Data from: Cascading effects of defaunation on the coexistence of two specialized insect seed predators

Identification of the mechanisms enabling stable coexistence of species with similar resource requirements is a central challenge in ecology. Such coexistence can be facilitated by species at higher trophic levels through complex multi-trophic interactions, a mechanism that could be compromised by ongoing defaunation.

We investigated cascading effects of defaunation on Pachymerus cardo and Speciomerus giganteus, the specialized insect seed predators of the Neotropical palm Attalea butyracea, testing the hypothesis that vertebrate frugivores and granivores facilitate their coexistence.

Laboratory experiments showed that the two seed parasitoid species differed strongly in their reproductive ecology. Pachymerus produced many small eggs that it deposited exclusively on the fruit exocarp (exterior). Speciomerus produced few large eggs that it deposited exclusively on the endocarp, which is normally exposed only after a vertebrate handles the fruit. When eggs of the two species were deposited on the same fruit, Pachymerus triumphed only when it had a long head start, and the loser always succumbed to intraguild predation.

We collected field data on the fates of 6569 Attalea seeds across sites in central Panama with contrasting degrees of defaunation and wide variation in the abundance of vertebrate frugivores and granivores. Speciomerus dominated where vertebrate communities were intact, whereas Pachymerus dominated in defaunated sites. Variation in the relative abundance of Speciomerus across all 84 sampling sites was strongly positively related to the proportion of seeds attacked by rodents, an indicator of local vertebrate abundance.

Synthesis. We show that two species of insect seed predators relying on the same host plant species are niche differentiated in their reproductive strategies such that one species has the advantage when fruits are handled promptly by vertebrates and the other when they are not. Defaunation disrupts this mediating influence of vertebrates and strongly favours one species at the expense of the other, providing a case study of the cascading effects of defaunation and its potential to disrupt coexistence of non-target species, including the hyperdiverse phytophagous insects of tropical forests.

解析资源需求相似的物种实现稳定共存的内在机制，是生态学领域的核心挑战之一。高营养级物种可通过复杂的多营养级相互作用（multi-trophic interactions）促进此类物种的稳定共存，而持续的动物区系丧失（defaunation）可能会破坏这一调控机制。

本研究以新热带棕榈（Attalea butyracea）的两种专性昆虫种子捕食者Pachymerus cardo与Speciomerus giganteus为研究对象，旨在验证“脊椎动物食果动物与食籽动物可促进二者共存”的假说，探究动物区系丧失对这两种昆虫的级联效应（cascading effects）。

室内实验结果显示，这两种种子寄生昆虫的繁殖生态学特征存在显著差异：Pachymerus cardo可产出大量小型卵粒，且仅将卵产于果实外果皮（exocarp）表面；而Speciomerus giganteus仅产出少量大型卵粒，且仅将卵产于果实内果皮（endocarp）表面——而内果皮通常仅在脊椎动物处理果实后才会暴露。当两种昆虫的卵被产于同一果实时，仅当Pachymerus cardo拥有足够长的产卵前置时间时才能胜出，落败一方总会死于集团内捕食（intraguild predation）。

研究团队在巴拿马中部的多个样地收集了6569颗新热带棕榈（Attalea butyracea）种子的命运数据，这些样地的动物区系丧失程度各不相同，脊椎动物食果者与食籽者的丰度也存在显著差异。结果显示，在脊椎动物群落完整的样地中，Speciomerus giganteus占据优势；而在动物区系丧失的样地中，Pachymerus cardo则为优势物种。在全部84个采样样地中，Speciomerus giganteus的相对丰度变化与被啮齿动物取食的种子比例呈显著正相关——而该比例可作为当地脊椎动物丰度的指示指标。

综合与结论：本研究证实，依赖同一寄主植物的两种昆虫种子捕食者，其繁殖策略存在明确的生态位分化——当果实被脊椎动物快速处理时，其中一种昆虫具备竞争优势；而当果实未被脊椎动物处理时，另一种昆虫则占据优势。动物区系丧失会破坏脊椎动物的这一中介调控作用，显著偏向其中一种物种而抑制另一种，本研究为动物区系丧失的级联效应及其可能破坏非靶标物种共存的现象提供了典型案例，其中也包括热带森林中高度多样的植食性昆虫（phytophagous insects）类群。