Toward a Coordinated Understanding of Hydro-Biogeochemical Root Functions in Tropical Forests for Application in Vegetation Models

Tropical forest root characteristics and resource acquisition strategies are underrepresented in vegetation and global models, hampering the prediction of forest–climate feedbacks for these carbon-rich ecosystems. Lowland tropical forests often have globally unique combinations of high taxonomic and functional biodiversity, rainfall seasonality, and strongly weathered infertile soils, giving rise to distinct patterns in root traits and functions compared with higher latitude ecosystems. We provide a roadmap for integrating recent advances in our understanding of tropical forest belowground function into vegetation models, focusing on water and nutrient acquisition. We offer comparisons of recent advances in empirical and model understanding of root characteristics that represent important functional processes in tropical forests. We focus on: (1) fine-root strategies for soil resource exploration, (2) coupling and trade-offs in fine-root water vs nutrient acquisition, and (3) aboveground–belowground linkages in plant resource acquisition and use. We suggest avenues for representing these extremely diverse plant communities in computationally manageable and ecologically meaningful groups in models for linked aboveground–belowground hydro-nutrient functions. Tropical forests are undergoing warming, shifting rainfall regimes, and exacerbation of soil nutrient scarcity caused by elevated atmospheric CO2. The accurate model representation of tropical forest functions is crucial for understanding the interactions of this biome with the climate

Belowground uptake strategies: how fine-root traits determine tree growth

The growth of trees depends on photosynthetic carbon gain by the leaves, which in turn relies on water and nutrient acquisition by the fine roots. Because the availability of carbon, water and nutrients fluctuates, trees can adjust their leaf and fine-root functional traits to maintain their resource uptake and growth rates. Aboveground, the variation in leaf traits is closely related to light availability, light uptake and tree growth. Within species, leaves show general, plastic responses to their light environment, so that trees can still intercept light when its availability changes. Across species, leaf traits are coordinated along a leaf economics spectrum (LES), which reflects species resource strategies. On the one end of this spectrum, acquisitive species have leaves that allow fast resource uptake and therefore fast tree growth. Conversely, species with a conservative strategy acquire resources more slowly, but retain them longer, so they can tolerate low resource availability. Belowground, the relationships between fine-root functional traits, water and nutrient availability and acquisition, and tree growth are expected to be similar to those aboveground, but are still poorly understood. Understanding these relationships is essential as tree growth results from the simultaneous uptake of above- and belowground resources. Therefore, this thesis examines how fine-root traits relate to growth, and focuses on across- and within-species variation in tree root traits. We first tested whether plant resource strategies can explain drought effects on tree growth across 10 common tree species that ranged from acquisitive to conservative species (Chapter 2). Based on tree-ring analyses, we found that the growth rates of all species were significantly lower in years with dry summers. Although the strength of these growth responses differed, these differences were not related to species resource strategies. However, when groundwater levels receded, acquisitive species grew slower but conservative species did not, which suggests root trait differences across these species. Drought effects on tree growth may thus not always be fully explained from an acquisitive or conservative resource strategy. We further evaluated whether a root economics spectrum (RES) parallel to a LES can explain variation in fine-root functional traits across species (Chapter 3). Our literature review shows no consistent evidence for an RES, due to three fundamental differences between fine roots and leaves. First, fine-root traits are not only aimed at increased resource uptake or conservation, but are also constrained by the soil environment. Second, the relationships between traits and function are far less clear for roots than for leaves. Third, the expected relationships between fine-root traits and resource uptake are obscured by mycorrhizal fungi. Revealing the links between fine-root traits, resource acquisition, and growth across species, therefore requires a multidimensional approach that incorporates these different interacting variables. Chapter 4 examines intraspecific variation in fine-root traits and mycorrhizal biomass in Fagus sylvatica L. and Picea abies L. forests on a poor, sandy soil and a resource-rich clay soil in the Netherlands. Both species increased their fine-root mass and fine-root growth rates on the sandy soils compared to the clay soils, but fine-root morphology did not differ between the soil types. In the P. abies stands, ectomycorrhizal biomass was larger on sand than on clay, possibly increasing tree resource uptake. Besides the strong increase in fine-root mass observed for both species, species may thus also differ in their fine-root plasticity strategies to cope with various soil environments. To understand tree growth from below- and aboveground trait integration, we explored the impacts of fine-root mass and morphology on nutrient acquisition and tree fitness using a whole-tree growth model (Chapter 5). More specifically, we tested which combination(s) of fine-root mass and specific root length (SRL) led to optimal fitness, based on the uptake benefits (i.e. increasing the belowground uptake area) and carbon costs (i.e. turnover and respiration) of these traits. Our results show that tree fitness increased with fine-root mass but especially through an increase in SRL. Furthermore, both a combination of high fine-root mass and low SRL, and of low fine-root mass and high SRL, resulted in similar net carbon gain, indicating that alternative strategies that may lead to similar fitness. To conclude, trees rely on various uptake strategies to ensure belowground resource uptake and tree growth in different environments. Specific root length is often expected to be tightly linked to tree growth, but this thesis shows that there is little support for this hypothesised relationship. Consequently, the functional meaning of SRL requires further study. Instead, fine-root mass and mycorrhizal symbiosis may present more important alternatives to enhance water and nutrient uptake, both across and within species. Moreover, to cope with the highly complex soil (resource) environment, species have adopted various other uptake strategies besides fine-root mass, morphology and mycorrhiza. This thesis stresses that a multidimensional root-trait framework is needed to link fine-root traits to tree growth, that can accommodate this variety of fine-root traits and the diversity of the soil environment

