Abstract
Plants forage for nutrients by increasing their root length density (RLD) in nutrient-rich soil microsites through root morphological changes resulting in increased root biomass density (RBD), specific root length (SRL), or branching frequency (BF). It is commonly accepted that fast-growing species will forage more than slow-growing species. However, foraging responses may be due solely to differences in relative growth rates (RGR). There is little evidence, after the effects of RGR are removed, that the fast versus slow foraging theory is correct. In a pot study, we evaluated foraging of four grass species that differed in RGR: one fast-growing annual species, Bromus diandrus, two intermediate-growing species, annual Bromus hordeaceus and perennial Elymus glaucus, and one slow-growing perennial species, Nassella pulchra. We harvested plants either at a common time (plants varied in size) or at a common leaf number (plants similar size, surrogate for common biomass). By evaluating species at a common time, RGR influenced foraging. Conversely, by evaluating species at a common leaf number, foraging could be evaluated independent of RGR. When RGR was allowed to contribute to foraging (common time harvest), foraging and RGR were positively correlated. B. diandrus (fast RGR) foraged to a greater extent than did E. glaucus (intermediate RGR) and N. pulchra (slow RGR). E. glaucus (intermediate RGR) foraged to a greater extent than N. pulchra (slow RGR). Root growth within nutrient-rich microsites was due to significant increases in RBD, not to modifications of SRL or BF. However, when RGR was not allowed to influence foraging (common leaf number harvest), none of the four species significantly enhanced RLD in nutrient-rich compared to control microsites. This suggests that RGR strongly influenced the ability of these grass species to forage and also supports the need to evaluate plastic root traits independent of RGR.
Similar content being viewed by others
Abbreviations
- -:
-
BF Branching frequency—distance internal to internal branches—mm
- -:
-
RBD Root biomass density—Root biomass per soil volume—g m−3
- -:
-
RLD Root length density—Root length per soil volume—km m−3
- -:
-
RWR Root weight ratio—Root mass per total biomass—kg kg−1
- -:
-
SLA Specific leaf area—Leaf area per leaf biomass—m2 kg−1
- -:
-
SRL Specific root length—Root length per root biomass—km kg−1
- -:
-
RGR Relative growth rate—Δ biomass per total biomass per time—g g−1 day−1
- -:
-
RTD Root tissue density—Root biomass per root volume—kg m−3
References
Bartolome JW, Gemmill B (1981) The ecological status of Stipa pulchra (Poaceae) in California. Madroño 28:172–184
Bauhus J, Messier C (1999) Evaluation of fine root length and diameter measurements obtained using rhizo image analysis. Agron J 91:142–147
Bilbrough CJ, Caldwell MM (1995) The effects of shading and N status on root proliferation in nutrient patches by perennial grass Agropyron desertorum in the field. Oecologia 103:10–16
Bouma TJ, Nielsen KL, Koutstaal B (2000) Sample preparation and scanning protocol for computerized analysis of root length and diameter. Plant Soil 218:185–196
Caldwell MM (1994) Exploiting nutrients in fertile soil microsites. In: Caldwell MM, Pearcy RW (eds) Exploration of environmental heterogeneity by plants: ecophysiological processes above- and belowground. Academic Press, San Diego, pp 325–347
Campbell BD, Grime JP (1989) A comparative study of plant responsiveness to the duration of episodes of mineral nutrient enrichment. New Phytol 112:261–267
Coleman JS, McConnaughay KDM, Bazzaz FA (1993) Elevated CO2 and plant nitrogen-use: is reduced tissue concentration size-dependant. Oecologia 93:195–200
Coleman JS, McConnaughay KDM, Ackerly DD (1994) Interpreting phenotypic variation in plants. Trends Ecol Evol 9:187–191
Crick JC, Grime JP (1987) Morphological plasticity and mineral nutrient capture in two herbaceous species of contrasted ecology. New Phytol 107:403–414
Dahlgren RA, Singer MJ, Huang X (1997) Oak tree and grazing impacts on soil properties and nutrients in a California oak woodland. Biogeochemistry 39:45–64
Drew MC (1975) Comparisons of the effects of a localized supply of phosphate, nitrate, ammonium, and potassium on the growth of seminal root system, and shoot, in barley. New Phytol 75:479–490
Einsmann JC, Jones RH, Mou P, Mitchell RJ (1999) Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. J Ecol 87:609–619
Elberse WTH, Berendse F (1993) A comparative study of the growth and morphology of eight grass species from habitats with different nutrient availabilities. Funct Ecol 7:223–229
