Skip to main content
SpringerLink
Log in

Estimating Root Production: Comparison of 11 Methods in Shortgrass Steppe and Review of Biases

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Estimating root production has been difficult due to multiple potential biases associated with both old and new methods. This shortgrass steppe site is the only place we are aware of that can compare most methods including sequential coring, ingrowth cores, and ingrowth donuts, 14C pulse-isotope dilution, 14C pulse-isotope turnover, rhizotron windows, and minirhizotron, and indirect methods including nitrogen budget, carbon flux, simulation carbon flow model, and regression model. We used the studies at this site, other comparisons, a summary of potential directional biases, and different ways of calculating estimates in a logical, comparative approach of evaluating methods. Much of the literature for root production is based on sequential biomass coring, a method resulting in erroneous estimates. Root ingrowth estimates of production are generally conservative compared to minirhizotron and isotope turnover methods. The size of the ingrowth area may be the most important determinant of the underestimation. Estimates based on pulse-isotope dilution are also erroneous due to non-uniform labeling of tissues. Uniform labeling is not an assumption of the pulse-isotope turnover method, and this method has the least severe potential biases. Root production estimates from pulse-isotope turnover were lower than those using minirhizotron when the most common method of calculation was used. This agrees with literature concerning bomb 14C continuous-isotope labeling comparisons with minirhizotron, although some potential biases between isotope methods are different. However, good agreement between pulse-isotope turnover and minirhizotron were obtained when minirhizotron estimates were calculated from regression of decomposition versus production to equilibrium and when pulse-isotope turnover estimates were calculated from two-phase life-span regressions. This minirhizotron method bypasses biases associated with the artificial surface similar to root-cohort methods that may be practical only in mesic systems, and takes into account both short- and long-lived roots and corrects for soil-isotope contamination that the continuous-isotope labeling bomb 14C method is not able to account for. Comparisons of these direct methods are also made with four indirect methods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2

Similar content being viewed by others

References

  • Aber JD, Melillo JM, Nadelhoffer JK, McClaugherty CA, Pastor J. 1985. Fine root turnover in forest ecosystems in relation to quality and form of nitrogen availability: a comparison of two methods. Oecologia 66:317–21.

    Article  Google Scholar 

  • Ares J. 1976. Dynamics of the root system of blue grama. J Range Manage 29:208–13.

    Article  Google Scholar 

  • Arnone JAIII, Zaller JG, Spehn EM, Niklaus PA, Wells CE, Körner C. 2000. Dynamics of root systems in native grasslands: effects of elevated atmospheric CO2. New Phytol 147:73–85.

    Article  CAS  Google Scholar 

  • Biondini ME, Lauenroth WK, Sala OE. 1991. Correcting estimates of net primary production: are we overestimating plant production in rangelands? J Range Manage 44:194–8.

    Article  Google Scholar 

  • Burke IC, Mosier AR, Hook PB, Milchunas DG, Barrett JE, Vinton MA, McCulley RL, Kaye JP, Gill RA, Epstein HE, Kelly RH, Parton WJ, Yonker CM, Lowe P, Lauenroth WK. 2008. Biogeochemistry of soil organic matter and nutrient dynamics of shortgrass steppe ecosystems. In: Lauenroth WK, Burke IC, Eds. Ecology of the shortgrass steppe: a long-term perspective. New York: Oxford University Press. p 306–41.

    Google Scholar 

  • Caldwell MM, Camp LB. 1974. Belowground productivity of two cool desert communities. Oecologia 17:123–30.

    Article  Google Scholar 

  • Clark FE. 1977. Internal cycling of 15Nitrogen in a short-grass prairie. Ecology 58:1322–32.

    Article  CAS  Google Scholar 

  • Coffin DP, Lauenroth WK. 1991. Effects of competition on spatial distribution of roots of blue grama. J Range Manage 44:68–71.

    Article  Google Scholar 

  • Dahlman RC, Kucera CL. 1965. Root productivity and turnover in native prairie. Ecology 46:84–9.

    Article  Google Scholar 

  • Dahlman, RC, Kucera CL. 1967. Carbon-14 cycling in the root and soil components of a prairie ecosystem. In: Nelson DJ, Evans FC, Eds. Symposium on radioecology. Publication Number 272, U.S. Atomic Energy Commission, Radiation Ecology Section, and Clearinghouse for Federal Scientific and Technical Information. p 652–60.

  • Dahlman RC, Kucera CL. 1968. Tagging native grassland vegetation with carbon-14. Ecology 49:1199–203.

