No evidence that chronic nitrogen additions increase photosynthesis in mature sugar maple forests

Ecological Applications

Volumn 21, Issue 7, 2011, Pages 2413-2424

  Talhelm, A F ^a   Pregitzer, K S ^a   Burton, A J ^b  

^a UNIVERSITY OF IDAHO   (United States)

^b MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

Author keywords

Acer saccharum; Atmospheric deposition; Canopy tower measurements; Global change; Long term experiment; Nitrogen; Northern hardwoods; Stable isotopes; Sugar maple

Indexed keywords

CARBON; FERTILIZER; NITRATE; NITROGEN; OXYGEN;

ABOVEGROUND PRODUCTION; ATMOSPHERIC DEPOSITION; CANOPY; DECIDUOUS FOREST; GLOBAL CHANGE; GROWTH RATE; NITROGEN; NUTRIENT LIMITATION; PHOTOSYNTHESIS; STABLE ISOTOPE;

ACER; ARTICLE; CHEMISTRY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; TIME; TREE; UNITED STATES;

ACER; CARBON; CARBON ISOTOPES; FERTILIZERS; MICHIGAN; NITRATES; NITROGEN; OXYGEN; OXYGEN ISOTOPES; PHOTOSYNTHESIS; PLANT LEAVES; TIME FACTORS; TREES;

UNITED STATES;

ACER SACCHARUM;

EID: 80053999058     PISSN: 10510761     EISSN: None     Source Type: Journal    
DOI: 10.1890/10-2076.1     Document Type: Article

References (72)

