层面的影响；同时我们针对具有类似特征的生物防治系统的监测与管理提出建议，例如在受关注的非靶标种群周边移除靶标杂草。鉴于M. crucifer是现代杂草生物防治制剂中宿主特异性最低的物种之一，且小花鹤虱极有可能是其偏好性最高的非靶标寄主之一，因此我们的结论可推广至其他非靶标植物与生物防治系统。