Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Root growth and N dynamics in response to multi-year experimental warming, summer drought and elevated CO2 in a mixed heathland-grass ecosystem

M. F. Arndal A E , I. K. Schmidt A , J. Kongstad A , C. Beier B D and A. Michelsen C
+ Author Affiliations
- Author Affiliations

A Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, DK-1958 Frederiksberg C, Denmark.

B Department of Chemical and Biochemical Engineering, Technical University of Denmark, DTU, DK-2800 Kongens Lyngby, Denmark.

C Department of Biology, Terrestrial Ecology Section, Universitetsparken 15, University of Copenhagen, DK-2100 København Ø, Denmark.

D Present address: NIVA , Gaustadalléen 21,0349 Oslo, Norway.

E Corresponding author. Email: mfa@life.ku.dk

Functional Plant Biology 41(1) 1-10 https://doi.org/10.1071/FP13117
Submitted: 24 April 2013  Accepted: 18 July 2013   Published: 4 September 2013

Abstract

Ecosystems exposed to elevated CO2 are often found to sequester more atmospheric carbon due to increased plant growth. We exposed a Danish heath ecosystem to elevated CO2, elevated temperature and extended summer drought alone and in all combinations in order to study whether the expected increased growth would be matched by an increase in root nutrient uptake of NH4+-N and NO3 -N. Root growth was significantly increased by elevated CO2. The roots, however, did not fully compensate for the higher growth with a similar increase in nitrogen uptake per unit of root mass. Hence the nitrogen concentration in roots was decreased in elevated CO2, whereas the biomass N pool was unchanged or even increased. The higher net root production in elevated CO2 might be a strategy for the plants to cope with increased nutrient demand leading to a long-term increase in N uptake on a whole-plant basis. Drought reduced grass root biomass and N uptake, especially when combined with warming, but CO2 was the most pronounced main factor effect. Several significant interactions of the treatments were found, which indicates that the responses were nonadditive and that changes to multiple environmental changes cannot be predicted from single-factor responses alone.

Additional keywords: Calluna vulgaris, CLIMAITE, Deschampsia flexuosa, excised roots, ingrowth core, 15N-assay.


References

Albert KR, Ro-Poulsen H, Mikkelsen TN, Michelsen A, Van Der Linden L, Beier C (2011a) Effects of elevated CO2, warming and drought episodes on plant carbon uptake in a temperate heath ecosystem are controlled by soil water status. Plant, Cell & Environment 34, 1207–1222.
Effects of elevated CO2, warming and drought episodes on plant carbon uptake in a temperate heath ecosystem are controlled by soil water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsVKhtbg%3D&md5=7de76ee0dd0b3cc6823dd9c5b5f535efCAS |

Albert KR, Ro-Poulsen H, Mikkelsen TN, Michelsen A, Van Der Linden L, Beier C (2011b) Interactive effects of elevated CO2, warming, and drought on photosynthesis of Deschampsia flexuosa in a temperate heath ecosystem. Journal of Experimental Botany 62, 4253–4266.
Interactive effects of elevated CO2, warming, and drought on photosynthesis of Deschampsia flexuosa in a temperate heath ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVeit7jL&md5=7e3d6461615799be813ba953c2897c6eCAS | 21586430PubMed |

Andresen LC, Michelsen A, Jonasson S, Beier C, Ambus P (2009) Glycine uptake in heath plants and soil microbes responds to elevated temperature, CO2 and drought. Acta Oecologica 35, 786–796.
Glycine uptake in heath plants and soil microbes responds to elevated temperature, CO2 and drought.Crossref | GoogleScholarGoogle Scholar |

Andresen LC, Michelsen A, Jonasson S, Schmidt IK, Mikkelsen TN, Ambus P, Beier C (2010a) Plant nutrient mobilization in temperate heathland responds to elevated CO2, temperature and drought. Plant and Soil 328, 381–396.
Plant nutrient mobilization in temperate heathland responds to elevated CO2, temperature and drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1Wqs7k%3D&md5=db8b2dedd9146bb57d39e73fde9ed2efCAS |

Andresen L, Michelsen A, Ambus P, Beier C (2010b) Belowground heathland responses after 2 years of combined warming, elevated CO2 and summer drought. Biogeochemistry 101, 27–42.
Belowground heathland responses after 2 years of combined warming, elevated CO2 and summer drought.Crossref | GoogleScholarGoogle Scholar |