1. Aber, J. D., W. McDowell, K. Nadelhoffer, A. Magill, G. Bernston, M. Kamakea, S. McNulty, W. Currie, L. Rustad, and I. Fernandez. 1998. Nitrogen saturation in temperate forest ecosystems. BioScience 48:921-934. (Pubitemid 28494493)
2. Aber, J. D., K. J. Nadelhoffer, P. Steudler, and J. M. Melillo. 1989. Nitrogen saturation in northern forest ecosystems. BioScience 39:378-387.
3. Aber, J. D., S. V. Ollinger, and C. T. Driscoll. 1997. Modeling nitrogen saturation in forests ecosystems in response to land use and atmospheric deposition. Ecological Modelling 101:61-78. (Pubitemid 27288835)
4. Ågren, G. I., and E. Bosatta. 1988. Nitrogen saturation of terrestrial ecosystems. Environmental Pollution 54:185-197.
5. Araus, J. L., T. Amaro, Y. Zuhair, and M. M. Nachit. 1997. Effect of leaf structure and water status on carbon isotope discrimination in field-grown durum wheat. Plant, Cell and Environment 20:1484-1494. (Pubitemid 28073215)
6. 13C of early and latewood in 3-to 5-yearold rings of Douglas-fir. Trees 22:603-609.
7. Barbour, M. M. 2007. Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34:83-94.
8. Barbour, M. M., T. J. Andrews, and G. D. Farquhar. 2001. Correlations between oxygen isotope ratios of wood constituents of Quercus and Pinus samples from around the world. Australian Journal of Plant Physiology 28:335-348.
9. Baron, J. S., H. M. Rueth, A. M. Wolfe, K. R. Nydick, E. J. Allstott, J. T. Minear, and B. Moraska. 2000. Ecosystem responses to nitrogen deposition in the Colorado Front Range. Ecosystems 3:352-368.
10. Bauer, G. A., F. A. Bazzaz, R. Minocha, S. Long, A. Magill, J. Aber, and G. M. Berntson. 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. Forest Ecology and Management 196:173-186. (Pubitemid 38847892)
11. Boggs, J. L., S. G. McNulty, M. J. Gavanni, and J. M. Myers. 2005. Tree growth, foliar chemistry, and nitrogen cycling across a nitrogen deposition gradient in southern Appalachian deciduous forest. Canadian Journal of Forest Research 35:1901-1913. (Pubitemid 43035756)
12. Braun, E. L. 1950. Deciduous forests of eastern North America. Macmillan, New York, New York, USA.
13. Brooks, J. R., and R. Coulombe. 2009. Physiological responses to fertilization recorded in tree rings: isotopic lessons from a long-term fertilization trial. Ecological Applications 19:1044-1060.
14. - deposition reduces soil respiration in northern hardwood forests. Global Change Biology 10:1080-1091. (Pubitemid 38964502)
15. Cheng, L., and L. H. Fuchigami. 2000. Rubisco activation state decreases with increasing nitrogen content in apple leaves. Journal of Experimental Botany 51:1687-1694.
16. 18O in tree rings of Callitris columellaris provide evidence of a change in stomatal control of photosynthesis in response to regional changes in climate. Tree Physiology 28:1525-1533.
17. Dentener, F. et al. 2006. The global atmospheric environment for the next generation. Environmental Science and Technology 40:3586-3594. (Pubitemid 43841579)
18. De Vries, W., G. J. Reinds, P. Gundersen, and H. Sterba. 2006. The impact of nitrogen deposition on carbon sequestration in European forests and forest soils. Global Change Biology 12:1151-1173. (Pubitemid 43905667)
19. Egerton-Warburton, L. M., and E. B. Allen. 2000. Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecological Applications 10:484-496.
20. 2. Tree Physiology 29:777-788.
21. Eglin, T., F. Maunoury-Danger, C. Fresneau, C. Lelarge, B. Pollet, C. Lapierre, C. Francois, and C. Damesin. 2008. Biochemical composition is not the main factor influencing the variability in carbon isotope composition of tree rings. Tree Physiology 28:1619-1628.
22. Elvir, J. A., L. Rustad, G. B. Wiersma, I. J. Fernandez, A. S. White, and G. J. White. 2005. Eleven-year response of foliar chemistry to chronic nitrogen and sulfur additions at the Bear Brook Watershed in Maine. Canadian Journal of Forest Research 35:1402-1410. (Pubitemid 41483388)
23. Elvir, J. A., G. B. Wiersma, S. Bethers, and P. Kenlan. 2010. Effects of chronic ammonium sulfate treatment on the forest at the Bear Brook Watershed in Maine. Environmental Monitoring and Assessment 171:129-147.
24. Elvir, J. A., G. B. Wiersma, M. E. Day, M. S. Greenwood, and I. J. Fernandez. 2006. Effects of enhanced nitrogen deposition on foliar chemistry and physiological processes of forest trees at the Bear Brook Watershed in Maine. Forest Ecology and Management 221:207-214. (Pubitemid 43028434)
25. Evans, J. R. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9-19.
26. Farquhar, G. D., J. R. Ehleringer, and K. T. Hubick. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40:503-557.
27. 2 concentration. Geochimica et Cosmochimica Acta 63:1891-1903. (Pubitemid 30005542)
28. Galloway, J. N., A. R. Townsend, J. W. Erisman, M. Bekunda, Z. Cai, J. R. Freney, L. A. Martinelli, S. P. Seitzinger, and M. A. Sutton. 2008. Transformations of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889-892. (Pubitemid 351929578)
29. Gower, S., P. Reich, and Y. Son. 1993. Canopy dynamics and aboveground production of five tree species with different leaf longevities. Tree Physiology 12:327-345. (Pubitemid 24414859)
30. 3 effects on the physiological performance of different-aged trees. Plant, Cell and Environment 30:1023-1034. (Pubitemid 47037886)
31. 2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Functional Ecology 13:632-639.
32. Hobbie, E. A. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563-569.
33. Holland, E. A., B. H. Braswell, J. Sulzman, and J.-F. Lamarque. 2005. Nitrogen deposition onto the United States and Western Europe: synthesis of observations and models. Ecological Applications 15:38-57. (Pubitemid 40263567)
34. Hultine, K. R., and J. D. Marshall. 2000. Altitude trends in conifer leaf morphology and stable carbon isotope discrimination. Oecologia 123:32-40. (Pubitemid 30244377)
35. Hutchinson, T. C., S. A. Watmough, E. P. S. Sager, and J. D. Karagatzides. 1998. Effects of excess nitrogen deposition and soil acidification on sugar maple (Acer saccharum) in Ontario, Canada: an experimental study. Canadian Journal of Forest Research 28:299-310.
