Root foraging traits and competitive ability in heterogeneous soils

The responses of plant roots to nutrient patches in soil may be an important component of competitive ability. In particular, the scale, precision, and rate of foraging for patchy soil resources may influence competitive ability in heterogeneous soils. In a target–neighbor experiment in the field, per-individual and per-gram competitive effects were measured for six old-field species with known root foraging scale, precision, and rate. The presence and number of nutrient patches were also manipulated in a full factorial design. Number and presence of patches did not influence the outcome of competition. Competitive ability was not related to total plant size, growth rate, or root:shoot allocation, or to root foraging precision. Per-individual competitive effects were marginally correlated with root foraging scale (biomass of roots) and root foraging rate (time required to reach a patch). Therefore, competitive ability was more closely related to ability to quickly fill a soil volume with roots than to ability to preempt resource-rich patches.     

Improving the scale and precision of hypotheses to explain root foraging ability

Background

Numerous hypotheses have been proposed to explain the wide variation in the ability of plants to forage for resources by proliferating roots in soil nutrient patches. Comparative analyses have found little evidence to support many of these hypotheses, raising the question of what role resource-foraging ability plays in determining plant fitness and community structure.

Scope

In the present viewpoint, we respond to Grime''s (2007; Annals of Botany 99: 1017–1021) suggestion that we misinterpreted the scope of the scale–precision trade-off hypothesis, which states that there is a trade-off between the spatial scale over which plant species forage and the precision with which they are able to proliferate roots in resource patches. We use a meta-analysis of published foraging scale–precision correlations to demonstrate that there is no empirical support for the scale–precision trade-off hypothesis. Based on correlations between foraging precision and various plant morphological and ecophysiological traits, we found that foraging precision forms part of the ‘fast’ suite of plant traits related to rapid growth rates and resource uptake rates.

Conclusions

We suggest there is a need not only to examine correlations between foraging precision and other plant traits, but to expand our notion of what traits might be important in determining the resource-foraging ability of plants. By placing foraging ability in the broader context of plant traits and resource economy strategies, it will be possible to develop a new and empirically supported framework to understand how plasticity in resource uptake and allocation affect plant fitness and community structure.Key words: Root foraging, phenotypic plasticity, scale, precision, resource uptake strategies, traits     

Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms

1 Responses to spatial heterogeneity of soil nutrients were tested in 10 plant species that differ in life form and successional status, but which co-occur in the South Carolina coastal plain. The morphological responses of the root system were tested by assessing scale (represented by root mass and root length densities), precision (preferential proliferation of roots in nutrient-rich patches compared with less fertile patches) and discrimination (ability to detect and proliferate within the richest patches when patches vary in nutrient concentration). We also investigated sensitivity (growth benefits gained as spatial heterogeneity of nutrients increases, measured as total biomass).
2 Ten individuals of each species were grown in pots under four treatments that had differing nutrient distribution but the same overall nutrient addition. Plants were harvested when roots reached pot edge.
3 We observed high variation between species in scale, precision and sensitivity. No significant discrimination responses were observed, although greatest root mass density occurred at intermediate fertility levels for all species.
4 We rejected the hypothesis that scale and precision are negatively correlated. Indeed, in herbaceous species alone, scale and precision were positively correlated.
5 Sensitivity was not closely related to precision, indicating that proliferation of roots in fertile patches does not always yield growth benefits in heterogeneous soils. Further, some sensitive species had very low precision, suggesting that a positive growth response in heterogeneous environments may be related to plasticity in physiology or root life span, rather than morphology.
6 Plant life form was not correlated with precision or sensitivity. However, scale of response was greater in herbs than in woody plants, possibly because the two life forms develop root systems at different rates.     

Root foraging for patchy resources in eight herbaceous plant species

The root foraging strategy of a plant species can be characterized by measuring foraging scale, precision, and rate. Trade-offs among these traits have been predicted to contribute to coexistence of competitors. We tested for trade-offs among root foraging scale (total root mass and length of structural roots), precision (ln-ratio of root lengths in resource-rich and resource-poor patches), and rate (days required for roots to reach a resource-rich patch, or growth rate of roots within a resource-rich patch) in eight co-occurring species. We found that root foraging scale and precision were positively correlated, as were foraging scale and the rate of reaching patches. High relative growth rate of a species did not contribute to greater scale, precision, or rate of root foraging. Introduced species had greater foraging scale, precision, and rate than native species. The positive correlations between foraging scale and foraging precision and rate may give larger species a disproportionate advantage in competition for patchy soil resources, leading to size asymmetric competition below ground.     

