Successional Change in Phosphorus Stoichiometry Explains the Inverse Relationship between Herbivory and Lupin Density on Mount St. Helens

BackgroundThe average nitrogen-to-phosphorus ratio (N∶P) of insect herbivores is less than that of leaves, suggesting that P may mediate plant-insect interactions more often than appreciated. We investigated whether succession-related heterogeneity in N and P stoichiometry influences herbivore performance on N-fixing lupin (Lupinus lepidus) colonizing primary successional volcanic surfaces, where the abundances of several specialist lepidopteran herbivores are inversely related to lupin density and are known to alter lupin colonization dynamics. We examined larval performance in response to leaf nutritional characteristics using gelechiid and pyralid leaf-tiers, and a noctuid leaf-cutter. Methodology/Principal FindingsWe conducted four studies. First, growth of larvae raised on wild-collected leaves responded positively to leaf %P and negatively to leaf carbon (%C), but there was no effect of %N or quinolizidine alkaloids (QAs). Noctuid survival was also positively related to %P. Second, we raised gelechiid larvae on greenhouse-grown lupins with factorial manipulation of competitors and soil N and P. In the presence of competition, larval mass was highest at intermediate leaf N∶P and high %P. Third, survival of gelechiid larvae placed on lupins in high-density patches was greater when plant competitors were removed than on controls. Fourth, surveys of field-collected leaves in 2000, 2002, and 2003 indicated that both %P and %N were generally greater in plants from low-density areas. QAs in plants from low-density areas were equal to or higher than QAs in high-density areas. Conclusions/SignificanceOur results demonstrate that declines in lupin P content under competitive conditions are associated with decreased larval growth and survival sufficient to cause the observed negative relationship between herbivore abundance and host density. The results support the theoretical finding that declines in stoichiometric resource quality (caused here by succession) have the potential to cause a decrease in consumer abundance despite very dense quantities of the resource.研究背景 植食性昆虫的平均氮磷比（N∶P）低于植物叶片，这表明磷（P）在植物-昆虫互作中的调控作用可能比此前认知的更为普遍。本研究针对原生演替火山生境中定植的固氮羽扇豆（Lupinus lepidus）展开探究，旨在明确其氮磷化学计量学的演替相关异质性是否会影响植食性昆虫的生长表现——该生境中数种专一性鳞翅目植食昆虫的丰度与羽扇豆种群密度呈负相关，且已知这类昆虫会改变羽扇豆的定植动态。本研究分别选取麦蛾科（Gelechiidae）、螟蛾科（Pyralidae）的结叶幼虫以及夜蛾科（Noctuidae）的切叶幼虫，探究幼虫生长表现对叶片营养特征的响应。 研究方法与主要结果 本研究共开展四项实验：其一，以野外采集的叶片饲养幼虫，结果显示幼虫生长速率与叶片全磷百分比（%P）呈正相关，与叶片全碳百分比（%C）呈负相关，但全氮百分比（%N）及喹诺里西啶生物碱（quinolizidine alkaloids, QAs）未表现出显著影响；夜蛾幼虫的存活率同样与%P呈正相关。其二，在温室中种植羽扇豆，并通过析因实验设计调控竞争者、土壤氮与磷水平，以此饲养麦蛾幼虫。结果发现，在存在竞争者的条件下，幼虫体重在叶片N∶P处于中等水平且%P较高时达到峰值。其三，将麦蛾幼虫接种至高密度羽扇豆种群中，移除植物竞争者组的幼虫存活率显著高于对照组。其四，对2000、2002及2003年野外采集的叶片开展调查，结果显示低密度种群中的羽扇豆叶片%P与%N整体更高；而低密度种群植株的喹诺里西啶生物碱含量则等于或高于高密度种群植株。 研究结论与意义 本研究结果表明，竞争条件下羽扇豆叶片磷含量的下降，会导致幼虫生长与存活率显著降低，这足以解释已观测到的“植食昆虫丰度与寄主植物密度呈负相关”的现象。本研究结果支持相关理论预测：即由演替过程引发的化学计量学资源质量下降，即便寄主资源总量依然充足，仍有可能导致消费者种群丰度降低。