    Article  Google Scholar 

  • Eissenstat DM, Caldwell MM. 1988. Seasonal timing of root growth in favorable microsites. Ecology 69:870–3.

    Article  Google Scholar 

  • Eissenstat DM, Yanai RD. 1997. The ecology of root lifespan. Adv Ecol Res 27:1–60.

    Article  Google Scholar 

  • Fahey TJ, Bledsoe CS, Day FP, Ruess RW, Smucker AM. 1999. Fine root production and demography. In: Robertson GP, Bledsoe CS, Coleman D, Sollins P, Eds. Standard soil methods for long-term ecological research. New York: Oxford University Press. p 437–55.

    Google Scholar 

  • Fahey TJ, Hughs JW. 1994. Fine root dynamics in a northern hardwood forest ecosystem, Hubbard Brook Experimental Forest, NH. J Ecol 82:533–48.

    Article  Google Scholar 

  • Fitter AH. 1976. Effects of nutrient supply and competition from other species on root growth of Lolium perenne in soil. Plant Soil 45:177–89.

    Article  CAS  Google Scholar 

  • Fogel R. 1990. Root turnover and production in forest trees. Hortscience 25:270–3.

    Google Scholar 

  • Hansson AL, Andrén O. 1986. Below-ground plant production in a perennial grass ley (Festuca pratensis Huds.) assessed with different methods. J Appl Ecol 23:657–66.

    Article  Google Scholar 

  • Kurz WA, Kimmins JP. 1987. Analysis of some sources of error in methods used to determine fine root production in forest ecosystems: a simulation approach. Can J For Res 17:909–12.

    Article  Google Scholar 

  • Gaudinski JB, Trumbore SE, Davidson EA, Cook AC, Markewitz D, Richter DD. 2001. The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129:420–9.

    Google Scholar 

  • Geisler D, Ferree DC. 1984. Response of plants to root pruning. Hort Rev 6:155–88.

    Google Scholar 

  • Gill RA, Kelly RH, Parton WJ, Day KA, Jackson RB, Morgan JA, Scurlock JMO, Tieszen LL, Castle JV, Ojima DS, Zhang XS. 2002. Using simple environmental variables to estimate belowground productivity in grasslands. Global Ecol Biogeogr 11:79–86.

    Article  Google Scholar 

  • Hendrick RL, Pergitzer KS. 1993. Applications of minirhizotrons to understand root function in forests and other natural ecosystems. Plant Soil 185:293–304.

    Article  Google Scholar 

  • Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo D. 2006. Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:40–57.

    Article  Google Scholar 

  • Hendricks JJ, Nadelhoffer KJ, Aber JD. 1993. Assessing the role of fine roots in carbon and nitrogen cycling. Trends Ecol Evol 8:174–8.

    Article  Google Scholar 

  • Hendrickson AH, Veihmeyer FJ. 1931. Influence of dry soil on root extension. Plant Physiol 6:567–76.

    Article  CAS  PubMed  Google Scholar 

  • Hertel D, Leuschner C. 2002. A comparison of four different fine root production estimates with ecosystem carbon balance data in a Fagus-Quercus mixed forest. Plant Soil 239:237–51.

    Article  CAS  Google Scholar 

  • Higgens PAT, Jackson RB, Des Rosiers JM, Field CB. 2002. Root production and demography in a California annual grassland under elevated atmospheric carbon dioxide. Global Change Biol 8:841–50.

    Article  Google Scholar 

  • Jordan CF, Escalante G. 1980. Root productivity in an Amazonian rain forest. Ecology 61:14–18.

    Article  Google Scholar 

  • Joslin JD, Wolfe MH. 1999. Disturbance during minirhizotron installation can affect root observation data. Soil Sci Soc Am J 63:218–21.

    CAS  Google Scholar 

  • King JY, Mosier AR, Morgan JA, LeCain DR, Milchunas DG, Parton WJ. 2004. Plant nitrogen dynamics in shortgrass steppe under elevated atmospheric carbon dioxide. Ecosystems 7:147–60.

    CAS  Google Scholar 

  • Lauenroth WK. 2000. Methods of estimating belowground net primary production. In: Sala OE, Jackson RB, Mooney HA, Howarth RW, Eds. Methods in ecosystem science. New York: Springer-Verlag. p 58–71.

    Google Scholar 

  • Lauenroth WK, Hunt HW, Swift DM, Singh JS. 1986. Estimating aboveground net primary production in grasslands: a simulation approach. Ecol Model 33:297–314.