土壤养分空间异质性与植物根系的觅食反应

植物在长期进化过程中,为了最大限度地获取土壤资源,对养分的空间异质性产生各种可塑性反应．包括形态可塑性、生理可塑性、菌根可塑性等．许多植物种的根系在养分丰富的斑块中大量增生,增生程度种间差异较大,并受斑块属性(斑块大小、养分浓度)、营养元素种类和养分总体供应状况的影响．植物还通过调整富养斑块中细根的直径、分枝角、节问距以及空间构型来实现斑块养分的高效利用．根系的生理可塑性及菌根可塑性可能在一定程度上影响其形态可塑性．生理可塑性表现为处于不同养分斑块上的根系迅速调整其养分吸收速率,从而增加单位根系的养分吸收,对在时间上和空间上变化频繁的空间异质性土壤养分的利用具有重要意义,可在一定程度上弥补根系增生反应的不足．菌根可塑性目前研究较少,一些植物种的菌根代替细根实现在富养斑块中的增生．菌根增生的碳投入养分吸收效率较高、根系增生对增加养分吸收的作用较复杂,取决于养分离子在土壤中的移动性能以及是否存在竞争植物;对植物生长(竞争能力)的作用因种而异,一些敏感种由此获得生长效益,而其它一些植物种受影响较小．植物个体对土壤养分空间异质性反应能力和生长差异,影响其在群落中的地位和命运,最终影响群落组成及其结构．     

Context dependence in foraging behaviour of Achillea millefolium

Context-dependent foraging behaviour is acknowledged and well documented for a diversity of animals and conditions. The contextual determinants of plant foraging behaviour, however, are poorly understood. Plant roots encounter patchy distributions of nutrients and soil fungi. Both of these features affect root form and function, but how they interact to affect foraging behaviour is unknown. We extend the use of the marginal value theorem to make predictions about the foraging behaviour of roots, and test our predictions by manipulating soil resource distribution and inoculation by soil fungi. We measured plant movement as both distance roots travelled and time taken to grow through nutrient patches of varied quality. To do this, we grew Achillea millefolium in the centers of modified pots with a high-nutrient patch and a low-nutrient patch on either side of the plant (heterogeneous) or patch-free conditions (homogeneous). Fungal inoculation, but not resource distribution, altered the time it took roots to reach nutrient patches. When in nutrient patches, root growth decreased relative to homogeneous soils. However, this change in foraging behaviour was not contingent upon patch quality or fungal inoculation. Root system breadth was larger in homogeneous than in heterogeneous soils, until measures were influenced by pot edges. Overall, we find that root foraging behaviour is modified by resource heterogeneity but not fungal inoculation. We find support for predictions of the marginal value theorem that organisms travel faster through low-quality than through high-quality environments, with the caveat that roots respond to nutrient patches per se rather than the quality of those patches.     

外来入侵植物的根系觅养行为研究进展

土壤养分分布具有高度空间异质性, 植物的根系觅养行为是其对土壤养分异质性的一种适应。不同植物为了适应养分异质性会产生不同的根系觅养行为, 通过调整自身的根系觅养范围、觅养精度和觅养速度来更好地吸收利用土壤中的养分。外来植物与本地植物的竞争是决定其成功入侵的重要因素, 土壤养分等环境因素会影响它们之间的竞争关系。近年来, 外来入侵植物的觅养行为逐渐受到人们的关注, 关于入侵植物根系觅养行为的研究成果陆续出现: (1)总体来看, 外来入侵植物具有较强的根系觅养能力, 但根系觅养范围与觅养精度之间的权衡关系还不确定; (2)营养异质性会影响入侵植物与本地植物之间的竞争, 反过来, 二者之间的竞争也会影响根系觅养行为对营养异质性的响应; (3)丛枝菌根真菌(arbuscular mycorrhizal fungi, AMF)能够提高入侵植物的根系觅养能力, 外来植物入侵能够改变入侵植物对AMF的偏好性, 形成AMF对入侵的正反馈作用, 而本地植物与AMF的相互作用也会影响入侵植物的竞争力。未来还应加强营养异质环境下种间竞争和AMF共生对入侵植物根系觅养行为的影响机制研究, 以及全球变化背景下入侵植物根系觅养行为的变化与机制方面的研究, 可以更深入地认识外来植物的觅养行为在其成功入侵中的作用, 并为利用营养调控来防控入侵植物提供理论依据。     

