Understanding the ecosystem implications of the angiosperm rise to dominance: leaf litter decomposability among magnoliids and other basal angiosperms

Guofang Liu1#, William K. Cornwell2,7#, Xu Pan1,3, Kunfang Cao4,5, Xuehua Ye1, Zhenying Huang1, Ming Dong1,6* and Johannes H. C. Cornelissen2

1State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; 2Systems Ecology, Department of Ecological Science, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands; 3Graduate University of Chinese Academy of Sciences, Beijing 100049, China; 4Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan 666303, China; 5College of Forestry, Guangxi University, Nanning 530004, China; 6College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, China; and 7School of Biological, Earth and Environmental Science, University of New South Wales, Kensington 2052, Sydney, Australia
*Correspondence author: E-mail: dongming@hznu.edu.cn
#Equal first authors.

凋落物降解是碳和营养循环的关键驱动因子。基于现存的物种枯落物降解数据,一些进化分支的枯落物降解速率差异很大,这也意味着在被子植物的早期进化史中物种替换对碳和营养循环产生潜在影响。已有数据表明,与裸子植物、蕨类和苔藓植物相比,目前占绝对优势的核心真双子叶植物(eudicot)叶枯落物降解更快。这个分支演化中缺少一个关键拼图——基部被子植物(basal angiosperm)对过去碳和营养循环的作用。由于基部被子植物由于与水分运输能力有关的植物叶片和个体结构上的限制,因此可以假定这个分支的物种应该具有低的叶枯落物降解速率的资源维护型特点,高降解速率的叶片应出现在低矮植物上。 利用降解袋法进行同质园实验,总共选择物种128种,其中基部被子植物86种、核心真双子叶植物33种、裸子植物5种和蕨类4种,通过非线性拟合获取每个物种的衰减常数k值(降解速率)。结果表明:基部被子植物的降解速率远低于核心真双子叶植物,有趣的是基部被子植物中胡椒科分支的叶枯落物降解速率远高于基部被子植物其他分支。核心真双子叶植物的降解速率一般较高,而这个分支上的植物高度不一,从矮小草本到高大木本。这些结果意味着在被子植物早期进化史中木兰类植物不大可能是森林里的优势种,也不大可能产生资源获得型的叶子以及快速降解的叶枯落物。从裸子植物的低降解速率到被子植物的高降解速率的进化中,主要依靠核心真双子叶植物的进化。

Summary
1. Litter decomposition has been a key driver of carbon and nutrient cycling in the present and past. Based on extant species data, there is a great deal of variation in litter decomposability among major plant lineages, suggesting potential shifts in plant effects on carbon and nutrient cycling during the early evolutionary history of angiosperms.

2. Existing data suggest that eudicot species produce faster decomposing litter compared to gymnosperms, ferns and mosses. One of the missing puzzle pieces in this transition is the basal angiosperms, the functional role of which in past carbon and nutrient cycling has seldom been investigated. We hypothesized that owing to constraints on leaf and plant design related to hydraulic capacity, basal angiosperm trees should generally have resource conservative leaves of low decomposability and that fast-decomposing leaves may only be found in short-statured taxa.

3. We performed a litterbag experiment with simultaneous outdoor incubation of leaf litters in a common environment, including 86 basal angiosperm species (including the magnoliid lineage), 33 eudicots, five gymnosperms and four ferns. We fit a nonlinear model to the decomposition data, and each species’ decomposability was estimated using the proportional rate of mass loss through the experiment.

4. The mass loss rates were 59.2% lower in basal angiosperms than in eudicot trees. There was one exceptional group within basal angiosperms: the Piperales had higher k values than other magnoliid lineages, but all of the free-standing species were short. Eudicots had higher k values overall and covered a range of plant statures from small-statured herbs to big woody trees.

5. Synthesis. Understanding the ecosystem-level effects of the angiosperm rise to dominance is a crucial goal. Our results indicated that, among generally slow-decomposing magnoliid lineages, only the Piperales have fast decomposition rate associated with small plant statures. Thus it is unlikely that early magnoliid trees were both forest canopy dominants and produced resource acquisitive leaves turning into fast decomposable litter during the evolutionary history of angiosperms. Key-words: ancestral character state estimation, basal angiosperm, character diversification, evolution, growth form, leaf litter decomposability, magnoliids, Piperales, plant–soil (below-ground) interactions.