Patterns in intraspecific variation in root traits are species‐specific along an elevation gradient

International audience1- Intraspecific trait variation is an important driver of plant performance in different environments. Although roots acquire essential resources that vary with the environment, most studies have focused on intraspecific variation in leaf traits, and research on roots is often restricted to a few species. It remains largely unclear how and to what extent root traits vary with the environment and whether general intraspecific patterns exist across species.2- We compared intraspecific variation in specific root length (SRL), root diameter, root tissue density (RTD) and root branching density of 11 species along a 1,000 m elevation gradient in the French Alps. We tested (a) the extent of intraspecific versus interspecific root trait variation along the gradient, (b) whether intraspecific trait patterns with elevation were consistent among species and (c) whether environmental variables better explained intraspecific variation in root traits than elevation. Specifically, we hypothesised that within a species, root trait values would adjust to enhance resource acquisition (either through an increase in SRL or root diameter, and/or in branching density) and/or conservation (increased RTD) at higher elevations.3- Species identity explained most of the overall variation in root traits. Elevation explained only a minor proportion of intraspecific root trait variation, which was larger within than between elevations. Also, trait relationships with elevation rarely agreed with our hypotheses, varied strongly across species and were often differently related to environmental variation. Generally, climate, soil and vegetation properties better explained intraspecific root variation than elevation, but these relationships were highly species-dependent.4- Along complex environmental gradients where multiple properties simultaneously change, roots of different species vary in different ways, leading to species-specific patterns in intraspecific root trait variation. The lack of support for our hypotheses may be caused by the multiple interactions between environmental properties, small-scale soil heterogeneity, species phylogeny and changing plant–plant interactions. Our findings suggest that, to enhance our understanding of the effects of environmental change on plant performance, we need to better integrate the multiple dimensions of plant responses to change and measure a broader set of root traits and environmental variables

Functional ratios among leaf, xylem and phloem areas in branches change with shade tolerance, but not with local light conditions, across temperate tree species

Leaf, xylem and phloem areas drive the water and carbon fluxes within branches and trees, but their mutual coordination is poorly understood. We test the hypothesis that xylem and phloem areas increase relative to leaf area when species are selected for, or branches are exposed to, higher levels of light intensity. Trees of 10 temperate, broadleaved and deciduous, tree species were selected. Fifty-centimetre-long branches were collected from shaded and exposed conditions at a height of 3-4 m. We measured the total leaf area, xylem area, phloem area and leaf traits, as well as the area of the constituent cell types, for a stem section at the branch base. Xylem area : leaf area and phloem area : leaf area ratios did not differ consistently between sun and shade branches, but, as expected, they decreased with species' shade tolerance. Similar trends were observed for conductive cell areas in xylem and phloem. Trees of light-demanding species maintain higher water loss and carbon gain rates per leaf area by producing more xylem area and phloem area than shade-tolerant species. We call for more comparative branch studies as they provide an integrated biological perspective on functional traits and their role in the ecology of tree species.</p

Tree growth increases through opposing above‐ and belowground resource strategies

