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

Effects of nutrient supply on carbon and water economies of C4 grasses

Laura Rose A B F , Robert Buitenwerf B C , Michael Cramer D , Edmund C. February D and Steven I. Higgins B E
+ Author Affiliations
- Author Affiliations

A University of Freiburg, Faculty of Biology, Geobotany, Schaenzlestr. 1, 79104 Freiburg, Germany.

B University of Frankfurt, Institute of Physical Geography, Altenhoeferallee 1, 60438 Frankfurt, Germany.

C Aarhus University, Ecoinformatics and Biodiversity, Department of Bioscience, Ny Munkegade 114-116, Aarhus 8000 C, Denmark.

D Department of Biological Sciences, University of Cape Town, Private Bag X2, Rondebosch 7701, South Africa.

E Universität Bayreuth, Lehrstuhl für Pflanzenökologie, 95440 Bayreuth, Germany.

F Corresponding author. Email: laura.rose@biologie.uni-freiburg.de

Functional Plant Biology 45(9) 935-944 https://doi.org/10.1071/FP17359
Submitted: 11 June 2017  Accepted: 7 March 2018   Published: 19 April 2018

Abstract

C3 plants can increase nutrient uptake by increasing transpiration, which promotes the flow of water with dissolved nutrients towards the roots. However, it is not clear if this mechanism of nutrient acquisition, termed ‘mass flow’, also operates in C4 plants. This is an important question, as differences in mass flow capacity may affect competitive interactions between C3 and C4 species. To test if mass flow can be induced in C4 species, we conducted an experiment in a semiarid seasonal savanna in South Africa. We grew six C4 grasses in nutrient-poor sand and supplied no nutrients, nutrients to the roots or nutrients spatially separated from the roots. We measured the rates of photosynthesis and transpiration, water-use efficiency (WUE), nitrogen gain and biomass. For all species biomass, N gain, photosynthesis and transpiration were lowest in the treatment without any nutrient additions. Responses to different nutrient positioning varied among species from no effect on N gain to a 50% reduction when nutrients were spatially separated. The ability to access spatially separated nutrients showed a nonsignificant positive relationship with both the response of transpiration and the response of WUE to spatial nutrient separation. This indicates that nutrient acquisition is not regulated by decreasing WUE in C4 grasses. Overall, our study suggests that under elevated CO2, when evaporative demand is lower, C4 species may be at a competitive disadvantage to C3 species when it comes to nutrient acquisition.

Additional keywords: carbon dioxide, mass-flow, nitrogen, nutrient uptake, stomatal conductance, water-use efficiency.


References

Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant, Cell & Environment 30, 258–270.
The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlemu78%3D&md5=05630ffbb5d61ea4dda2bd5dab16a7c8CAS |

Allen LH, Kakani VG, Vu JCV, Boote KJ (2011) Elevated CO2 increases water use efficiency by sustaining photosynthesis of water-limited maize and sorghum. Journal of Plant Physiology 168, 1909–1918.
Elevated CO2 increases water use efficiency by sustaining photosynthesis of water-limited maize and sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFyns73E&md5=06356d8ab23eceffd3888f3f100126ddCAS |

Barber SA (1962) A diffusion and mass-flow concept of soil nutrient availability. Soil Science 93, 39–49.
A diffusion and mass-flow concept of soil nutrient availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXkslOktbY%3D&md5=be50a33f998126302e6ca42dfa4b73efCAS |

Barber SA (1995) ‘Soil nutrient bioavailability: a mechanistic approach.’ (Wiley: New York)

Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Bellasio C, Lundgren MR (2016) Anatomical constraints to C4 evolution: light harvesting capacity in the bundle sheath. New Phytologist 212, 485–496.
Anatomical constraints to C4 evolution: light harvesting capacity in the bundle sheath.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFWmurjJ&md5=f3f9abe250773fd5c9555531eba85a40CAS |

Bond WJ, Midgley GF (2012) Carbon dioxide and the uneasy interactions of trees and savannah grasses. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 601–612.
Carbon dioxide and the uneasy interactions of trees and savannah grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltV2rtbc%3D&md5=93fefb5268f0acac2a5001e26df863e4CAS |

Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=5ffc3e4d6e0895d012d3d57c68f91f46CAS |

Brueck H, Senbayram M (2009) Low nitrogen supply decreases water-use efficiency of oriental tobacco. Journal of Plant Nutrition and Soil Science 172, 216–223.
Low nitrogen supply decreases water-use efficiency of oriental tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlt1yhtL8%3D&md5=4bcb3f9213476c2383b5acf34a3cec53CAS |

