Root Ecology

Plant roots have greatly diversified in form and function since the emergence of the first land plants1,2, but the global organization of functional traits in roots remains poorly understood3,4. Here we analyse a global dataset of 10 functionally important root traits in metabolically active first-order roots, collected from 369 species distributed across the natural plant communities of 7 biomes. Our results identify a high degree of organization of root traits across species and biomes, and reveal a pattern that differs from expectations based on previous studies5,6 of leaf traits. Root diameter exerts the strongest influence on root trait variation across plant species, growth forms and biomes. Our analysis suggests that plants have evolved thinner roots since they first emerged in land ecosystems, which has enabled them to markedly improve their efficiency of soil exploration per unit of carbon invested and to reduce their dependence on symbiotic mycorrhizal fungi. We also found that diversity in root morphological traits is greatest in the tropics, where plant diversity is highest and many ancestral phylogenetic groups are preserved. Diversity in root morphology declines sharply across the sequence of tropical, temperate and desert biomes, presumably owing to changes in resource supply caused by seasonally inhospitable abiotic conditions. Our results suggest that root traits have evolved along a spectrum bounded by two contrasting strategies of root life: an ancestral ‘conservative’ strategy in which plants with thick roots depend on symbiosis with mycorrhizal fungi for soil resources and a more-derived ‘opportunistic’ strategy in which thin roots enable plants to more efficiently leverage photosynthetic carbon for soil exploration. These findings imply that innovations of belowground traits have had an important role in preparing plants to colonize new habitats, and in generating biodiversity within and across biomes.

Salinity can cause several challenges for plants, including water stress, mal-nutrition and accumulation of excess ions to potentially toxic levels. While salt exclusion, compartmentation and osmoregulation are the mechanisms particularly considered to increase the salt tolerance of plants, tolerance is determined by the integrating effects of several mechanisms at the cell, tissue and organ level.
Because roots are in direct contact with the soil solution, they are first to encounter excess salinity and are potentially the first sites of damage or “line of defence”. However, despite the likelihood that differences among root systems may (partially) underlie distinct salt tolerances, information on the phenotypical and physiological plasticity of root systems under salt stress is scant compared to aboveground organs.
This chapter reviews modifications among root size and architecture, morphological and anatomical root traits and root physiology under salinity. Furthermore, root elongation, halotropism and carbon metabolism of roots under salinity are addressed. The review explores the question of whether changes among roots are caused by ion toxicity or whether they could be an active response of plants, which may be of potential adaptive significance. A short overview of the chemical and physical properties of saline soils is given.

The drivers underlying the development of deep root systems, whether genetic or environmental, are poorly understood but evidence has accumulated that deep rooting could be a more widespread and important trait among plants than commonly anticipated from their share of root biomass. Even though a distinct classification of “deep roots” is missing to date, deep roots provide important functions for individual plants such as nutrient and water uptake but can also shape plant communities by hydraulic lift (HL). Subterranean fauna and microbial communities are highly influenced by resources provided in the deep rhizosphere and deep roots can influence soil pedogenesis and carbon storage.Despite recent technological advances, the study of deep roots and their rhizosphere remains inherently time-consuming, technically demanding and costly, which explains why deep roots have yet to be given the attention they deserve. While state-of-the-art technologies are promising for laboratory studies involving relatively small soil volumes, they remain of limited use for the in situ observation of deep roots. Thus, basic techniques such as destructive sampling or observations at transparent interfaces with the soil (e.g., root windows) which have been known and used for decades to observe roots near the soil surface, must be adapted to the specific requirements of deep root observation. In this review, we successively address major physical, biogeochemical and ecological functions of deep roots to emphasize the significance of deep roots and to illustrate the yet limited knowledge. In the second part we describe the main methodological options to observe and measure deep roots, providing researchers interested in the field of deep root/rhizosphere studies with a comprehensive overview. Addressed methodologies are: excavations, trenches and soil coring approaches, minirhizotrons (MR), access shafts, caves and mines, and indirect approaches such as tracer-based techniques.