    Article  Google Scholar 

  • Lauenroth WK, Milchunas DG. 1991. The shortgrass steppe. In: Coupland RT, Ed. Natural grasslands, introduction and western hemisphere. Ecosystems of the World 8A. Amsterdam: Elsevier. p 183–226.

    Google Scholar 

  • LeCain DR, Morgan JA, Milchunas DG, Mosier AR, Nelson JA, Smith DP. 2006. Root biomass of individual species, and root size characteristics after five years of CO2 enrichment on native shortgrass steppe. Plant Soil 279:219–28.

    Article  CAS  Google Scholar 

  • Leetham JW, Milchunas DG. 1985. The composition and distribution of soil microarthropods in the shortgrass steppe in relation to the soil water, root biomass, and grazing by cattle. Pedobiologia 28:311–25.

    Google Scholar 

  • Litton CM, Raich JW, Ryan MG. 2007. Carbon allocation in forest ecosystems. Global Change Biol 13:2089–109.

    Article  Google Scholar 

  • Litton CM, Giardina CP. 2008. Below-ground carbon flux and partitioning: global patterns and response to temperature. Functional Ecol 22:941–54.

    Article  Google Scholar 

  • Lund ZF, Pearson RW, Buchanan GA. 1970. An implanted soil mass technique to study herbicide effects on root growth. Weed Sci 18:279–81.

    CAS  Google Scholar 

  • Luo Y. 2003. Uncertainties in interpretation of isotope signals for estimation of fine root longevity: theoretical considerations. Global Change Biol 9:1118–29.

    Article  Google Scholar 

  • Matamala R, Gonzalez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH. 2003. Impact of fine root turnover on forest NPP and soil C sequestration potential. Science 302:1385–7.

    Article  CAS  PubMed  Google Scholar 

  • McCulley RL, Burke IC, Nelson JA, Lauenroth WK, Knapp AK, Kelly EF. 2005. Regional patterns in carbon cycling across the Great Plains of North America. Ecosystems 8:106–21.

    Article  CAS  Google Scholar 

  • McNaughton SJ, Milchunas DG, Frank DA. 1996. How can primary productivity be measured in grazing ecosystems? Ecology 77:974–7.

    Article  Google Scholar 

  • Milchunas DG, Lauenroth WK. 1992. Carbon dynamics and estimates of primary production by harvest, C14 dilution, and C14 turnover. Ecology 73:593–607.

    Article  Google Scholar 

  • Milchunas DG, Lauenroth WK. 2001. Belowground primary production by carbon isotope decay and long-term root biomass dynamics. Ecosystems 4:139–50.

    Article  CAS  Google Scholar 

  • Milchunas DG, Lauenroth WK, Singh JS, Hunt HW, Cole CV. 1985. Root turnover and production by 14C dilution: implications of carbon partitioning in plants. Plant Soil 88:353–65.

    Article  CAS  Google Scholar 

  • Milchunas DG, Mosier AR, Morgan JA, LeCain D, King JY, Nelson JA. 2005a. Root production and tissue quality in a shortgrass steppe exposed to elevated CO2: Using a new ingrowth method. Plant Soil 268:111–22.

    Article  CAS  Google Scholar 

  • Milchunas DG, Morgan JA, Mosier AR, LeCain D. 2005b. Root dynamics and demography in shortgrass steppe under elevated CO2, and comments on minirhizotron methodology. Global Change Biol 11:1837–55.

    Article  Google Scholar 

  • Morgan JA, Mosier AR, Milchunas DG, LeCain DR, Nelson JA, Parton WJ. 2004. CO2 enhances productivity but alters species composition and reduces forage quality in the Colorado shortgrass steppe. Ecol Appl 14:208–19.

    Article  Google Scholar 

  • Mosier AR, Parton WJ, Martin RE, Valentine DW, Ojima DS, Schimel DS, Burke IC. 2008. Soil-atmosphere exchange of trace gases in the Colorado Shortgrass Steppe. In: Lauenroth WK, Burke IC, Eds. Ecology of the shortgrass steppe: a long-term perspective. New York: Oxford University Press. p 342–72.

    Google Scholar 

  • Nadelhoffer KJ. 2000. The potential effects of N deposition on fine root-production in forest ecosystems. New Phytol 147:131–9.

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Aber JD, Melillo JM. 1985. Fine roots, net primary production, and soil nitrogen availability: a new hypothesis. Ecology 66:1377–90.

