Abstract
Longleaf pine savannas house a diverse community of herbaceous N2-fixing legume species that have the potential to replenish nitrogen (N) losses from fire. Whether legumes fill this role depends on the factors that regulate symbiotic fixation, including soil nutrients such as phosphorus (P) and molybdenum (Mo) and the growth and fixation strategies of different species. In greenhouse experiments, we determined how these factors influence fixation for seven species of legumes grown in pure field soil from two different regions of the southeastern US longleaf pine ecosystem. We first added P and Mo individually and in combination, and found that P alone constrained fixation. Phosphorus primarily influenced fixation by regulating legume growth. Second, we added N to plants and found that species either downregulated fixation (facultative strategy) or maintained fixation at a constant rate (obligate strategy). Species varied nearly fourfold in fixation rate, reflecting differences in growth rate, taxonomy and fixation strategy. However, fixation responded strongly to P addition across all species in our study, suggesting that the P cycle regulates N inputs by herbaceous legumes.
Similar content being viewed by others
References
Alberty RA (2005) Thermodynamics of the mechanism of the nitrogenase reaction. Biophys Chem 114:115–120. https://doi.org/10.1016/j.bpc.2004.11.009
Antonovics J (1980) Concepts of resource allocation and partitioning in plants. In: Staddon JER (ed) Limits to action: the allocation of individual behavior. Acadmic Press, New York
Augusto L, Delerue F, Gallet-Budynek A, Achat DL (2013) Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Glob Biogeochem Cycles 27:804–815. https://doi.org/10.1002/gbc.20069
Batterman SA, Wurzburger N, Hedin LO (2013) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101:1400–1408. https://doi.org/10.1111/1365-2745.12138
Becking JH (1961) A requirement of molybdenum for the symbiotic nitrogen fixation in alder (Alnus glutinosa Gaertn.). Plant Soil 15:217–227
Bindu J, Ramabhadran A (2010) Effect of concentration of dispersing agent on the grain size distribution of fine grained soil. In: Annu Conf Indian Geotech Soc Mumbai
Boring, LR, Hendricks JJ, Wilson CA, Mitchell RJ (2004) Season of burn and nutrient losses in a longleaf pine ecosystem. Int J Wildland Fire 13:443–453
Boring L, Hendricks J, Taylor R, Markewitz D (2017) Ecosystem processes and restoration. In: Kirkman L, Jack S (eds) Ecological restoration and management of longleaf pine forests. CRC Press, Boca Raton, pp 123–139
Brkic S, Milakovic Z, Kriestek A, Antunovic M (2004) Pea yield and its quality depending on inoculation, nitrogen and molybdenum fertilization. Plant Soil Environ 50:39–45
Carter MR (1993) Soil sampling and methods of analysis. CRC Press, Boca Raton
Cathey SE, Boring LR, Sinclair TR (2010) Assessment of N2 fixation capability of native legumes from the longleaf pine–wiregrass ecosystem. Environ Exp Bot 67:444–450. https://doi.org/10.1016/j.envexpbot.2009.09.006
Craft CB, Chiang C (2002) Forms and amounts of soil nitrogen and phosphorus across a longleaf pine-depressional wetland landscape. Soil Sci Soc Am J Madison 66:1713–1721
D’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209. https://doi.org/10.2134/jeq2001.2206
Dickens E (2001) Fertilization options for longleaf pine stands on marginal soils with economic implications. In: Proc 31st Annu For Econ 67–72
Dilustro JJ, Collins BS, Duncan LK, Sharitz RR (2002) Soil texture, land-use intensity, and vegetation of Fort Benning upland forest sites. J Torrey Bot Soc 129:289–297. https://doi.org/10.2307/3088700
Dixon ROD, Wheeler CT (1983) Biochemical, physiological and environmental aspects of symbiotic nitrogen fixation. In: Gordon JC, Wheeler CT (eds) Biological nitrogen fixation in forest ecosystems: foundations and applications. Springer, Netherlands, pp 107–171
Doyle JJ (2011) Phylogenetic perspectives on the origins of nodulation. Mol Plant Microbe Interact 24:1289–1295. https://doi.org/10.1094/MPMI-05-11-0114
Fenner M, Lee WG (1989) Growth of seedlings of pasture grasses and legumes deprived of single mineral nutrients. J Appl Ecol 26:223. https://doi.org/10.2307/2403663
Finzi AC, Rodgers VL (2009) Bottom-up rather than top-down processes regulate the abundance and activity of nitrogen fixing plants in two Connecticut old-field ecosystems. Biogeochemistry 95:309–321. https://doi.org/10.1007/s10533-009-9338-4
Greweling T (1976) Chemical analysis of plant tissue. Search Agric 6:1–35
Hainds MJ, Mitchell RJ, Palik BJ et al (1999) Distribution of native legumes (Leguminosae) in frequently burned longleaf pine (Pinaceae)-wiregrass (Poaceae) ecosystems. Am J Bot 86:1606. https://doi.org/10.2307/2656797
Hiers JK, Mitchell RJ (2007) The influence of burning and light availability on N2-fixation of native legumes in longleaf pine woodlands. J Torrey Bot Soc 134:398–409 https://doi.org/10.3159/1095-5674(2007)134[398:TIOBAL]2.0.CO;2
