Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis Yong Li, Shuli Niu*, Guirui Yu The following Supporting Information is available for this article: Fig. S1 Response of leaf N concentration to P addition. Table S1 Papers included in this study for establishing the database. (a) (b) Mean Tropical forest Grassland Tundra Wetland 0.97(104) 0.97(71) 0.96(50) 1.04(13) 0.97(17) 1.03(18) 0.94(13) 0.90(19) 1.02(17) 0.99(20) NaH2PO4 Ca(H2PO4)2 1.03(5) 1.01(5) 0.97(72) 0.92(37) <5 g m-2 5-10 g m-2 10-15 g m-2 >15 g m-2 0.96(30) 0.97(39) 1.02(10) 0.98(25) 0.93(29) 1.03(23) 0.92(6) 1.00(13) ≤ 3 yr >3 yr 0.98(83) 1.00(55) 0.95(21) 0.87(15) Herbaceous Woody 0.96(38) 0.98(43) 0.92(34) 1.03(16) .4 .6 .8 1.0 Response ratio 1.2 1.4 .4 .6 .8 1.0 1.2 1.4 Response ratio Fig. S1 Responses of leaf N concentration to P addition. (a) only P addition, and (b) P plus N addition (N addition was considered as control and P+N addition as P treatment). The dot with error bars indicates the mean effect size with the 95% CI. Table S1 Papers included in this study for establishing the database. No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 References Aerts R, Berendse F (1988) The effect of increased nutrient availability on vegetation dynamics in wet heathlands. Vegetatio, 76, 63-69. Anisfeld S, Hill T (2012) Fertilization Effects on Elevation Change and Belowground Carbon Balance in a Long Island Sound Tidal Marsh. Estuaries and Coasts, 35, 201-211. Barger N, D'antonio C, Ghneim T, Cuevas E (2003) Constraints to colonization and growth of the African grass, Melinis minutiflora, in a Venezuelan savanna. Plant Ecology, 167, 31-43. Barger NN, D'antonio CM, Ghneim T, Brink K, Cuevas E (2002) Nutrient Limitation to Primary Productivity in a Secondary Savanna in Venezuela1. Biotropica, 34, 493-501 Bennett LT, Adams MA (2001) Response of a perennial grassland to nitrogen and phosphorus additions in sub-tropical, semi-arid Australia. Journal of Arid Environments, 48, 289-308. Blair BC, Perfecto I (2008) Root proliferation and nutrient limitations in a Nicaraguan rain forest. Caribbean Journal of Science, 44, 36-42 Boelman NT, Stieglitz M, Rueth HM, Sommerkorn M, Griffin KL, Shaver GR, Gamon JA (2003) Response of NDVI, biomass, and ecosystem gas exchange to long-term warming and fertilization in wet sedge tundra. Oecologia, 135, 414-421. Bowman WD, Theodose TA, Schardt JC, Conant RT (1993) Constraints of Nutrient Availability on Primary Production in Two Alpine Tundra Communities. Ecology, 74, 20852097. Bret-Harte MS, Garc a EA, Sacr VM, Whorley JR, Wagner JL, Lippert SC, Chapin FS (2004) Plant and soil responses to neighbour removal and fertilization in Alaskan tussock tundra. Journal of Ecology, 92, 635-647. Chalmers A, Mcintyre S, Whalley RDB, Reid N (2005) Grassland species response to soil disturbance and nutrient enrichment on the Northern Tablelands of New South Wales. Australian Journal of Botany, 53, 485-499. Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proceedings of the National Academy of Sciences, 103, 10316-10321. Corbin J, Avis P, Wilbur R (2003) The role of phosphorus availability in the response of soil nitrogen cycling, understory vegetation and arbuscular mycorrhizal inoculum potential to elevated nitrogen inputs. Water, Air, and Soil Pollution, 147, 141-162. Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytologist, 179, 829-836 D'antonio CM, Mack MC (2006) Nutrient Limitation in a Fire-derived, Nitrogen-rich Hawaiian Grassland1. Biotropica, 38, 458-467. Davidson EA, Carvalho CJRD, Vieira ICG et al. (2004) Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecological Applications, 14, S150-S163. Feller I, Mckee K, Whigham D, O'neill J (2003) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry, 62, 145-175. Feller IC (1995) Effects of Nutrient Enrichment on Growth and Herbivory of Dwarf Red Mangrove (Rhizophora Mangle). Ecological Monographs, 65, 477-505. Fynn RWS, O'connor TG (2005) Determinants of community organization of a South African mesic grassland. Journal of Vegetation Science, 16, 93-102. 