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.

已知植物入侵和隨后的群落變化會影響營養(yǎng)循環(huán)，但大多數(shù)此類研究側(cè)重于富營養(yǎng)化效應(yīng)。針對植物引起的營養(yǎng)減少的效應(yīng)以及同時發(fā)生的機制的研究則相對較少。在這項研究中，我們發(fā)現(xiàn)通常作為侵入種的椰子的入侵作用通過間接的影響,中止了外來海洋入侵物種對陸地生態(tài)系統(tǒng)的侵入:對鳥類的影響 - 鳥類會盡量避免筑巢在椰子樹種群中，因此減少了從海洋環(huán)境帶來的關(guān)鍵營養(yǎng)物質(zhì)輸入。這些海洋物質(zhì)輸入的下降導(dǎo)致了土壤養(yǎng)分的減少，葉片營養(yǎng)質(zhì)量的下降，葉片的適度性下降及食草動物的減少。這種營養(yǎng)耗竭的過程比植物種群入侵導(dǎo)致的富營養(yǎng)化模式更為典型。對于空間中外來能量中斷對生態(tài)系統(tǒng)的影響的研究表明其尚未受到接受群落變化的干擾，如植物群落轉(zhuǎn)變。在熱帶和亞熱帶地區(qū)的椰子植物入侵的普遍性使得這些研究特別值得注意。

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. 

同樣重要的是，美洲黑斑病的近況提供了一個強有力的范例，說明植物群落的變化如何可以顯著影響同種異體營養(yǎng)的供應(yīng)，從而重塑生態(tài)系統(tǒng)的能量流。 椰子種群轉(zhuǎn)移|間接效應(yīng)|海鳥|熱帶島嶼通過刺激自下而上的能量流動，一個獨特的營養(yǎng)供應(yīng)鏈塑造了大部分生態(tài)系統(tǒng)的動態(tài)平衡（1,2）。輔助能的這種提高可以引發(fā)接收食物網(wǎng)中大量的級聯(lián)變化（3-5）。近期的幾篇文章已經(jīng)證明，在食物鏈頂端的外來捕食者可以通過影響這些輔助能的傳遞（如鳥類）引發(fā)生態(tài)系統(tǒng)級聯(lián)效應(yīng)，從而引發(fā)生態(tài)系統(tǒng)結(jié)構(gòu)和功能的全面轉(zhuǎn)變（6,7） ）。然而自上而下的影響可能不是輔助能中斷的唯一機制。在這里，我們證明椰子科植物的增殖通過為鳥類棲息地造成不良影響而造成相似的營養(yǎng)物質(zhì)消耗，具有較高的效果。鑒于這種植物在熱帶地區(qū)的全球擴散，我們的觀察有廣泛的適用性。更寬泛地說，這一觀察結(jié)果表明，同種異體輔助能可能受到受體系統(tǒng)物種特征的阻礙，使接受者體系比以前承認的輔助能運動更為積極。已經(jīng)確定的是，一種物種的生物入侵通常可以通過改變營養(yǎng)循環(huán)（8,9）在入侵的生態(tài)系統(tǒng)中具有級聯(lián)效應(yīng)。然而，在引入植物改變營養(yǎng)循環(huán)的大多數(shù)病例研究中，級聯(lián)效應(yīng)是由于植物對土壤的輸入增加（來自增加的凋落物或直接固氮）的結(jié)果）（10,11）。推測是引進物種通常從營養(yǎng)豐富中獲益（12）。然而，最近的工作記錄了一些入侵植物在低營養(yǎng)環(huán)境中表現(xiàn)良好（13）表明，需要對專門從事低營養(yǎng)系統(tǒng)的引進植物進行更多的研究。 椰子可能起源于東南亞，然后通過天然（水）和人為散布（14）從這個起點開始區(qū)域輻射�？颇�斯的單一主要立場現(xiàn)在在世界各地的熱帶和亞熱帶周圍的許多島嶼和沿海森林中是常見的（參見Cocos nuci-fera：SI文本中的帕爾米拉的歷史和當前狀態(tài)）。在Palmyra環(huán)礁的Nucifera優(yōu)勢梯度上工作，這項研究考察了Nucifera增殖對生態(tài)系統(tǒng)生態(tài)學的影響。我們首先考察了在Nucifera和普通天然樹種之間的棲息地偏好，Pisonia grandis和Tournefortia argentea都在橫斷面和寬度范圍內(nèi)。然后，我們檢查了無花果優(yōu)勢對土壤和葉面營養(yǎng)水平的影響，以及葉面營養(yǎng)對葉片適口性和食草動物變化的影響。最后，為了證明高的椰子豐度是低土壤養(yǎng)分的一個原因而不是低土壤養(yǎng)分的影響（因為已知棕櫚能夠持續(xù)存在低營養(yǎng)土壤），我們比較了由疏浚填充物和天然產(chǎn)物制成的胰島之間的營養(yǎng)水平含有不同森林類型的小島。這種比較也使我們限制了營養(yǎng)物質(zhì)變化發(fā)生的最長時間。