Meta-analysis of marine nutrient-enrichment experiments: systematic variation in the magnitude of nutrient limitation

Nutrient bioassay experiments have been performed in many marine and estuarine environments around the world. Although protocols have been relatively uniform, these experiments have yielded mixed results, implicating nitrogen, phosphorus, silica, iron, and several other elements as factors limiting phytoplankton growth. Meta-analysis has the potential to explain much of this variation by exploring the relationship between the magnitude of limitation and various environmental characteristics. We quantified limitation with a simple metric, Δr, that estimates the change in the per unit growth rate of phytoplankton directly attributable to addition of a specific nutrient, such as nitrogen, iron, or phosphorus. Preliminary analyses indicated that experiments lasting 1 d exhibited time lags in the numerical response of phytoplankton to nutrient addition, while experiments lasting greater than 7 d confounded nutrient limitation with processes such as increased grazing or depletion of other nutrients. Thus, we restricted the meta-analysis to results from 2-7 d experiments. These analyses showed that phosphorus enrichment usually had little impact on phytoplankton growth, while enrichments of nitrogen and iron increased phytoplankton growth by 0.1-0.3 d-1. Nutrient limitation due to N, P, and Fe varied significantly among sites. Nitrogen limitation was greatest in nearshore, nutrient-polluted, and temperate environments (where most experiments have been performed), while phosphorus and iron limitation were strongest in open ocean, unpolluted, and tropical ecosystems, or those receiving pollutants with high N:P ratios. Because phosphorus-enrichment studies have been most often performed in relatively polluted coastal waters, the possible role of phosphorus in limiting primary production in unpolluted oceanic systems may have been underestimated.Examining heterogeneity of responses of different systems to experiments is a valuable application of meta-analysis and can facilitate the development of new ecological insights.全球诸多海洋与河口生境均已开展营养物生物测定（nutrient bioassay）实验。尽管实验方案相对统一，但此类实验得到的结果却存在较大分歧，表明氮、磷、硅、铁及其他多种元素均可能为浮游植物（phytoplankton）生长的限制因子。元分析（meta-analysis）可通过探究限制强度与各类环境特征间的关联，为解释该差异提供有效途径。我们采用简便指标Δr对限制作用进行量化，该指标可估算由特定营养物（如氮、铁或磷）添加直接导致的浮游植物单位生长速率变化。初步分析显示，时长1天的实验会出现浮游植物对营养物添加的数值响应时滞现象，而时长超过7天的实验则会将营养限制与牧食作用增强、其他营养物耗竭等过程相混淆。因此，我们将本次元分析限定于时长2~7天的实验结果。分析结果表明，磷富集通常对浮游植物生长影响甚微，而氮与铁富集可使浮游植物生长速率提升0.1~0.3 d⁻¹。由氮、磷、铁引发的营养限制在不同采样点间存在显著差异。氮限制在近岸、受营养盐污染的温带生境（此类生境也是多数实验的开展地）中最为显著，而磷与铁限制则在开阔大洋、未受污染的热带生态系统，或接收高氮磷比污染物的生态系统中最为突出。由于磷富集相关研究多在污染程度较高的近岸海域开展，因此磷在未受污染的大洋系统中限制初级生产（primary production）的潜在作用可能被低估了。探究不同生态系统对实验的响应异质性是元分析极具价值的应用方向，该方法可助力新生态学认知的形成与发展。