Diel patterns of autotrophic and heterotrophic respiration among phenological stages

Improved understanding of the links between aboveground production and allocation of photosynthate to belowground processes and the temporal variation in those links is needed to interpret observations of belowground carbon cycling processes. Here, we show that combining a trenching manipulation with high‐frequency soil respiration measurements in a temperate hardwood forest permitted identification of the temporally variable influence of roots on diel and seasonal patterns of soil respiration. The presence of roots in an untrenched plot caused larger daily amplitude and a 2–3 h delay in peak soil CO₂ efflux relative to a root‐free trenched plot. These effects cannot be explained by differences in soil temperature, and they were significant only when a canopy was present during the growing season. This experiment demonstrated that canopy processes affect soil CO₂ efflux rates and patterns at hourly and seasonal time scales, and it provides evidence that root and microbial processes respond differently to environmental factors.     

Tree-girdling to separate root and heterotrophic respiration in two Eucalyptus stands in Brazil

The release of carbon as CO₂ from belowground processes accounts for about 70% of total ecosystem respiration. Insights about factors controlling soil CO₂ efflux are constrained by the challenge of apportioning sources of CO₂ between autotrophic tree roots (and mycorrhizal fungi) and heterotrophic microorganisms. In some temperate conifer forests, the reduction in soil CO₂ efflux after girdling (phloem removal) has been used to separate these sources. Girdling stops the flow of carbohydrates to the belowground portion of the ecosystem, which should slow respiration by roots and mycorrhizae while heterotrophic respiration should remain constant or be enhanced by the decomposition of newly dead roots. Therefore, the reduction in CO₂ efflux after girdling should be a conservative estimate of the belowground flux of C from trees. We tested this approach in two tropical Eucalyptus plantations. Tree canopies remained intact for more than 3 months after girdling, showing no reduction in light interception. The reduction in soil CO₂ efflux averaged 16–24% for the 3-month period after girdling. The reduction in CO₂ efflux was similar for plots with one half of the trees girdled and those with all of the trees girdled. Girdling did not reduce live fine root biomass for at least 5 months after treatment, indicating that large reserves of carbohydrates in the root systems of Eucalyptus trees maintained the roots and root respiration. Our results suggest that the girdling approach is unlikely to provide useful insights into the contribution of tree roots and heterotrophs to soil CO₂ efflux in this type of forest ecosystem.     

Beech carbon productivity as driver of ectomycorrhizal abundance and diversity

We tested the hypothesis that carbon productivity of beech ( Fagus sylvatica ) controls ectomycorrhizal colonization, diversity and community structures. Carbon productivity was limited by long-term shading or by girdling. The trees were grown in compost soil to avoid nutrient deficiencies. Despite severe limitation in photosynthesis and biomass production by shading, the concentrations of carbohydrates in roots were unaffected by the light level. Shade-acclimated plants were only 10% and sun-acclimated plants were 74% colonized by ectomycorrhiza. EM diversity was higher on roots with high than at roots with low mycorrhizal colonization. Evenness was unaffected by any treatment. Low mycorrhizal colonization had no negative effects on plant mineral nutrition. In girdled plants mycorrhizal colonization and diversity were retained although ¹⁴C-leaf feeding showed almost complete disruption of carbon transport from leaves to roots. Carbohydrate storage pools in roots decreased upon girdling. Our results show that plant carbon productivity was the reason for and not the result of high ectomycorrhizal diversity. We suggest that ectomycorrhiza can be supplied by two carbon routes: recent photosynthate and stored carbohydrates. Storage pools may be important for ectomycorrhizal survival when photoassimilates were unavailable, probably feeding preferentially less carbon demanding EM species as shifts in community composition were found.     