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) Exploration of environmental heterogeneity by plants: ecophysiological processes above- and belowground. Academic Press, San Diego, pp 305–323
Fransen B, de Kroon H, Berendse F (1998) Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115:351–358
Fransen B, Blijjenburg J, de Kroon H (1999a) Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant Soil 211:179–189
Fransen B, de Kroon H, de Kovel CGF, Van Den Bosch F (1999b) Disentangling the effects of root foraging and inherent growth rate on plant biomass accumulation in heterogeneous environments: a modeling study. Ann Bot 84:305–311
Granato TC, Raper CD (1989) Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. J Exp Bot 40:236–257
Grime JP, Hunt R (1975) Relative growth rates: its range and adaptive significance in a local flora. J Ecol 63:393–422
Grime JP, Campbell BD, Mackey JML, Crick JC (1991) Root plasticity, nitrogen capture and competitive ability. In: Atkinson D (ed) Plant root growth: an ecological perspective. Blackwell, Oxford, pp 381–397
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
Gross KL, Pregitzer KS, Burton AJ (1995) Spatial variation in nitrogen availability in three successional plant communities. J Ecol 83:357–367
Huante P, Rincón E, Chapin FS III (1998) Foraging for nutrients, responses to changes in light, and competition in tropical deciduous tree seedlings. Oecologia 117:209–216
Hutchingson MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Adv Ecol Res 25:159–238
Jackson LE (1985) Ecological origins of California's Mediterranean grasses. J Biogeogr 12:349–361
Jackson LE, Strauss RB, Firestone MK, Bartolome JW (1988) Plant and soil nitrogen dynamics on California annual grassland. Plant Soil 110:9–17
Jackson LE, Strauss RB, Firestone MK, Bartolome JW (1990) Influences of tree canopies on grassland productivity and nitrogen dynamics in deciduous oak savanna. Agric Ecosyst Environ 32:89–105
Jackson RB, Caldwell MM (1992) Shading and the capture of localized soil nutrients: nutrient contents, carbohydrates, and root uptake kinetics of a perennial tussock grass. Oecologia 91:457–462
Jackson RB, Caldwell MM (1993) Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–692
Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261
Larigauderie A, Richards JH (1994) Root proliferation characteristics of seven perennial arid-land grasses in nutrient-enriched microsites. Oecologia 99:102–111
Lonn M, Sandberg A, Redbo-Torstensson P (1998) Fitness-related traits of allozyme genotypes in Bromus hordeaceus L. (Poaceae) associated with field habitat and experimental flooding. Biol J Linn Soc 64:207–222
Passioura JB, Wetselaar R (1972) Consequences of banding nitrogen fertilizer in soil. II. Effects on the growth of wheat roots. Plant Soil 36:461–473
Poorter H, Pothmann P (1992) Growth and carbon economy of a fast-growing and slow-growing grass species as dependent on ontogeny. New Phytol 120:159–166
Rice SA, Bazzaz FA (1989) Quantification of plasticity of plant traits in response to light intensity: comparing phenotypes at a common weight. Oecologia 78:502–507
Robinson D, Rorison IH (1987) Root hairs and plant growth at low nitrogen availabilities. New Phytol 107:681–693
Robinson D, Rorison IH (1988) Plasticity in grass species in relation to nitrogen supply. Funct Ecol 2:249–257
Ryel RJ, Caldwell MM, Manwarring JH (1996) Temporal dynamics of soil spatial heterogeneity in sagebrush-wheatgrass steppe during a growing season. Plant Soil 184:299–309
SAS/SAT (1995) User's Guide, Release 6.03 Edition. SAS Institute, Cary, N.C.
Van de Vijver CADM, Boot RGA, Poorter H, Lambers H (1993) Phenotypic plasticity in response to nitrate supply of an inherently fast-growing species from a fertile habitat and an inherently slow-growing species from an infertile habitat. Oecologia 96:548–554
Van Vuuren MMI, Robinson D, Griffiths BS (1996) Nutrient inflow and root proliferation during the exploitation of a temporally spatially discrete source of nitrogen in soil. Plant Soil 178:185–192
Welker JM, Gordon DR, Rice KJ (1991) Capture and allocation of nitrogen by Quercus douglassi seedlings in competition with annual and perennial grasses. Oecologia 87:459–466
Acknowledgements
This research was supported by the National Science Foundation (Grant DEB-99-81711 to C.S.B.). We would like to thank Scott Olmstead for countless hours of research assistance and Dr. Mitchell Watnik for statistical advice.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aanderud, Z.T., Bledsoe, C.S. & Richards, J.H. Contribution of relative growth rate to root foraging by annual and perennial grasses from California oak woodlands. Oecologia 136, 424–430 (2003). https://doi.org/10.1007/s00442-003-1275-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-003-1275-7