Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests

Canadian Journal of Forest Research

Volumn 40, Issue 9, 2010, Pages 17666-1780

  Vadeboncoeur, Matthew A ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE CATIONS; CO-LIMITATION; DECIDUOUS FOREST; EXPERIMENTAL EVIDENCE; FACTORIAL EXPERIMENT; FERTILIZATION EXPERIMENT; FOREST PRODUCTIVITY; HARDWOOD FORESTS; HIGH RATE; META-ANALYSIS; N DEPOSITION; N FERTILIZATION; NUTRIENT ADDITION; PRIMARY PRODUCTION; SHORT SUPPLY; SINGLE ELEMENT; SYNERGISTIC EFFECT; TEMPERATE FORESTS; WEIGHTED MEAN;

CALCIUM; EXPERIMENTS; NITROGEN FERTILIZERS; SOILS;

NUTRIENTS;

CALCIUM; CATION; DECIDUOUS FOREST; FERTILIZER APPLICATION; FORESTRY PRODUCTION; META-ANALYSIS; NITROGEN; NUTRIENT LIMITATION; PHOSPHORUS; PHYSIOLOGICAL RESPONSE; PRIMARY PRODUCTION; SOIL TYPE; TEMPERATE FOREST;

UNITED STATES;

EID: 77958074611     PISSN: 00455067     EISSN: 12086037     Source Type: Journal    
DOI: 10.1139/X10-127     Document Type: Article

References (82)