Carbohydrate sources and sinks in woody plants

Each perennial woody plant is a highly integrated system of competing carbohydrate sinks (utilization sites). Internal competition for carbohydrates is shown by changes in rates of carbohydrate movement from sources to sinks and reversals in direction of carbohydrate transport as the relative sink strengths of various organs change. Most carbohydrates are produced in foliage leaves but some are synthesized in cotyledons, hypocotyls, buds, twigs, stems, flowers, fruits, and strobili. Although the bulk of the carbohydrate pool moves to sinks through the phloem, some carbohydrates are obtained by sinks from the xylem sap. Sugars are actively accumulated in the phloem and move passively to sinks along a concentration gradient. The dry weight of a mature woody plant represents only a small proportion of the photosynthate it produced. This discrepancy results not only from consumption of plant tissues by herbivores and shedding of plant parts, but also from depletion of carbohydrates by respiration, leaching, exudation, secretion, translocation to other plants through root grafts and mycorrhizae and losses to parasites. Large spatial and temporal variations occur in the use of reserve- and currently produced carbohydrates in metabolism and growth of shoots, stems, roots, and reproductive structures. A portion of the carbohydrate pool is diverted for production of chemicals involved in defense against fungi, herbivores, and competing plants. Woody plants accumulate carbohydrates during periods of excess production and deplete carbohydrates when the rate of utilization exceeds the rate of production. Stored carbohydrates play an important role in metabolism, growth, defense, cold hardiness, and postponement or prevention of plant mortality.     

Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year

Limitations in available techniques to separate autotrophic (root) and soil heterotrophic respiration have hampered the understanding of forest C cycling. The former is here defined as respiration by roots, their associated mycorrhizal fungi and other micro‐organisms in the rhizosphere directly dependent on labile C compounds leaked from roots. In order to separate the autotrophic and heterotrophic components of soil respiration, all Scots pine trees in 900 m² plots were girdled to instantaneously terminate the supply of current photosynthates from the tree canopy to roots. Högberg et al. (Nature 411, 789–792, 2001) reported that autotrophic activity contributed up to 56% of total soil respiration during the first summer of this experiment. They also found that mobilization of stored starch (and likely also sugars) in roots after girdling caused an increased apparent heterotrophic respiration on girdled plots. Herein a transient increase in the δ¹³C of soil CO₂ efflux after girdling, thought to be due to decomposition of ¹³C‐enriched ectomycorrhizal mycelium and root starch and sugar reserves, is reported. In the second year after girdling, when starch reserves of girdled tree roots were exhausted, calculated root respiration increased up to 65% of total soil CO₂ efflux. It is suggested that this estimate of its contribution to soil respiration is more precise than the previous based on one year of observation. Heterotrophic respiration declined in response to a 20‐day‐long 6 °C decline in soil temperature during the second summer, whereas root respiration did not decline. This did not support the idea that root respiration should be more sensitive to variations in soil temperature. It is suggested that above‐ground photosynthetic activity and allocation patterns of recent photosynthates to roots should be considered in models of responses of forest C balances to global climate change.     

Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate

Dissolved organic carbon (DOC) is an important component in the terrestrial carbon cycle. Yet, the relative importance of different inputs of DOC to the soil solution remains uncertain. Here, we used a large-scale forest girdling experiment to examine how the supply of recent photosynthate to tree roots and their mycorrhizal fungi affects DOC, in particular low-molecular weight organic acids (LMWOA). We also studied effects of tree girdling on non-structural carbohydrates in microorganism, and examined the effects of freezing of soil and the presence of roots in the soil samples on soil solution DOC and LMWOA in this experiment. The concentration of DOC was reduced by 40%, while citrate was reduced by up to 90% in the soil solution by the girdling treatment. Other LMWOA such as oxalate, succinate, formate and propionate were unaffected by the girdling. We also found that girdling reduced the concentrations of trehalose (by 50%), a typical fungal sugar, and of monosaccharides (by 40%) in microorganisms in root-free soil. The effect of freezing on DOC concentrations was marked in samples from control plots, but insignificant in samples from girdled plots. Release of DOC from cell lysis after freezing was attributed equally to roots and to microorganisms. Our observations suggest a direct link from tree photosynthesis through roots and their mycorrhizal fungi to soil solution chemistry. This direct link should impact solute transport and speciation, mineral weathering and C dynamics in the soil compartment. Importantly, our finding of a substantial photosynthate driven production of DOC challenges the paradigm that DOC is mainly the result of decomposition of organic matter.     