    Article  Google Scholar 

  • Nadelhoffer KJ, Raich JW. 1992. Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73:1139–47.

    Article  Google Scholar 

  • Nadelhoffer KJ, Raich JW, Aber JD. 1998. A global trend in belowground carbon allocation: comment. Ecology 79:1822–5.

    Google Scholar 

  • Neill C. 1992. Comparison of soil coring and ingrowth methods for measuring belowground production. Ecology 73:1918–21.

    Article  Google Scholar 

  • Norby RJ, Jackson RB. 2000. Root dynamics and global change: seeking an ecosystem perspective. New Phytol 147:3–12.

    Article  CAS  Google Scholar 

  • Pages L, Bengough AG. 1997. Modeling minirhizotron observations to test experimental procedures. Plant Soil 189:81–9.

    Article  CAS  Google Scholar 

  • Parton WJ, Schimel DS, Cole CV, Ojima DS. 1987. Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci Soc Am J 51:1173–9.

    Article  CAS  Google Scholar 

  • Parton WJ, Stewart JWB, Cole CV. 1988. Dynamics of C, N, P and S in grassland soils: a model. Biogeochemistry 5:109–31.

    Article  CAS  Google Scholar 

  • Parton WJ, Singh JS, Coleman DC. 1978. A model of production and turnover of roots in shortgrass prairie. J Appl Ecol 15:515–41.

    Article  CAS  Google Scholar 

  • Pendall E, Del Grosso S, King JY, LeCain DR, Milchunas DG, Morgan JA, Mosier AR, Ojima DS, Parton WA, Tans PP, White JWC. 2003. Elevated atmospheric CO2 effects and soil water feedbacks on soil respiration components in a Colorado grassland. Global Biogeochem Cycles 17:15-1–13.

    Google Scholar 

  • Persson HA. 1978. Root dynamics in a young Scots pine stand in central Sweden. Oikos 30:508–19.

    Article  Google Scholar 

  • Persson HA. 1979. Fine-root production, decomposition and mortality in forest ecosystems. Vegetation 41:101–9.

    Article  Google Scholar 

  • Raich JW, Nadelhoffer KJ. 1989. Belowground carbon allocation in forest ecosystems: global trends. Ecology 70:1346–54.

    Article  Google Scholar 

  • Ruess RW, Hendrick RL, Burton AJ, Pregitzer KS, Sveinbjornssön B, Allen MF, Maurer GE. 2003. Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska. Ecol Monogr 73:643–62.

    Article  Google Scholar 

  • Ruess RW, Hendrick RL, Vogel JG, Sveinbjörnsson B. 2006. The role of fine roots in the functioning of Alaskan boreal forests. In: Chapin FSIII, Oswood MW, Van Cleve K, Viereck LA, Verbyla DL, Eds. Alaska’s changing boreal forest. New York: Oxford University Press. p 189–210.

    Google Scholar 

  • Ruess RW, Van Cleve K, Yarie J, Viereck LA. 1996. Contributions of fine root production and turnover to carbon and nitrogen cycling in taiga forests of the Alaskan interior. Canadian Journal of Forest Research 26:1326–36.

    Article  CAS  Google Scholar 

  • Sala OE, Biondini ME, Lauenroth WK. 1988. Bias in estimates of primary production: an analytical solution. Ecol Model 44:43–55.

    Article  Google Scholar 

  • Schimel DS, Stillwell MA, Woodmansee RG. 1985. Biogeochemistry of C, N, and P in a soil catena of the shortgrass steppe. Ecology 66:276–82.

    Article  CAS  Google Scholar 

  • Senft RL. 1983. The redistribution of nitrogen by cattle. Ph.D. dissertation, Colorado State University, Fort Collins, 198 pp.

  • Sims PL, Singh JS. 1978. The structure and function of ten western North American grasslands. III. Net primary production, turnover and efficiency of energy capture and water use. J Ecol 66:573–97.

    Article  Google Scholar 

  • Singh JS, Lauenroth WK, Hunt HW, Swift DM. 1984. Bias and random errors in estimators of net root production: a simulation approach. Ecology 65:1760–4.

    Article  Google Scholar 

  • Steele SJ, Gower ST, Vogel JG, Norman JM. 1997. Root mass, net primary production and turnover in aspen, jack pine and black spruce forests in Saskatchewan and Manitoba, Canada. Tree Physiol 17:577–87.