Studying functional traits and their relationships with tree growth has proved a powerful approach for understanding forest structure. These relationships are often expected to follow the classical resource economics perspective, where acquisitive leaves combined with acquisitive roots are expected to enhance resource uptake and tree growth. However, evidence for coordinated leaf and roots trait effects on growth is scarce and it remains poorly understood how these traits together determine tree growth. Here, we tested how leaf and root trait combinations explain tree growth.We collected data on leaf and root traits of 10 common tree species, and on soil carbon (C) and nitrogen (N) concentrations in a temperate forest in Michigan, US. Tree growth was calculated as the stem diameter increment between three censuses measured across 13,000 trees and modelled as a function of different combinations of leaf and root traits and soil properties.The two best models explaining tree growth included both specific leaf area (SLA), root diameter and soil C or N concentration, but their effects on growth were contingent on each other: thick roots were associated with high growth rates but only for trees with low SLA, and high SLA was related to fast growth but only for trees with thin roots. Soil C and N% negatively impacted the growth of trees with high SLA or high root diameter.Synthesis. In this study, resource economics did not explain the relationships between leaf and root traits and tree growth rates. First, for trees with low or intermediate SLA, thick roots may be considered as acquisitive, as they were associated with faster tree growth. Second, trees did not coordinate their leaf and root traits according to plant resource economics but enhanced their growth rates by combining thick (acquisitive) roots with conservative (low SLA) leaves or vice versa. Our study indicates the need to re‐evaluate the combined role of leaves and roots to unveil the interacting drivers of tree growth and, ultimately, of forest structure and suggests that different adaptive whole‐tree phenotypes coexist.Trees did not coordinate their leaf and root traits according to resource economics to improve their growth. Instead, they grew faster by combining conservative leaves and thick, acquisitive roots, and vice versa. The faster growth of thick‐rooted trees may be attributed to higher mycorrhization, which enhances soil resource uptake. Thus, traits of one organ may modulate the effects of another organ on growth, suggesting the local coexistence of different whole‐tree phenotypes.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/170826/1/jec13729.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/170826/2/jec13729_am.pd

Tree growth increases through opposing above‐ground and below‐ground resource strategies

Studying functional traits and their relationships with tree growth has proved a powerful approach for understanding forest structure. These relationships are often expected to follow the classical resource economics perspective, where acquisitive leaves combined with acquisitive roots are expected to enhance resource uptake and tree growth. However, evidence for coordinated leaf and roots trait effects on growth is scarce and it remains poorly understood how these traits together determine tree growth. Here, we tested how leaf and root trait combinations explain tree growth.We collected data on leaf and root traits of 10 common tree species, and on soil carbon (C) and nitrogen (N) concentrations in a temperate forest in Michigan, US. Tree growth was calculated as the stem diameter increment between three censuses measured across 13,000 trees and modelled as a function of different combinations of leaf and root traits and soil properties.The two best models explaining tree growth included both specific leaf area (SLA), root diameter and soil C or N concentration, but their effects on growth were contingent on each other: thick roots were associated with high growth rates but only for trees with low SLA, and high SLA was related to fast growth but only for trees with thin roots. Soil C and N% negatively impacted the growth of trees with high SLA or high root diameter.Synthesis. In this study, resource economics did not explain the relationships between leaf and root traits and tree growth rates. First, for trees with low or intermediate SLA, thick roots may be considered as acquisitive, as they were associated with faster tree growth. Second, trees did not coordinate their leaf and root traits according to plant resource economics but enhanced their growth rates by combining thick (acquisitive) roots with conservative (low SLA) leaves or vice versa. Our study indicates the need to re‐evaluate the combined role of leaves and roots to unveil the interacting drivers of tree growth and, ultimately, of forest structure and suggests that different adaptive whole‐tree phenotypes coexist.Trees did not coordinate their leaf and root traits according to resource economics to improve their growth. Instead, they grew faster by combining conservative leaves and thick, acquisitive roots, and vice versa. The faster growth of thick‐rooted trees may be attributed to higher mycorrhization, which enhances soil resource uptake. Thus, traits of one organ may modulate the effects of another organ on growth, suggesting the local coexistence of different whole‐tree phenotypes.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/170826/1/jec13729.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/170826/2/jec13729_am.pd

Incorporating belowground traits: avenues towards a whole-tree perspective on performance

Tree performance depends on the coordinated functioning of interdependent leaves, stems and (mycorrhizal) roots. Integrating plant organs and their traits, therefore, provides a more complete understanding of tree performance than studying organs in isolation. Until recently, our limited understanding of root traits impeded such a whole-tree perspective on performance, but recent developments in root ecology provide new impetuses for integrating the below- and aboveground. Here, we identify two key avenues to further develop a whole-tree perspective on performance and highlight the conceptual and practical challenges and opportunities involved in including the belowground. First, traits of individual roots need to be scaled up to the root system as a whole to determine belowground functioning, e.g. total soil water and nutrient uptake, and hence performance. Second, above- and belowground plant organs need to be mechanistically connected to account for how they functionally interact and to investigate their combined impacts on tree performance. We further identify mycorrhizal symbiosis as the next frontier and emphasize several courses of actions to incorporate these symbionts in whole-tree frameworks. By scaling up and mechanistically integrating (mycorrhizal) roots as argued here, the belowground can be better represented in whole-tree conceptual and mechanistic models; ultimately, this will improve our estimates of not only the functioning and performance of individual trees, but also the processes and responses to environmental change of the communities and ecosystems they are part of