疏叶骆驼刺根系对土壤异质性和种间竞争的响应

近年来, 植物根系对土壤异质性的响应和植物根系之间的相互作用一直是研究的热点。过去的研究主要是针对一年生短命植物进行的, 而且多是在人工控制的温室条件下进行的。而对于多年生植物根系对养分异质性和竞争的综合作用研究很少。该文对塔里木盆地南缘多年生植物疏叶骆驼刺(Alhagi sparsifolia)根系生长对养分异质性和竞争条件的响应途径与适应策略进行了研究, 结果表明: (1)在无竞争的条件下, 疏叶骆驼刺根系优先向空间大的地方生长, 即使另一侧有养分斑块存在, 其根系也向着空间大的一侧生长; (2)在有竞争的条件下, 疏叶骆驼刺根系生长依然是优先占领空间大的一侧, 但是竞争者的存在抑制了疏叶骆驼刺的生长, 导致其枝叶生物量和根系生物量都明显减少(p < 0.01), 而养分斑块的存在促进了疏叶骆驼刺根系的生长; (3)疏叶骆驼刺根系的生长不仅需要养分, 也需要足够的空间, 空间比养分更重要; (4)有竞争者存在的时候, 两株植物的根系都先长向靠近竞争者一侧的空间, 即先占据“共有空间”。研究结果对理解植物根系觅食行为和植物对环境的适应策略有重要意义。     

植物根系养分捕获塑性与根竞争

为了更有效地从土壤中获取养分, 植物根系在长期的进化与适应中产生了一系列塑性反应, 以响应自然界中广泛存在的时空异质性。同时, 植物根系的养分吸收也要面对来自种内和种间的竞争。多种因素都会影响植物根竞争的结果, 包括养分条件、养分异质性的程度、根系塑性的表达等。竞争会改变植物根系的塑性反应, 比如影响植物根系的空间分布; 植物根系塑性程度差异也会影响竞争。已有研究发现根系具有高形态塑性和高生理塑性的植物在长期竞争过程中会占据优势。由于不同物种根系塑性的差异, 固定的对待竞争的反应模式在植物根系中可能并不存在, 其响应随竞争物种以及土壤环境因素的变化而变化。此外, 随着时间变化, 根系塑性的反应及其重要性也会随之改变。植物对竞争的反应可能与竞争个体之间的亲缘关系有关, 有研究表明亲缘关系近的植物可能倾向于减小彼此之间的竞争。根竞争对植物的生存非常重要, 但目前还没有研究综合考虑植物的各种塑性在根竞争中的作用。另外根竞争对群落结构的影响尚待深入的研究。     

Growth Consequences of Soil Nutrient Heterogeneity for two Old-field Herbs,Ambrosia artemisiifoliaandPhytolacca americana, Grown Individually and in Combination