1. Aber, J.D., Nadelhoffer, K.J., Steudler, P., and Melillo, J.M. 1989. Nitrogen saturation in northern forest ecosystems. Bioscience, 39(6): 378-386. doi:10.2307/1311067.
2. Arnqvist, G., and Wooster, D. 1995. Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol. Evol. 10(6): 236-240. doi:10.1016/S0169-5347(00)89073-4.
3. Auchmoody, L.R. 1982. Response of young black cherry stands to fertilization. Can. J. For. Res. 12(2): 319-325. doi:10.1139/x82-046.
4. Bigelow, S., and Canham, C. 2007. Nutrient limitation of juvenile trees in a northern hardwood forest: calcium and nitrate are preeminent. For. Ecol. Manag. 243(2-3): 310-319. doi:10.1016/j. foreco.2007.03.027.
5. Bloom, A.J., Chapin, F.S., and Mooney, H.A. 1985. Resource limitation in plants - an economic analogy. Annu. Rev. Ecol. Syst. 16: 363-392. doi:10.1146/annurev.es.16.110185.002051.
6. Blum, J.D., Klaue, A., Nezat, C.A., Driscoll, C.T., Johnson, C.E., Siccama, T.G., Eagar, C., Fahey, T.J., and Likens, G.E. 2002. Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature, 417(6890): 729-731. doi:10.1038/nature00793. PMID:12066181.
7. Boutin, R., and Robitaille, G. 1995. Increased soil nitrate losses under mature sugar maple trees affected by experimentally induced deep frost. Can. J. For. Res. 25(4): 588-602. doi:10.1139/x95-066.
8. Bowen, J.L., and Valiela, I. 2001. Historical changes in atmospheric nitrogen deposition to Cape Cod, Massachusetts, USA. Atmos. Environ. 35(6): 1039-1051. doi:10.1016/S1352-2310(00)00331-9.
9. Chalot, M., and Brun, A. 1998. Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol. Rev. 22(1): 21-44. doi:10.1111/j.1574-6976.1998.tb00359.x. PMID:9640645.
10. Chapin, F.S., III, Vitousek, P.M., and Cleve, K.V. 1986. The nature of nutrient limitation in plant communities. Am. Nat. 127(1): 48-58. doi:10.1086/284466.
11. Chapin, F.S., III, Bloom, A.J., Field, C.B., and Waring, R.H. 1987. Plant responses to multiple environmental factors. Bioscience, 37(1): 49-57. doi:10.2307/1310177.
12. Cogbill, C.V., Burk, J., and Motzkin, G. 2002. The forests of presettlement New England, USA: spatial and compositional patterns based on town proprietor surveys. J. Biogeogr. 29(10-11): 1279-1304. doi:10.1046/j.1365-2699.2002.00757.x.
13. Côté, B., O'Halloran, I., Hendershot, W.H., and Spankie, H. 1995. Possible interference of fertilization in the natural recovery of a declining sugar maple stand in southern Quebec. Plant Soil, 168-169(1): 471-480. doi:10.1007/BF00029359.
14. Davidson, E.A., and Howarth, R.W. 2007. Environmental science: nutrients in synergy. Nature, 449(7165): 1000-1001. doi:10.1038/4491000a. PMID:17960233.
15. Dyke, A.S., Moore, A., and Robertson, L. 2003. Deglaciation of North America. Open File 1574. Geological Survey of Canada, Ottawa, Ont.
16. Ellis, R.C. 1979. Response of crop trees of sugar maple, white ash, and black cherry to release and fertilization. Can. J. For. Res. 9(2): 179-188. doi:10.1139/x79-032.
17. Elser, J.J., Bracken, M.E., Cleland, E.E., Gruner, D.S., Harpole, W.S., Hillebrand, H., Ngai, J.T., Seabloom, E.W., Shurin, J.B., and Smith, J.E. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10(12): 1135-1142. doi:10.1111/j.1461-0248.2007.01113.x. PMID:17922835.
18. Elvir, J.A., Wiersma, G.B., White, A.S., and Fernandez, I.J. 2003. Effects of chronic ammonium sulfate treatment on basal area increment in red spruce and sugar maple at the Bear Brook Watershed in Maine. Can. J. For. Res. 33(5): 862-869. doi:10.1139/x03-016.
19. Fahey, T.J., Battles, J.J., and Wilson, G.F. 1998. Responses of early successional northern hardwood forests to changes in nutrient availability. Ecol. Monogr. 68(2): 183-212. doi:10.1890/0012-9615(1998)068[0183:ROESNH]2.0.CO;2.
20. Federer, C.A., Hornbeck, J.W., Tritton, L.M., Martin, C.W., Pierce, R.S., and Smith, C.T. 1989. Long-term depletion of calcium and other nutrients in eastern US forests. Environ. Manag. 13(5):593-601. doi:10.1007/BF01874965.
