School of Molecular and Life Sciences, Curtin University, Kent Street, Bentley, WA 6102, Australia.
Ecological Health Network, 1330 Beacon St., Suite 355a, Brookline, MA 02446, USA.
Ann Bot. 2022 Dec 31;130(7):927-938. doi: 10.1093/aob/mcac134.
While isotopic enrichment of nitrogen (15N) and carbon (13C) is often used to determine whether carnivorous plant species capture and assimilate nutrients from supplemental sources such as invertebrate prey or mammal excreta (heterotrophic nutrition), little is known about how successful the different strategies deployed by carnivorous plants are at obtaining supplemental nutrition. The collection of mammalian faeces by Nepenthes (tropical pitcher plants) is the result of a highly specialized biological mutualism that results in heterotrophic nitrogen gain; however, it remains unknown how effective this strategy is in comparison to Nepenthes species not known to collect mammalian faeces.
We examined how isotopic enrichment varied in the diverse genus Nepenthes, among species producing pitchers for invertebrate capture and species exhibiting mutualisms for the collection of mammal excreta. Enrichment factors were calculated from δ15N and δ13C values from eight Nepenthes species and naturally occurring hybrids along with co-occurring reference (non-carnivorous) plants from three mountain massifs in Borneo: Mount Kinabalu, Mount Tambuyukon and Mount Trus Madi.
All Nepenthes examined, except N. edwardsiana, were significantly enriched in 15N compared to co-occurring non-carnivorous plants, and 15N enrichment was more than two-fold higher in species with adaptations for the collection of mammal excreta compared with other Nepenthes.
The collection of mammal faeces clearly represents a highly effective strategy for heterotrophic nitrogen gain in Nepenthes. Species with adaptations for capturing mammal excreta occur exclusively at high elevation (i.e. are typically summit-occurring) where previous studies suggest invertebrate prey are less abundant and less frequently captured. As such, we propose this strategy may maximize nutritional return by specializing towards ensuring the collection and retention of few but higher-value N sources in environments where invertebrate prey may be scarce.
尽管氮（15N）和碳（13C）的同位素富集通常用于确定肉食植物物种是否从补充来源（如无脊椎动物猎物或哺乳动物粪便）中捕获和同化营养物质（异养营养），但对于肉食植物不同策略获得补充营养的成功程度知之甚少。猪笼草（热带食虫植物）收集哺乳动物粪便，是一种高度专业化的生物互利共生的结果，导致异养氮的获得；然而，目前尚不清楚这种策略与那些已知不收集哺乳动物粪便的猪笼草物种相比，其效果如何。
我们研究了不同的猪笼草属中同位素富集的变化，这些物种包括产生用于捕获无脊椎动物的瓶状体的物种和表现出收集哺乳动物粪便的互利共生的物种。从婆罗洲三个山脉（京那巴鲁山、坦布幼昆山和特鲁苏马迪山）的八种猪笼草物种和自然发生的杂种以及共现的参考（非肉食性）植物中，计算了 δ15N 和 δ13C 值的富集因子。
除了 N. edwardsiana 之外，所有被检查的猪笼草都明显比共现的非肉食性植物富集 15N，而具有收集哺乳动物粪便适应能力的物种的 15N 富集程度比其他猪笼草高出两倍以上。
收集哺乳动物粪便显然是猪笼草获得异养氮的一种非常有效的策略。具有捕捉哺乳动物粪便适应能力的物种仅在高海拔（即通常是山顶）出现，在那里以前的研究表明无脊椎动物猎物较少且较不频繁地捕获。因此，我们提出这种策略可能通过专门收集和保留少数但更高价值的 N 源来最大化营养回报，特别是在无脊椎动物猎物可能稀缺的环境中。
