Review of root nutrient foraging plasticity and root competition of plants

Expand
  • Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China

Received date: 2012-04-24

  Revised date: 2012-09-18

  Online published: 2012-11-09

Abstract

In order to effectively absorb nutrients from naturally heterogeneous soil, plant roots employ various plastic responses to the environment heterogeneity through evolution and adaptation. In addition, plant roots also face competition from both intra- and inter-specific competitors. Factors affecting the outputs of root competition include nutrient availability, scale and degree of soil heterogeneity and ability of root plasticity. Competition adds a new dimension to plants; plant roots may alter their normal plastic responses, e.g., root competition will affect the spatial distribution of root systems. Different plastic responses of roots will in turn influence root competition per se. Previous studies have revealed that plants with high root morphological plasticity and high physiological plasticity achieved competitive advantages. Plants differ in their root nutrient foraging plasticity, and therefore may not have fixed ways of responding to competition. The uniqueness and traits of species need to be considered in comprehending the mechanisms of their plastic responses of root foraging in competition and the consequences. The responses of roots to competitors may also be influenced by the competitors, and the competitive status of the plant may change. Closely related plants may be more likely to avoid the competition from each other. A few studies have focused on integration of root competition and root foraging plasticity, as well as the impact of root competition on the community structure. This review is intended to discuss this issue.

Cite this article

WANG Peng, MOU Pu, LI Yun-Bin . Review of root nutrient foraging plasticity and root competition of plants[J]. Chinese Journal of Plant Ecology, 2012 , 36(11) : 1184 -1196 . DOI: 10.3724/SP.J.1258.2012.01184

