亚热带27种木本植物叶片性状对植食作用的影响: 验证生长-防御权衡假说

doi:10.17521/cjpe.2023.0290

摘要/Abstract

摘要：

木本植物的植食率存在巨大的种间差异, 并极大地调控着森林生态系统功能。生长-防御权衡假说认为, 植物的固有生长率决定着其在防御和生长方面的投资权衡, 从而影响植食率的种间变异。但生长-防御权衡假说的普适性仍然存在巨大争议, 尤其在物种高度丰富的亚热带森林。该研究测量了12种与植食性昆虫适口性相关的叶片性状, 并通过大样本调查植物物种的植食率, 探究亚热带地区27种木本植物叶片性状的权衡关系以及这些性状对植食率和植物生长率的影响。该研究发现: 1)控制性状的系统发育依赖性后, 物种在空间上的排序并没有呈现一维的“生长-防御”权衡; 2)缩合单宁和可溶性酚含量等化学防御性状对植食率没有显著影响; 3)物种固有的生长速度与化学防御物质之间也并没有表现出权衡关系。该研究结果没有支持生长-防御权衡假说的观点, 亚热带森林的植物在进化上可能同时经历环境和天敌的强烈选择, 使植物表现出更加灵活的性状组合来适应复杂的生物和非生物环境。

关键词: 植物防御, 生态系统功能, 单宁含量, 植物-昆虫互作, 系统发育主成分, 权衡策略

Abstract:

Aims Differences in herbivory among plant species can greatly affect the functioning of forest ecosystems. However, little is known about the main drivers causing interspecific differences in herbivore damage among tree species. The growth-defence trade-off hypothesis posits that the intrinsic growth rate of plant species governs resource allocation between defense and growth, thereby shaping interspecific variation in herbivory. However, the validity of this hypothesis is extensively debated, especially in highly species-rich subtropical forests.

Methods We quantified leaf herbivore damage in 27 native tree species in a tree species diversity experiment conducted in subtropical China. We measured 12 leaf traits associated with insect palatability and relative growth rates of 27 tree species. Using a combination of phylogenetic multivariate analyses, we assessed trade-offs between leaf traits and the relative effect of these traits on leaf herbivore damage.

Important findings We found 1) neither phylogenetic principal component analysis nor hierarchical cluster analysis supported the idea that species displayed one-dimensional trade-off; 2) Conventional strategies, such as content of condensed tannins, are not strongly involved as a defence against herbivores; 3) No significant trade-off between plant intrinsic growth rate and chemical defence traits for the 27 studied tree species. Our results do not support arguments for growth-defense trade-off hypothesis. Rather, plants exhibit a range of combinations of leaf traits. We suggest this lack of a one-dimensional trade-off may be adaptive, resulting from selective pressure to adopt a different combination of defences to coexisting species.

Key words: plant defense, ecosystem function, tannin content, plant-insect interactions, phylogenetic principal component, trade-off strategies

王振宇, 黄志群. 亚热带27种木本植物叶片性状对植食作用的影响: 验证生长-防御权衡假说. 植物生态学报, 2024, 48(11): 1501-1509. DOI: 10.17521/cjpe.2023.0290

WANG Zhen-Yu, HUANG Zhi-Qun. Effects of leaf traits on herbivory across 27 woody plants in the subtropical forest: testing the growth-defense trade-off hypothesis. Chinese Journal of Plant Ecology, 2024, 48(11): 1501-1509. DOI: 10.17521/cjpe.2023.0290

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2023.0290

https://www.plant-ecology.com/CN/Y2024/V48/I11/1501

图/表 6

图1 亚热带森林27种木本植物的系统发育树和叶片植食率(平均值±标准差)。括号内数字为重复数。

Fig. 1 Phylogenetic tree and leaf damage (%) on young, fully expanded leaves of 27 tree species in subtropical forests (mean ± SD). Number of repetitions in parentheses.

图2 亚热带12个叶片性状的系统发育主成分分析(PPCA, A)与前两个系统发育主成分轴上的物种坐标(B)。Cellulose, 纤维素含量; C:N, 碳氮比; LA, 叶面积; LC, 叶碳含量; LDMC, 叶干物质含量; Lignin, 木质素含量; LN, 叶氮含量; LP, 叶磷含量; LT, 叶厚度; Phenolics, 可溶性酚含量; SLA, 比叶面积; Tannin, 单宁含量。

Fig. 2 Biplot of the factor loadings for traits on the first two axes of the phylogenetic principal component analysis (PPCA, A) and biplot of species coordinates arrayed on the first two axes of the phylogenetic principal component analysis (B). Cellulose, cellulose content; C:N, carbon:nitrogen; LA, leaf area; LC, leaf carbon content; LDMC, leaf dry matter content; Lignin, lignin content; LN, leaf nitrogen content; LP, leaf phosphorus content; LT, leaf thickness; Phenolics, soluble phenolics content; SLA, specific leaf area; Tannin, tannin content.