21. Fenn, M.E., Huntington, T.G., Mclaughlin, S.B., Eagar, C., Gomez, A., and Cook, R.B. 2006. Status of soil acidification in North America. J. For. Sci. 52: 3-13.
22. Finn, R.F., and Tyron, H.H. 1942. The comparative influence of leaf mould and inorganic fertilizers on the growth of red oak. Black Rock For. Pap. No. 1(17). Black Rock Forest, Cornwallon-the-Hudson, N.Y.
23. Finn, R.F., and White, D.P. 1966. Commercial fertilizers increase growth in a yellow-poplar plantation. J. For. 64: 809-810.
24. Finzi, A.C. 2009. Decades of atmospheric deposition have not resulted in widespread phosphorus limitation or saturation of tree demand for nitrogen in southern New England. Biogeochemistry, 92(3): 217-229. doi:10.1007/s10533-009-9286-z.
25. Fyles, J.W., Côté, B., Courchesne, F., Hendershot, W.H., and Savoie, S. 1994. Effects of base cation fertilization on soil and foliage nutrient concentrations, and litter-fall and throughfall nutrient fluxes in a sugar maple forest. Can. J. For. Res. 24(3): 542-549. doi:10.1139/x94-071.
26. Gradowski, T., and Thomas, S.C. 2006. Phosphorus limitation of sugar maple growth in central Ontario. For. Ecol. Manag. 226(1-3): 104-109. doi:10.1016/j.foreco.2005.12.062.
27. Gradowski, T., and Thomas, S.C. 2008. Responses of Acer saccharum canopy trees and saplings to P, K and lime additions under high N deposition. Tree Physiol. 78: 173-185. doi:10.1093/ treephys/28.2.173.
28. Gusewell, S. 2004. N:P ratios in terrestrial plants: variation and functional significance. New Phytol. 164(2): 243-266. doi:10. 1111/j.1469-8137.2004.01192.x.
29. Hedges, L.V., Gurevitch, J., and Curtis, P.S. 1999. The meta-analysis of response ratios in experimental ecology. Ecology, 80(4): 1150-1156. doi:10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2.
30. Hobbie, E.A. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology, 87(3): 563-569. doi:10.1890/05-0755. PMID:16602286.
31. Houston, D.R. 1987. Forest tree declines of past and present: current understanding. Can. J. Plant Pathol. 9: 349-360.
32. Houston, D.R. 1999. History of sugar maple decline. In Sugar Maple Ecology and Health: Proceedings of an International Symposium. Edited by Stephen B. Horsley and Robert P. Long. U.S. For. Serv. Gen. Tech. Rep. NE-261. pp. 19-26.
33. Hoyle, M.C. 1969. Response of yellow birch in acid subsoil to macronutrient additions. Soil Sci. 108(5): 354-358.
34. Jiao, Y., Whalen, J.K., and Hendershot, W.H. 2007. Phosphate sorption and release in a sandy-loam soil as influenced by fertilizer sources. Soil Sci. Soc. Am. J. 71: 118-124. doi:10.2136/ sssaj2006.0028.
35. Juice, S.M., Fahey, T.J., Siccama, T.G., Driscoll, C.T., Denny, E.G., Eagar, C., Cleavitt, N.L., Minocha, R., and Richardson, A.D. 2006. Response of sugar maple to calcium addition to northern hardwood forest. Ecology, 87(5): 1267-1280. doi:10.1890/0012-9658(2006)87[1267:ROSMTC]2.0.CO;2. PMID:16761605.
36. Karnig, J.J. 1972. Nitrogen fertilizer increases diameter growth of northern red oak. J. For. 70: 629.
37. Kobe, R.K., Likens, G.E., and Eagar, C. 2002. Tree seedling growth and mortality responses to manipulations of calcium and aluminum in a northern hardwood forest. Can. J. For. Res. 32(6): 954-966. doi:10.1139/x02-018.
38. Lea, R., Tierson, W.C., and Leaf, A.L. 1979. Growth responses of northern hardwoods to fertilization. For. Sci. 25: 597-604.
39. LeBauer, D.S., and Treseder, K.K. 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology, 89(2): 371-379. doi:10.1890/06-2057.1. PMID: 18409427.
40. Leech, R., and Kim, Y. 1990. Methods to investigate fertilization as a means to improve growth and sugar yield of sugar maple. Commun. Soil. Sci. Plant Anal. 21(17): 2029-2051. doi:10.1080/00103629009368357.
41. Lovett, G.M., Weathers, K.C., Arthur, M.A., and Schultz, J.C. 2004. Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry, 67(3): 289-308. doi:10.1023/B:BIOG.0000015786.65466.f5.