References

1 Aerts R, Chapin FS III ( 1999). The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research, 30, 1-67.
2 Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM ( 2003). Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science, 301, 1377-1380.
3 Bartelheimer M, Steinlein T, Beyschlag W ( 2006). Aggregative root placement: a feature during interspecific competition in inland sand-dune habitats. Plant and Soil, 280, 101-114.
4 Bending GD, Read DJ ( 1995). The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytologist, 130, 401-409.
5 Berntson GM, Wayne PM ( 2000). Characterizing the size dependence of resource acquisition within crowded plant populations. Ecology, 81, 1072-1085.
6 Blair B ( 2001). Effect of soil nutrient heterogeneity on the symmetry of belowground competition. Plant Ecology, 156, 199-203.
7 Bliss K, Jones RH, Mitchell RJ, Mou PP ( 2002). Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior? New Phytologist, 154, 409-417.
8 Bradshaw AD ( 1965). Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics, 13, 115-155.
9 Bray SR, Kitajima K, Sylvia DM ( 2003). Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecological Applications, 13, 565-574.
10 Brisson J, Reynolds JF ( 1994). The effect of neighbors on root distribution in a creosotebush ( Larrea tridentata) population. Ecology, 75, 1693-1702.
11 Brisson J, Reynolds JF ( 1997). Effects of compensatory growth on population processes: a simulation study. Ecology, 78, 2378-2384.
12 Burns IG ( 1991). Short- and long-term effects of a change in the spatial distribution of nitrate in the root zone on N uptake, growth and root development of young lettuce plants. Plant, Cell & Environment, 14, 21-33.
13 Cahill JF Jr ( 1999). Fertilization effects on interactions between above- and belowground competition in an old field. Ecology, 80, 466-480.
14 Cahill JF Jr, Casper BB ( 1999). Growth consequences of soil nutrient heterogeneity for two old-field herbs, Ambrosia artemisiifolia and Phytolacca americana, grown individually and in combination. Annals of Botany, 83, 471-478.
15 Cahill JF Jr, Casper BB ( 2000). Investigating the relationship between neighbor root biomass and belowground competition: field evidence for symmetric competition belowground. Oikos, 90, 311-320.
16 Cahill JF Jr, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, St Clair CC ( 2010). Plants integrate information about nutrients and neighbors. Science, 328, 1657.
17 Caldwell MM, Dudley LM, Lilieholm B ( 1992). Soil solution phosphate, root uptake kinetics and nutrient acquisition: implications for a patchy soil environment. Oecologia, 89, 305-309.
18 Caldwell MM, Manwaring JH, Durham SL ( 1991a). The microscale distribution of neighbouring plant roots in fertile soil microsites. Functional Ecology, 5, 765-772.
19 Caldwell MM, Manwaring JH, Jackson RB ( 1991b). Exploitation of phosphate from fertile soil microsites by three Great Basin perennials when in competition. Functional Ecology, 5, 757-764.
20 Callaway RM, Aschehoug ET ( 2000). Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science, 290, 521-523.
21 Callaway RM, Newingham B, Zabinski CA, Mahall BE ( 2001). Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecology Letters, 4, 429-433.
22 Callaway RM, Pennings SC, Richards CL ( 2003). Phenotypic plasticity and interactions among plants. Ecology, 84, 1115-1128.
23 Campbell BD, Grime JP, Mackey JML ( 1991). A trade-off between scale and precision in resource foraging. Oecologia, 87, 532-538.
24 Casper BB, Jackson RB ( 1997). Plant competition under- ground. Annual Review of Ecology and Systematics, 28, 545-570.
25 Chalot M, Brun A ( 1998). Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiology Reviews, 22, 21-44.
26 Charnov EL ( 1976). Optimal foraging, the marginal value theorem. Theoretical Population Biology, 9, 129-136.
27 Coomes DA, Grubb PJ ( 2000). Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecological Monographs, 70, 171-207.
28 D’Antonio CM, Mahall BE ( 1991). Root profiles and competition between the invasive, exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. American Journal of Botany, 78, 885-894.
29 Day KJ, Hutchings MJ, John EA ( 2003a). The effects of spatial pattern of nutrient supply on yield, structure and mortality in plant populations. Journal of Ecology, 91, 541-553.
30 Day KJ, John EA, Hutchings MJ ( 2003b). The effects of spatially heterogeneous nutrient supply on yield, intensity of competition and root placement patterns in Briza media and Festuca ovina. Functional Ecology, 17, 454-463.
31 de Kroon H, Huber H, Stuefer JF, van Groenendael JM ( 2005). A modular concept of phenotypic plasticity in plants. New Phytologist, 166, 73-82.
32 de Kroon H, Mommer L, Nishiwaki A ( 2003). Root competition: towards a mechanistic understanding. In: de Kroon H, Visser EJW eds. Root Ecology. Springer-Verlag, Berlin. 215-234.
33 de Kroon H, Visser EJW, Huber H, Mommer L, Hutchings MJ ( 2009). A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant, Cell & Environment, 32, 704-712.
