Towards a multidimensional root trait framework: a tree root review
The search for a root economics spectrum (RES) has been sparked by recent interest in trait-based plant ecology. By analogy with the one-dimensional leaf economics spectrum (LES), fine-root traits are hypothesised to match leaf traits which are coordinated along one axis from resource acquisitive to...
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| Published in | The New phytologist Vol. 211; no. 4; pp. 1159 - 1169 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
New Phytologist Trust
01.09.2016
Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The search for a root economics spectrum (RES) has been sparked by recent interest in trait-based plant ecology. By analogy with the one-dimensional leaf economics spectrum (LES), fine-root traits are hypothesised to match leaf traits which are coordinated along one axis from resource acquisitive to conservative traits. However, our literature review and meta-level analysis reveal no consistent evidence of an RES mirroring an LES. Instead the RES appears to be multidimensional. We discuss three fundamental differences contributing to the discrepancy between these spectra. First, root traits are simultaneously constrained by various environmental drivers not necessarily related to resource uptake. Second, above- and belowground traits cannot be considered analogues, because they function differently and might not be related to resource uptake in a similar manner. Third, mycorrhizal interactions may offset selection for an RES. Understanding and explaining the belowground mechanisms and trade-offs that drive variation in root traits, resource acquisition and plant performance across species, thus requires a fundamentally different approach than applied aboveground. We therefore call for studies that can functionally incorporate the root traits involved in resource uptake, the complex soil environment and the various soil resource uptake mechanisms – particularly the mycorrhizal pathway – in a multidimensional root trait framework. |
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| AbstractList | Contents 1159 I. 1159 II. 1161 III. 1164 IV. 1166 1167 References 1167 SUMMARY: The search for a root economics spectrum (RES) has been sparked by recent interest in trait‐based plant ecology. By analogy with the one‐dimensional leaf economics spectrum (LES), fine‐root traits are hypothesised to match leaf traits which are coordinated along one axis from resource acquisitive to conservative traits. However, our literature review and meta‐level analysis reveal no consistent evidence of an RES mirroring an LES. Instead the RES appears to be multidimensional. We discuss three fundamental differences contributing to the discrepancy between these spectra. First, root traits are simultaneously constrained by various environmental drivers not necessarily related to resource uptake. Second, above‐ and belowground traits cannot be considered analogues, because they function differently and might not be related to resource uptake in a similar manner. Third, mycorrhizal interactions may offset selection for an RES. Understanding and explaining the belowground mechanisms and trade‐offs that drive variation in root traits, resource acquisition and plant performance across species, thus requires a fundamentally different approach than applied aboveground. We therefore call for studies that can functionally incorporate the root traits involved in resource uptake, the complex soil environment and the various soil resource uptake mechanisms – particularly the mycorrhizal pathway – in a multidimensional root trait framework. The search for a root economics spectrum (RES) has been sparked by recent interest in trait-based plant ecology. By analogy with the one-dimensional leaf economics spectrum (LES), fine-root traits are hypothesised to match leaf traits which are coordinated along one axis from resource acquisitive to conservative traits. However, our literature review and meta-level analysis reveal no consistent evidence of an RES mirroring an LES. Instead the RES appears to be multidimensional. We discuss three fundamental differences contributing to the discrepancy between these spectra. First, root traits are simultaneously constrained by various environmental drivers not necessarily related to resource uptake. Second, above- and belowground traits cannot be considered analogues, because they function differently and might not be related to resource uptake in a similar manner. Third, mycorrhizal interactions may offset selection for an RES. Understanding and explaining the belowground mechanisms and trade-offs that drive variation in root traits, resource acquisition and plant performance across species, thus requires a fundamentally different approach than applied aboveground. We therefore call for studies that can functionally incorporate the root traits involved in resource uptake, the complex soil environment and the various soil resource uptake mechanisms – particularly the mycorrhizal pathway – in a multidimensional root trait framework. Contents 1159 I. 1159 II. 1161 III. 1164 IV. 1166 1167 References 1167 Summary The search for a root economics spectrum (RES) has been sparked by recent interest in trait‐based plant ecology. By analogy with the one‐dimensional leaf economics spectrum (LES), fine‐root traits are hypothesised to match leaf traits