Andresen LC, Michelsen A, Jonasson S, Strom L (2011) Seasonal changes in nitrogen availability, and root and microbial uptake of 15N13C-phenylalanine and 15N-ammonium in situ at a temperate heath. Applied Soil Ecology 51, 94–101.
Seasonal changes in nitrogen availability, and root and microbial uptake of 15N13C-phenylalanine and 15N-ammonium in situ at a temperate heath.Crossref | GoogleScholarGoogle Scholar |

Arnone JA, Zaller JG, Spehn EM, Niklaus PA, Wells CE, Korner C (2000) Dymamics of root systems in native grasslands, effects of elevated atmospheric CO2. New Phytologist 147, 73–85.
Dymamics of root systems in native grasslands, effects of elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1ylt7g%3D&md5=22b6639288f6867534e8b9bec5743ba5CAS |

Barnard R, Barthes L, Leadley PW (2006) Short-term uptake of N15 by a grass and soil micro-organisms after long-term exposure to elevated CO2. Plant and Soil 280, 91–99.
Short-term uptake of N15 by a grass and soil micro-organisms after long-term exposure to elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslOrs78%3D&md5=6c29133c0810490bac9f4da7a9c2d586CAS |

Bassirirad H (2000) Kinetics of nutrient uptake by roots: responses to global change. New Phytologist 147, 155–169.
Kinetics of nutrient uptake by roots: responses to global change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1yltL8%3D&md5=9d898896002c8ccb0376bf95e5e8ad24CAS |

Bassirirad H, Reynolds JF, Virginia RA, Brunelle MH (1997) Growth and root NO3– and PO4 3– uptake capacity of three desert species in response to atmospheric CO2 enrichment. Australian Journal of Plant Physiology 24, 353–358.
Growth and root NO3– and PO4 3– uptake capacity of three desert species in response to atmospheric CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |

Bassirirad H, Prior SA, Norby RJ, Rogers HH (1999) A field method of determining NH4+ and NO3– uptake kinetics in intact roots: Effects of CO2 enrichment on trees and crop species. Plant and Soil 217, 195–204.
A field method of determining NH4+ and NO3– uptake kinetics in intact roots: Effects of CO2 enrichment on trees and crop species.Crossref | GoogleScholarGoogle Scholar |

Bielenberg DG, Bassirirad H (2005) Nutrient acquisition of terrestrial plants in a changing climate. In ‘Nutrient acquisition by plants. An ecological perspective. Vol. 181’. (Ed. H Bassirirad H) pp. 311–330. (Springer-Verlag, Berlin)

Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4, 43–54.
Elevated CO2 reduces the nitrogen concentration of plant tissues.Crossref | GoogleScholarGoogle Scholar |

de Graaf MCC, Bobbink R, Roelofs JGM, Verbeek PJM (1998) Differential effects of ammonium and nitrate on 3 heathland species. Plant Ecology 135, 185–196.
Differential effects of ammonium and nitrate on 3 heathland species.Crossref | GoogleScholarGoogle Scholar |

Dijkstra FA, Blumenthal D, Morgan JA, LeCain DR, Follett RF (2010) Elevated CO2 effects on semi-arid grassland plants in relation to water availability and competition. Functional Ecology 24, 1152–1161.
Elevated CO2 effects on semi-arid grassland plants in relation to water availability and competition.Crossref | GoogleScholarGoogle Scholar |

Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Advances in Ecological Research 27, 1–60.
The ecology of root lifespan.Crossref | GoogleScholarGoogle Scholar |

Falkengren-Grerup U, Schöttelndreier M (2004) Vascular plants as indicators of nitrogen enrichment in soil. Plant Ecology 172, 51–62.
Vascular plants as indicators of nitrogen enrichment in soil.Crossref | GoogleScholarGoogle Scholar |

Franck VM, Hungate BA, Chapin FS, Field CB (1997) Decomposition of litter produced under elevated CO2: dependence on plant species and nutrient supply. Biogeochemistry 36, 223–237.
Decomposition of litter produced under elevated CO2: dependence on plant species and nutrient supply.Crossref | GoogleScholarGoogle Scholar |

Gavito ME, Curtis PS, Mikkelsen TN, Jakobsen I (2001) Interactive effects of soil temperature, atmospheric carbon dioxide and soil N on root development, biomass and nutrient uptake of winter wheat during vegetative growth. Journal of Experimental Botany 52, 1913–1923.
Interactive effects of soil temperature, atmospheric carbon dioxide and soil N on root development, biomass and nutrient uptake of winter wheat during vegetative growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXms12ksbo%3D&md5=b983cb686b1d989ac864f1a4d37cbae3CAS | 11520880PubMed |

