New Phytologist ( IF 9.4 ) Pub Date : 2022-06-28 , DOI: 10.1111/nph.18345 Maria Sporbert 1, 2, 3 , Desiree Jakubka 1, 2 , Solveig Franziska Bucher 1, 2 , Isabell Hensen 1, 3 , Martin Freiberg 4 , Katja Heubach 5 , Andreas König 5 , Birgit Nordt 6 , Carolin Plos 1, 2, 3 , Ilona Blinova 7 , Aletta Bonn 1, 8, 9 , Barbara Knickmann 10 , Tomáš Koubek 11 , Anja Linstädter 12 , Tereza Mašková 11, 13 , Richard B Primack 14 , Christoph Rosche 1, 3 , Manzoor A Shah 15 , Albert-Dieter Stevens 6 , Katja Tielbörger 16 , Sabrina Träger 1, 3 , Christian Wirth 1, 4, 17 , Christine Römermann 1, 2
Introduction
The timing of phenological events (such as leaf emergence, flowering, fruiting and leaf senescence) is crucial for species resource acquisition and reproductive success (e.g. plant–pollinator interaction, Nord & Lynch, 2009; Liu et al., 2021). Phenology also has important implications for biotic interactions (e.g. herbivory) as well as for competitive hierarchies and ecosystem processes (Heberling et al., 2019; Kudo & Cooper, 2019). Many studies have demonstrated that plants are now leafing out earlier and flowering earlier in response to a warming climate (Blinova et al., 2003; Root et al., 2003; Wolkovich et al., 2012; Bucher et al., 2018; Menzel et al., 2020; Rosbakh et al., 2021). Plant functional traits (i.e. the morphological and physiological properties of plant species), affect species growth, reproduction and survival (Violle et al., 2007). There is some evidence that differences in functional traits among species may also be associated with interspecific variation in plant phenology (Sun & Frelich, 2011; Craine et al., 2012; Wolkovich & Cleland, 2014; Bucher et al., 2018; König et al., 2018; Bucher & Römermann, 2020; Segrestin et al., 2020; Liu et al., 2021).
Although > 85% of the species found in temperate ecosystems are herbaceous (Ellenberg & Leuschner, 2010), phenological research has disproportionately focused on trees and shrubs (Estrella et al., 2007; Vitasse et al., 2011; Panchen et al., 2014). While flowering times of herbaceous species, especially the onset of flowering or fruiting, are well studied (Fitter & Fitter, 2002; Craine et al., 2012; Segrestin et al., 2020; Renner et al., 2021), there is relatively little data available on leaf out times and later stages of phenology, such as leaf senescence and fruit maturation (Gallinat et al., 2015; Bucher & Römermann, 2021). Previous studies have found evidence which indicates that phenology is phylogenetically conserved, such that more closely related species tend to flower or leaf out at similar times (Bolmgren & Cowan, 2008; Davies et al., 2013). Therefore, species cannot be regarded as statistically independent, and one has to account for phylogenetic relationships when investigating predictors of phenological timing (Davis et al., 2010, 2013).
To expand our knowledge of herbaceous plant phenology, studies are needed in environments which are easily accessible, which can be replicated, and in which plants are easily identifiable and can be monitored throughout a growing season. Botanical gardens fulfil all of these requirements: they contain taxonomically and ecologically diverse collections of species, and plants are often maintained in specific locations, making them easier to find in a relatively small area throughout the year (Primack & Miller-Rushing, 2009; Huang et al., 2018; Primack et al., 2021).
The PhenObs initiative (www.idiv.de/en/phenobs.html) is an open network of botanical gardens across the Northern Hemisphere, where researchers and citizen scientists monitor the phenology of a large set of herbaceous species following standardized protocols (Nordt et al., 2021). With this approach, the PhenObs network broadens the geographic and climatic scope of phenological research on herbaceous species that previously often focused on local observations or small sets of species. As part of this network, plant phenology is also being linked to the study of plant functional traits to understand observed interspecific variations. Functional traits have been used to assign species to ecological groups and as proxies for more complex species characteristics such as species environmental tolerances, competitive ability and dispersal ability (Table 1). Key functional traits that are widely used include plant height, leaf area, specific leaf area (SLA; i.e. the ratio between leaf dry weight and leaf area), leaf nitrogen (N) content (Gaudet & Keddy, 1988; Bolmgren & Cowan, 2008; Moles et al., 2009; Sun & Frelich, 2011; Bucher et al., 2018; König et al., 2018; Liu et al., 2021), leaf dry matter content (LDMC, i.e. the ratio between leaf dry and leaf fresh weight), leaf carbon I content (Pérez-Harguindeguy et al., 2013) and seed mass (Primack, 1987; Moles & Westoby, 2003; Bolmgren & Cowan, 2008).