which are coordinated along one axis from resource acquisitive to conservative traits. However, our literature review and meta‐level analysis reveal no consistent evidence of an RES mirroring an LES. Instead the RES appears to be multidimensional. We discuss three fundamental differences contributing to the discrepancy between these spectra. First, root traits are simultaneously constrained by various environmental drivers not necessarily related to resource uptake. Second, above‐ and belowground traits cannot be considered analogues, because they function differently and might not be related to resource uptake in a similar manner. Third, mycorrhizal interactions may offset selection for an RES. Understanding and explaining the belowground mechanisms and trade‐offs that drive variation in root traits, resource acquisition and plant performance across species, thus requires a fundamentally different approach than applied aboveground. We therefore call for studies that can functionally incorporate the root traits involved in resource uptake, the complex soil environment and the various soil resource uptake mechanisms – particularly the mycorrhizal pathway – in a multidimensional root trait framework. 1159 I. I. Introduction One of the basic principles of trait-based plant ecology is the trade-off between plant growth and survival (Grime, ; Kobe et al., ; Craine, ). This trade-off implies that plants invest in trait attributes that allow either fast resource acquisition and therefore fast growth, or defence and conservation of acquired resources such as carbon (C), nitrogen (N) and phosphorus (P) which allow survival under adverse conditions. The growth-survival trade-off has been demonstrated clearly in leaf traits that span a continuum from acquisitive to conservative leaves (Reich et al., ; Wright et al., ). On the one hand, the former are characterised by a high specific leaf area (leaf area per leaf mass, SLA), high assimilation and respiration rates, and high nutrient concentrations, which enhance both light interception and C fixation (Fig. ). These acquisitive traits come at the expense of large resource losses due to high metabolic rates, increased susceptibility to herbivory and short lifespan. On the other hand, conservative leaves are equipped for long-term resource retention by having high tissue densities and low respiration rates. These traits enhance their lifespan, but decrease their light interception efficiency and photosynthetic rates (Reich et al., , ; Wright et al., ). This so-called leaf economics spectrum (LES, Wright et al., ) has been successfully linked to plant performance (Reich et al., ; Poorter & Bongers, ), species distribution and interactions (Sterck et al., ), and ecosystem processes (Reich et al., ; Díaz et al., , ; Grigulis et al., ). Currently, research efforts are directed to test whether the fine-root traits of trees can be positioned within a similar framework, that is, the root economics spectrum (RES) (e.g. Comas & Eissenstat, , ; Withington et al., ; McCormack et al., ; Chen et al., ; Kong et al., ; Liu et al., ; Valverde-Barrantes et al., ). Based on assumed trait coordination between above- and belowground organs, it has been hypothesised that root functional traits can also be grouped in trait syndromes associated with fast resource acquisition or enhanced resource conservation. This search for an RES similar to the LES builds on the premise that acquisitive leaves with high evaporative demand and photosynthetic rates require acquisitive roots to ensure sufficient water and nutrient supply to maintain these processes, and ultimately to achieve fast plant growth (Eissenstat, ; Reich, ). Conversely, plants that have conservative leaves with lower water and nutrient requirements, but also lower photosynthetic rates, should retain resources longer. They may thus require long-lived roots with lower respiration and uptake rates, resulting in slow plant growth. It is therefore hypothesised that leaf traits are matched by parallel root traits along the acquisitive-conservative resource spectrum (Grime et al., ; Reich et al., ; Freschet et al., ; Liu et al., ; Reich, ; Valverde-Barrantes et al., ). As already demonstrated for leaves in the LES, an RES could offer a relevant framework to provide further insights into plant, vegetation and ecosystem processes, and responses to the soil environment and global change. For example, the grouping of species along an RES could help to understand their performance (growth and survival) or distribution across soil resource gradients. However, the existence of an RES analogous to the LES is currently debated, because of contradictory results within and among studies (e.g. Withington et al., ; McCormack et al., ; Mommer & Weemstra, ; Chen et al., ; Kong et al., ). This study aims to clarify the uncertainty concerning the existence of an RES by reviewing the available evidence for the RES hypothesis within individual studies and by performing a meta-level analysis (Smith et al., ) to test the RES hypothesis across those studies. In addition to root trait relationships, we also reviewed the literature on correlations between the leaf and root traits of the LES and of the RES. This study focuses on the fine-root traits of trees. This is important as recent papers show that for herbaceous species, root trait correlations provide a better match with the RES than for woody species (Roumet et al., ). This suggests that root trait correlations may be fundamentally different for woody species. Our literature review is based on 18 studies that compared the root traits expected to play a role in an RES across more than two tree species (Supporting Information Table S1). Our meta-level analysis was carried out on a subset of 14 studies (Table S1), because not all studies provided root trait data at the individual species level, and one study already comprised a meta-analysis. This meta-level analysis was based on raw data and did not include calculating effect sizes, and therefore does not comply with the standards of a meta-analysis (Vetter et al., ; Koricheva & Gurevitch, ). 