On the relevance of intraspecific trait variability—A synthesis of 56 dry grassland sites across Europe☆
Introduction
Recent research has identified that plant traits of different species co-vary with other traits (Reich, 2014; Reich et al., 1999; Wright et al., 2004), with environmental conditions (Ivanova et al., 2019; Tautenhahn et al., 2008), land-use (Römermann et al., 2009), phenology (König et al., 2018), and species distributions (Stahl et al., 2014) suggesting that traits reflect the strategies plants use to cope with the environment. Furthermore, plant traits have been used to predict feedbacks of vegetation on ecosystem processes (Musavi et al., 2015; Reichstein et al., 2014) and to inform ecosystem models (Kattge et al., 2009). Such analyses pool measured trait values into species mean trait values, while the intraspecific trait variability (in the following called ITV) is generally ignored (Pérez-Harguindeguy et al., 2013). However, traits vary not only between species (in the following called BTV) but also within species (Schlichting, 1986). ITV can be due to phenotypic plasticity within one genotype or genotypic variation within one species (Franks et al., 2014; Fridley and Grime, 2015; Leimu and Fischer, 2008; Nicotra et al., 2010).
The basic assumption behind ignoring ITV in trait based research is that ITV is smaller than BTV (Kattge et al., 2011; Westoby et al., 2002). Indeed, many studies have shown that BTV exceeds ITV (Albert et al., 2010; Cornelissen et al., 2003; Kattge et al., 2011; Roche et al., 2004; Steinbeiss et al., 2008; Garnier et al., 2019), yet other studies have found ITV to be substantial relative to BTV (Jung et al., 2010; Mitchell and Bakker, 2014). However, none of these studies analyzed ITV over large spatial extents covering the species distribution ranges for co-occurring species and therefore likely underestimate ITV. It has further been shown that also BTV increases with spatial extent (Siefert et al., 2015), suggesting that the relative contribution of ITV is unimportant in large scale studies. On the other hand, the effects of changing site conditions along a large gradient also shape ITV, which implies that the relative contribution of ITV vs. BTV to overall trait variability depends on the strength of site effects on ITV relative to the strength of site effects on species turnover (Leps et al., 2011; Rosbakh et al., 2015).
The primary source of ITV is assumed to be between population variation (in the following called ITVbp; Albert et al., 2010) and thus ITV has mainly been studied along spatial, environmental, or management gradients (Auger and Shipley, 2013; Bucher et al., 2016; Fajardo and Piper, 2011; Hulshof et al., 2013; Soper Gorden et al., 2016; Sun et al., 2015). The literature on how within population variability (in the following called ITVwp) contributes to ITV is limited. Phenology (Römermann et al., 2016), ontogeny (Coleman et al., 1994), micro-site, or biotic effects (Le Bagousse-Pinguet et al., 2015) have been identified as sources of ITVwp. The relative importance of within versus between population ITV is highly relevant for trait based research because ITVbp may be predictable from e.g. regional effects whereas ITVwp seems to be controlled by local effects, which are less predictable.The variability of traits, whether between species, between populations, or within populations, has mostly been studied on a trait by trait basis. However, a multivariate perspective that considers several traits can improve the understanding of functional adaptations of plants to the environment (Albert et al., 2010; Díaz et al., 2016). The n-dimensional trait space which can be occupied by a species can be interpreted as the species functional niche (Boucher et al., 2013), similar to the original niche concept (Hutchinson, 1957) of an n-dimensional space of environmental conditions in which a species needs to complete its life cycle. The mean trait values of a species can determine its niche position along gradients, and intraspecific trait variability determines its niche breadth (Stahl et al., 2014; Violle and Jiang, 2009). Such n-dimensional trait niches can be adequately described using hypervolumes (Blonder, 2018), which therefore provide a measure of functional diversity (Lamanna et al., 2014). Despite the conceptual appeal, the relative contributions of BTV, ITVbp, and ITVwp in the multivariate trait space have yet to be quantified.