| Trait | Function, ecological meaning | Reported link to phenology |
|---|---|---|
| Plant height | Competitive ability, productivity (Gaudet & Keddy, 1988; Moles et al., 2009) | Smaller plants are associated with earlier flowering (Bolmgren & Cowan, 2008; Sun & Frelich, 2011; Segrestin et al., 2020; Liu et al., 2021) and earlier fruiting (Vile et al., 2006; Liu et al., 2021) |
| Leaf area | Competitive ability Díaz et al. (2004), productivity, light interception, leaf energy and water balance (Díaz et al., 2016) | Large-leafed species are associated with later leaf out (Sun et al., 2006; ZhiGuo et al., 2011) |
| Specific leaf area (SLA; ratio between leaf dry weight and leaf area) | Productivity, competitive ability, growth performance (Wright et al., 2004; Pérez-Harguindeguy et al., 2013) | Species with higher SLA are associated with later flowering (Sun & Frelich, 2011; König et al., 2018) and earlier leaf senescence (Bucher & Römermann, 2021) |
| Leaf dry matter content (LDMC; ratio between leaf dry and leaf fresh weight) | Competitive ability, resistance to physical hazards, productivity (Pérez-Harguindeguy et al., 2013) | Species with higher LDMC are associated with later leaf senescence (Bucher & Römermann, 2021) |
| Mass-based leaf carbon content | Structural compounds, performance (Larcher, 1994) | Species with higher leaf carbon content are associated with earlier flowering (Bucher et al., 2018) and later leaf senescence (Bucher & Römermann, 2021) |
| Mass-based leaf nitrogen content | Productivity, photosynthetic capacity (Wright et al., 2004; Bucher et al., 2018) | Species with higher leaf nitrogen content are associated with earlier flowering (Craine et al., 2012; Bucher et al., 2018) and earlier leaf senescence (Bucher & Römermann, 2021) |
| Seed mass | Regeneration (Leishman & Murray, 2001) | Species with heavier seeds are associated with earlier flowering (Primack, 1987; Vile et al., 2006; Bolmgren & Cowan, 2008) |
Previous studies have focused mainly on just one stage, or a few stages, of plant phenology and functional traits. As a result, it is unclear to what extent plant functional traits are associated with successive stages in plant phenology and which plant functional traits are the most important when aiming to predict plant phenology from traits. Studies on successive phenological stages are crucial in advancing the field of plant phenology as they allow researchers to focus on key functional traits associated with plant phenology. Further, such studies will clarify the mediating role of plant functional traits for responses in plant phenology to changes in climate. We therefore carried out a large-scale study of herbaceous plant phenology and functional traits at multiple botanical gardens using the standard protocols of the PhenObs initiative (Nordt et al., 2021). Here, we focus on seven functional traits that capture the essence of plant form and function, and that were identified in previous studies as relating to phenology (Table 1). For example, we expect plant height, a trait related to plant biomass production and competitive ability, to be positively associated with the onset of flowering, a relationship that has been found in several studies (see Table 1). More specifically, we investigate whether these functional traits are associated with various vegetative and reproductive stages in phenology and whether they might be used in the future as a substitute for time-intensive phenological monitoring.
We monitored the phenology of 212 perennial herbaceous plant species throughout the whole growing season across five botanical gardens in Germany, capturing the onset, end, and duration of vegetative (i.e. initial growth, leafing out and senescence) and reproductive (i.e. flowering and fruiting) phenological events. We combined information on species phenology with functional trait measurements for the same populations.