1159 II. II. The root economics spectrum The root traits expected to feature in the RES are based on a parallel with the key leaf traits in the LES: SLA, leaf N content, maximum photosynthetic rate, respiration rate and leaf lifespan (Fig. ). These traits are related to three leaf processes involved in plant growth and survival. First, SLA relates to leaf resource interception at a given biomass investment. Second, leaf N content, photosynthetic rate and respiration rate are related to leaf C gain. Third, leaf lifespan refers to the conservation of biomass. Assuming functional similarity between leaves and fine roots, the critical fine-root traits in the RES are therefore expected to be: specific root length (root length per root mass, SRL), root N content, root water and nutrient uptake rate, root respiration rate and root lifespan (Fig. ). Similar to leaf traits in the LES, it is expected that SRL reflects the root uptake area at a given biomass cost; root N content, uptake rate and respiration rate are expected to be associated with net soil resource acquisition rate; and root lifespan reflects the degree of biomass conservation. In both the LES and RES it is expected that most traits (SLA/SRL, N content, photosynthetic/resource uptake rates and respiration rates) will decrease from an acquisitive to a conservative strategy, whereas lifespan will increase (Fig. ). Several studies have assessed the support for the RES hypothesis across tree species. In addition to the five key traits, most of these studies measured root diameter and root C : N ratios, and calculated tissue density (from root length, diameter and mass), although their aboveground parallels (leaf thickness, C : N ratio and tissue density) are less explicitly incorporated in the LES. These additional root traits are expected to increase from the acquisitive to the conservative side of the RES (Fig. ), because they have been found to contribute to root lifespan and thus to resource conservation (Wahl & Ryser, ; Gu et al., ): thick roots are sometimes assumed to be long-lived due to their relatively large stele cross-sectional area that protects them from mechanical, herbivore and drought stress, and to have low N content and therefore slow metabolism due to their relatively small cortex area (Eissenstat & Achor, ; Wahl & Ryser, ; Guo et al., ). However, the exact mechanisms underlying these correlations between these root traits and root lifespan are not fully clear yet: for example, Kong et al. demonstrate that thicker roots have a relatively large cortex area, and other anatomical features such as a well-developed exodermis may also drive the longer lifespan of thicker roots (Withington et al., ). In turn, other traits in the RES (e.g. nutrient and water uptake rates, respiration rates, and root lifespan) are measured far less frequently than their aboveground counterparts (i.e. photosynthetic and respiration rates and leaf lifespan). In order to maintain the functional parallel with leaves, RES studies have examined absorptive rather than transporting roots. These functional groups were initially separated on the basis of their diameter (e.g. all roots < 1 or 2 mm diameter were considered absorptive), but although both traits may be partially correlated, root order rather than diameter has since proved to be a better proxy for root functioning (Pregitzer et al., ; McCormack et al., ). We therefore focus mainly on studies that compared all or some of these RES traits (Table S1) on first- to third-order roots (first-order roots being the most distal). Because data on root uptake and respiration rate across species are scarce, especially in relation to other root traits, our analysis was restricted to three RES traits: SRL, root N content and root lifespan. As only one study measured both root N content and root lifespan (Valverde-Barrantes et al., ), we related root lifespan to root C : N ratios - for which more data were available - instead. We also tested for relationships between these RES traits and root diameter, root tissue density and root C : N ratios. 