Plants cause ecosystem nutrient depletion via the interruption of bird-derived spatial subsidies

 

Plant introductions and subsequent community shifts are known to affect nutrient cycling, but most such studies have focused on nutrient enrichment effects. The nature of plant-driven nutrient depletions and the mechanisms by which these might occur are relatively poorly understood. In this study we demonstrate that the proliferation of the commonly introduced coconut palm, Cocos nucifera, interrupts the flow of allochthonous marine subsidies to terrestrial ecosystems via an indirect effect: impact on birds. Birds avoid nesting or roosting in C. nucifera, thus reducing the critical nutrient inputs they bring from the marine environment. These decreases in marine subsidies then lead to reductions in available soil nutrients, decreases in leaf nutrient quality, diminished leaf palatability, and reduced herbivory. This nutrient depletion path- way contrasts the more typical patterns of nutrient enrichment that follow plant species introductions. Research on the effects of spatial subsidy disruptions on ecosystems has not yet examined interruptions driven by changes within the recipient community, such as plant community shifts. The ubiquity of coconut palm introductions across the tropics and subtropics makes these obser- vations particularly noteworthy.

已知植物入侵和随后的群落变化会影响营养循环，但大多数此类研究侧重于富营养化效应。针对植物引起的营养减少的效应以及同时发生的机制的研究则相对较少。在这项研究中，我们发现通常作为侵入种的椰子的入侵作用通过间接的影响,中止了外来海洋入侵物种对陆地生态系统的侵入:对鸟类的影响 - 鸟类会尽量避免筑巢在椰子树种群中，因此减少了从海洋环境带来的关键营养物质输入。这些海洋物质输入的下降导致了土壤养分的减少，叶片营养质量的下降，叶片的适度性下降及食草动物的减少。这种营养耗竭的过程比植物种群入侵导致的富营养化模式更为典型。对于空间中外来能量中断对生态系统的影响的研究表明其尚未受到接受群落变化的干扰，如植物群落转变。在热带和亚热带地区的椰子植物入侵的普遍性使得这些研究特别值得注意。

Equally important, the case of C. nucifera provides a strong demonstration of how plant community changes can dramatically impact the supply of allochthonous nutrients and thereby reshape energy flow in ecosystems. Cocos nucifera | community shifts | indirect effects | seabird | tropical islands A llochthonous nutrient subsidies shape the dynamics of a broad range of ecosystems by stimulating bottom-up pro- ductivity (1, 2). This increase in productivity can then trigger a vast array of cascading changes in recipient food webs (3–5). Several recent articles have demonstrated that introduced predators operating near the top of food webs can initiate these kinds of cascading effects on ecosystems by impacting the vectors of these subsidies, such as birds, triggering whole-scale shifts in ecosystem structure and function (6, 7). Yet top-down effects may not be the only mechanism by which spatial subsidies are disrupted. Here, we demonstrate that the proliferation of the coconut palm, Cocos nucifera, causes similar nutrient depletions with higher order effects by creating poor habitat for birds. Given the global proliferation of this plant in the tropics, our obser- vations have a wide application. Even more broadly, this obser- vation suggests that allochthonous subsidies may be blocked by the characteristics of species in the recipient system, making the recipient system a more active player in subsidy movement than has previously been acknowledged. It is well established that the biological invasion of one species can have cascading effects across the invaded ecosystem, often through alteration of nutrient cycling (8, 9). However, in the majority of case studies where introduced plants have altered the nutrient cycle, the cascading effects have been as a result of increased inputs to the soil from the plants (either from increased litterfall or direct nitrogen fixation) (10, 11). The presumption is that introduced species generally profit from nutrient enrichment (12). However, recent work documenting that some invasive plants perform well in low-nutrient environ- ments (13) suggests that more research on introduced plants specializing in low-nutrient systems is needed. C. nucifera likely originated in Southeast Asia and then radi- ated regionally from this point of origin both via natural (water) and anthropogenic dispersal (14). Near monodominant stands of Cocos are now commonplace in many island and coastal forests around the tropics and subtropics of the world (see Cocos nuci- fera: Historyand CurrentStatus atPalmyra in theSI Text).Working across a gradient of C. nucifera dominance at Palmyra atoll, this study examined the impact of C. nucifera proliferation on eco- system ecology. We first examined habitat preferences of birds between C. nucifera and the common native tree species, Pisonia grandis andTournefortia argentea,both on transect- andatoll-wide scales. We then examined the effects of C. nucifera dominance on levels of soil and foliar nutrients, and the consequent effects of changes in foliar nutrients on leaf palatability and herbivory. Finally, to document that high C. nucifera abundance is a cause rather than an effect of low soil nutrients (because palms are known to be able to persist in low-nutrient soils), we compared nutrient levels between islets made from dredge fill and natural islets containing different forest types. This comparison also allowed us to constrain the maximum time over which nutrient changes occur. Our results indicate that C. nucifera can dramat- ically impact allochthonous nutrients supply, with higher order effects on these ecosystems. We suggest that plant-driven alter- ations of spatial subsidies of the kind we observed at Palmyra are probably widespread, and can substantially shape nutrient flow across ecosystems and trigger cascading ecosystem changes. 