表1 亚热带森林27种木本两两性状间系统发育最小二乘(PGLS)模型系数

Table 1 Coefficient of univariate phylogenetic generalized least squares (PGLS) models for trait pairs of 27 woody species in subtropical forests

性状 Trait	LA	LP	LT	LC	LN	LDMC	SLA	Tannin	Phenolics	Cellulose	Lignin
LP	-0.93^***
LT	0.79^***	-0.56^***
LC	1.13^**	-1.20^***	1.20^***
LN	0.19	0.77	0.21	-0.39
LDMC	0.32	-1.08^**	0.89	0.37	-0.35^*
SLA	-0.85^***	0.89^***	-1.24^***	-0.44^***	0.14	-0.36^***
Tannin	-0.59^***	0.49^***	-0.72^***	-0.22^***	0.00	-0.12^*	0.42^***
Phenolics	-0.72^**	0.94^***	-1.09^***	-0.56^***	0.01	-0.30^*	0.81^***	1.57^***
Cellulose	-0.68^**	0.27	-0.30	-0.28	0.01	0.21	-0.11	0.24	-0.19
Lignin	-1.20^***	0.79^***	-1.48^***	-0.20	-0.05	-0.20	0.77^***	2.01^***	0.38	0.11
C:N	0.24	-1.07^**	0.25	0.68^*	-0.90^***	0.51^*	-0.91^*	-0.57	-0.31	-0.18	0.04

表2 亚热带森林27种木本植物叶片性状在前4个系统发育主成分(PPCA)上的因子载荷

Table 2 Factor loadings of the first four components of phylogenetic principal component analysis (PPCA) on traits of 27 woody species in subtropical forests

	PPCA 1	PPCA 2	PPCA 3	PPCA 4
叶面积 Leaf area	0.90	-0.38	-0.01	-0.02
叶磷含量 Leaf phosphorus content	-0.90	-0.11	0.36	0.00
叶厚度 Leaf thickness	0.96	-0.08	0.15	-0.01
叶碳含量 Leaf carbon content	0.67	0.00	-0.60	-0.30
叶氮含量 Leaf nitrogen content	-0.06	-0.32	0.67	-0.59
碳氮比 Carbon:nitrogen	0.21	0.30	-0.75	0.47
叶干物质含量 Leaf dry matter content	0.43	0.66	-0.16	0.31
比叶面积 Specific leaf area	-0.85	-0.38	0.10	-0.18
单宁含量 Tannin content	-0.98	-0.05	-0.10	0.00
可溶性酚含量 Soluble phenolics content	-0.70	-0.46	0.14	0.48
纤维素含量 Cellulose content	-0.19	0.84	0.42	-0.05
木质素含量 Lignin content	-0.80	0.09	-0.40	-0.30

图3 亚热带森林物种分层聚类图。底部的每个分支代表一个物种。

Fig. 3 Phenogram from hierarchical cluster analysis in subtropical forests. Each branch at the bottom of the phenogram represents one species.

图4 系统发育最小二乘(PGLS)最优模型中叶片功能性状和相对生长率对植食率的影响(A)以及PGLS最优模型中叶片功能性状对相对生长率的影响(B)。点和线分别表示系数的平均值和95%的置信区间。Cellulose, 纤维素含量; LDMC, 叶干物质含量; LP, 叶磷含量; RGR, 相对生长率; Tannin, 单宁含量。*, p < 0.05; ***, p < 0.001。

Fig. 4 Effects of leaf traits and relative growth rates on the mean proportion of leaf damage by insect herbivores in most parsimonious phylogenetic generalized least squares (PGLS) model (A), and effects of leaf functional traits on relative growth rate in most parsimonious PGLS model (B). Points and lines show the means and 95% credible intervals of the coefficients, respectively. Cellulose, cellulose content; LDMC, leaf dry matter content; LP, leaf phosphorus content; RGR, relative growth rate; Tannin, tannin content. *, p < 0.05; ***, p < 0.001.

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