Buitenwerf R, Bond WJ, Stevens N, Trollope WSW (2012) Increased tree densities in South African savannas: >50 years of data suggests CO2 as a driver. Global Change Biology 18, 675–684.
Increased tree densities in South African savannas: >50 years of data suggests CO2 as a driver.Crossref | GoogleScholarGoogle Scholar |

Cernusak LA, Winter K, Turner BL (2011) Transpiration modulates phosphorus acquisition in tropical tree seedlings. Tree Physiology 31, 878–885.
Transpiration modulates phosphorus acquisition in tropical tree seedlings.Crossref | GoogleScholarGoogle Scholar |

Christin PA, Osborne CP (2014) The evolutionary ecology of C4 plants. New Phytologist 204, 765–781.
The evolutionary ecology of C4 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVOgurnK&md5=0763fbe941cf2ccc50c44bba02273633CAS |

Collatz GJ, Berry JA, Clark JS (1998) Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past, and future. Oecologia 114, 441–454.
Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past, and future.Crossref | GoogleScholarGoogle Scholar |

Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment: stomatal function in the regulation of gas exchange. Symposia of the Society for Experimental Biology 31, 471–505.

Cramer MD, Hoffmann V, Verboom GA (2008) Nutrient availability moderates transpiration in Ehrharta calycina. New Phytologist 179, 1048–1057.
Nutrient availability moderates transpiration in Ehrharta calycina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur3N&md5=60a4694ea2cd0c125ae197dc75efe15aCAS |

Cramer MD, Hawkins HJ, Verboom GA (2009) The importance of nutritional regulation of plant water flux. Oecologia 161, 15–24.
The importance of nutritional regulation of plant water flux.Crossref | GoogleScholarGoogle Scholar |

Deryng D, Elliott J, Folberth C, Müller C, Pugh TAM, Boote KJ, Conway D, Ruane AC, Gerten D, Jones JW, Khabarov N, Olin S, Schaphoff S, Schmid E, Yang H, Rosenzweig C (2016) Regional disparities in the beneficial effects of rising CO2 concentrations on crop water productivity. Nature Climate Change 6, 786–790.
Regional disparities in the beneficial effects of rising CO2 concentrations on crop water productivity.Crossref | GoogleScholarGoogle Scholar |

Dow GJ, Bergmann DC, Berry JA (2014) An integrated model of stomatal development and leaf physiology. New Phytologist 201, 1218–1226.
An integrated model of stomatal development and leaf physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVehu74%3D&md5=32bf95b65015f4245c03957694258115CAS |

Ehleringer JR (1978) Implications of quantum yield differences on the distributions of C3 and C4 grasses. Oecologia 31, 255–267.
Implications of quantum yield differences on the distributions of C3 and C4 grasses.Crossref | GoogleScholarGoogle Scholar |

Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285–299.
C4 photosynthesis, atmospheric CO2, and climate.Crossref | GoogleScholarGoogle Scholar |

Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 33, 317–345.
Stomatal conductance and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=7896d0b46634bc74b52a111a48deabbeCAS |

Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106, 10343–10347.
Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1Giurg%3D&md5=cc06171f17d740d9699808aa6e0e1111CAS |

Garrish V, Cernusak LA, Winter K, Turner BL (2010) Nitrogen to phosphorus ratio of plant biomass versus soil solution in a tropical pioneer tree, Ficus insipida. Journal of Experimental Botany 61, 3735–3748.
Nitrogen to phosphorus ratio of plant biomass versus soil solution in a tropical pioneer tree, Ficus insipida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7jL&md5=b3a1734dce7348ce0b643d3b75b52a73CAS |

Higgins SI, Scheiter S (2012) Atmospheric CO2 forces abrupt vegetation shifts locally, but not globally. Nature 488, 209–212.
Atmospheric CO2 forces abrupt vegetation shifts locally, but not globally.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWjtLrJ&md5=d2fc1b4b78e05d9e76bb562ce667fb8eCAS |

Lambers H, Chapin FS, III, Pons TL (2008) ‘Plant physiological ecology.’ (Springer: New York)

Lenth RV (2016) Least-squares means: the R package lsmeans. Journal of Statistical Software 69, 1–33.
Least-squares means: the R package lsmeans.Crossref | GoogleScholarGoogle Scholar |

Liu H, Osborne CP (2015) Water relations traits of C4 grasses depend on phylogenetic lineage, photosynthetic pathway, and habitat water availability. Journal of Experimental Botany 66, 761–773.
Water relations traits of C4 grasses depend on phylogenetic lineage, photosynthetic pathway, and habitat water availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGisLjI&md5=574ee04a4e2e3dea8d9580da27e766d1CAS |

Morgan JA, Pataki DE, Körner C, Clark H, Del Grosso SJ, Grünzweig JM, Knapp AK, Mosier AR, Newton PCD, Niklaus PA, Nippert JB, Nowak RS, Parton WJ, Polley HW, Shaw MR (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140, 11–25.
Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3oslKksQ%3D%3D&md5=6e7074c0f4330d3d78104890c00dbbddCAS |

Osborne CP Freckleton RP 2009 Ecological selection pressures for C4 photosynthesis in the grasses. Proceedings of the Royal Society B-Biological Sciences 276 1753 1760 10.1098/rspb.2008.1762

Pau S, Edwards EJ, Still CJ (2013) Improving our understanding of environmental controls on the distribution of C3 and C4 grasses. Global Change Biology 19, 184–196.
Improving our understanding of environmental controls on the distribution of C3 and C4 grasses.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2015) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 15 March 2018].