    CAS  PubMed  Google Scholar 

  • Steen E. 1983. Usefulness of the mesh bag method in quantitative root studies. In: Atkinson D, Ed. Plant root growth, an ecological perspective Brit Ecol Soc Special Publ No 10. London: Blackwell Scientific Publications. p 75–86.

    Google Scholar 

  • Steen E. 1991. Variation of root growth in a grass ley studied with a mesh bag technique. Swedish J Agric Res 14:93–7.

    Google Scholar 

  • Steingrobe B, Schmid H, Claassen N. 2000. The use of the ingrowth core method for measuring root production of arable crops B influence of soil conditions inside the ingrowth core on root growth. J Plant Nutr Soil Sci 163:612–22.

    Google Scholar 

  • Steingrobe B, Schmid H, Claassen N. 2001. The use of the ingrowth core method for measuring root production of arable crops B influence of soil and root disturbance during installation of the bags on root ingrowth into the cores. Eur J Agron 15:143–51.

    Article  Google Scholar 

  • Swinnen J, Van Veen JA, Merckx R. 1994a. Losses of 14C from roots of pulse-labeled wheat and barley during washing from soil. Plant Soil 166:93–9.

    Article  CAS  Google Scholar 

  • Swinnen J, Van Veen JA, Merckx R. 1994b. 14C pulse-labeling of field-grown spring wheat: an evaluation of its use in rhizosphere carbon budget estimations. Soil Biol Biochem 26:161–70.

    Article  Google Scholar 

  • Swinnen J, Van Veen JA, Merckx R. 1994c. Rhizosphere carbon fluxes in field-grown spring wheat: model calculations based on 14C partitioning after pulse-labeling. Soil Biol Biochem 26:171–82.

    Article  Google Scholar 

  • Swinnen J, Van Veen JA, Merckx R. 1995. Root decay and turnover of rhizodeposits in field-grown winter wheat and spring barley estimated by 14C pulse labeling. Soil Biol Biochem 27:211–17.

    Article  CAS  Google Scholar 

  • Tierney GL, Fahey TJ. 2001. Evaluating minirhizotron estimates of fine root longevity and production in the forest floor of a temperate broadleaf forest. Plant Soil 229:167–76.

    Article  CAS  Google Scholar 

  • Tierney GL, Fahey TJ. 2002. Fine root turnover in a northern hardwood forest: a direct comparison of the radiocarbon and minirhizotron methods. Can J For Res 32:1692–7.

    Article  Google Scholar 

  • Trumbore SE, Gaudinski JB. 2003. The secret lives of roots. Science 302:1344–5.

    Article  CAS  PubMed  Google Scholar 

  • Vogt KA, Vogt DJ, Bloomfield J. 1998. Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level. Plant Soil 200:71–89.

    Article  CAS  Google Scholar 

  • Weaver JE. 1958. Classification of root systems of forbs of grassland and a comparison of their significance. Ecology 39:393–401.

    Article  Google Scholar 

  • Withington JM, Elkin AD, Bułlaj B, Olesińnski J, Tracy KN, Bouma TJ, Oleksyn J, Anderson LJ, Modrzyńnski J, Reich PB, Eissenstat DM. 2003. The impact of material used for minirhizotron tubes for root research. New Phytol 160:533–44.

    Article  Google Scholar 

Download references

Acknowledgments

Funding during various periods of this work was provided by the Shortgrass Steppe LTER (NSF DEB-0217631, 0823405), The Terrestrial Ecology and Climate Change Initiative, NSF IBN-9524068 and USDA NRICGP-98-134, NSF DEB-9708596, and the USDA, Agricultural Research Service, Soil-Plant-Nutrient Research Unit and Rangeland Resources Research Unit, Fort Collins, CO. I thank the LTER and ARS field crews for the intensive amount of work involved in root studies, and Judy Hendryx for sample prep work in the lab. Roger Ruess and an anonymous reviewer provided many useful technical additions, as well as suggestions that helped make the complex nature of the presentation more readable.

Author information

Authors and Affiliations

  1. Forest, Rangeland, and Watershed Stewardship Department, Colorado State University, Ft. Collins, Colorado, 80523, USA

    Daniel G. Milchunas

Authors
  1. Daniel G. Milchunas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel G. Milchunas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Milchunas, D.G. Estimating Root Production: Comparison of 11 Methods in Shortgrass Steppe and Review of Biases. Ecosystems 12, 1381–1402 (2009). https://doi.org/10.1007/s10021-009-9295-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-009-9295-8

Keywords

Search

Navigation