42. Mader, D.L., Thompson, B.W., and Wells, J.P. 1969. Influence of nitrogen on sugar maple decline. Mass. Agric. Exp. Stn. Bull. 582: 1-19.
43. Magill, A.H., Aber, J.D., Currie, W.S., Nadelhoffer, K.J., Martin, M.E., McDowell, W.H., Melillo, J.M., and Steudler, P. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. For. Ecol. Manag. 196(1): 7-28. doi:10.1016/j.foreco.2004.03.033.
44. Magnani, F., Mencuccini, M., Borghetti, M., Berbigier, P., Berninger, F., Delzon, S., Grelle, A., Hari, P., Jarvis, P.G., Kolari, P., Kowalski, A.S., Lankreijer, H., Law, B.E., Lindroth, A., Loustau, D., Manca, G., Moncrieff, J.B., Rayment, M., Tedeschi, V., Valentini, R., and Grace, J. 2007. The human footprint in the carbon cycle of temperate and boreal forests. Nature, 447(7146): 849-851. doi:10.1038/nature05847. PMID:17568744.
45. Mercer, R.D. 1974. Foliar nutrient levels and fertilization response of sugar maple in a mixed hardwood stand in central New Brunswick. University of New Brunswick, Fredericton, N.B.
46. Mitchell, H.L., and Chandler, R.F. 1939. The nitrogen nutrition and growth of certain deciduous trees of northeastern United States. Black Rock For. Pap. No. 1(11). Black Rock Forest, Cornwallon-the-Hudson, N.Y.
47. Mitchell, M.J., Driscoll, C.T., Owen, J.S., Schaefer, D., Michener, R., and Raynal, D.J. 2001. Nitrogen biogeochemistry of three hardwood ecosystems in the Adirondack Region of New York. Biogeochemistry, 56(2): 93-133. doi:10.1023/A:1013001710569.
48. Mohren, G.M., Burg, J., and Burger, F.W. 1986. Phosphorus deficiency induced by nitrogen input in Douglas fir in the Netherlands. Plant Soil, 95(2): 191-200. doi:10.1007/BF02375071.
49. Moore, J.-D., and Houle, D. 2009. Soil solution and sugar maple response to NH4NO3 additions in a base-poor northern hardwood forest of Québec, Canada. Environ. Monit. Assess. 155(1-4): 177-190. doi:10.1007/s10661-008-0427-y. PMID:18696241.
50. Moore, J., and Ouimet, R. 2006. Ten-year effect of dolomitic lime on the nutrition, crown vigor, and growth of sugar maple. Can. J. For. Res. 36(7): 1834-1841. doi:10.1139/X06-081.
51. Naples, B.K., and Fisk, M.C. 2010. Belowground insights into nutrient limitation in northern hardwood forests. Biogeochemistry, 97(2-3): 109-121. doi:10.1007/s10533-009-9354-4.
52. Nave, L.E., Vance, E.D., Swanston, C.W., and Curtis, P.S. 2010. Harvest impacts on soil carbon storage in temperate forests. For. Ecol. Manag. 259(5): 857-866. doi:10.1016/j.foreco.2009. 12.009.
53. Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V., Underwood, E.C., D'Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P., and Kassem, K.R. 2001. Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience, 51(11): 933-938. doi:10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2.
54. Ouimet, R., and Fortin, J. 1992. Growth and foliar nutrient status of sugar maple: incidence of forest decline and reaction to fertilization. Can. J. For. Res. 22(5): 699-706. doi:10.1139/x92-093.
55. Paré, D., and Bernier, B. 1989. Origin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can. J. For. Res. 19(1): 24-34. doi:10.1139/x89-004.
56. Paul, E.A. (Editor). 2007. Soil microbiology, ecology, and biogeochemistry. Academic Press, Oxford, U.K.
57. Payette, S., Fortin, M., and Morneau, C. 1996. The recent sugar maple decline in southern Quebec: probable causes deduced from tree rings. Can. J. For. Res. 26(6): 1069-1078. doi:10.1139/x26-118.
58. Pregitzer, K.S., Burton, A.J., Zak, D.R., and Talhelm, A.F. 2008. Simulated chronic nitrogen deposition increases carbon storage in northern temperate forests. Glob. Change Biol. 14: 142-153. doi:10.1111/j.1365-2486.2007.01465.x.
59. Rosenthal, R. 1979. The file drawer problem and tolerance for null results. Psychol. Bull. 86(3): 638-641. doi:10.1037/0033- 909. 86.3.638.
60. Safford, L.O. 1973. Fertilization increases diameter growth of birch-beech-maple trees in New Hampshire. U.S. For. Serv. Res. Note NE-182.
