Mycorrhizal-herbivore interactions and the competitive release of subdominant tallgrass prairie species

Plant-microbial-herbivore interactions play a crucial role in the structuring and maintenance of plant communities and biodiversity, yet these relationships are complex. In grassland ecosystems, herbivores have the potential to greatly influence the survival, growth, and reproduction of plants. However, few studies examine interactions of above- and belowground grazing and AM mycorrhizal symbiosis on plant community structure. We established experimental mesocosms containing an assemblage of eight tallgrass prairie grass and forb species in native prairie soil, maintained under mycorrhizal and nonmycorrhizal conditions, with and without native herbivorous soil nematodes, and with and without grasshopper herbivory. Using factorial analysis of variance and principal component analysis, we examined: a) the independent and interacting effects of above- and belowground herbivores on AM symbiosis in tallgrass prairie mesocosms, b) independent and interacting effects of above- and belowground herbivores and mycorrhizal fungi on plant community structure, and c) potential influences of mycorrhizal responsiveness of host plants on herbivory tolerance, and concomitant shifts in plant community composition. Treatment effects were characterized by interactions between AM fungi and both aboveground and belowground herbivores, while herbivore effects were additive. The dominance of mycorrhizal-dependent C4 grasses in the presence of AMF symbiosis was increased (p < 0.0001) by grasshopper herbivory but reduced (p < 0.0001) by nematode herbivory. Cool-season C3 grasses exhibited a competitive release in the absence of AMF symbiosis but this effect was largely reversed in the presence of grasshopper herbivory. Forbs showed species-specific responses to both AM fungal inoculation and the addition of herbivores. Biomass of the grazing-avoidant, facultatively mycotrophic forb Brickellia eupatorioides increased (p < 0.0001) in the absence of AMF symbiosis and with grasshopper herbivory, while AMF-related increases in the aboveground biomass of mycorrhizal-dependent forbs Rudbeckia hirta and Salvia azurea were eradicated (p < 0.0001) by grasshopper herbivory. In contrast, nematode herbivory enhanced (p = 0.001) the contribution of Salvia azurea to total biomass.

Synthesis: Our research indicates that AM symbiosis is the key driver of the dominance of C4 grasses in the tallgrass prairie, with foliar and root herbivory being two mechanisms for the maintenance of plant diversity.

Methods
Experimental tallgrass prairie plant communities were constructed and maintained in large mesocosms grown in a greenhouse facility at Kansas State University in Manhattan, KS, USA. Data collected includes end-of-season biomass production and colonization of roots by AM fungi.

植物-微生物-草食动物互作在植物群落与生物多样性的构建及维持中发挥至关重要的作用，然而此类关系纷繁复杂。在草原生态系统中，草食动物可对植物的存活、生长与繁殖产生极大影响。但目前鲜有研究探讨地上、地下放牧以及丛枝菌根（arbuscular mycorrhizal，AM）共生对植物群落结构的综合调控作用。本研究构建了包含8种高草草原禾本科与杂类草物种的中型实验生态系统（mesocosms），所用土壤取自原生高草草原，分别设置菌根与非菌根培养条件，添加或不添加原生草食性土壤线虫，同时设置有或无蝗虫取食的处理。本研究采用析因方差分析与主成分分析，探究以下三方面内容：a）地上与地下草食动物对高草草原中型实验生态系统中AM共生的独立及交互作用效应；b）地上、地下草食动物与菌根真菌对植物群落结构的独立及交互作用效应；c）宿主植物的菌根响应性对草食动物耐受能力的潜在影响，以及由此引发的植物群落组成变化。

实验结果显示，AM真菌与地上、地下草食动物间的交互作用决定了处理效应的特征，而草食动物的效应则呈加性模式。在AM真菌共生存在的情况下，依赖菌根的C4禾本科植物的优势度因蝗虫取食而显著提升（p < 0.0001），却因线虫取食而显著降低（p < 0.0001）。冷季型C3禾本科植物在无AM真菌共生时表现出竞争释放效应，但该效应在蝗虫取食存在时基本被逆转。杂类草对AM真菌接种及草食动物添加均表现出物种特异性响应。避牧性兼性菌养型杂类草Brickellia eupatorioides的生物量在无AM真菌共生且存在蝗虫取食时显著提升（p < 0.0001）；而依赖菌根的杂类草Rudbeckia hirta与Salvia azurea的地上生物量因AM真菌产生的增幅被蝗虫取食完全抵消（p < 0.0001）。与之相反，线虫取食可提升Salvia azurea对群落总生物量的贡献（p = 0.001）。

综合结论：本研究表明，AM共生是高草草原中C4禾本科植物占据优势的核心驱动因子，而地上与地下草食作用是维持植物多样性的两大关键机制。

方法：本研究在美国堪萨斯州曼哈顿市堪萨斯州立大学的温室设施内，构建并培育了大型中型实验生态系统中的高草草原植物群落。所采集的实验数据包括季末生物量产量以及AM真菌对植物根系的定殖率。