Intraspecific trait variation influences physiological performance and fitness in the South Africa shrub genus Protea (Proteaceae)

Abstract

Background and Aims Global plant trait datasets commonly identify trait relationships that are interpreted to reflect fundamental trade-offs associated with plant strategies, but often these trait relationships are not identified when evaluating them at smaller taxonomic and spatial scales. In this study we evaluate trait relationships measured on individual plants for five widespread Protea species in South Africa to determine whether broad-scale patterns of structural trait (e.g. leaf area) and physiological trait (e.g. photosynthetic rates) relationships can be detected within natural populations, and if these traits are themselves related to plant fitness. Methods We evaluated the variance structure (i.e. the proportional intraspecific trait variation relative to among-species variation) for nine structural traits and six physiological traits measured in wild populations. We used a multivariate path model to evaluate the relationships between structural traits and physiological traits, and the relationship between these traits and plant size and reproductive effort. Key Results While intraspecific trait variation is relatively low for structural traits, it accounts for between 50 and 100 % of the variation in physiological traits. Furthermore, we identified few trait associations between any one structural trait and physiological trait, but multivariate regressions revealed clear associations between combinations of structural traits and physiological performance (R2 = 0.37–0.64), and almost all traits had detectable associations with plant fitness. Conclusions Intraspecific variation in structural traits leads to predictable differences in individual-level physiological performance in a multivariate framework, even though the relationship of any particular structural trait to physiological performance may be weak or undetectable. Furthermore, intraspecific variation in both structural and physiological traits leads to differences in plant size and fitness. These results demonstrate the importance of considering measurements of multivariate phenotypes on individual plants when evaluating trait relationships and how trait variation influences predictions of ecological and evolutionary outcomes.

Alternative designs lead to similar performance when traits and performance vary on different axes

“…On each individual, Nolting et al (2021) also measured area-based, light-saturated photosynthetic rates (Aarea), stomatal conductance (gs), and instantaneous water-use efficiency (WUEInstan) in the field. They collected branches to measure sapwood-specific hydraulic (which was not certified by peer review) is the author/funder.…”

“…The copyright holder for this preprint this version posted October 8, 2022. ; https://doi.org/10.1101/2022.10.05.511045 doi: bioRxiv preprint conductivity (Ks) following Espino and Schenk (2011), and quantified the Huber value of each stem (the sapwood cross-sectional area of a stem relative to the total one-sided leaf area per area, (Mencuccini and Bonosi 2001)) on which hydraulic measures were recorded, to calculate leaf-specific conductivity (LSC, sapwood-specific conductivity divided by total leaf area of the stem, Tyree and Zimmerman 2002) and leaf-specific photosynthetic rates (LSP, light-saturated photosynthetic rate per area divided by Huber value). From the stems and leaves on which physiological traits were measured, Nolting et al (2021) measured a suite of structural traits (e.g., traits related to organ morphology and allocation): leaf area (LA, cm 2 ), leaf mass per area (LMA, g cm -2 ), lamina density (LD, g cm -3 ), leaf length-width ratio (LWR, unitless), stomatal pore length (SL, mm), stomatal pore density (SD, mm -2 ), bark thickness (BT, mm), and wood density (WD, g cm -3 ). These structural and physiological performance traits were chosen based on the large literature in plant functional ecology suggesting that they are key indices of carbon uptake and allocation and water-use strategies (see Nolting et al 2021 for further discussion of functional significance of each trait, and of trait complexes).…”

“…Even within local plant communities and assemblages the trait variation observed among co-occurring species can span orders of magnitude (Wright et al 2004; Baraloto et al 2010; Aiello-Lammens et al 2017) and can be greater than expected given regional species pools (Swenson et al 2012). As these examples suggest, it is common to find substantial trait variation at almost any scale, even among individuals within a species growing at a single site (Messier et al 2010; Umaña and Swenson 2019; Nolting et al 2021; Taseski et al 2021). In contrast, substantial performance differences are less commonly documented, especially among co-occurring species (Becker et al 1999; Worthy et al 2020; Nolting et al 2021).…”

“…As these examples suggest, it is common to find substantial trait variation at almost any scale, even among individuals within a species growing at a single site (Messier et al 2010; Umaña and Swenson 2019; Nolting et al 2021; Taseski et al 2021). In contrast, substantial performance differences are less commonly documented, especially among co-occurring species (Becker et al 1999; Worthy et al 2020; Nolting et al 2021). Why do we fail to see large differences in performance when we see large differences in individual structural traits that are related to performance?…”

“…Here we use an extensive collection of structural and physiological performance traits measured on individual plants to demonstrate that multivariate combinations of structural traits differ markedly among species but lead to similar physiological performance among co-occurring Protea s pecies sampled from natural communities in the Cape Floristic Region, South Africa (data originally published in Nolting et al 2021). We develop a simple model to explain these results, and we conclude that the presence of persistent ‘alternative designs’ (i.e., large variation among species in individual structural traits that converge on similar performance, (Marks and Lechowicz 2006; Marks 2007)) within natural communities could be the result of selection that minimizes performance differences among species.…”