1. Plant functional traits have revealed trade-offs related to life-history adaptations, geographical
distributions, and ecosystem processes. Fine roots are essential in plant resource acquisition
and play an important role in soil carbon cycling. Nonetheless, root trait variation is still
poorly quantified and rarely related to the rest of the plant.
2. We examined chemical and morphological traits of 34 temperate arbuscular mycorrhizal
tree species, representing three main angiosperm clades (super-orders asterid, magnoliid and
rosid). We tested to what extent fine root chemical and morphological traits were correlated
similarly to the leaf economical spectrum (LES) or were structured by ancestral affiliations
among species.
3. Root traits did not display the same trade-offs as leaves (e.g. specific root length was not correlated
with root N, whereas specific leaf area was correlated with leaf N). Moreover, 75% of
below-ground traits were phylogenetically structured according to Pagel’s k and Abouheif’s
Cmean autocorrelation tests, as opposed to 28% of above-ground traits. Magnoliids showed
thicker, less branched roots than asterids or rosids, but rosid roots exhibited lower N and higher
non-acid-hydrolysable (e.g. lignin) content than other species. In contrast, leaf traits did not differ
significantly among super-orders. At the whole-tree level, chemical traits such as nitrogen tissue
content and lignin content were correlated between above and below-ground organs.
4. The distribution of root traits in woody temperate trees was better explained by shared
ancestry than by the nutrient content and structural trade-offs expected by the LES hypothesis.
Root chemistry and morphology differed substantially among species belonging to different
super-orders, suggesting deep divergences in resource acquisition strategies among major
angiosperm groups. Although we found partial support for the idea of whole-plant integration
based on corresponding nitrogen content across all organs (i.e. a plant economics spectrum),
our study stresses phylogenetic affiliation as the primary driver of root trait distributions
among angiosperms, a pattern that could be easily overlooked based solely on above-ground
observations.

Few studies describe root distributions at the species level in diverse forests, although
belowground species interactions and traits are often assumed to affect fine-root biomass
(FRB).

We used molecular barcoding to study how FRB of trees relates to soil characteristics, species
identity, root diversity, and root traits, and how these relationships are affected by proximity
to ecotones in a temperate forest landscape.

We found that soil patch root biomass increased in response to soil resources across all species,
and there was little belowground vertical or horizontal spatial segregation among species.
Root traits and species relative abundance did not explain significant variation in FRB
after correcting for soil fertility. A positive relationship between phylogenetic diversity and
FRB indicated significant belowground overyielding attributable to local root diversity. Finally,
variation in FRB explained by soil fertility and diversity was reduced near ecotones, but only
because of a reduction in biomass in periodically anoxic areas.

These results suggest that symmetric responses to soil properties are coupled with complementary
species traits and interactions to explain variation in FRB among soil patches. In addition,
landscape-level dispersal among habitats and across ecotones helps explain variation in
the strength of these relationships in complex landscapes.

We investigated fine root biomass and distribution patterns in a species-rich temperate Carpinus–Quercus–Fagus–Tilia forest and searched for experimental evidence of symmetry or asymmetry in belowground competition. We conducted extensive root coring and applied the recently introduced in situ-root growth chamber technique for quantifying fine root growth under experimentally altered intra- and interspecific root neighbourhoods in the intact stand. In 75% of all soil cores, fine roots of more than two tree species were present indicating a broad overlap of the root systems of neighbouring trees. Quercus trees had more than ten times less fine root biomass in relation to aboveground biomass or productivity (stem growth) and a much higher leaf area index/root area index ratio than Carpinus, Fagus and Tilia trees. The root growth chamber experiments indicated a high belowground competitive ability of Fagus in interspecific interactions, but a low one of Quercus. We conclude that (1) interspecific root competition is ubiquitous in this mixed stand, (2) root competition between trees can be clearly asymmetric, and (3) tree species may be ranked according to their belowground competitive ability. Fagus was found to be the most successful species in belowground competition which matches with its superiority in aboveground competition in this forest community.

Fine root dynamics play an important role in the cycling of carbon belowground. Previous studies have indicated that CO2 enrichment results in increased root productivity, mortality and relative turnover; however, our understanding of the duration and long-term trends of this effect are limited. Non-destructive minirhizotron observation tubes were used to measure effects of elevated CO2 on root dynamics and survivorship in a fire dominated scrub-oak ecosystem. Open-top chambers were exposed to elevated atmospheric CO2 for 10 years at Kennedy Space Center, Florida. In this study, initial fine root dynamics from an earlier published study from this experiment (Dilustro et al., 2002) were compared to our findings 5 years later. Significant increases in root productivity, mortality, and turnover due to CO2 enrichment were no longer present after 9 years of treatment. However, the vertical variation in these parameters suggests the upper 50 cm of the soil are the most dynamic. A greater proportion of the fine roots were deeper in the soil profile later in the study, but no CO2 effect was observed. Survivorship analysis suggested the smallest fine roots (i.e. <0.1 mm in diameter and <0.25 mm in length) were most susceptible to mortality. In addition, increased root persistence was correlated with greater soil depth, suggesting that a nutrient and water limited scrub-oak ecosystem at root closure or carrying capacity produces larger, longer-lived fine roots at greater depths. Mean root diameter increased in the upper and lower portions of the soil profile. Seasonal cohort analysis implied that roots appearing in the spring and summer typically had the highest risk of mortality in the fall, although environmental factors influencing this relationship are not clear. The results from this study indicated that CO2 enrichment is no longer driving changes in fine root dynamics, but rather root closure in the upper portions of the soil profile seem to be the strongest influence. Fine roots comprise nearly 25% of the total plant biomass in the scrub-oak ecosystem and their turnover and persistence is an important pathway for carbon inputs into the soil. In order to develop accurate predictive models of the impacts of increasing anthropogenic CO2 on carbon cycling, it is imperative to examine long-term fine root dynamics rather than just shorter observations that could result in misleading conclusions regarding ecosystem responses.