Plant species can respond to small scale soil nutrient heterogeneityby proliferating roots or increasing nutrient uptake kineticsin nutrient-rich patches. Because root response to heterogeneitydiffers among species, it has been suggested that the distributionof soil resources could influence the outcome of interspecificcompetition. However, studies testing how plants respond toheterogeneity in the presence of neighbours are lacking. Inthis study, individuals of two species,Phytolacca americanaL.andAmbrosia artemisiifoliaL. were grown individually and incombination in soils with either a homogeneous or heterogeneousnutrient distribution. Above-ground biomass of individuallygrown plants of both species was greater when fertilizer waslocated in a single patch than when the same amount of fertilizerwas distributed evenly throughout the soil. Additionally, bothspecies proliferated roots in high-nutrient patches.A. artemisiifoliaexhibitedlarger root:shoot ratios, increased nitrogen depletion fromnutrient patches, and a higher growth rate thanP. americana,suggestingA. artemisiifoliais better suited to find and rapidlyexploit nutrient patches. In contrast to individually grownplants, soil nutrient distribution had no effect on final above-groundplant biomass for either species when grown with neighbours,even though roots were still concentrated in high nutrient patches.This study demonstrates that increased growth of isolated plantsas a consequence of localized soil nutrients is not necessarilyan indication that heterogeneity will affect interspecific encounters.In fact, despite a significant below-ground response, soil nutrientheterogeneity was inconsequential to above-ground performancewhen plants were grown with neighbours.Copyright 1999 Annalsof Botany Company Phytolacca americana, pokeweed,Ambrosia artemisiifolia, ragweed, nutrient heterogeneity, root proliferation, plasticity, foraging, nutrient patches.     

Invasive clonal plant species have a greater root-foraging plasticity than non-invasive ones

Clonality is frequently positively correlated with plant invasiveness, but which aspects of clonality make some clonal species more invasive than others is not known. Due to their spreading growth form, clonal plants are likely to experience spatial heterogeneity in nutrient availability. Plasticity in allocation of biomass to clonal growth organs and roots may allow these plants to forage for high-nutrient patches. We investigated whether this foraging response is stronger in species that have become invasive than in species that have not. We used six confamilial pairs of native European clonal plant species differing in invasion success in the USA. We grew all species in large pots under homogeneous or heterogeneous nutrient conditions in a greenhouse, and compared their nutrient-foraging response and performance. Neither invasive nor non-invasive species showed significant foraging responses to heterogeneity in clonal growth organ biomass or in aboveground biomass of clonal offspring. Invasive species had, however, a greater positive foraging response in terms of root and belowground biomass than non-invasive species. Invasive species also produced more total biomass. Our results suggest that the ability for strong root foraging is among the characteristics promoting invasiveness in clonal plants.     

The timing and degree of root proliferation in fertile-soil microsites for three cold-desert perennials

Summary Root proliferation in nutrient-rich soil patches is an important mechanism facilitating nutrient capture by plants. Although the phenomenon of root proliferation is well documented, the specific timing of this proliferation has not been investigated. We studied the timing and degree of root proliferation for three perennial species common to the Great Basin region of North America: a shrub, Artemisia tridentata, a native tussock grass, Agropyron spicatum, and an introduced tussock grass, Agropyron desertorum. One day after we applied nutrient solution to small soil patches, the mean relative growth rate of Agropyron desertorum roots in these soil patches was two to four times greater than for roots of the same plants in soil patches reated with distilled water. Most of the increased root growth came from thin, laterally branching roots within the patches. This rapid and striking root proliferation by Agropyron desertorum occurred in response to N-P-K enrichment as well as to P or N enrichment alone. A less competitive bunchgrass, Agrophyron spicatum, showed no tendency to proliferate roots in enriched soil patches during these two-week experiments. The shrub Artemisia tridentata proliferated roots within one day of initial solution injection in the N-enrichment experiment, but root proliferation of this species was more gradual and less consistent in the N-P-K and P-enrichment experiments, respectively. The ability of Agropyron desertorum to proliferate roots rapidly may partly explain both its general competitive success and its superior ability to exploit soil nutrients compared to Agropyron spicatum in Great Basin rangelands of North America.     

Influence of root herbivory on plant communities in heterogeneous nutrient environments

While plant species respond differently to nutrient patches, the forces that drive this variability have not been extensively examined. In particular, the role of herbivory in modifying plant-resource interactions has been largely overlooked. We conducted a glasshouse study in which nutrient heterogeneity and root herbivory were manipulated, and used differences in foraging among plant species to predict the influence of root herbivores on these species in competition. We also tracked the influence of neighborhood composition, heterogeneity, and herbivory on whole-pot plant biomass. When herbivores were added to mixed-species neighborhoods, Eupatorium compositifolium, the most precise forager, was the only plant species to display a reduction in shoot biomass. Neighborhood composition had the greatest influence on whole-pot biomass, followed by nutrient heterogeneity; root herbivory had the smallest influence. These results suggest that root herbivory is a potential cost of morphological foraging in roots. Root herbivores reduced standing biomass and influenced the relative growth of species in mixed communities, but their effect was not strong enough at the density examined to overwhelm the bottom-up effects of resource distribution.     