34 Derner JD, Briske DD ( 1999). Does a tradeoff exist between morphological and physiological root plasticity? A comparison of grass growth forms. Acta Oecologica, 20, 519-526.
35 Drew MC, Nye PH ( 1970). The supply of nutrient ions by diffusion to plant roots in soil III. Uptake of phosphate by roots of onion, leek, and rye-grass. Plant and Soil, 33, 545-563.
36 Druebert C, Lang C, Valtanen K, Polle A ( 2009). Beech carbon productivity as driver of ectomycorrhizal abundance and diversity. Plant, Cell & Environment, 32, 992-1003.
37 Edwards EJ, Benham DG, Marland LA, Fitter AH ( 2004). Root production is determined by radiation flux in a temperate grassland community. Global Change Biology, 10, 209-227.
38 Einsmann JC, Jones RH, Mou P, Mitchell RJ ( 1999). Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. Journal of Ecology, 87, 609-619.
39 Eissenstat D, Caldwell M ( 1988). Seasonal timing of root growth in favorable microsites. Ecology, 69, 870-873.
40 Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL ( 2000). Building roots in a changing environment: implications for root longevity. New Phytologist, 147, 33-42.
41 Eissenstat DM, Yanai RD ( 1997). The ecology of root lifespan. Advances in Ecological Research, 27, 1-60.
42 Ek H ( 1997). The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal association with Betula pendula. New Phytologist, 135, 133-142.
43 Ettema CH, Wardle DA ( 2002). Spatial soil ecology. Trends in Ecology and Evolution, 17, 177-183.
44 Falik O, Reides P, Gersani M, Novoplansky A ( 2003). Self/ non-self discrimination in roots. Journal of Ecology, 91, 525-531.
45 Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H ( 2012). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 109, 2666-2671.
46 Fitter AH ( 1991). Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia, 47, 350-355.
47 Fitter AH (1994). Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. In: Caldwell MM, Pearcy RW eds. Exploitation of Environmental Heterogeneity of Plants. Academic Press, New York. 305-323.
48 Fitter AH, Williamson L, Linkohr B, Leyser O ( 2002). Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proceedings of the Royal Society B: Biological Sciences, 269, 2017-2022.
49 Fransen B, de Kroon H, Berendse F ( 2001). Soil nutrient heterogeneity alters competition between two perennial grass species. Ecology, 82, 2534-2546.
50 Genney DR, Alexander IJ, Hartley SE ( 2002). Soil organic matter distribution and below-ground competition between Calluna vulgaris and Nardus stricta. Functional Ecology, 16, 664-670.
51 Gersani M, Abramshy Z, Falik O (1998). Density-dependent habitat selection in plants. Evolutionary Ecology, 12, 223-234.
52 Gersani M, Brown JS, O’Brien EE, Maina GM, Abramsky Z (2001). Tragedy of the commons as a result of root competition. Journal of Ecology, 89, 660-669.
53 Goldberg DE, Rajaniemi T, Gurevitch J, Stewart-Oaten A ( 1999). Empirical approaches to quantifying interaction intensity: competition and facilitation along productivity gradients. Ecology, 80, 1118-1131.
54 Grime JP ( 1979). Plant Strategies and Vegetation Processes. John Wiley & Sons, New York. 222.
55 Gross KL, Peters A, Pregitzer KS ( 1993). Fine root growth and demographic responses to nutrient patches in four old- field plant species. Oecologia, 95, 61-64.
56 Gruntman M, Novoplansky A ( 2004). Physiologically mediated self/non-self discrimination in roots. Proceedings of the National Academy of Sciences of the United States of America, 101, 3863-3867.
57 Harrison KA, Bol R, Bardgett RD ( 2007). Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology, 88, 989-999.
58 Helgason T, Fitter A ( 2005). The ecology and evolution of the arbuscular mycorrhizal fungi. Mycologist, 19, 96-101.
59 Hodge A ( 2004). The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist, 162, 9-24.
60 Hodge A ( 2006). Plastic plants and patchy soils. Journal of Experimental Botany, 57, 401-411.
61 Hodge A, Robinson D, Griffiths BS, Fitter AH ( 1999). Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell & Environment, 22, 811-820.
62 Huber-Sannwald E, Pyke DA, Caldwell MM ( 1996). Morphological plasticity following species-specific recognition and competition in two perennial grasses. American Journal of Botany, 83, 919-931.
63 Hutchings MJ, John EA, Wijesinghe DK ( 2003). Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology, 84, 2322-2334.
64 Jackson RB, Caldwell MM ( 1996). Integrating resource heterogeneity and plant plasticity: modelling nitrate and phosphate uptake in a patchy soil environment. Journal of Ecology, 84, 891-903.
65 Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED ( 1996). A global analysis of root distributions for terrestrial biomes. Oecologia, 108, 389-411.
66 Jackson RB, Mooney HA, Schulze ED ( 1997). A global budget for fine root biomass, surface area, and nutrient contents. Proceedings of the National Academy of Sciences of the United States of America, 94, 7362-7366.
67 Jakobsen I, Chen BD, Munkvold L, Lundsgaard T, Zhu YG ( 2005). Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant, Cell & Environment, 28, 928-938.
68 Jane?ek ?, Jane?ková P, Lep? J ( 2004). Influence of soil heterogeneity and competition on growth features of three meadow species. Flora, 199, 3-11.