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Can functional traits predict vegetative and reproductive phenology of herbaceous species through the entire growing season? Phenology is assumed to be phylogenetically conserved; therefore, we expect that closely related species show greater similarities in the timing of phenological events than expected by chance. Further, we ask: are specific traits more important than the underlying phylogeny in predicting phenology?
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Which functional traits are most important at predicting herbaceous species phenology at each stage of the growing season?
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Are associations between phenology and functional traits consistent across the growing conditions of the different botanical gardens?
中文翻译：
功能性状影响营养和生殖植物物候的模式——一项多植物园研究
介绍
物候事件（如出叶、开花、结果和叶片衰老）的时间对于物种资源获取和繁殖成功至关重要（例如植物-传粉者相互作用，Nord & Lynch， 2009 年；Liu等人， 2021 年）。物候学对生物相互作用（例如食草）以及竞争等级和生态系统过程也具有重要意义（Heberling等人， 2019 年；Kudo 和 Cooper， 2019 年）。许多研究表明，随着气候变暖，植物现在更早开花，更早开花（Blinova等人， 2003 年；Root等人， 2003 年；沃尔科维奇等人， 2012；Bucher等人， 2018 年；Menzel等人， 2020 年；罗斯巴赫等人， 2021 年）。植物功能性状（即植物物种的形态和生理特性）影响物种的生长、繁殖和生存（Violle等， 2007）。有证据表明，物种间功能性状的差异也可能与植物物候的种间变异有关（Sun & Frelich, 2011 ; Craine et al ., 2012 ; Wolkovich & Cleland, 2014; Bucher等人， 2018 年；König等人， 2018 年；Bucher & Römermann， 2020 年；Segrestin等人， 2020 年；刘等人， 2021）。
尽管在温带生态系统中发现的 > 85% 的物种是草本的（Ellenberg & Leuschner, 2010），但物候研究却不成比例地集中在树木和灌木上（Estrella等人， 2007 年；Vitasse等人， 2011 年；Panchen等人， 2014 年）。虽然对草本植物的开花时间，尤其是开花或结果的开始时间进行了深入研究（Fitter & Fitter， 2002；Craine等人， 2012 年；Segrestin等人， 2020 年；Renner等人， 2021 年）)，关于叶片脱落时间和物候后期阶段的可用数据相对较少，例如叶片衰老和果实成熟（Gallinat等人， 2015 年；Bucher 和 Römermann， 2021 年）。先前的研究发现证据表明物候学在系统发育上是保守的，因此更密切相关的物种倾向于在相似的时间开花或开花（Bolmgren & Cowan, 2008 ; Davies et al ., 2013）。因此，物种不能被认为是统计独立的，在研究物候时间的预测因子时必须考虑系统发育关系（Davis et al ., 2010 , 2013）。
为了扩展我们对草本植物物候学的了解，需要在易于访问、可复制、植物易于识别并可在整个生长季节监测的环境中进行研究。植物园满足所有这些要求：它们包含在分类学和生态学上多样化的物种集合，并且植物通常保存在特定位置，因此全年在相对较小的区域内更容易找到它们（Primack & Miller-Rushing， 2009；Huang等人， 2018 年；Primack等人， 2021 年）。
