Dynamic species-specific metabolic changes in the trees exposed to chronic N+S additions at the Bear Brook Watershed in Maine, USA
- 40 Downloads
Red spruce (Picea rubens Sarg.) and American beech (Fagus grandifolia Ehrh.) nutritional imbalances observed during 1998–2000 in response to nitrogen additions beginning in 1989 at Bear Brook Watershed in Maine, USA, were reversed by 2013. However, nitrogen-containing metabolites continued to accumulate to detoxify ammonia. While sugar maple (Acer saccharum Marsh.) was N-limited and benefitted from N+S additions, spruce and birch established new homeostatic status via adjusting cellular metabolism.
Increased deposition of atmospheric N leads to changes in forest productivity. Effects of added N+S on changes in cellular metabolism will yield information on species-specific sensitivity to N+S.
To evaluate foliar metabolic changes in American beech (Fagus grandifolia Ehrh.), sugar maple (Acer saccharum Marsh.), and red spruce (Picea rubens Sarg.) that were exposed to ammonium sulfate [(NH4)2SO4); ~ 28.8 kg S ha−1 yr−1 and 25.2 kg N ha−1 yr−1] additions at West Bear Watershed (WBW) starting in 1989 until the end of this experiment, while East Bear Watershed served as a reference.
Foliage was collected in 1998–2000 and 2013. Sapwood plugs were also collected in 2013. All were analyzed for ions and metabolites using HPLC and ICP.
During 1998–2000, only N+S-treated beech and spruce foliage had a reduction in Ca and Mg. All species had significantly higher content of N-rich metabolites. In 2013, ammonia detoxification continued in the absence of nutrient deficiencies. Significant changes in growth promoting metabolites occurred only in maple throughout this study.
Metabolic changes indicated that sugar maple at this site was and still is N-limited, whereas red spruce and American beech had to make metabolic adjustments in order to survive under chronic N+S inputs. We conclude that even in the absence of knowledge about individual species tolerance limits for nutrients and critical N load for the site, monitoring with a suite of metabolites that are centrally connected to both C and N pathways could be a very useful tool in assessing stress from nutrient imbalance in various tree species.
KeywordsAmerican beech Bear brook watershed in Maine Foliar metabolism Nitrogen plus sulfur addition Red spruce Sugar maple
free amino acids
basal area increment
Bear Brook Watershed in Maine
East Bear Watershed
West Bear Watershed
The authors are grateful to Dr. Walter Shortle, Dr. Gabriela Martinez, and Prof. Subhash Minocha for their suggestions at various steps in data analysis and/or to improve the manuscript; to the field crew for help in sample collection; and to Kenneth R. Dudzik for technical assistance.
Rakesh Minocha designed and wrote the manuscript with assistance from Swathi Turlapati (postdoctoral fellow) who also helped process some data. Stephanie Long (senior technician) helped with field collections and analyses, processing of all metabolic data. Ivan Fernandez helped with manuscript writing and editing and field collections of 2013.
This work was funded by the USDA Forest Service.
Compliance with ethical standards
Conflict of interest
The authors of this work do not have any conflict of interest statement.
- Bauer GA, Bazzaz FA, Minocha R, Long S, Magill A, Aber J, Berntson GM (2004) Effects of chronic N additions on tissue chemistry, photosynthetic capacity, and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States. For Ecol Manag 196:173–186CrossRefGoogle Scholar
- Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Marcos JG, Fluch S, Fraga MF, Guevara MÁ, Abarca D, Johnsen Ø, Maury S, Strauss SH, Campbell MM, Rohde A, Díaz-Sala C, Cervera MT (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecology and Evolution 3:399–415. https://doi.org/10.1002/ece3.461 CrossRefPubMedCentralGoogle Scholar
- Chen H, Zheng Y, Zhan J, He C, Wang Q (2017) Comparative metabolic profiling of the lipid-producing green microalga Chlorella reveals that nitrogen and carbon metabolic pathways contribute to lipid metabolism. Biotechnology for Biofuels 10:153. https://doi.org/10.1186/s13068-017-0839-4 CrossRefPubMedCentralGoogle Scholar
- Ericsson A, Walheim M, Norden LG, Näsholm T (1995) Concentrations of mineral nutrients and arginine in needles of Picea abies trees from different areas in southern Sweden in relation to nitrogen deposition and humus form. Ecol Bull 44:147–157Google Scholar
- Finzi AC, Breemen NV, Canham CD (1998) Canopy tree-soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8:440–446Google Scholar
- Lichtenthaler HK, Rinderle U (1988a) Chlorophyll fluorescence as vitality indicator in forest decline research. In: Lichtenthaler HKE (ed) Applications of chlorophyll Fluorescenc!a. Kluwer Academic Publishers, Dordrecht, pp 133–139Google Scholar
- Linder S (1995) Foliar analysis for detecting and correcting nutrient imbalances in Norway spruce. Ecol Bull 44:178–190Google Scholar
- Lloyd J (1999) The CO2 dependence of photosynthesis, plant growth responses to elevated CO2 concentrations and their interaction with soil nutrient status, II. Temperate and boreal forest productivity and thc combined effects of increasing CO2 concentrations and increased nitrogen deposition at a global scale. Funct Ecol 13:439–459CrossRefGoogle Scholar
- Majumdar R, Barchi B, Turlapati S, Gagne M, Minocha R, Long S, Minocha SC (2016) Glutamate, ornithine, arginine, proline and polyamine metabolic interactions: the pathway is regulated at the post-transcriptional level. Front Plant Sci 7:78. https://doi.org/10.3389/fpls.2016.00078 CrossRefPubMedCentralGoogle Scholar
- Minocha R, Long S, Turlapati SA, Fernandez I (2018) Dynamic species-specific metabolic changes in the trees exposed to chronic N+S additions at the Bear Brook Watershed in Maine, USA. Fort Collins, CO: Forest Service Research Data Archive. V1. [Dataset]. doi: https://doi.org/10.2737/RDS-2018-0058
- Nihlgard B (1985) The ammonium hypothesis: an additional explanation to the forest dieback in Europe. AMBIO 14:2–8Google Scholar
- Pinchot CC et al. (2017) Development of new Dutch elm disease-tolerant selections for restoration of the American elm in urban and forested landscapes. In: Sniezko, Richard A.; Man, Gary; Hipkins, Valerie; Woeste, Keith; Gwaze, David; Kliejunas, John T.; McTeague, Brianna A., tech. cords. (ed) Gene conservation of tree species-banking on the future. Proceedings of a workshop. Gen. Tech. Rep. PNW-GTR-963, Portland: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, pp 53–63Google Scholar
- Quinn TR, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3:13–17 doi:http://www.nature.com/ngeo/journal/v3/n1/suppinfo/ngeo721_S1.html CrossRefGoogle Scholar
- Schaberg P, Minocha R, Long S, Halman J, Hawley G, Eagar C (2011) Calcium addition at the Hubbard Brook Experimental Forest increases the capacity for stress tolerance and carbon capture in red spruce (Picea rubens) trees during the cold season. Trees 25:1053–1061. https://doi.org/10.1007/s00468-011-0580-8 CrossRefGoogle Scholar
- Shortle WC, Smith KT (1988) Aluminum-induced calcium deficiency syndrome in declining red spruce. Sci Cult 240:1017–1018Google Scholar
- Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161. https://doi.org/10.3389/fpls.2017.00161 CrossRefPubMedCentralGoogle Scholar
- Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. https://doi.org/10.1890/1051-0761(1997)007[0737:haotgn]2.0.co;2Google Scholar