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 Güsewell S, Koerselman W, Verhoeven JTA (2002) Time-dependent effects of fertilization on plant biomass in floating fens. Journal of Vegetation Science, 13, 705-718. Güsewell S, Koerselman W, Verhoeven JTA (2003) Biomass N:P ratios as indicators of nutrients limitation for plant populations in wetlands. Ecological Applications, 13, 372-384 Gleeson SK, Good RE (2003) Root allocation and multiple nutrient limitation in the New Jersey Pinelands. Ecology Letters, 6, 220-227 Gleeson SK, Good RE (2010) Root growth response to water and nutrients in the New Jersey Pinelands. Canadian Journal of Forest Research, 40, 167-172 Gordon C, Wynn JM, Woodin SJ (2001) Impacts of increased nitrogen supply on high Arctic heath: the importance of bryophytes and phosphorus availability. New Phytologist, 149, 461471 Gower S, Vitousek P (1989) Effects of nutrient amendments on fine root biomass in a primary successional forest in Hawai'i. Oecologia, 81, 566-568 Grogan P, Chapin FS, Iii (2000) Nitrogen limitation of production in a Californianannual grassland: The contribution of arbuscularmycorrhizae. Biogeochemistry, 49, 37-51 Haag RW (1974) Nutrient limitations to plant production in two tundra communities. Canadian Journal of Botany, 52, 103-116 Harcombe PA (1977) The Influence of Fertilization on Some Aspects of Succession in a Humid Tropical Forest. Ecology, 58, 1375-1383 Helmisaari H-S, Hallbäcken L (1999) Fine-root biomass and necromass in limed and fertilized Norway spruce (Picea abies (L.) Karst.) stands. Forest Ecology and Management, 119, 99110 Herbert D, Fownes J (1995) Phosphorus limitation of forest leaf area and net primary production on a highly weathered soil. Biogeochemistry, 29, 223-235 Herbert DA, Fownes JH, Vitousek PM (1999) Hurricane Damage to a Hawaiian Forest: Nutrient Supply Rate Affects Resistance and Resilience. Ecology, 80, 908-920 Hobbs RJ, Gulmon SL, Hobbs VJ, Mooney HA (1988) Effects of fertiliser addition and subsequent gopher disturbance on a serpentine annual grassland community. Oecologia, 75, 291-295 Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of Soil Resources on Plant Invasion and Community Structure in Californian Serpentine Grassland. Ecology, 71, 478-491 Jefferies RL, Perkins N (1977) The Effects on the Vegetation of the Additions of Inorganic Nutrients to Salt Marsh Soils at Stiffkey, Norfolk. Journal of Ecology, 65, 867-882 Kiehl K, Esselink P, Bakker JP (1997) Nutrient limitation and plant species composition in temperate salt marshes. Oecologia, 111, 325-330 Kirkham FW, Mountford JO, Wilkins RJ (1996) The Effects of Nitrogen, Potassium and Phosphorus Addition on the Vegetation of a Somerset Peat Moor Under Cutting Management. Journal of Applied Ecology, 33, 1013-1029 Koide RT, Huenneke LF, Hamburg SP, Mooney HA (1988) Effects of Applications of Fungicide, Phosphorus and Nitrogen on the Structure and Productivity of an Annual Serpentine Plant Community. Functional Ecology, 2, 335-344 Lawrence D (2001) Nitrogen and phosphorus enhance growth and luxury consumption of four secondary forest tree species in Borneo. Journal of Tropical Ecology, 17, 859-869 Mcgroddy ME, Silver WL, De Oliveira RC, De Mello WZ, Keller M (2008) Retention of phosphorus in highly weathered soils under a lowland Amazonian forest ecosystem. Journal 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 of Geophysical Research: Biogeosciences, 113, G04012 Mckell CM, Goodin C, Perrier E (1959) Annual range fertilization in relation to soil moisture depletion. Journal of Range Management Archives, 12, 189-193 Mirmanto E, Proctor J, Green J, Nagy L, Suriantata (1999) Effects of Nitrogen and Phosphorus Fertilization in a Lowland Evergreen Rainforest. Philosophical Transactions: Biological Sciences, 354, 1825-1829 Newbery DM, Chuyong GB, Green JJ, Songwe NC, Tchuenteu F, Zimmermann L (2002) Does low phosphorus supply limit seedling establishment