PhenObs 倡议 (www.idiv.de/en/phenobs.html) 是一个横跨北半球的开放式植物园网络，研究人员和公民科学家在其中按照标准化协议监测大量草本物种的物候学 (Nordt等人) ., 2021）。通过这种方法，PhenObs 网络拓宽了草本物种物候研究的地理和气候范围，这些物种以前通常侧重于当地观察或小群物种。作为该网络的一部分，植物物候学也与植物功能性状的研究相关联，以了解观察到的种间变异。功能性状已被用于将物种分配到生态群中，并作为更复杂的物种特征的代表，例如物种环境耐受性、竞争能力和分散能力（表 1）。广泛使用的关键功能性状包括株高、叶面积、比叶面积（SLA；即叶干重与叶面积之比）、叶氮（N）含量（Gaudet & Keddy， 1988；Bolmgren & Cowan， 2008 年；鼹鼠等人， 2009；Sun & Frelich， 2011 年；Bucher等人， 2018 年；König等人， 2018 年；Liu et al ., 2021 )、叶片干物质含量 (LDMC, 即叶片干重与叶片鲜重的比值)、叶片碳 I 含量 (Pérez-Harguindeguy et al ., 2013 ) 和种子质量 (Primack, 1987 ; Moles & Westoby， 2003 年；Bolmgren & Cowan， 2008 年）。
| 特征 | 功能、生态意义 | 报告的物候学链接 |
|---|---|---|
| 株高 | 竞争能力、生产力（Gaudet & Keddy， 1988 年；Moles等人， 2009 年） | 较小的植物与较早开花（Bolmgren 和 Cowan， 2008 年；Sun 和 Frelich， 2011 年；Segrestin等人， 2020 年；Liu等人， 2021 年）和较早结果（Vile等人， 2006 年；Liu等人， 2021 ) |
| 叶面积 | 竞争能力 Díaz等人。( 2004 ), 生产力, 光拦截, 叶能量和水分平衡 (Díaz et al ., 2016 ) | 大叶种与晚出叶有关（Sun et al ., 2006 ; ZhiGuo et al ., 2011） |
| 比叶面积（SLA；叶干重与叶面积之比） | 生产力、竞争能力、增长绩效（Wright等人， 2004 年；Pérez-Harguindeguy等人， 2013 年） | SLA 较高的物种与开花较晚（Sun & Frelich, 2011 ; König et al ., 2018）和叶片衰老较早（Bucher & Römermann, 2021）有关 |
| 叶干物质含量（LDMC；叶干重与叶鲜重之比） | 竞争能力、对物理危害的抵抗力、生产力（Pérez-Harguindeguy等人， 2013 年） | 具有较高 LDMC 的物种与较晚的叶片衰老有关 (Bucher & Römermann, 2021 ) |
| 基于质量的叶片碳含量 | 结构化合物，性能（Larcher， 1994 年） | 叶碳含量较高的物种与较早开花 (Bucher et al ., 2018 ) 和较晚的叶片衰老 (Bucher & Römermann, 2021 )有关 |
| 基于质量的叶片氮含量 | 生产力、光合能力（Wright等人， 2004 年；Bucher等人， 2018 年） | 叶片氮含量较高的物种与较早开花（Craine等人， 2012 年；Bucher等人， 2018 年）和较早的叶片衰老（Bucher & Römermann， 2021 年）有关 |
| 种子质量 | 再生 (Leishman & Murray, 2001 ) | 种子较重的物种与较早开花有关（Primack， 1987；Vile等， 2006；Bolmgren & Cowan， 2008） |
以前的研究主要集中在植物物候和功能性状的一个或几个阶段。因此，目前尚不清楚植物功能性状在多大程度上与植物物候的连续阶段相关，以及在旨在从性状预测植物物候学时哪些植物功能性状是最重要的。对连续物候阶段的研究对于推进植物物候学领域至关重要，因为它们使研究人员能够专注于与植物物候学相关的关键功能性状。此外，这些研究将阐明植物功能性状在植物物候学对气候变化的反应中的中介作用。等人， 2021 年）。在这里，我们专注于捕捉植物形态和功能本质的七种功能特征，这些特征在以前的研究中被确定为与物候学有关（表 1）。例如，我们预计植物高度（与植物生物量生产和竞争能力相关的特征）与开花开始呈正相关，这种关系已在多项研究中发现（见表 1）。更具体地说，我们调查这些功能性状是否与物候学中的各种营养和生殖阶段相关，以及它们是否可能在未来用作时间密集型物候监测的替代品。
我们在德国五个植物园的整个生长季节监测了 212 种多年生草本植物物种的物候，捕获了营养（即初始生长、分叶和衰老）和生殖（即开花和结果）的开始、结束和持续时间物候事件。我们将物种物候学信息与相同种群的功能性状测量相结合。
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功能性状能否预测草本植物整个生长季节的营养和生殖物候？物候学被认为是系统发育保守的；因此，我们预计密切相关的物种在物候事件发生的时间上表现出比偶然预期更大的相似性。此外，我们问：在预测物候学方面，特定性状是否比潜在的系统发育更重要？
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哪些功能性状对预测生长季节每个阶段的草本物种物候最重要？
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物候学和功能性状之间的关联在不同植物园的生长条件下是否一致？
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