61. Safford, L.O. 1982. Correlation of greenhouse bioassay with field response to fertilizer by paper birch. Plant Soil, 64(2): 167-176. doi:10.1007/BF02184248.
62. Safford, L.O., and Czapowskyj, M.M. 1986. Fertilizer stimulates growth and mortality in a young Populus-Betula stand: 10-year results. Can. J. For. Res. 16(4): 807-813. doi:10.1139/x86-143.
63. Safford, L.O., and Filip, S.M. 1974. Biomass and nutrient content of 4-year-old fertilized and unfertilized northern hardwood stands. Can. J. For. Res. 4(4): 549-554. doi:10.1139/x74-079.
64. Salonius, P.O., Fisher, R.A., and Mahendrappa, M.K. 1982. An alternative method of measuring fertilizer effects in forest stands. Can. J. For. Res. 12(2): 146-150. doi:10.1139/x82-022.
65. Schmitt, M.D., Czapowskyj, M.M., Safford, L.O., and Leaf, A.L. 1981. Biomass and elemental uptake in fertilized and unfertilized Betula papyrifera Marsh. and Populus grandidentata Michx. Plant Soil, 60(1): 111-121. doi:10.1007/BF02377116.
66. Sparks, D.L. 2003. Environmental soil chemistry. Academic Press, London, U.K.
67. Stanturf, J.A. 1983. Effects of added nitrogen on trees and soil of deciduous forests in southern New York. Ph.D. dissertation, Cornell University, Ithaca, N.Y.
68. Clair, St. S.B., Sharpe, W.E., and Lynch, J.P. 2008. Key interactions between nutrient limitation and climatic factors in temperate forests: a synthesis of the sugar maple literature. Can. J. For. Res. 38: 401-414. doi:10.1139/X07-161.
69. Stevens, P.A., Harrison, A.F., Jones, H.E., Williams, T., and Hughes, S. 1993. Nitrate leaching from a Sitka spruce plantation and the effect of fertilisation with phosphorus and potassium. For. Ecol. Manag. 58(3-4): 233-247. doi:10.1016/0378- 127(93)90147-F.
70. Stone, D.M. 1980. Fertilization of a pole-sized maple stand: 10-year results. Can. J. For. Res. 10: 158-163. doi:10.1139/x80-028.
71. Thomas, R.Q., Canham, C.D., Weathers, K.C., and Goodale, C.L. 2010. Increased tree carbon storage in response to nitrogen deposition in the US. Nat. Geosci. 3: 3-17. doi:10.1038/ngeo721.
72. Tilman, D. 1985. The resource-ratio hypothesis of plant succession. Am. Nat. 125(6): 827-852. doi:10.1086/284382.
73. Treseder, K.K. 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol. 164(2): 347-355. doi:10.1111/j.1469-8137.2004.01159.x.
74. Treseder, K.K., and Vitousek, P.M. 2001. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology, 82(4): 946-954. doi:10.1890/0012-9658(2001)082[0946:EOSNAO]2.0.CO;2.
75. Tripler, C.E., Canham, C.D., Inouye, R.S., and Schnurr, J.L. 2002. Soil nitrogen availability, plant luxury consumption, and herbivory by white-tailed deer. Oecologia (Berl.), 133(4): 517-524. doi:10.1007/s00442-002-1046-x.
76. Vitousek, P.M., and Farrington, H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry, 37(1): 63-75. doi:10.1023/A:1005757218475.
77. Vitousek, P.M., and Howarth, R.W. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry, 13(2): 87-115. doi:10.1007/BF00002772.
78. Walker, T.W., and Syers, J.K. 1976. The fate of phosphorus during pedogenesis. Geoderma, 15(1): 1-19. doi:10.1016/0016- 061(76)90066-5.
79. Wallace, Z.P., Lovett, G.M., Hart, J.E., and Machona, B. 2007. Effects of nitrogen saturation on tree growth and death in a mixedoak forest. For. Ecol. Manag. 243(2-3): 210-218. doi:10.1016/j. foreco.2007.02.015.
80. Ward, W.W., and Bowersox, T.W. 1970. Upland oak response to fertilization with nitrogen, phosphorus, and calcium. For. Sci. 16: 113-120. doi:10.1139/x88-116.
81. Wilmot, T.R., Ellsworth, D.S., and Tyree, M.T. 1996. Base cation fertilization and liming effects on nutrition and growth of Vermont sugar maple stands. For. Ecol. Manag. 84(1-3): 123-134. doi:10.1016/0378-1127(96)03743-7.
82. Zaccherio, M.T., and Finzi, A.C. 2007. Atmospheric deposition may affect northern hardwood forest composition by altering soil nutrient supply. Ecol. Appl. 17(7): 1929-1941. doi:10.1890/ 06-2067.1. PMID:17974332.