Hiers JK, Mitchell RJ, Boring LR et al (2003) Legumes native to longleaf pine savannas exhibit capacity for high N2-fixation rates and negligible impacts due to timing of fire. New Phytol 157:327–338. https://doi.org/10.1046/j.1469-8137.2003.00679.x
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Hungate BA, Stiling PD, Dijkstra P et al (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291–1292. https://doi.org/10.1126/science.1095549
Karimian N, Cox FR (1979) Molybdenum availability as predicted from selected soil chemical properties. Agron J 71:63–65. https://doi.org/10.2134/agronj1979.00021962007100010015x
Lavoie M, Starr G, Mack MC et al (2010) Effects of a prescribed fire on understory vegetation, carbon Pools, and soil nutrients in a longleaf pine-slash pine forest in Florida. Nat Areas J 30:82–94. https://doi.org/10.3375/043.030.0109
Lee YY, Son Y (2005) Diurnal and seasonal patterns of nitrogen fixation in an Alnus hirsuta plantation of Central Korea. J Plant Biol 48:332–337
Lewis CE (1977) Longleaf pine responds through age 15 to early fertilization. Dept Agric For Serv Southeast For Exp Stn 239:1–7
LPWG (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66:44–77. https://doi.org/10.12705/661.3
Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15:1409–1416. https://doi.org/10.1080/00103628409367568
Menge DNL, Wolf A, Funk JL (2015) Diversity of nitrogen fixation strategies in Mediterranean legumes. Nat Plants 1:15064. https://doi.org/10.1038/nplants.2015.64
National Climatic Data Center (NCDC) (2017) 1981–2010 Normals. https://www.ncdc.noaa.gov/cdo-web/datatools/normals. Accessed 2 May 2017
Nelson NS (1987) An acid-persulfate digestion procedure for determination of phosphorus in sediments. Commun Soil Sci Plant Anal 18:359–369. https://doi.org/10.1080/00103628709367826
Norden H, Kirkman LK (2006) Field guide to common legume species of the longleaf pine ecosystem. Joseph W. Jones Ecological Research Center Publication, Newton, GA
Pate J (1996) Photoassimilate partitioning and consumption in nitrogen-fixing crop legumes. Photoassimilate distribution in plants and crops. Mercel Dekker, New York, pp 467–477
Peet RK (2007) Ecological classification of longleaf pine woodlands. The longleaf pine ecosystem. Springer, New York, pp 51–93
Pequerul A, Pérez C, Madero P et al (1993) A rapid wet digestion method for plant analysis. Optimization of plant nutrition. Springer, Dordrecht, pp 3–6
Perreijn C (2002) Symbiotic nitrogen fixation by leguminous trees in tropical rain forest in Guyana. Tropenbos Guyana Series 11, Utrecht
Raison RJ, Khanna PK, Woods PV (1984) Mechanisms of element transfer to the atmosphere during vegetation fires. Can J For Res 15:1–5. https://doi.org/10.1007/s13398-014-0173-7.2
Robertson G, Coleman D, Bledsoe C, Sollins P (1999) Standard soil methods for long-term ecological research, 2nd edn. Oxford University Press, New York
Sheffer E, Batterman SA, Levin SA, Hedin LO (2015) Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nat Plants 1:15182. https://doi.org/10.1038/nplants.2015.182
Sprent JI (2009) Legume nodulation. Wiley, Oxford
Van Lear DH, Carroll WD, Kapeluck PR, Johnson R (2005) History and restoration of the longleaf pine-grassland ecosystem: implications for species at risk. For Ecol Manag 211:150–165. https://doi.org/10.1016/j.foreco.2005.02.014
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115. https://doi.org/10.1007/BF00002772
Wiggers MS, Hiers JK, Barnett A et al (2017) Seed heat tolerance and germination of six legume species native to a fire-prone longleaf pine forest. Plant Ecol 218:151–171. https://doi.org/10.1007/s11258-016-0674-x
Wilson CA, Mitchell RJ, Hendricks JJ, Boring LR (1999) Patterns and controls of ecosystem function in longleaf pine wire grass savannas. Can J For Res 29:743–751
Wurzburger N, Hedin LO (2016) Taxonomic identity determines N2 fixation by canopy trees across lowland tropical forests. Ecol Lett 19:62–70. https://doi.org/10.1111/ele.12543
Acknowledgements
We thank A. Barón, D. Blount, E. Coughlin, A. Johnson, A. Martin, J. Minucci, M. Patillo, C. Phillips, C. Timpone, B. Walker and S. Wilson for their assistance in the field, greenhouse and laboratory. We are grateful to D. Markewitz, J. Minucci, J. O’Brien and C. Phillips for their constructive comments on the manuscript. This research was supported by the Strategic Environmental Research and Development Program (RC-2328).
Author information
Authors and Affiliations
Contributions
MRA, LOH, EAH and NW designed the experiments, MRA conducted the research, MRA, JAT and NW analyzed the data, MRA, JAT, LOH and NW wrote the manuscript and EAH provided editorial advice.
Corresponding author
Additional information
Communicated by Jason P. Kaye.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ament, M.R., Tierney, J.A., Hedin, L.O. et al. Phosphorus and species regulate N2 fixation by herbaceous legumes in longleaf pine savannas. Oecologia 187, 281–290 (2018). https://doi.org/10.1007/s00442-018-4129-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4129-z