Dispersal and nutrient limitations of decomposition above the forest floor: evidence from experimental manipulations of epiphytes and macronutrients

1. Decomposition is a major component of global carbon cycling. However, approximately 50% of wood necromass and a small proportion of leaf litter do not contact the forest floor, and the factors that regulate the decomposition above the forest floor are largely untested. We hypothesized that separation from soil resources causes slower decomposition rates above the forest floor. Specifically, we tested whether slower decomposition results from decreased nutrient availability (the nutrient limitation hypothesis) and/or microbial dispersal limitation (the dispersal limitation hypothesis) in the absence of soil resources. 2. We tested these hypotheses by combining experimental manipulations of epiphytes and macronutrient fertilization with elemental analyses and community metabarcoding (fungi and prokaryotes). Specifically, we compared wood stick and cellulose decomposition among three treatments: an unaltered trunk section, an epiphyte mat, and a “removal treatment” where an epiphyte mat was removed to test the effect of soil resources. We also performed a factorial fertilization experiment to test the effects of nitrogen (N) and phosphorus (P) on the decomposition of suspended cellulose. 3. Decomposition rates were fastest on the epiphyte mats, intermediate in the removal treatment, and slowest in the controls. Phosphorus addition increased decomposition rates in the fertilization experiment, and greater P concentrations, along with some micronutrients, were associated with increased rates of decomposition on the epiphyte mats and in the removal treatments. Locally dispersed fungi dominated the wood stick communities, indicating that fungal dispersal is limited in the canopy, and fungal saprotrophs were associated with increased rates of decomposition on the epiphytes. 4. These experiments show that slowed decomposition above the forest floor is caused, in part, by separation from soil resources. Moreover, our findings provide support for both the nutrient limitation and dispersal limitation hypotheses and indicate that mechanisms regulating canopy-level decomposition differ from those documented on the forest floor. This demonstrates the need for a holistic approach to decomposition that considers the vertical position of necromass as it decomposes. Further experimentation is necessary to quantify interactions between community assembly processes, nutrient availability, substrate traits, and microclimate.

1. 分解作用是全球碳循环的核心组成部分。然而，约50%的木质残体（wood necromass）以及少量枯落叶（leaf litter）并未接触林地表层（forest floor），而调控林地表层以上分解过程的相关因子在很大程度上尚未得到实证验证。本研究提出假说：与土壤资源脱离会导致林地表层以上的分解速率减缓。具体而言，我们将检验：在缺乏土壤资源的条件下，分解速率减缓是否源于养分可利用性降低（养分限制假说，nutrient limitation hypothesis）和/或微生物扩散限制（扩散限制假说，dispersal limitation hypothesis）。2. 我们通过将附生植物（epiphyte）与大量元素施肥（macronutrient fertilization）的实验操控手段，与元素分析、针对真菌与原核生物的群落宏条形码测序（community metabarcoding）相结合，对上述假说开展验证。具体而言，我们比较了三种处理组的木棍与纤维素分解情况：未做修饰的树干切段、附生植物垫（epiphyte mat），以及“移除处理组”——移除附生植物垫以验证土壤资源的调控效应。此外，我们还实施了析因施肥实验，以检验氮（N）与磷（P）对悬浮纤维素分解的影响。3. 实验结果表明，附生植物垫上的分解速率最快，移除处理组居中，对照组最慢。施肥实验中，磷添加显著提升了分解速率；附生植物垫与移除处理组中，更高的磷浓度与部分微量元素的存在，均与分解速率提升呈显著正相关。木棍定殖的真菌群落以本地扩散类群为主，表明冠层内真菌扩散存在明显限制；而真菌腐养生物（fungal saprotrophs）与附生基质上的分解速率提升显著相关。4. 本研究证实，林地表层以上的分解过程减缓，部分源于其与土壤资源的脱离。此外，研究结果同时为养分限制假说与扩散限制假说提供了支持，并表明调控冠层尺度分解过程的机制，与林地表层已报道的分解调控机制存在显著差异。这一发现凸显了采用整体性研究范式开展分解研究的必要性，即需考虑残体在分解进程中的垂直空间位置。未来仍需开展进一步实验，以量化群落组装（community assembly）过程、养分可利用性、基质性状与微气候（microclimate）之间的交互作用。