同样重要的是，美洲黑斑病的近况提供了一个强有力的范例，说明植物群落的变化如何可以显著影响同种异体营养的供应，从而重塑生态系统的能量流。 椰子种群转移|间接效应|海鸟|热带岛屿通过刺激自下而上的能量流动，一个独特的营养供应链塑造了大部分生态系统的动态平衡（1,2）。辅助能的这种提高可以引发接收食物网中大量的级联变化（3-5）。近期的几篇文章已经证明，在食物链顶端的外来捕食者可以通过影响这些辅助能的传递（如鸟类）引发生态系统级联效应，从而引发生态系统结构和功能的全面转变（6,7） ）。然而自上而下的影响可能不是辅助能中断的唯一机制。在这里，我们证明椰子科植物的增殖通过为鸟类栖息地造成不良影响而造成相似的营养物质消耗，具有较高的效果。鉴于这种植物在热带地区的全球扩散，我们的观察有广泛的适用性。更宽泛地说，这一观察结果表明，同种异体辅助能可能受到受体系统物种特征的阻碍，使接受者体系比以前承认的辅助能运动更为积极。已经确定的是，一种物种的生物入侵通常可以通过改变营养循环（8,9）在入侵的生态系统中具有级联效应。然而，在引入植物改变营养循环的大多数病例研究中，级联效应是由于植物对土壤的输入增加（来自增加的凋落物或直接固氮）的结果）（10,11）。推测是引进物种通常从营养丰富中获益（12）。然而，最近的工作记录了一些入侵植物在低营养环境中表现良好（13）表明，需要对专门从事低营养系统的引进植物进行更多的研究。 椰子可能起源于东南亚，然后通过天然（水）和人为散布（14）从这个起点开始区域辐射。科莫斯的单一主要立场现在在世界各地的热带和亚热带周围的许多岛屿和沿海森林中是常见的（参见Cocos nuci-fera：SI文本中的帕尔米拉的历史和当前状态）。在Palmyra环礁的Nucifera优势梯度上工作，这项研究考察了Nucifera增殖对生态系统生态学的影响。我们首先考察了在Nucifera和普通天然树种之间的栖息地偏好，Pisonia grandis和Tournefortia argentea都在横断面和宽度范围内。然后，我们检查了无花果优势对土壤和叶面营养水平的影响，以及叶面营养对叶片适口性和食草动物变化的影响。最后，为了证明高的椰子丰度是低土壤养分的一个原因而不是低土壤养分的影响（因为已知棕榈能够持续存在低营养土壤），我们比较了由疏浚填充物和天然产物制成的胰岛之间的营养水平含有不同森林类型的小岛。这种比较也使我们限制了营养物质变化发生的最长时间。