Journal of Ecology 2016, 104, 1311–1313
doi: 10.1111/1365-2745.12605
COMMENTARY
Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum: Commentary on Kramer-Walter et al. (2016) Oscar J. Valverde-Barrantes1,2* and Christopher B. Blackwood3 ~o de Dina ^mica Ambiental, Instituto Nacional de Pesquisas da Amazo ^ nia (INPA), Manaus 69060-001, Coordenacß a Brazil; 2International Center of Tropical Botany (ICTB), Florida International University (FIU), Miami, FL 33199, USA; and 3Department of Biological Sciences, Kent State University, Kent, OH 44240, USA 1
Fine roots are complex and complicated organs to study. The logistic difficulties to access them and a poor understanding of relationships between form and function have left belowground plant organs largely oversimplified or ignored in most ecological studies. Fortunately, since the seminal work of Pregitzer et al. (2002), there have been an increasing number of ecologists focused on quantifying and understanding the functional role of living roots in terrestrial ecosystems. The field of root ecology has progressed from the traditional view of roots as passive organs in charge of anchorage and nutrient absorption to the view that roots have a more dynamic role as drivers of soil organic carbon (Rasse, Rumpel & Dignac 2005), nutrient cycling (Phillips et al. 2012) and the composition and productivity of plant communities (Bardgett, Mommer & de Vries 2014; Valverde-Barrantes et al. 2015). In addition, an increasing effort to link above- and below-ground organs within individuals (Withington et al. 2006) and across species (Holdaway et al. 2011) is providing us with more realistic information to scale plant function from communities to biomes, improving our capacity to understand global biogeography and biogeochemical cycles. An excellent example of the importance of this integrative perspective comes from Kramer-Walter et al. (2016) in this issue of Journal of Ecology. Kramer-Walter et al. (2016) compare leaf, stem and root functional traits of 66 of the most common native woody species in New Zealand. By measuring traits under controlled conditions and then relating community-level traits to environmental gradients, they addressed two pivotal questions in plant ecology: (i) Is there evidence of a root economic spectrum (RES) among root traits and is it coupled to a broader plant economic spectrum (PES)? and (ii) How do traits and/or the integrated plant economic spectrum reflect plant adaptations to their natural habitats, particularly with respect to soil fertility? Their results revealed higher complexity in the integration of functional traits in roots with respect to leaf trait integration. Moreover, Kramer-Walter et al. (2016) showed that although part of the variation in root traits, along with leaf and stem traits, corresponds with environmental *Correspondence author: E-mail
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gradients, there are potential additional factors driving trait variation below-ground that has not been properly quantified in root ecology.
Explaining departures from the RES: evolution and multidimensionality of roots The idea behind the plant economic spectrum, that all plant traits should be correlated with a single axis of variation reflecting a fundamental compromise between resource assimilation, growth and life span, goes back many years (Grime 1977). As explained by Raich (2014), the rationale behind a common axis of variation explaining trait syndromes at the entire plant level centres on the hypothesis that ‘being fast at acquiring and processing carbon, water or nutrients in leaves, stems or roots is advantageous only when acquiring and processing of all resources is fast for all organ systems, otherwise plants will possess excess capacity which is costly and wasteful’. Nevertheless, fine root traits have proved difficult to integrate within this framework. Commonly, fine root traits measured and reportedly linked to the RES are diameter, specific root length (SRL), root tissue density (RTD) and root nitrogen content (RNC; Raich 2014). From the RES perspective, traits positively associated with nutrient uptake capacity, like high SRL, should correlate negatively with tissue investment (RTD) and diameter and positively with metabolic activity (RNC). However, evidence for these trends in roots is weak at best. Inconsistencies with the expected RES trends are pervasive in the literature, particularly among woody plants. In trees, there have been multiple reports of poor or non-significant relationships between SRL and RTD (Withington et al. 2006; Ostonen et al. 2007; Comas & Einssestat 2009; McCormack et al. 2012) or RNC and SRL (Comas & Einssestat 2009; Holdaway et al. 2011; Kong et al. 2014). However, herbaceous and particularly graminoid plants seem to couple better with the RES syndromes (Roumet et al. 2016). Important conclusions can be drawn from these apparent contradictions. First, as shown by Kramer-Walter et al. (2016) roots are multidimensional. In other words, traits typically associated with
© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society