Knowledge about the root system structure and the uptake efficiency of root orders is critical to understand the adaptive plasticity of plants towards salt stress. Thus, this study describes the phenological and physiological plasticity of Citrus volkameriana rootstocks under severe NaCl stress on the level of root orders. Phenotypic root traits known to influence uptake processes, for example frequency of root orders, specific root area, cortical thickness, and xylem traits, did not change homogeneously throughout the root system, but changes after 6 months under 90 mM NaCl stress were root order specific. Chloride accumulation significantly increased with decreasing root order, and the Cl− concentration in lower root orders exceeded those in leaves. Water flux densities of first-order roots decreased to <20% under salinity and did not recover after stress release. The water flux densities of higher root orders changed marginally under salinity and increased 2- to 6-fold in second and third root orders after short-term stress release. Changes in root order frequency, morphology, and anatomy indicate rapid and major modification of C. volkameriana root systems under salt stress. Reduced water uptake under salinity was related to changes of water flux densities among root orders and to reduced root surface areas. The importance of root orders for water uptake changed under salinity from root tips towards higher root orders. The root order-specific changes reflect differences in vulnerability (indicated by the salt accumulation) and ontogenetic status, and point to functional differences among root orders under high salinity.

Three varieties of olive, Barnea, Arbequina and Proline, varying in salt tolerance, were examined to check the sensitivity of their root system hydraulic properties to salinity. Up to three levels of saline water (EC = 1.2, 4.2 and 7.5 dS m−1) were used for long-term irrigation of mature trees. Specific conductivities and embolism rates of roots and branches were estimated by low-pressure conductivity measurement; variability and plasticity of root and branch axial conductivities were calculated. Cross-sections of roots were analysed with respect to xylem anatomy. Barnea, and to a minor degree Arbequina, were found to be more salt-resistant than Proline. Axial root hydraulics under salt stress reacted in a more plastic fashion than branch conductivities. Increased specific conductivities of roots, different plasticities of root hydraulics and modifications in mean conduit diameters can be dismissed as foremost reasons of the observed differences in salt resistance. Instead, a high within-population variability in root conductivity, as found in the salt-tolerant Barnea and Arbequina varieties, coming to full effect in high conductivity roots of Barnea trees, and an increased bimodal distribution of conduit sizes may represent favourable traits to enhance water uptake in soils with heterogeneous salinity.

Background Studying root biomass, root system distribution and belowground interactions is essential for understanding the composition of plant communities, the impact of global change, and terrestrial biogeochemistry. Most soil samples and minirhizotron pictures hold roots of more than one species or plant individual. The identification of taxa by their roots would allow species-specific questions to be posed; information about root affiliation to plant individuals could be used to determine intra-specific competition. Scope Researchers need to be able to discern plant taxa by roots as well as to quantify abundances in mixed root samples. However, roots show less distinctive features that permit identification than aboveground organs. This review discusses the primary use of available methods, outlining applications, shortcomings and future developments. Conclusion Methods are either non-destructive, e.g. visual examination of root morphological criteria in situ, or require excavated and excised root samples. Among the destructive methods are anatomical keys, chemotaxonomic approaches and molecular markers. While some methods allow for discerning the root systems of individual plants, others can distinguish roots on the functional group or plant taxa level; methods such as IR spectroscopy and qPCR allow for quantifying the root biomass proportion of species without manual sorting.

