Cross-system synthesis of consumer and nutrient resource control on producer biomass

Nutrient availability and herbivory control the biomass of primary producer communities to varying degrees across ecosystems. Ecological theory, individual experiments in many different systems, and system-specific quantitative reviews have suggested that 1) bottom-up control is pervasive but top-down control is more influential in aquatic habitats relative to terrestrial systems, and 2) bottom-up and top-down forces are interdependent, with statistical interactions that synergize or dampen relative influences on producer biomass. We used simple dynamic models to review ecological mechanisms that generate independent versus interactive responses of community-level biomass. We calibrated these mechanistic predictions with the metrics of factorial meta-analysis and tested their prevalence across freshwater, marine and terrestrial ecosystems with a comprehensive meta-analysis of 191 factorial manipulations of herbivores and nutrients. Our analysis showed that producer community biomass increased with fertilization across all systems, although increases were greatest in freshwater habitats. Herbivore removal generally increased producer biomass in both freshwater and marine systems, but its effects were inconsistent on land. With the exception of marine temperate rocky reef systems that showed positive synergism of nutrient enrichment and herbivore removal, experimental studies showed limited support for statistical interactions between nutrient and herbivory treatments on producer biomass. Top-down control of herbivores, compensatory behavior of multiple herbivore guilds, spatial and temporal heterogeneity of interactions, and herbivore-mediated nutrient recycling may lower the probability of consistent interactive effects on producer biomass. Continuing studies should expand the temporal and spatial scales of experiments, particularly in understudied terrestrial systems; broaden factorial designs to manipulate independently multiple producer resources (e.g. nitrogen, phosphorus, light), multiple herbivore taxa or guilds (e.g. vertebrates and invertebrates), and multiple trophic levels; and - in addition to measuring producer biomass - assess the responses of species diversity, community composition, and nutrient status.养分有效性（nutrient availability）与植食作用（herbivory）在不同生态系统中以各异的强度调控初级生产者群落（primary producer communities）的生物量。生态学理论、针对诸多不同系统的单项实验，以及针对特定系统的定量综述均表明：其一，上行控制（bottom-up control）普遍存在，但相较于陆地生态系统，下行控制（top-down control）在水生生境中的影响更为显著；其二，上行与下行作用力相互依存，二者的统计交互作用可协同或削弱对生产者生物量的相对调控效应。 我们借助简单动态模型，梳理了可引发群落生物量独立响应与交互响应的生态学机制。我们通过析因元分析（factorial meta-analysis）的指标对这些机制性预测进行校准，并针对淡水、海洋与陆地生态系统开展了一项涵盖191项植食者与养分操控析因实验的综合元分析，以此检验这些预测的普遍性。 分析结果显示，所有生态系统中，生产者群落生物量均随施肥（fertilization）处理而提升，不过淡水生境中的提升幅度最大。移除植食者通常会使淡水与海洋系统中的生产者生物量增加，但在陆地系统中其效应并不一致。除温带海洋岩礁系统表现出养分富集与植食者移除的正向协同效应（synergism）外，其余实验研究均未为养分与植食作用处理对生产者生物量的统计交互作用提供足够支持。植食者的下行控制、多植食者功能群（guilds）的补偿行为（compensatory behavior）、种间互作的时空异质性，以及植食者介导的养分循环，均可能降低此类交互作用对生产者生物量产生稳定一致影响的概率。 后续研究应从三方面拓展：一是扩大实验的时空尺度，尤其针对研究不足的陆地生态系统；二是拓展析因实验设计，以独立操控多种生产者资源（如氮、磷、光照）、多种植食者类群或功能群（如脊椎动物与无脊椎动物），以及多个营养级（trophic levels）；三是除测定生产者生物量外，还需评估物种多样性（species diversity）、群落组成（community composition）与养分状况（nutrient status）的响应。