Raven JA (2008) Transpiration: how many functions? New Phytologist 179, 905–907.
Transpiration: how many functions?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FP&md5=972391a8aac62dd7041e065dd4b13a07CAS |

Rose L, Coners H, Leuschner C (2012) Effects of fertilization and cutting frequency on the water balance of a temperate grassland. Ecohydrology 5, 64–72.
Effects of fertilization and cutting frequency on the water balance of a temperate grassland.Crossref | GoogleScholarGoogle Scholar |

Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341–370.
The evolution of C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVymuro%3D&md5=41994fe9b2d313e79a8dd5e786dd9b2fCAS |

Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011) Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156, 832–843.
Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrk%3D&md5=5dcddd5fbf8cc5d0d1fb3cbee102302eCAS |

Sinninghe Damsté JS, Verschuren D, Ossebaar J, Blokker J, van Houten R, van der Meer MTJ, Plessen B, Schouten S (2011) A 25,000-year record of climate-induced changes in lowland vegetation of eastern equatorial Africa revealed by the stable carbon-isotopic composition of fossil plant leaf waxes. Earth and Planetary Science Letters 302, 236–246.
A 25,000-year record of climate-induced changes in lowland vegetation of eastern equatorial Africa revealed by the stable carbon-isotopic composition of fossil plant leaf waxes.Crossref | GoogleScholarGoogle Scholar |

Spriggs EL, Christin PA, Edwards EJ (2014) C4 photosynthesis promoted species diversification during the Miocene grassland expansion. PLoS One 9, e97722
C4 photosynthesis promoted species diversification during the Miocene grassland expansion.Crossref | GoogleScholarGoogle Scholar |

Strebel O, Duynisveld WHM (1989) Nitrogen supply to cereals and sugar beet by mass flow and diffusion on a silty loam soil. Zeitschrift für Pflanzenernährung und Bodenkunde 152, 135–141.
Nitrogen supply to cereals and sugar beet by mass flow and diffusion on a silty loam soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFKitLg%3D&md5=6c21442f447b482f28a1e0df79652feeCAS |

Taylor SH, Hulme SP, Rees M, Ripley BS, Woodward FI, Osborne CP (2010) Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment. New Phytologist 185, 780–791.
Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFKns7s%3D&md5=13394ca7bdab8a09710bb08838fe7a48CAS |

Wang G, Feng X (2012) Response of plants water use efficiency to increasing atmospheric CO2 concentration. Environmental Science & Technology 46, 8610–8620.
Response of plants water use efficiency to increasing atmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVGrs7k%3D&md5=1c2aeaa2528329bbbe3748d09184b4f3CAS |

Way DA, Katul GG, Manzoni S, Vico G (2014) Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective. Journal of Experimental Botany 65, 3683–3693.
Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective.Crossref | GoogleScholarGoogle Scholar |

Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends in Ecology & Evolution 21, 261–268.
Land-plant ecology on the basis of functional traits.Crossref | GoogleScholarGoogle Scholar |

Wilkinson S, Bacon MA, Davies WJ (2007) Nitrate signalling to stomata and growing leaves: interactions with soil drying, ABA, and xylem sap pH in maize. Journal of Experimental Botany 58, 1705–1716.
Nitrate signalling to stomata and growing leaves: interactions with soil drying, ABA, and xylem sap pH in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeisrs%3D&md5=4fca8fa64a45bbf958562cedf40e5895CAS |

Wong SC (1979) Stomatal behaviour in relation to photosynthesis. PhD thesis. The Australian National University, Canberra.

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M, et al (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=f752755637bf822e879e8c9d3c0bbf3cCAS |

Yanai J, Robinson D, Young IM, Kyuma K, Kosaki T (1998) Effects of the chemical form of inorganic nitrogen fertilizers on the dynamics of the soil solution composition and on nutrient uptake by wheat. Plant and Soil 202, 263–270.
Effects of the chemical form of inorganic nitrogen fertilizers on the dynamics of the soil solution composition and on nutrient uptake by wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsVygt7k%3D&md5=f37c4eedd316ccbf2f059b7b9f268414CAS |