In this study, we investigate the degree of ITV relative to BTV and the degree of ITVwp relative to ITVbp for five co-occurring dry grassland species that were sampled over a wide geographic gradient capturing most of their environmental space in Central Europe. We analyse the data using both a univariate trait by trait perspective and a multivariate perspective that examines all traits jointly in the n-dimensional trait space. We also investigate the potential of predicting ITVbp from climate variables. Specifically, we address the following questions:
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What is the magnitude of ITV relative to BTV over a large spatial extent?
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Is ITV primarily due to ITVwp or ITVbp?
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Is between population variability consistent across species or species specific and related to climate?
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Do univariate and multivariate trait perspectives yield consistent patterns?
We will address these questions for five co-occurring species (Plantago media L., Campanula glomerata L., Trifolium montanum L., Centaurea jacea L., and Salvia pratensis L.) from 56 dry grassland sites across Europe. This study is unique with respect to the sampling of most of the species co-occurrence range which facilitates unbiased estimates on the relative importance of ITV versus BTV. European dry grasslands represent suitable study systems as they have usually comparable management and land-use histories (Poschlod and WallisDeVries, 2002). Dry grassland species need to cope with nutrient-poor and dry conditions and accordingly show morphological and eco-physiological adaptations to the stressful environment. Differences in trait values between populations of the same species have been observed in these habitats (Lauterbach et al., 2013), making them interesting study systems in particular in the context of climate and / or land use changes.
Section snippets
Study sites and species
We studied the trait variability of the five focal species Plantago media L., Campanula glomerata L., Trifolium montanum L., Centaurea jacea L., and Salvia pratensis L. on 56 dry grassland sites across Europe (Fig. 1). These species are endemic to dry grassland habitats (Korneck, 1996; Oberdorfer et al., 1978). Our five study species are all hemicryptophytes and typically co-occur over wide gradients in Europe (Kalwij et al., 2014). The study sites have similar land-use histories and soil
Univariate analysis of trait variability
The boxplots of trait distributions per species across all sites in Fig. 3 shows that ITV is large. The ANOVA analysis revealed that overall trait variability of all considered traits depends significantly on “species”, “site effects”, and their interaction (Table 2). These three factors together accounted for between 55% (plant width) and 85% (stomata density) of overall trait variability (Fig. 4). The remaining unexplained variability represents ITVwp which can be attributed to
Intraspecific versus between species trait variability
In the univariate analyses the measured trait variability was dominated by intraspecific trait variability (ITV) relative to between species trait variability (BTV) for 9 out of 14 traits. For some traits such as specific leaf area ITV accounts for 92% of the overall trait variability. Even when considering groups of traits in an n-dimensional space ITV exceeded BTV except for the group of stomata traits ( = 44%). The dominance of ITV is surprising, given that previous studies have
found
Implications for trait-based research
We demonstrated that the assumption of negligible ITV is inappropriate in our large-scale synthesis of dry grasslands when analysing trait variability trait by trait. For the five observed dry grassland species ITV exceeds BTV for the majority of traits. However, we could also show that in the multivariate trait space ITV is smaller than BTV if a sufficiently large number of traits (∼4) are considered jointly. Overall the effect of ITV relative to BTV decreases rapidly with increasing trait
Research data for this article
Due to ongoing PhD theses based on this data-set the raw data remain confidential and cannot be shared within this publication. However, the data will be available in future publications.
Data not available / the data that has been used is confidential.
Acknowledgements
We are thankful to all cooperating scientists for support in field work and site selection in the different countries. Anna Golinko, Andrea Bauer, Franziska Pfeiffer, Verena Wommer and Dörte Bachmann helped with trait measurements in the field. We thank Jürgen Dengler and the European dry grassland group (EDDG) for looking for collaborators, finding sites and Ute Jandt to help defining adequate focal species. The leaf nutrient analyses were cooperatively performed at the laboratory of the Dry
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This article is part of a special issue entitled: “Functional traits explaining plant responses to past and future climate changes” published at the journal Flora 254C, 2019.
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Authors contributed equally to this work.