长白山阔叶红松林3个主要树种的非结构性碳储存特征

非结构性碳水化合物(NSC,包括可溶性糖和淀粉)作为树木生命代谢的关键物质之一,在树木器官中的储存特征受到了广泛关注,但NSC在器官内部具有不同功能的组织间(韧皮部与木质部)的分配和权衡还不清楚.本研究以长白山阔叶红松林的3个优势树种——红松、水曲柳和紫椴为研究对象,对比分析NSC在根、树干韧皮与木质部中的浓度和分配特征.结果表明: 树木韧皮部和木质部间的NSC浓度差异显著,总体分配趋势为韧皮部以可溶性糖为主,而木质部以淀粉为主.树干外侧(以年轮划分,0～20年)、中段(20～40年)和内侧(>40年)的NSC浓度在不同树种间差异显著,而根中的差异不显著.红松和水曲柳树干韧皮部可溶性总糖浓度显著高于紫椴,在木质部中差异不显著.本研究结果表明,树体内部NSC在韧皮部和木质部上的分配存在明显分异,这与树种的演替阶段及组织的功能进化有关.研究结果对于深入理解温带树木的碳储存特征和分配机理具有参考意义.     

Ammonium and nitrate uptake by soybean during recovery from nitrogen deprivation

Soybean [Glycine max (L.) Merrill] plants that had been subjected to 15 d of nitrogen deprivation were resupplied for 10 d with 1.0 mol m-3 nitrogen provided as NO3-, NH4+, or NH4(+) + NO3- in flowing hydroponic culture. Plants in a fourth hydroponic system received 1.0 mol m-3 NO3- during both stress and resupply periods. Concentrations of soluble carbohydrates and organic acids in roots increased 210 and 370%, respectively, during stress. For the first day of resupply, however, specific uptake rates of nitrogen, determined by ion chromatography as depletion from solution, were lower for stressed than for non-stressed plants by 43% for NO3- resupply, by 32% for NH4(+) + NO3- resupply, and 86% for NH4+ resupply. When specific uptake of nitrogen for stressed plants recovered to rates for non-stressed plants at 6 to 8 d after nitrogen resupply, carbohydrates and organic acids in their roots had declined to concentrations lower than those of non-stressed plants. Recovery of nitrogen uptake capacity of roots thus does not appear to be regulated simply by the content of soluble carbon compounds within roots. Solution concentrations of NH4+ and NO3- were monitored at 62.5 min intervals during the first 3 d of resupply. Intermittent 'hourly' intervals of net influx and net efflux occurred. Rates of uptake during influx intervals were greater for the NH4(+)-resupplied than for the NO3(-)-resupplied plants. For NH4(+)-resupplied plants, however, the hourly intervals of efflux were more numerous than for NO3(-)-resupplied plants. It thus is possible that, instead of repressing NH4+ influx, increased accumulation of amino acids and NH4+ in NH4(+)-resupplied plants inhibited net uptake by stimulation of efflux on NH4+ absorbed in excess of availability of carbon skeletons for assimilation. Entry of NH4+ into root cytoplasm appeared to be less restricted than translocation of amino acids from the cytoplasm into the xylem.     

Defoliation and mycorrhizal symbiosis: a functional balance between carbon sources and below-ground sinks

Herbivory is generally assumed to negatively influence mycorrhizal fungi because of reduced photosynthate to support mycorrhizae following defoliation. We examined effects of 60% and 100% defoliation (excluding current year needles) on tree growth and ectomycorrhizal associations of 10–15 year old Scots pines ( Pinus sylvestris ). Over 98% of short roots were colonized by mycorrhizal fungi, and contrary to expectation, defoliation did not decrease the proportion of living fungi in fine roots. Furthermore, defoliation did not alter the ratios of produced needle biomass to the biomass of fine roots or living fungi in fine roots. The composition of mycorrhizal morphotypes was changed, however, which suggests competition among different mycorrhizal growth forms owing to their carbon demands. We propose that these outcomes are a consequence of a functional balance between carbon sources in plant foliage and below-ground sinks, i.e. growing roots and mycorrhizal associates.     