and tree growth in groves of ectomycorrhizal trees in a central African rainforest? New Phytologist, 156, 297-311 Ngai JT, Jefferies RL (2004) Nutrient limitation of plant growth and forage quality in Arctic coastal marshes. Journal of Ecology, 92, 1001-1010 Niinemets , Kull K (2005) Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils. Acta Oecologica, 28, 345356 Øien D-I (2004) Nutrient limitation in boreal rich-fen vegetation: A fertilization experiment. Applied Vegetation Science, 7, 119-132 Olde Venterink H, Van Der Vliet RE, Wassen MJ (2001) Nutrient limitation along a productivity gradient in wet meadows. Plant and Soil, 234, 171-179 Ostertag R (2001) Effects of Nitrogen and Phosphorus Availability on Fine-Root Dynamics in Hawaiian Montane Forests. Ecology, 82, 485-499 Pauli D, Peintinger M, Schmid B (2002) Nutrient enrichment in calcareous fens: effects on plant species and community structure. Basic and Applied Ecology, 3, 255-266 Pietikäinen A, Kytöviita MM, Vuoti U (2005) Mycorrhiza and seedling establishment in a subarctic meadow: Effects of fertilization and defoliation. Journal of Vegetation Science, 16, 175-182 Raich J, Russell A, Crews T, Farrington H, Vitousek P (1996) Both nitrogen and phosphorus limit plant production on young Hawaiian lava flows. Biogeochemistry, 32, 1-14 Rejmánková E (2001) Effect of experimental phosphorus enrichment on oligotrophic tropical marshes in Belize, Central America. Plant and Soil, 236, 33-53 Sarmiento G, Da Silva MP, Naranjo ME, Pinillos M (2006) Nitrogen and phosphorus as limiting factors for growth and primary production in a flooded savanna in the Venezuelan Llanos. Journal of Tropical Ecology, 22, 203-212 Scowcroft PG, Silva JA (2005) Effects of phosphorus fertilization, seed source, and soil type on growth of Acacia koa. Journal of Plant Nutrition, 28, 1581-1603 Shaver GR, Bret-Harte MS, Jones MH, Johnstone J, Gough L, Laundre J, Chapin FS, Iii (2001) Species Composition Interacts with Fertilizer to Control Long-Term Change in Tundra Productivity. Ecology, 82, 3163-3181 Soudzilovskaia NA, Onipchenko VG, Cornelissen JHC, Aerts R (2005) Biomass production, N:P ratio and nutrient limitation in a Caucasian alpine tundra plant community. Journal of Vegetation Science, 16, 399-406 Stark S, Grellmann D (2002) Soil Microbial Responses to Herbivory in an Arctic Tundra Heath at Two Levels of Nutrient Availability. Ecology, 83, 2736-2744 Stevens GN, Jones RH (2006) Patterns in soil fertility and root herbivory interact to influence fine-root dynamics. Ecology, 87, 616-624 Tanner EVJ, Kapos V, Franco W (1992) Nitorgen and Phosphorus Fertilization Effects on Venezuelan Montane Forest Trunk Growth and Litterfall. Ecology, 73, 78-86 58 59 60 61 62 63 64 65 Tanner EVJ, Kapos V, Freskos S, Healey JR, Theobald AM (1990) Nitrogen and Phosphorus Fertilization of Jamaican Montane Forest Trees. Journal of Tropical Ecology, 6, 231-238 Turitzin SN (1982) Nutrient Limitations to Plant Growth in a California Serpentine Grassland. American Midland Naturalist, 107, 95-99 Van Der Hoek D, Van Mierlo Anita JEM, Van Groenendael JM (2004) Nutrient limitation and nutrient-driven shifts in plant species composition in a species-rich fen meadow. Journal of Vegetation Science, 15, 389-396 Van Wijnen HJ, Bakker JP (1999) Nitrogen and phosphorus limitation in a coastal barrier salt marsh: the implications for vegetation succession. Journal of Ecology, 87, 265-272 Verhoeven JTA, Schmitz MB (1991) Control of Plant Growth by Nitrogen and Phosphorus in Mesotrophic Fens. Biogeochemistry, 12, 135-148 Vitousek P, Farrington H (1997) Nutrient limitation and soil development: Experimental test of a biogeochemical theory. Biogeochemistry, 37, 63-75 Vitousek P, Walker L, Whiteaker L, Matson P (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry, 23, 197-215 Willems JH, Peet RK, Bik L (1993) Changes in chalk-grassland structure and species richness resulting from selective nutrient additions. Journal of Vegetation Science, 4, 203-212