Department of Animal Ecology and Tropical Biology, Biocenter, University of Würzburg, Würzburg, Germany.
PLoS One. 2013 May 22;8(5):e63556. doi: 10.1371/journal.pone.0063556. Print 2013.
Many plants combat herbivore and pathogen attack indirectly by attracting predators of their herbivores. Here we describe a novel type of insect-plant interaction where a carnivorous plant uses such an indirect defence to prevent nutrient loss to kleptoparasites. The ant Camponotus schmitzi is an obligate inhabitant of the carnivorous pitcher plant Nepenthes bicalcarata in Borneo. It has recently been suggested that this ant-plant interaction is a nutritional mutualism, but the detailed mechanisms and the origin of the ant-derived nutrient supply have remained unexplained. We confirm that N. bicalcarata host plant leaves naturally have an elevated (15)N/(14)N stable isotope abundance ratio (δ(15)N) when colonised by C. schmitzi. This indicates that a higher proportion of the plants' nitrogen is insect-derived when C. schmitzi ants are present (ca. 100%, vs. 77% in uncolonised plants) and that more nitrogen is available to them. We demonstrated direct flux of nutrients from the ants to the host plant in a (15)N pulse-chase experiment. As C. schmitzi ants only feed on nectar and pitcher contents of their host, the elevated foliar δ(15)N cannot be explained by classic ant-feeding (myrmecotrophy) but must originate from a higher efficiency of the pitcher traps. We discovered that C. schmitzi ants not only increase the pitchers' capture efficiency by keeping the pitchers' trapping surfaces clean, but they also reduce nutrient loss from the pitchers by predating dipteran pitcher inhabitants (infauna). Consequently, nutrients the pitchers would have otherwise lost via emerging flies become available as ant colony waste. The plants' prey is therefore conserved by the ants. The interaction between C. schmitzi, N. bicalcarata and dipteran pitcher infauna represents a new type of mutualism where animals mitigate the damage by nutrient thieves to a plant.
许多植物通过吸引其食草动物的捕食者来间接抵御草食动物和病原体的侵害。在这里，我们描述了一种新型的昆虫与植物的相互作用，其中一种肉食性植物利用这种间接防御来防止其被偷窃者掠夺营养。蚂蚁 Camponotus schmitzi 是婆罗洲肉食性猪笼草 Nepenthes bicalcarata 的专性栖息者。最近有研究表明，这种蚂蚁与植物的相互作用是一种营养互惠关系，但蚂蚁提供的营养的详细机制和来源仍未得到解释。我们证实，当 C. schmitzi 蚂蚁定植于 N. bicalcarata 宿主植物叶片时，这些叶片的自然（15）N/（14）N 稳定同位素丰度比值（δ（15）N）会升高。这表明，当 C. schmitzi 蚂蚁存在时，植物的氮有更高比例来自昆虫（约 100%，而未定植的植物为 77%），而且它们有更多的氮可用。我们在一个（15）N 脉冲追踪实验中证明了营养物质直接从蚂蚁流向宿主植物。由于 C. schmitzi 蚂蚁仅以其宿主的花蜜和猪笼草内容物为食，因此升高的叶片 δ（15）N 不能用经典的蚂蚁喂养（拟蚁食）来解释，而必须源自猪笼草陷阱更高的效率。我们发现，C. schmitzi 蚂蚁不仅通过保持猪笼草表面清洁来提高猪笼草的捕获效率，还通过捕食双翅目猪笼草内生物（内生动物）来减少猪笼草营养物质的损失。因此，猪笼草原本会通过飞出的苍蝇而损失的营养物质，现在成为了蚂蚁 colony 的废物而变得可用。这些植物的猎物因此被蚂蚁所保护。C. schmitzi、N. bicalcarata 和双翅目猪笼草内生动物之间的相互作用代表了一种新的互惠关系，其中动物通过减少营养掠夺者对植物的损害来保护植物。