36. 2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytologist 173:463-480. (Pubitemid 46098886)
37. 2. Trees 21:151-159.
38. Körner, C., G. D. Farquhar, and S. C. Wong. 1991. Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88:30-40.
39. LeBauer, D. S., and K. K. Treseder. 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371-379. (Pubitemid 351550035)
40. Lilleskov, E. A., T. J. Fahey, T. R. Horton, and G. M. Lovett. 2002. Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104-115. (Pubitemid 34067682)
41. Littell, R. C., G. C. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS system for mixed models. SAS Institute, Cary, North Carolina, USA.
42. Long, S. P., and C. J. Bernacchi. 2003. Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 54:2393-2401. (Pubitemid 37379253)
43. MacDonald, N. W., A. J. Burton, H. O. Liechty, J. A. Witter, K. S. Pregitzer, G. D. Mroz, and D. D. Richter. 1992. Ion leaching in forest ecosystems along a Great Lakes air pollution gradient. Journal of Environmental Quality 21:614-623.
44. Magnani, F., et al. 2007. The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:848-852.
45. Monclus, R., E. Dreyer, F. M. Delmotte, M. Villar, D. Delay, E. Boudouresque, J.-M. Petit, N. Marron, C. Brechet, and F. Brignolas. 2005. Productivity, leaf traits, and carbon isotope discrimination in 29 Populus deltoides × P. nigra clones. New Phytologist 167:53-62. (Pubitemid 40885828)
46. Nadelhoffer, K. J., B. A. Emmett, P. Gundersen, O. J. Kjonaas, C. J. Koopmans, P. Schleppi, A. Tietema, and R. F. Wright. 1999. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145-148.
47. Niinemets, U., A. Diaz-Espejo, J. Flexas, J. Galmes, and C. R. Warren. 2009. Role of mesophyll conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany 60:2249-2270.
48. 2 and land use history on the carbon dynamics of northern hardwoods forests. Global Change Biology 8:545-562. (Pubitemid 34707194)
49. Poorter, H., U. Niinemets, L. Poorter, I. J. Wright, and R. Villar. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182:565-588.
50. 18O trends across overstory environments in whole foliage and cellulose of three Pinus species. Journal of the American Society for Mass Spectrometry 19:1330-1335.
51. 18O and radial growth responses of residual red pine to variable retention harvesting. Tree Physiology 30:326-334.
52. Pregitzer, K. S., A. J. Burton, D. R. Zak, and A. F. Talhelm. 2008. Simulated chronic nitrogen deposition increases carbon storage in northern temperate forests. Global Change Biology 14:142-153. (Pubitemid 350226916)
53. Pregitzer, K. S., D. R. Zak, A. J. Burton, J. A. Ashby, and N. W. MacDonald. 2004. Chronic nitrate additions dramatically increase the export of carbon and nitrogen from northern hardwood ecosystems. Biogeochemistry 68:179-197. (Pubitemid 39444280)
54. Ryan, M. G., D. Binkley, J. H. Fownes, C. P. Giardina, and R. S. Senock. 2004. An experimental test of the causes of forest growth decline with stand age. Ecological Monographs 74:393-414. (Pubitemid 39182901)
55. Schaberg, P. G., T. D. Perkins, and S. G. McNulty. 1997. Effects of chronic low-level N additions on foliar elemental concentrations, morphology, and gas exchange of mature montane red spruce. Canadian Journal of Forest Research 27:1622-1629. (Pubitemid 28038029)
56. Scheidegger, Y., M. Saurer, M. Bahn, and R. Siegwolf. 2000. Linking oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350-357.
57. Seibt, U., A. Rajabi, H. Griffiths, and J. A. Berry. 2008. Carbon isotopes and water-use efficiency: sense and sensitivity. Oecologia 155:441-454.
58. 3 leaves. Plant, Cell and Environment 30:1035-1040. (Pubitemid 47174279)
59. Sievering, H., I. Fernandez, J. Lee, J. Hom, and L. Rustad. 2000. Forest canopy uptake of atmospheric nitrogen deposition at eastern U. S. conifer sites: carbon storage implications? Global Biogeochemical Cycles 14:1153-1159. (Pubitemid 32281830)
60. Skrzypek, G., A. Kaluzny, and M. O. Jedrysek. 2007. Carbon stable isotope analyses of mosses-comparisons of bulk organic matter and extracted nitrocellulose. Journal of the American Society for Mass Spectrometry 18:1453-1458. (Pubitemid 47088988)
61. 13C between deciduous and evergreen species. Botany 86:1233-1241.
62. Taylor, A. M., J. R. Brooks, B. Lachenbruch, J. J. Morrell, and S. Voelker. 2008. Correlation of carbon isotope ratios in the cellulose and wood extractives of Douglas-fir. Dendronchronologia 26:125-131.
63. Thomas, R. Q., C. D. Canham, K. C. Weathers, and C. L. Goodale. 2010. Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geoscience 3:13-17.
64. van Diepen, L. T. A. 2008. The role and diversity of arbuscular mycorrhizal fungi in Acer saccharum dominated forest ecosystems under natural and N-amended conditions. Dissertation. Michigan Technological University, Houghton, Michigan, USA.
65. van Diepen, L. T. A., E. A. Lilleskov, K. S. Pregitzer, and R. M. Miller. 2007. Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen amendments. New Phytologist 176:175-183. (Pubitemid 47352914)
66. van Diepen, L. T. A., E. A. Lilleskov, K. S. Pregitzer, and R. M. Miller. 2010. Simulated nitrogen deposition causes a decline of intra-and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems 13:683-695.
67. 13C of a-cellulose and bulk wood in the mangrove tree Rhizophora mucronata: implications for dendrochemistry. Chemical Geology 219:275-282. (Pubitemid 40757676)
68. Warren, C. R., M. A. Adams, and Z. Chen. 2000. Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Australian Journal of Plant Physiology 27:407-416. (Pubitemid 30351622)
69. Warren, C. R., E. Dreyer, and M. A. Adams. 2003. Photosynthesis-Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores. Trees 17:359-366. (Pubitemid 36803477)
70. - deposition increases soil organic matter by slowing decomposition. Ecological Applications 18:2016-2027.
71. Zar, J. H. 1999. Biostatistical analysis. Fourth edition. Prentice-Hall, Upper Saddle River, New Jersey, USA.
72. Zogg, G. P., D. R. Zak, K. S. Pregitzer, and A. J. Burton. 2000. Microbial immobilization and the retention of anthropogenic nitrate in northern hardwoods forests. Ecology 81:1858-1866. (Pubitemid 30466612)