Density-dependent effects of simultaneous root and floral herbivory on plant fitness and defense

Plants are attacked by multiple herbivores, and depend on a precise regulation of responses to cope with a wide range of antagonists. Simultaneous herbivory can occur in different plant compartments, which may pose a serious threat to plant growth and reproduction. In particular, plants often face co-occurring root and floral herbivory, but few studies have focused on such interactions. Here, we investigated in the field the combined density-dependent effects of root-chewing cebrionid beetle larvae and flower-chewing pierid caterpillars on the fitness and defense of a semiarid Brassicaceae herb. We found that the fitness impact of both herbivore groups was independent and density-dependent. Increasing root herbivore density non-significantly reduced plant fitness, while the relationship between increasing floral herbivore density and the reduction they caused in both seed number and seedling emergence was non-linear. The plant defensive response was non-additive with regard to the different densities of root and floral herbivores; high floral herbivore density provoked compensatory investment in reproduction, and this tolerance response was combined with aboveground chemical defense induction when also root herbivore density was high. Plants may thus prioritize specific trait combinations in response to varying combined below- and aboveground herbivore densities to minimize negative impacts on fitness.

植物会受到多种植食者的侵袭，需精准调控自身防御响应以应对各类拮抗生物。不同植物组织可同时发生植食为害，这会对植物的生长与繁殖造成严重威胁。具体而言，植物常同时面临地下根系与地上花部的植食为害，但目前针对这类交互作用的研究仍较为匮乏。本研究通过野外实验，探究了取食根系的伪叶甲科（Cebrionidae）甲虫幼虫与取食花部的粉蝶科（Pieridae）蝶类幼虫的密度联合效应，对一种半干旱地区十字花科（Brassicaceae）草本植物适合度与防御特性的影响。研究结果表明，两类植食者对植物适合度的影响均为独立且密度依赖的。随着根系植食者密度升高，植物适合度呈现统计上不显著的下降；而花部植食者密度升高时，其导致的种子数量与幼苗出苗率下降均呈非线性关系。植物的防御响应对根系与花部植食者的不同密度组合呈现非加性模式；当花部植食者密度较高时，植物会启动繁殖补偿投入，而当根系植食者密度同时升高时，这种耐受性响应会与地上化学防御的诱导共同发挥作用。因此，植物可针对地下与地上植食者密度的动态组合，优先调控特定性状组合，以最大限度降低植食为害对自身适合度的负面影响。