69 Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB ( 2003). Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology, 84, 1895-1908.
70 Kembel SW, Cahill JF Jr ( 2005). Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. The American Naturalist, 166, 216-230.
71 Kembel SW, de Kroon H, Cahill JF, Mommer L ( 2008). Improving the scale and precision of hypotheses to explain root foraging ability. Annals of Botany, 101, 1295-1301.
72 King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P ( 2002). Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytologist, 154, 389-398.
73 Leuschner C, Hertel D, Coners H, Büttner V ( 2001). Root competition between beech and oak: a hypothesis. Oecologia, 126, 276-284.
74 Liu YB ( 刘延滨), Mou P ( 牟溥 ) ( 2010). Mycorrhizal plasticity of plant nutrient foraging: a review of ectomycorrhizal plasticity. Chinese Journal of Plant Ecology (植物生态学报), 34, 1472-1484. (in Chinese with English abstract)
75 Liu YJ, Shi GX, Mao L, Cheng G, Jiang SJ, Ma XJ, An LZ, Du GZ, Johnson NC, Feng HY ( 2012). Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytologist, 194, 523-535.
76 Mahall BE, Callaway RM ( 1996). Effects of regional origin and genotype on intraspecific root communication in the desert shrub Ambrosia dumosa(Asteraceae). American Journal of Botany, 83, 93-98.
77 McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G ( 2002). Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature, 415, 68-71.
78 Mokany K, Raison RJ, Prokushkin AS ( 2006). Critical analysis of root: shoot ratios in terrestrial biomes. Global Change Biology, 12, 84-96.
79 Mommer L, van Ruijven J, de Caluwe H, Smit-Tiekstra AE, Wagemaker CAM, Ouborg NJ, B?gemann GM, van der Weerden GM, Berendse F, de Kroon H ( 2010). Unveiling below-ground species abundance in a biodiversity experiment: a test of vertical niche differentiation among grassland species. Journal of Ecology, 98, 1117-1127.
80 Mommer L, van Ruijven J, Jansen C, van de Steeg HM, de Kroon H ( 2011a). Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory? Functional Ecology, 26, 66-73.
81 Mommer L, Visser EJW, van Ruijven J, de Caluwe H, Pierik R, de Kroon H ( 2011 b). Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions. Plant and Soil, 344, 347-360.
82 Moora M, Zobel M ( 1996). Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia, 108, 79-84.
83 Moora M, Zobel M ( 1998). Can arbuscular mycorrhiza change the effect of root competition between conspecific plants of different ages? Canadian Journal of Botany, 76, 613-619.
84 Mou P, Jones RH, Mitchel, RJ, Zutter B ( 1995). Spatial distribution of roots in sweetgum and loblolly pine monocultures and relations with above-ground biomass and soil nutrients. Functional Ecology, 9, 689-699.
85 Newsham KK, Fitter AH, Watkinson AR ( 1995). Multi- functionality and biodiversity in arbuscular mycorrhizas. Trends in Ecology and Evolution, 10, 407-411.
86 Novoplansky A, Goldberg DE ( 2001). Effects of water pulsing on individual performance and competitive hierarchies in plants. Journal of Vegetation Science, 12, 199-208.
87 Oleszek WA, Hoagland RE, Zablotowicz RM (1999). Ecological significance of plant saponins. In: Inderjit D, Dakshini KMM, Foy CL eds. Principles and Practices in Plant Ecology: Allelochemical Interactions. CRC Press LLC, Boca Raton. 451-465.
88 Perry LG, Thelen GC, Ridenour WM, Weir TL, Callaway RM, Paschke MW, Vivanco JM ( 2005). Dual role for an allelochemical: (±)-catechin from Centaurea maculosa root exudates regulates conspecific seedling establishment. Journal of Ecology, 93, 1126-1135.
89 Peterson RL, Massicotte HB, Melville LH (2004). Mycorrhizas: Anatomy and Cell Biology. NRC Research Press, Ottawa, Canada.
90 Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL ( 2002). Fine root architecture of nine North American trees. Ecological Monographs, 72, 293-309.
91 Pregitzer KS, Hendrick RL, Fogel R ( 1993). The demography of fine roots in response to patches of water and nitrogen. New Phytologist, 125, 575-580.
92 Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL ( 1997). Relationships among root branch order, carbon, and nitrogen in four temperate species. Oecologia, 111, 302-308.
93 Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR ( 1998). Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiology, 18, 665-670.
94 Pugnaire FI, Luque MT ( 2001). Changes in plant interactions along a gradient of environmental stress. Oikos, 93, 42-49.
95 Putz FE, Canham CD ( 1992). Mechanisms of arrested succession in shrublands: root and shoot competition between shrubs and tree seedlings. Forest Ecology and Management, 49, 267-75.
96 Rajaniemi TK ( 2003). Evidence for size asymmetry of belowground competition. Basic and Applied Ecology, 4, 239-247.
97 Rajaniemi TK ( 2007). Root foraging traits and competitive ability in heterogeneous soils. Oecologia, 153, 145-152.
98 Rajaniemi TK, Allison VJ, Goldberg DE ( 2003). Root competition can cause a decline in diversity with increased productivity. Journal of Ecology, 91, 407-416.
99 Read DJ ( 1991). Mycorrhizas in ecosystems. Cellular and Molecular Life Sciences, 47, 376-391.