根间相互作用对玉米与马铃薯响应异质氮的调控

近年研究表明养分异质促进植物多样性与群落生产力的正相关性。然而,相关的促进机制还很不清楚。以农田生态系统下作物多样性群体(玉米马铃薯间作体系)为例,在盆栽条件下采用控释性氮肥构建养分异质性,通过目标植物法设计根间作用处理,探讨根系的觅养行为,植株个体生长和总生产力对土壤氮空间分布和根间作用的响应特征。结果表明:根间作用提高作物的觅养精确度(F=3.017,P=0.094),在异质性条件下马铃薯的根冠比增加(P=0.001),而玉米的根冠比则不论在均质性还是异质性条件下均显著降低(F=4.781,P=0.039);氮异质性显著地提高在根间作用下两作物的生物量生产(P=0.021),明显增加总生产力LER(Land equivalent ratio)(F=4.171,P=0.064),显著地降低相对关系指数RII(Relative interaction index)值(F=5.636,P=0.026),显著降低玉米的根冠比(F=4.273,P=0.049),增加根间作用下马铃薯的根冠比,而在无竞争下则降低。上述结果说明,非资源性的根间作用激发玉米和马铃薯对异质性氮的觅养能力,这可能是为什么异质性养分环境促进植物多样性与群体生产力正向关系的重要原因;结果还表明觅养能力的激发主要来自非资源性的根间作用机制,因此本研究验证了植物对异质性养分和竞争者的协同响应理论。而有关的非资源性根间作用机制,例如种间识别作用等值得进一步深入探讨。     

Root plasticity of native and invasive Great Basin species in response to soil nitrogen heterogeneity

Soil nutrients are heterogeneously distributed in natural systems. While many species respond to this heterogeneity through root system plasticity, little is known about how the magnitude of these responses may vary between native and invasive species. We quantified root morphological and physiological plasticity of co-occurring native and invasive Great Basin species in response to soil nitrogen heterogeneity and determined if trade-offs exist between these foraging responses and species relative growth rate or root system biomass. The nine study species included three perennial bunchgrasses, three perennial forbs, and three invasive perennial forbs. The plants were grown in large pots outdoors. Once a week for 4 weeks equal amounts of ¹⁵NH₄ ¹⁵NO₃ were distributed in the soil either evenly through the soil profile, in four patches, or in two patches. All species acquired more N in patches compared to when N was applied evenly through the soil profile. None of the species increased root length density in enriched patches compared to control patches but all species increased root N uptake rate in enriched patches. There was a positive relationship between N uptake rate, relative growth rate, and root system biomass. Path analysis indicated that these positive interrelationships among traits could provide one explanation of how invasive forbs were able to capture 2 and 15-fold more N from enriched patches compared to the native grasses and forbs, respectively. Results from this pot study suggest that plant traits related to nutrient capture in heterogeneous soil environments may be positively correlated which could potentially promote size-asymmetric competition belowground and facilitate the spread of invasive species. However, field experiments with plants in different neighbor environments ultimately are needed to determine if these positive relationships among traits influence competitive ability and invader success.     

A trade-off between scale and precision in resource foraging

Summary There is widespread uncertainty about the nature and role of morphological plasticity in resource competition in plant communities. We have assayed the foraging characteristics of leaf canopies and root systems of eight herbaceous plants of contrasted ecology using new techniques to create controlled patchiness in light and mineral nutrient supply. The results are compared with those of a conventional competition experiment. Measurements of dry matter partitioning and growth in patchy conditions indicate a consistent positive association between the foraging characteristics of roots and shoots, supporting the hypothesis of strong interdependence of competitive abilities for light and mineral nutrients. Differences are identified in the abilities of dominant and subordinate plants to forage on coarse and fine scalcs. It is suggested that a trade-off exists in the scale (“high” in dominants) and precision (high in subordinates) with which resources are intercepted and that this trade-off contributes to diversity in communities of competing plants.     