Continental‐scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks

Most tree roots on Earth form a symbiosis with either ecto‐ or arbuscular mycorrhizal fungi. Nitrogen fertilization is hypothesized to favor arbuscular mycorrhizal tree species at the expense of ectomycorrhizal species due to differences in fungal nitrogen acquisition strategies, and this may alter soil carbon balance, as differences in forest mycorrhizal associations are linked to differences in soil carbon pools. Combining nitrogen deposition data with continental‐scale US forest data, we show that nitrogen pollution is spatially associated with a decline in ectomycorrhizal vs. arbuscular mycorrhizal trees. Furthermore, nitrogen deposition has contrasting effects on arbuscular vs. ectomycorrhizal demographic processes, favoring arbuscular mycorrhizal trees at the expense of ectomycorrhizal trees, and is spatially correlated with reduced soil carbon stocks. This implies future changes in nitrogen deposition may alter the capacity of forests to sequester carbon and offset climate change via interactions with the forest microbiome.     

Depth-dependent effects of ericoid mycorrhizal shrubs on soil carbon and nitrogen pools are accentuated under arbuscular mycorrhizal trees

Plant mycorrhizal associations influence the accumulation and persistence of soil organic matter and could therefore shape ecosystem biogeochemical responses to global changes that are altering forest composition. For instance, arbuscular mycorrhizal (AM) tree dominance is increasing in temperate forests, and ericoid mycorrhizal (ErM) shrubs can respond positively to canopy disturbances. Yet how shifts in the co-occurrence of trees and shrubs with different mycorrhizal associations will affect soil organic matter pools remains largely unknown. We examine the effects of ErM shrubs on soil carbon and nitrogen stocks and indicators of microbial activity at different depths across gradients of AM versus ectomycorrhizal (EcM) tree dominance in three temperate forest sites. We find that ErM shrubs strongly modulate tree mycorrhizal dominance effects. In surface soils, ErM shrubs increase particulate organic matter accumulation and weaken the positive relationship between soil organic matter stocks and indicators of microbial activity. These effects are strongest under AM trees that lack fungal symbionts that can degrade organic matter. In subsurface soil organic matter pools, by contrast, tree mycorrhizal dominance effects are stronger than those of ErM shrubs. Ectomycorrhizal tree dominance has a negative influence on particulate and mineral-associated soil organic matter pools, and these effects are stronger for nitrogen than for carbon stocks. Our findings suggest that increasing co-occurrence of ErM shrubs and AM trees will enhance particulate organic matter accumulation in surface soils by suppressing microbial activity while having little influence on mineral-associated organic matter in subsurface soils. Our study highlights the importance of considering interactions between co-occurring plant mycorrhizal types, as well as their depth-dependent effects, for projecting changes in soil carbon and nitrogen stocks in response to compositional shifts in temperate forests driven by disturbances and global change.     

Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis

Simple, readily utilizable carbohydrates, necessary for growth and maintenance of large numbers of microbes are rare in forest soils. Among other types of mutualistic interactions, the formation of ectomycorrhizas, a symbiosis between tree roots and certain soil fungi, is a way to overcome nutrient and carbohydrate limitations typical for many forest ecosystems. Ectomycorrhiza formation is typical for trees in boreal and temperate forests of the northern hemisphere and alpine regions world-wide. The main function of this symbiosis is the exchange of fungus-derived nutrients for plant-derived carbohydrates, enabling the colonization of mineral nutrient-poor environments. In ectomycorrhizal symbiosis up to 1/3 of plant photoassimilates could be transferred toward the fungal partner. The creation of such a strong sink is directly related to the efficiency of fungal hexose uptake at the plant/fungus interface, a modulated fungal carbohydrate metabolism in the ectomycorrhiza, and the export of carbohydrates towards soil growing hyphae. However, not only the fungus but also the plant partner increase its expression of hexose importer genes at the plant/fungus interface. This increase in hexose uptake capacity of plant roots in combination with an increase in photosynthesis may explain how the plant deals with the growing fungal carbohydrate demand in symbiosis and how it can restrict this loss of carbohydrates under certain conditions to avoid fungal parasitism.     

Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula

Niche differentiation in soil horizons, host species and natural nutrient gradients contribute to the high diversity of ectomycorrhizal fungi in boreal forests. This study aims at documenting the diversity and community composition of ectomycorrhizal fungi of Norway spruce ( Picea abies ) and silver birch ( Betula pendula ) seedlings in five most abundant microsites in three Estonian old-growth forests. Undisturbed forest floor, windthrow mounds and pits harboured more species than brown- and white-rotted wood. Several species of ectomycorrhizal fungi were differentially represented on either hosts, microsites and sites. Generally, the most frequent species in dead wood were also common in forest floor soil. Ordination analyses suggested that decay type determined the composition of EcM fungal community in dead wood. Root connections with in-growing mature tree roots from below affected the occurrence of certain fungal species on seedling roots systems in dead wood. This study demonstrates that ectomycorrhizal fungi differentially establish in certain forest microsites that is attributable to their dispersal and competitive abilities. Elevated microsites, especially decayed wood, act as seed beds for both ectomycorrhizal forest trees and fungi, thus affecting the succession of boreal forest ecosystems.     

云南普洱季风常绿阔叶林不同林层非结构性碳水化合物特征

在聚类分析的基础上,研究云南普洱季风常绿阔叶林主要物种非结构性碳水化合物(NSC)及其组分浓度、分配和季节性动态在林冠层、亚冠层和林下层间的变化特征.结果表明:亚冠层中可溶性糖及NSC浓度最高,分别为3.9%和13.3%,可溶性糖淀粉比在林下层最低,为0.76,而淀粉浓度则在各林层间无显著性差异.3个林层的可溶性糖均主要分配在叶片中,淀粉和NSC主要分配在根中.亚冠层中叶片和树干的可溶性糖浓度显著高于林冠层和林下层,枝和根的可溶性糖浓度在3个林层间无显著性差异;叶片的淀粉浓度则随林层高度降低而增加,但根淀粉浓度则是在林下层最低,为10.7%,枝和树干的淀粉浓度在3个林层间无显著差异;叶片NSC浓度为林冠层(10.7%)显著低于亚冠层(12.3%)和林下层(12.0%),但根的NSC浓度在林下层中最低,为14.2%;林下层叶片、枝、树干中可溶性糖淀粉比值均最低,但根的可溶性糖淀粉比值最低值出现在林冠层(0.79).3个林层NSC及其组分均存在显著的季节性变化,可溶性糖及可溶性糖淀粉比均为雨季显著高于旱季,而淀粉和NSC浓度则均在旱季中较高.不同林层NSC及其组分浓度的差异反映了不同高度树种碳利用策略的差异,部分地解释了物种的共存机制.     

Frankia and Alnus rubra Canopy Roots: An Assessment of Genetic Diversity, Propagule Availability, and Effects on Soil Nitrogen

The ecological importance of microbial symbioses in terrestrial soils is widely recognized, but their role in soils that accumulate in forest canopies is almost entirely unknown. To address this gap, this study investigated the Frankia–Alnus rubra symbiosis in canopy and forest floor roots at Olympic National Park, WA, USA. Sixteen mature A. rubra trees were surveyed and Frankia genetic diversity in canopy and forest floor nodules was assessed with sequence-based nifH analyses. A seedling bioassay experiment was conducted to determine Frankia propagule availability in canopy and forest floor soils. Total soil nitrogen from both environments was also quantified. Nodules were present in the canopies of nine of the 16 trees sampled. Across the study area, Frankia canopy and forest floor assemblages were similar, with both habitats containing the same two genotypes. The composition of forest floor and canopy genotypes on the same tree was not always identical, however, suggesting that dispersal was not a strictly local phenomenon. Frankia seedling colonization was similar in canopy soils regardless of the presence of nodules as well as in forest floor soils, indicating that dispersal was not likely to be a major limiting factor. The total soil nitrogen of canopy soils was higher than that of forest floor soils, but the presence of Frankia nodules in canopy soils did not significantly alter soil nitrogen levels. Overall, this study indicates that the Frankia–A. rubra symbiosis is similar in canopy and forest floor environments. Because canopy roots are exposed to different environmental conditions within very small spatial areas and because those areas can be easily manipulated (e.g., fertilizer or watering treatments), they present microbial ecologists with a unique arena to examine root–microbe interactions.     