Gessler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H (1998) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytologist 138, 275–285.
Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlOlsrw%3D&md5=fa303d409e74e9873b8403d5e63c01cbCAS |

Gill RA, Anderson LJ, Polley HW, Johnson HB, Jackson RB (2006) Potential nitrogen constraints on soil carbon sequestration under low and elevated atmospheric CO2. Ecology 87, 41–52.
Potential nitrogen constraints on soil carbon sequestration under low and elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 16634295PubMed |

Glass AD (2005) Homeostatic processes for the optimization of nutrient absorption: physiology and molecular biology. In ‘Nutrient acquisition by plants. An ecological perspective. Vol. 181’. (Ed. H Bassirirad) pp. 117–146. (Springer-Verlag, Berlin)

Göransson H, Wallander H, Ingerslev M, Rosengren U (2006) Estimating the relative nutrient uptake from different soil depths in Quercus robur, Fagus sylvatica and Picea abies. Plant and Soil 286, 87–97.
Estimating the relative nutrient uptake from different soil depths in Quercus robur, Fagus sylvatica and Picea abies.Crossref | GoogleScholarGoogle Scholar |

Göransson H, Fransson AM, Jonsson-Belyazid U (2007) Do oaks have different strategies for uptake of N, K and P depending on soil depth? Plant and Soil 297, 119–125.
Do oaks have different strategies for uptake of N, K and P depending on soil depth?Crossref | GoogleScholarGoogle Scholar |

Gorissen A, Cotrufo MF (2000) Decomposition of leaf and root tissue of three perennial grass species grown at two levels of atmospheric CO2 and N supply. Plant and Soil 224, 75–84.
Decomposition of leaf and root tissue of three perennial grass species grown at two levels of atmospheric CO2 and N supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVejsbk%3D&md5=1a732ebd4465e4712528bc503bd60198CAS |

Gutschick VP, Pushnik JC (2005) Internal regulation of nutrient uptake by relative growth rate and nutrient-use efficiency. In ‘Nutrient acquisition by plants. An ecological perspective. Vol. 181. (Ed. H Bassirirad) pp. 63–88. (Springer-Verlag, Berlin)

Jackson RB, Reynolds HL (1996) Nitrate and ammonium uptake for single- and mixed-species communities grown at elevated CO2. Oecologia 105, 74–80.
Nitrate and ammonium uptake for single- and mixed-species communities grown at elevated CO2.Crossref | GoogleScholarGoogle Scholar |

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.
A global budget for fine root biomass, surface area, and nutrient contents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksFOmtL4%3D&md5=208b2ce3d1222830d1670a255106e8d9CAS | 11038557PubMed |

Jin VL, Evans RD (2007) Elevated CO2 increases microbial carbon substrate use and nitrogen cycling in Mojave Desert soils. Global Change Biology 13, 452–465.
Elevated CO2 increases microbial carbon substrate use and nitrogen cycling in Mojave Desert soils.Crossref | GoogleScholarGoogle Scholar |

Jones HE, Quarmby C, Harrison AF (1991) A root bioassay test for nitrogen deficiency in forest trees. Forest Ecology and Management 42, 267–282.
A root bioassay test for nitrogen deficiency in forest trees.Crossref | GoogleScholarGoogle Scholar |

Kongstad J, Schmidt IK, Riis-Nielsen T, Beier C, Arndal MF, Mikkelsen TN (2012) High resilience in heathland plants to changes in temperature, drought and CO2 in combination: results from the CLIMAITE experiment. Ecosystems 15, 269–283.
High resilience in heathland plants to changes in temperature, drought and CO2 in combination: results from the CLIMAITE experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtFOhsb8%3D&md5=9ba0a50a96b1fea4cf8e310a3e503050CAS |

Larsen KS, Andresen LC, Beier C, Jonasson S, Albert KR, Ambus P, Arndal MF, Carter MS, Christensen S, Holmstrup M, Ibrom A, Kongstad J, Van Der Linden L, Maraldo K, Michelsen A, Mikkelsen TN, Pilegaard K, Prieme A, Ro-Poulsen H, Schmidt IK, Selsted MB, Stevnbak K (2011) Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Global Change Biology 17, 1884–1899.
Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments.Crossref | GoogleScholarGoogle Scholar |

Luo Y, Su B, Currie WS, Dukes JS, Finzi AC, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54, 731–739.
Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide.Crossref | GoogleScholarGoogle Scholar |

Marschner H (1995) ‘Marschner’s mineral nutrition of higher plants.’ 2nd edn. (Academic Press, London)