1. Correlations between root traits are inconsistent In terms of correlations between root lifespan and other root traits, the RES is little supported by data. As expected from the RES hypothesis, within the individual studies reviewed, the trait most consistently and positively correlated with root lifespan across species is root diameter (Gu et al., ; McCormack et al., ; Adams et al., ; Hansson et al., ), although not in the study by Withington et al. (Table ). Withington et al. attributed their failure to find significant correlations to the limited variation in root diameter across their study species (in their study it ranged between 0.36 and 0.62 mm across 11 tree species, but in, for example, the study by McCormack et al. , it ranged between 0.22 and 0.64 mm across 12 tree species). Our meta-level analysis also demonstrated that root diameter was the trait most strongly correlated to root lifespan (Fig. S1d; Table S2). In line with the RES h The search for a root economics spectrum ( RES ) has been sparked by recent interest in trait‐based plant ecology. By analogy with the one‐dimensional leaf economics spectrum ( LES ), fine‐root traits are hypothesised to match leaf traits which are coordinated along one axis from resource acquisitive to conservative traits. However, our literature review and meta‐level analysis reveal no consistent evidence of an RES mirroring an LES . Instead the RES appears to be multidimensional. We discuss three fundamental differences contributing to the discrepancy between these spectra. First, root traits are simultaneously constrained by various environmental drivers not necessarily related to resource uptake. Second, above‐ and belowground traits cannot be considered analogues, because they function differently and might not be related to resource uptake in a similar manner. Third, mycorrhizal interactions may offset selection for an RES . Understanding and explaining the belowground mechanisms and trade‐offs that drive variation in root traits, resource acquisition and plant performance across species, thus requires a fundamentally different approach than applied aboveground. We therefore call for studies that can functionally incorporate the root traits involved in resource uptake, the complex soil environment and the various soil resource uptake mechanisms – particularly the mycorrhizal pathway – in a multidimensional root trait framework. Contents Summary 1159 I. Introduction 1159 II. The root economics spectrum 1161 III. Why the one‐dimensional resource economics spectrum does not work for tree roots 1164 IV. Outlook 1166 Acknowledgements 1167 References 1167 |
| Author | Thomas W. Kuyper4 Frank J. Sterck Eric J. W. Visser Jasper van Ruijven Liesje Mommer Godefridus M. J. Mohren Monique Weemstra |
| Author_xml | – sequence: 1 givenname: Monique surname: Weemstra fullname: Weemstra, Monique organization: Wageningen University – sequence: 2 givenname: Liesje surname: Mommer fullname: Mommer, Liesje organization: Wageningen University – sequence: 3 givenname: Eric J. W. surname: Visser fullname: Visser, Eric J. W. organization: Radboud University Nijmegen – sequence: 4 givenname: Jasper surname: Ruijven fullname: Ruijven, Jasper organization: Wageningen University – sequence: 5 givenname: Thomas W. surname: Kuyper fullname: Kuyper, Thomas W. organization: Wageningen University – sequence: 6 givenname: Godefridus M. J. surname: Mohren fullname: Mohren, Godefridus M. J. organization: Wageningen University – sequence: 7 givenname: Frank J. surname: Sterck fullname: Sterck, Frank J. organization: Wageningen University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27174359$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2016 New Phytologist Trust 2016 Wageningen University. New Phytologist © 2016 New Phytologist Trust 2016 Wageningen University. New Phytologist © 2016 New Phytologist Trust. Copyright © 2016 New Phytologist Trust Wageningen University & Research |
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| Keywords | resource acquisition trait syndromes mycorrhizal symbiosis functional traits root economics spectrum (RES) |
| Language | English |
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| Snippet | The search for a root economics spectrum (RES) has been sparked by recent interest in trait-based plant ecology. By analogy with the one-dimensional leaf... Contents 1159 I. 1159 II. 1161 III. 1164 IV. 1166 1167 References 1167 Summary The search for a root economics spectrum (RES) has been sparked by recent... The search for a root economics spectrum ( RES ) has been sparked by recent interest in trait‐based plant ecology. By analogy with the one‐dimensional leaf... Contents 1159 I. 1159 II. 1161 III. 1164 IV. 1166 1167 References 1167 SUMMARY: The search for a root economics spectrum (RES) has been sparked by recent... 1159 I. I. Introduction One of the basic principles of trait-based plant ecology is the trade-off between plant growth and survival (Grime, ; Kobe et al., ;... |
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| SubjectTerms | Aluminum Bosecologie en Bosbeheer Carbon dioxide Carboxylic acids Climate effects Conservation Drought Economics Ecosystems edaphic factors fine roots Forest Ecology and Forest Management functional traits Graduate schools Herbivores Herbivory Leaves Leerstoelgroep Bosecologie en bosbeheer Life span Mycorrhizae - physiology mycorrhizal symbiosis Nature Conservation and Plant Ecology Natuurbeheer en Plantenecologie Nutrient requirements PE&RC Photosynthesis Physiology Plant ecology Plant Ecology and Nature Conservation Plant growth Plant Leaves - physiology Plant resources Plant Roots - physiology Plant species Plant tissues Plantenecologie en Natuurbeheer Plants Quantitative Trait, Heritable resource acquisition Resource conservation Respiration root economics spectrum (RES) soil Soil pH Tansley reviews trait syndromes trees Trees - physiology uptake mechanisms |
| Title | Towards a multidimensional root trait framework: a tree root review |
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