Tree seedling performance and below-ground properties in stands of invasive and native tree species

The establishment and subsequent impacts of invasive plant species often involve interactions or feedbacks with the below-ground subsystem. We compared the performance of planted tree seedlings and soil communities in three ectomycorrhizal tree species at Craigieburn, Canterbury, New Zealand – two invasive species (Pseudotsuga menziesii, Douglas-fir; Pinus contorta, lodgepole pine) and one native (Nothofagus solandri var. cliffortioides, mountain beech) – in monodominant stands. We studied mechanisms likely to affect growth and survival, i.e. nutrient competition, facilitation of carbon and nutrient transfer through mycorrhizal networks, and modification of light and soil conditions by canopy trees. Seedlings were planted in plastic tubes filled with local soil, and placed in monospecific stands. Effects of root competition from trees and mycorrhizal connections on seedling performance were tested by root trenching and use of tubes with or without a fine mesh (20 μm), allowing mycorrhizal hyphae (but not roots) to pass through. Survival and growth were highest in stands of Nothofagus and lowest under Pseudotsuga. Surprisingly, root trenching and mesh treatments had no effect on seedling performance, indicating canopy tree species affected seedling performance through reduced light availability and altered soil conditions rather than below-ground suppression from root competition or mycorrhizal facilitation. Seedlings in Pseudotsuga stands had lower mycorrhizal colonisation, likely as a result of the lower light levels. Soil organic matter levels, microbial biomass, and abundance and diversity of microbe-consuming nematodes were all highest under Nothofagus, and nematode community assemblages differed strongly between native and non-native stand types. The negative effects of non-native trees on nematodes relative to Nothofagus are likely due to the lower availability of soil organic matter and microbial biomass in these stands, and therefore lower availability of resources for nematodes. This study shows that established stands of non-native invasive tree species may adversely affect tree seedlings and soil communities through modifications of the microenvironment both above and below ground. As such, invasion and domination of new landscapes by these species is likely to result in fundamental shifts in community- and ecosystem-level properties relative to those under native forest cover.     

Rapid in vitro ectomycorrhizal infection onPinus densiflora roots byTricholoma matsutake

The root systems of 11-wk-oldPinus densiflora seedlings were inoculated with a hyphal suspension ofTricholoma matsutake and aseptically incubated for 4 wk in a forest soil without supplying exogenous carbohydrates. One week following inoculation, fungal hyphae had colonized the root surface and bound soil particles together establishing a root-substrate continuum. Fungal hyphae were visible within the main root cortex following clearing bleaching and staining. In the ensuing days, fungal colonization was observed within elongating lateral roots in which Hartig net formation was confirmed 4 wk after inoculation. This is the first report of rapid ectomycorrhizal infection ofP. densiflora seedings byT. matsutake.     

Termination of belowground C allocation by trees alters soil fungal and bacterial communities in a boreal forest

The introduction of photosynthates through plant roots is a major source of carbon (C) for soil microbial biota and shapes the composition of fungal and bacterial communities in the rhizosphere. Although the importance of this process, especially to ectomycorrhizal fungi, has been known for some time, the extent to which plant belowground C allocation controls the composition of the wider soil community is not understood. A tree-girdling experiment enabled studies of the relationship between plant C allocation and microbial community composition. Girdling involves cutting the phloem of trees to prevent photosynthates from entering the soil. Four years after girdling, fungal and bacterial communities were characterized using DNA-based profiles and cloning and sequencing. Data showed that girdling significantly altered fungal and bacterial communities compared with the control. The ratio of ectomycorrhizal to saprobic fungal sequences significantly decreased in girdled treatments, and this decline was found to correlate with the fungal phospholipid fatty acid biomarker 18:2ω6,9. Bacterial communities also varied in the abundance of the two dominant phyla Acidobacteria and Alphaproteobacteria . Concomitant changes in fungal and bacterial communities suggest linkages between these two groups and point toward plant belowground C allocation as a key determinant of microbial community composition.     

Root distribution in an Amazonian seasonal forest as derived from δ13C profiles

Carbon isotope ratios of the main stem in trees, saplings, and seedlings were correlated with their main stem diameter in an Amazonian seasonal forest. This correlation became the basis of using carbon isotope ratios of roots from various levels of the soil profile in order to determine root distribution from emergent, canopy and subcanopy trees, saplings and herbaceous understorey plants. It was observed that the distribution of roots in the soil profile is horizontally and vertically heterogeneous. Pockets of roots from saplings or herbaceous understorey plants were found as deep as 4 m and pockets of roots from emergent trees were found as shallow as 1 m depth.