100 Rewald B, Leuschner C ( 2009). Belowground competition in a broad-leaved temperate mixed forest: pattern analysis and experiments in a four-species stand. European Journal of Forest Research, 128, 387-398.
101 Robinson D ( 1994). The responses of plants to non-uniform supplies of nutrients. New Phytologist, 127, 635-674.
102 Robinson D ( 2001). Root proliferation, nitrate inflow and their carbon costs during nitrogen capture by competing plants in patchy soil. Plant and Soil, 232, 41-50.
103 Robinson D, Hodge A, Griffiths BS, Fitter AH ( 1999). Plant root proliferation in nitrogen-rich patches confers competitive. Proceedings of the Royal Society B: Biological Sciences, 266, 431-435.
104 Robinson D, Linehan DJ, Gordon DC ( 1994). Capture of nitrate from soil by wheat in relation to root length, nitrogen inflow and availability. New Phytologist, 128, 297-305.
105 Ryel RJ, Caldwell MM, Manwaring JH ( 1996). Temporal dynamics of soil spatial heterogeneity in sagebrush- wheatgrass steppe during a growing season. Plant and Soil, 184, 299-309.
106 Salguero-Gómez R, Casper BB ( 2011). Introducing short roots in a desert perennial: anatomy and spatiotemporal foraging responses to increased precipitation. New Phytologist, 191, 173-83.
107 Schenk HJ ( 2006). Root competition: beyond resource depletion. Journal of Ecology, 94, 725-739.
108 Schenk HJ, Callaway RM, Mahall BE ( 1999). Spatial root segregation: Are plants territorial? Advances in Ecological Research, 28, 145-180.
109 Schwinning S, Weiner J ( 1998). Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia, 113, 447-455.
110 Seifert E, Bever JD, Maron JL ( 2009). Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology, 90, 1055-1062.
111 Semchenko M, Hutchings MJ, John EA ( 2007). Challenging the tragedy of the commons in root competition: confounding effects of neighbour presence and substrate volume. Journal of Ecology, 95, 252-260.
112 Smith MD, Hartnett DC, Wilson GWT ( 1999). Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia, 121, 574-582.
113 St John TV, Coleman DC, Reid CPP ( 1983). Association of vesicular-arbuscular mycorrhizal hyphae with soil organic particles. Ecology, 64, 957-959.
114 Tilman D (1988). Plant Strategies and the Dynamics and Structure of Plant Communities. Princeton University Press, Princeton.
115 Tingey DT, Phillips DL, Johnson MG ( 2000). Elevated CO2 and conifer roots: effects on growth, life span and turnover. New Phytologist, 147, 87-103.
116 Tinker PB, Nye PH (2000). Solute Movement in the Rhizosphere. Oxford University Press, Oxford.
117 Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D ( 2005). Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytologist, 167, 493-508.
118 Twolan-Strutt L, Keddy PA ( 1996). Above- and belowground competition intensity in two contrasting wetland plant communities. Ecology, 77, 259-270.
119 van der Werf A, Kooijman A, Welschen R, Lambers H ( 1988). Respiratory energy costs for the maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex acudformis. Physiologia Plantarum, 72, 483-491.
120 van Vuuren MMI, Robinson D, Griffiths BS (1996). Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant and Soil, 178, 185-192.
121 Volder A, Smart DR, Bloom AJ, Eissenstat DM ( 2005). Rapid decline in nitrate uptake and respiration with age in fine lateral roots of grape: implications for root efficiency and competitive effectiveness. New Phytologist, 165, 493-501.
122 von Wettberg EJ, Weiner J ( 2003). Larger Triticum aestivum plants do not preempt nutrient-rich patches in a glasshouse experiment. Plant Ecology, 169, 85-92.
123 Wallenda T, Read DJ ( 1999). Kinetics of amino acid uptake by ectomycorrhizal roots. Plant, Cell & Environment, 22, 179-187.
124 Wang LX, Mou PP, Jones RH ( 2006). Nutrient foraging via physiological and morphological plasticity in three plant species. Canadian Journal of Forest Research, 36, 164-173.
125 Weiner J ( 1985). Size hierarchies in experimental populations of annual plants. Ecology, 66, 743-752.
126 West HM (1996). Influence of arbuscular mycorrhizal infection on competition between Holcus lanatus and Dactylis glomerta. Journal of Ecology, 84, 429-438.
127 Wijesinghe DK, John EA, Beurskens S, Hutchings MJ ( 2001). Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. Journal of Ecology, 89, 927-983.
128 Wijesinghe DK, John EA, Hutchings MJ ( 2005). Does pattern of soil resource heterogeneity determine plant community structure? An experimental investigation. Journal of Ecology, 93, 99-112.
129 Wilson JB ( 1988). Shoot competition and root competition. Journal of Applied Ecology, 25, 279-296.
130 Wilson SD, Tilman D ( 1995). Competitive responses of eight old-field plant species in four environments. Ecology, 76, 1169-1180.
131 Xia MX, Guo DL, Pregitzer KS ( 2010). Ephemeral root modules in Fraxinus mandshurica. New Phytologist, 188, 1065-1074.
132 Zabinski CA, Quinn L, Callaway RM ( 2002). Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Functional Ecology, 16, 758-765.
133 Zhang H, Forde BG ( 1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science, 279, 407-409.
Outlines

/