Michelsen A, Graglia E, Schmidt IK, Jonasson S, Sleep D, Quarmby C (1999) Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath. New Phytologist 143, 523–538.
Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath.Crossref | GoogleScholarGoogle Scholar |

Mikkelsen TN, Beier C, Jonasson S, Holmstrup M, Schmidt IK, Ambus P, Pilegaard K, Michelsen A, Albert K, Andresen LC, Arndal MF, Bruun N, Christensen S, Danbaek S, Gundersen P, Jorgensen P, Linden LG, Kongstad J, Maraldo K, Prieme A, Riis-Nielsen T, Ro-Poulsen H, Stevnbak K, Selsted MB, Sorensen P, Larsen KS, Carter MS, Ibrom A, Martinussen T, Miglietta F, Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2, warming and drought: the CLIMAITE project. Functional Ecology 22, 185–195.

Mokany K, Raison RJ, Prokushkin AS (2006) Critical analysis of root : shoot ratios in terrestrial biomes. Global Change Biology 12, 84–96.
Critical analysis of root : shoot ratios in terrestrial biomes.Crossref | GoogleScholarGoogle Scholar |

Newbery RM, Wolfenden J, Mansfield TA, Harrison AF (1995) Nitrogen, phosphorus and potassium uptake and demand in Agrostis capillaris – the influence of elevated CO2 and nutrient supply. New Phytologist 130, 565–574.
Nitrogen, phosphorus and potassium uptake and demand in Agrostis capillaris – the influence of elevated CO2 and nutrient supply.Crossref | GoogleScholarGoogle Scholar |

Nielsen PL, Andresen LC, Michelsen A, Schmidt IK, Kongstad J (2009) Seasonal variations and effects of nutrient applications on N and P and microbial biomass under two temperate heathland plants. Applied Soil Ecology 42, 279–287.
Seasonal variations and effects of nutrient applications on N and P and microbial biomass under two temperate heathland plants.Crossref | GoogleScholarGoogle Scholar |

Norby RJ, Iversen CM (2006) Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87, 5–14.
Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest.Crossref | GoogleScholarGoogle Scholar | 16634292PubMed |

Phillips DL, Johnson MG, Tingey DT, Catricala CE, Hoyman TL, Nowak RS (2006) Effects of elevated CO2 on fine root dynamics in a Mojave Desert community: a FACE study. Global Change Biology 12, 61–73.
Effects of elevated CO2 on fine root dynamics in a Mojave Desert community: a FACE study.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Australian Journal of Plant Physiology 27, 595–607.
The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslars7w%3D&md5=a3d2f27999e5246c93b798e253182489CAS |

Pregitzer KS, King JS (2005) Effects of soil temperature on nutrient uptake. In ‘Nutrient acquisition by plants. An ecological perspective. Vol. 181’. (Ed. H Bassirirad) pp. 277–310. (Springer-Verlag, Berlin)

Rogers HH, Runion GB, Krupa SV (1994) Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environmental Pollution 83, 155–189.
Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7psFOlsw%3D%3D&md5=ff859787d9e8f7b36d9c23f08116704aCAS | 15091762PubMed |

Rosengren U, Sleep D, Jones HE, Thelin G (2003) Increasing the sensitivity of the 15N root bioassay technique: suggested procedures. Communications in Soil Science and Plant Analysis 34, 2363–2373.
Increasing the sensitivity of the 15N root bioassay technique: suggested procedures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVKgsbw%3D&md5=9c6befa010f238615865ed1317875791CAS |

Sindhøj E, Andrén O, Kätterer T, Marissink M, Pettersson R (2004) Root biomass dynamics in a semi-natural grassland exposed to elevated atmospheric CO2 for five years. Acta Agriculturae Scandinavica, Section B – Soil & Plant Science 54, 50–59.
Root biomass dynamics in a semi-natural grassland exposed to elevated atmospheric CO2 for five years.Crossref | GoogleScholarGoogle Scholar |

Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (Eds) (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, 2007. (Cambridge University Press: Cambridge, UK and New York)

Taub DR, Wang XZ (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. Journal of Integrative Plant Biology 50, 1365–1374.
Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyltb7M&md5=bf9571602e061c14e68c915828f22544CAS | 19017124PubMed |

Volder A, Anderson LJ, Smart DR, Bloom AJ, Lakso AN, Eissenstat DM (2009) Estimating nitrogen uptake of individual roots in container- and field-grown plants using a 15N-depletion approach. Functional Plant Biology 36, 621–628.
Estimating nitrogen uptake of individual roots in container- and field-grown plants using a 15N-depletion approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVegu74%3D&md5=e8092c67073e9c6b63ee51f09903b416CAS |