水曲柳幼苗根系对土壤养分和水分空间异质性的反应

通过沙培试验方法,研究了温室条件下水曲柳幼苗在施肥和浇水区,非施肥和非浇水区中根系生长,生物量分布,地下部分与地上部分关系,细根直径等特征。结果表明,土壤养分和水分的空间异质性对水曲柳幼苗根系生长和分布有明显影响。在施肥区和浇水区根系生长快,密度大,生物量高,而在非施肥和非浇水区根系生长受到抑制,根系密度小,生物量低,与非施肥区相比,施肥区细根直径下降,有利于根系对养分和水分的运输,但是在非浇水区     

The effects of shading and N status on root proliferation in nutrient patches by the perennial grass Agropyron desertorum in the field

Competition for light can affect exploitation of spatially heterogeneous soil resources. To evaluate the influence of shoot status on root growth responses in nutrient-rich soil patches, we studied the effects of shading and whole-plant nitrogen status on root growth in N-enriched and nonenriched patches by mature Agropyron desertorum plants growing in the field with below-ground competition. Roots in enriched patches had greater length to weight ratios (specific root length, SRL), indicating increased absorptive surface areas, compared with roots in control patches. Increased SRL was due to increased production and length of higher order laterals rather than morphological changes in roots of the same branching order. Although the pattern of root growth rates in patches was the same for shaded and unshaded plants, the magnitude of this response to enriched patches was damped by shading. Root relative growth rates (RGR) in N-enriched patches were reduced by more than 50% by short-term shading treatments (60% reduction in photosynthetic flux density), while root RGR in unenriched patches was unaffected by shading. Unexpectedly, plants with higher nitrogen status had greater root RGR in enriched patches than plants that had not received nitrogen supplement, again with no detectable effect on root RGR in the unenriched patches. Therefore, while both shading and plant N status affected the ability of roots to exploit enriched patches by proliferation, there was no stimulation or suppression of root growth in the unenriched, control patches. Thus, plants already under competitive pressure above ground for light and below ground for nutrients should be less able to rapidly respond to opportunities presented in nutrient patches and pulses.     

Shading and the capture of localized soil nutrients: nutrient contents,carbohydrates, and root uptake kinetics of a perennial tussock grass

Summary The ability to exploit spatial and temporal heterogeneity in soil resources can be one factor important to the competitive balance of plants. Competition above-ground may limit selective plant responses to below-ground heterogeneity, since mechanisms such as root proliferation and alterations in uptake kinetics are energy-dependent processes. We studied the effect of shading on the ability of the perennial tussock grassAgropyron desertorum to take up nutrients from enriched soil microsites in two consecutive growing seasons. Roots of unshaded plants selectively increased phosphate uptake capacity in enriched soil microsites (mean increases of up to 73%), but shading eliminated this response. There were no changes in ammonium uptake capacity for roots in control and enriched patches for either shaded or unshaded plants. The 9-day shade treatments significantly reduced total nonstructural carbohydrate (TNC) concentrations for roots in 1990, but had no apparent effect on root carbohydrates in 1991 despite dramatic reductions in shoot TNC and fructan concentrations. Enrichment of the soil patches resulted in significantly greater phosphate concentrations in roots of both shaded and unshaded plants, with less dramatic differences for nitrogen and no changes in potassium concentrations. In many respects the shaded plants did surprisingly well, at least in terms of apparent nutrient acquisition. The effects of aboveground competition on nutrient demand, energy requirements, and belowground processes are discussed for plants exploiting soil resource heterogeneity.     

Competition for patchy soil resources reduces community evenness

The presence of small-scale patches of soil resources has been predicted to increase competition, because multiple species will proliferate roots in the same small area, and therefore decrease plant diversity. I tested whether such patches reduced species evenness in a community of four old-field species, both with and without interspecific interactions. In species mixtures, patches reduced evenness, while in ??communities?? constructed via combined monocultures, in which species did not compete, patches increased evenness. Therefore, the reduction in evenness in response to patches was due to changes in competition. Community-level changes may be attributable to plant foraging traits??in species with low foraging precision, competition reduced abundance much more in patchy soils than in even soils, while in species with high root foraging precision, the effect of competition was similar in patchy and even soils.