Salt stress is known to influence water use and carbon allocation in trees; however, information about the effects of salt exposure on water uptake and below-ground carbon investment is scant, especially for adult trees. Consequently, this study examined these variables in two mature olive varieties (Olea europaea L.) that differ in their NaCl tolerance: Barnea (tolerant) and Proline (sensitive). Trees were irrigated using water with electrical conductivities of 1.2, 4.2 (both varieties) and 7.5 dS m−1 (Barnea only) for 11 years. At each treatment level, we measured soil properties, root morphology, root biomass:necromass ratio, root xylem sap osmolality, and root sap-flow as well as leaf conductance and morphology. Both varieties exhibited reduced fine root biomass under salinity which was only partially compensated for by higher specific root areas under moderate salinity. Proline variety exhibited a smaller fine root system under moderate salinity than Barnea trees, likely causing the lower sap-flow density in coarse roots of Proline compared to Barnea. The higher biomass:necromass ratio of the Barnea root system under moderate salinity is indicative of lower root turnover rates and thus a more efficient carbon use than in Proline trees. Besides differences in ion exclusion capacities, the ability of the fine root system to resist the deleterious effects of salinity seems to affect the salt resistance of mature olive varieties by influencing water uptake and carbon allocation.

Research highlights
► Under salinity salt-tolerant olive trees have an higher fine root biomass than salt-sensitive trees. ► Under salinity salt-resistant olive trees sustain an higher root sap-flow density than salt-sensitive trees. ► Salt-sensitive olive trees possess a lower root biomass:necromass ratio under salinity than salt-tolerant ones. ► The ability of fine roots to resist the deleterious effects of NaCl affects the salt resistance of mature olives varieties.

Atmospheric carbon dioxide levels are increasing and are predicted to double this century. The implications of this rise on vegetation structure and function are not well understood. Measurement of root growth response to elevated atmospheric carbon dioxide is critical to understanding plant responses and soil carbon input. We investigated the effects of elevated carbon dioxide on fine root growth using open top chambers with both ambient and elevated (700 ppm) CO2 treatments in an oak-palmetto scrub ecosystem at Kennedy Space Center, FL. Minirhizotron tubes installed in each elevated and control chamber were sampled for root length density (mm cm−2) every 3 months. Carbon dioxide enrichment of the chambers began May 15, 1996. By December 1997, root length density (RLD) increased to 7.53 mm cm−2 for the control chambers and 21.36 mm cm−2 for the enriched chambers in the top 101-cm of soil. Vertical distribution of fine roots was unchanged under elevated carbon dioxide. Fine root production increased with elevated carbon dioxide, and mortality and turnover were higher in the elevated chambers by the last sample date in 1997. The increased rates of fine root growth coupled with no change in decomposition rate suggest a potential increased rate of carbon input into the soil. However, these results only represent the first 21 months post-fire and recovery to root closure could just be faster in the elevated CO2 atmosphere.

Background: Below-ground competition as a major structuring force in plant communities can be either symmetric or asymmetric with important consequences for the coexistence of plants. It is a matter of controversy whether asymmetry in competition increases with resource availability or not. Aims: This study tested the hypotheses that root competition between mature Fagus sylvatica and Quercus petraea trees is asymmetric and that asymmetry is more pronounced in non-water-limited environments. Methods : Initially equal-sized tree fine roots were grown for 365–390 days in root growth chambers in situ and exposed to competition by either a conspecific or an allospecific root. Relative root growth rate was used to determine asymmetry in root competition. Different soil moisture regimes were considered by conducting a throughfall reduction experiment and by including data from earlier experiments with contrasting moisture regimes. Results: The competitive interaction between Fagus and Quercus fine roots is asymmetric; root morphology appears to depend on the presence of a competitor; and asymmetry in root competition increases with increasing soil moisture availability. Conclusions: Below-ground competition in temperate broad-leaved mixed forests can be as asymmetric as competition for light, with asymmetry decreasing with increasing water shortage.

Plants can develop novel adaptations for nutrient acquisition in nutrient-limited ecosystems. These adaptations include colonization by roots of tree trunks and logs that can act as nutrient reservoirs. Termites may facilitate this root colonization by digging tunnels and accelerating decomposition in logs and tree trunks. We measured the frequency with which above-ground tree root colonization co-occurs with the presence of termites or their tunnels inside living trees above 20 cm dbh (n = 178) and dead tree trunks and logs at least 15 cm in diameter (n = 146) in a Bornean tropical forest. Roots above the soil surface co-occur with termite tunnels 39% more frequently than expected by chance in trunks of living trees and 17% more frequently than expected by chance in logs. By categorizing logs according to hardness through ease of penetration, we found that softer logs at a late stage of decay did not show co-occurrence of termite activity and roots to the same extent as harder logs. This suggests that trees forage where termites have removed physical barriers to colonization. In this fashion, termites may accelerate nutrient cycling in tropical rain forests.