1312 O. J. Valverde-Barrantes & C. B. Blackwood the high resource acquisition, such as low tissue density or high nitrogen, can vary independently in roots. They seem to exhibit a large range of evolutionarily successful trait combinations (i.e. large phenotypic morphospace; Donovan et al. 2011), unlike the highly constrained covariance of traits observed in foliar tissues. Secondly, how well root traits correlate with hypothetical RES and PES axes may depend on the functional or phylogenetic group studied, which is also a sharp contrast with the seemingly universal economics of foliar tissues (Wright et al. 2004). We propose that the root tissue phenotypic morphospace is broader than in leaf tissues because root function can be maximized using a more diverse set of traits that can be equally successful during selection. In fact, the orthogonal variation in SRL and RTD detected by Kramer-Walter et al. (2016) could be the result of different adaptive processes, without clear parallels in foliar tissues. For instance, we recently compared the anatomy of first order roots of 117 species and found a ninefold difference in stele diameter between the thinnest and thickest species, but a 16-fold difference in total diameter (Valverde-Barrantes et al. 2016). This implies that some species with larger root diameters were not increasing investment in structural tissue as expected from a RES perspective, but were actually increasing parenchymatous cortical tissue to maximize habitat for arbuscular mycorrhizal fungi. As a result of alternative adaptations for resource acquisition (maximizing surface area or mycorrhizal fungal habitat), some species increased diameter, and reduced SRL and RTD at the same time. In an analogous comparison, leaves should be able to reduce SLA and density, but increase thickness at the same time, a combination that would be rapidly selected against due to the poor balance between construction cost and the efficiency of intercepting light (Donovan et al. 2011). The importance of the phylogenetic structuring of root traits is another remarkable result from Kramer-Walter et al. (2016) that has been increasingly resonating in root ecology (Kong et al. 2014). The strong phylogenetic structuring of root traits suggests that root trait syndromes have evolved slowly since major phylogenetic divergences (e.g. between magnoliid, asterid and rosid clades; Valverde-Barrantes et al. 2016). Root traits show stronger phylogenetic inertia than is found in leaf traits (Cornwell et al. 2014). The study of Kramer-Walter et al. (2016) suggests that the appearance of particular functional root syndromes was limited to a few evolutionary events, followed by independent divergence. In future, further studies disentangling the role of plant evolution and the acquisition of alternative trait syndromes will be pivotal in the understanding of current root trait patterns and functions.
Root traits from a global perspective Possibly the main contribution from Kramer-Walter’s paper is their projection of community-level plant trait syndromes into an ecological context. Similar to a previous work by Holdaway et al. (2011), this study emphasizes the adaptive value
of functional traits in the composition of plant communities along soil fertility gradients. More importantly, Kramer-Walter et al. (2016) showed that the community-level root traits that correlated with soil fertility were the same root traits that also aligned with the PES at the species level. Communitylevel variation in their second root trait dimension was left unrelated to any environmental gradients. While the KramerWalter et al. (2016) study is a step in the right direction of revealing the importance of root traits in community assembly, this analysis also leaves many questions unanswered. For example, is the second axis of root trait variation that they identify associated with other environmental gradients? Are other root traits, instead of being related to environmental gradients, overdispersed among coexisting species in order to reduce competitive interactions (e.g. Valverde-Barrantes et al. 2015)? What is the role of intraspecific variation and individual plasticity in determining the distribution of actual root traits in the field? Finally, are we missing important traits, like the relationship between root stele and total diameter (Kong et al. 2014) or root hair length (Holdaway et al. 2011) with respect to mycorrhizal colonization, that would better explain the axes of variation observed in fine roots? As any good research project, Kramer-Walter et al. (2016) not only help answer interesting questions, but open new exciting research opportunities with their work.
Conclusions The idea of a common axis of variation explaining strategies in resource uptake and use in plants has been a robust conclusion from analysis of leaves and stems of thousands of species globally (Raich 2014). Therefore, it seems logical to assume a parallel axis explaining the less studied root tissues. However, it is clear that, although the idea is partially accurate, it is also sorely incomplete. The recognition of the complexity in resource acquisition by roots and its inherent multidimensionality highlighted by Kramer-Walter et al. (2016) is a valuable advance in the field. Similarly, the important recognition that Kramer-Walter did on the adaptive value of particular root traits to environmental conditions and the importance of a phylogenetic perspective in the conformation of trait syndromes could help enormously to disentangle the factors involved in soil resource acquisition by plants. Since fine roots represent a large fraction of the net primary productivity of many ecosystems, and have shown the strongest responses to environmental alterations (Iversen 2014), the recognition of a multidimensional-phylogenetic framework could have important implications in the future of functional ecology and representation of roots in biosphere models. Doubtless, there is still much work to do to understand how plant traits reflect adaptations to environmental cues, but the acknowledgement of fine root complexity is definitely a step in the right direction.
Data accessibility This paper does not use data.
© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology, 104, 1311–1313
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