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.

用于杂草经典生物防治的昆虫，通常能够利用靶标杂草的近缘物种进行取食、产卵或幼虫发育，但其取食偏好与适合度表现均有所降低。当发生非靶标植食作用且疑似会降低单个植株的存活率、生长量或繁殖力，且昆虫能够在非靶标寄主上繁殖时，表征植食作用发生的时空格局与强度，对于预测其潜在的种群水平效应具有重要价值。本研究针对一种取食根部的生防控虫象甲十字根象甲（Mogulones crucifer）开展了一项新颖的释放后控制性田间试验：该象甲曾在加拿大被释放用于防治牧场杂草药用牛舌草（Cynoglossum officinale），本试验旨在验证其能否在非靶标植物小花鹤虱（Hackelia micrantha）上定殖。除药用牛舌草外，十字根象甲对鹤虱属（Hackelia spp.）植物的取食偏好与适合度表现最高。我们在加拿大的牧场样地中释放了十字根象甲，这些样地内自然分布有小花鹤虱种群，且小花鹤虱或与靶标杂草混生，或几乎无靶标杂草生长。在释放后的三个夏季（第0、1、2年），我们对取食周边植株的成年象甲进行监测；随后通过破坏性取样部分植株，以测定十字根象甲的产卵量。另有7个非试验样地的相关数据，这些样地分别在0、3、4年前释放过该象甲，从中我们获取了额外的产卵量与幼虫发育数据。释放两年后，在无药用牛舌草的试验样地中未检测到十字根象甲，且非靶标植食作用仅表现为罕见的低水平溢出效应。在90%的靶标植株中，成年象甲植食作用的可见证据（即茎部伤痕）与产卵行为存在关联，但在非靶标植株中这一比例仅为30%。基于生态避难所理论，我们推断：由于植食作用存在时间、空间与概率性三重避难所，十字根象甲的溢出效应不太可能对非靶标种群造成种群水平影响；据此我们针对具有类似特征的生物防治系统，提出了监测与管理建议，例如移除关注的非靶标种群周边的靶标植物。由于十字根象甲是现代杂草生防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，因此可以认为，本研究结论普遍适用于其他非靶标植物与生物防治系统。