How does biodiversity thrive in phosphorus-limited tropical forests

Ewuketu Linger , Richard T. Corlett , J. Aaron Hogan , Wenxing Long

Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) : 77

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Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) :77 DOI: 10.1007/s11676-026-02018-x
Review Article
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How does biodiversity thrive in phosphorus-limited tropical forests
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Abstract

Tropical forests, renowned for their exceptional biodiversity, often thrive despite inherently low soil phosphorus (P) availability. However, a comprehensive synthesis of the mechanisms that facilitate the coexistence of diverse species, and how these mechanisms respond to P addition, remains poorly understood. This review consolidates research findings on how tropical forest biodiversity is sustained under low P conditions, how P addition influences the overall biodiversity system, identifies research gaps, and suggests future directions. The relationship between P and biodiversity is complex: while P-limited forests support high diversity, P addition may lead to species disappearance, raising the question of why some forests that maintain high species diversity under P limitation continue to do so, while others experience a decline in diversity following P addition. Despite P limitation, forests can support high species diversity through adaptive strategies such as resource partitioning and P-use efficiency, which enable diverse communities to flourish. In low-P environments, species conserve P through resorption from older tissues and allocation to leaves, promoting photosynthesis and growth. These species exhibit lower specific leaf area and higher leaf dry matter content. While functional diversity is constrained, species diversity remains high as species adopt similar strategies. Specialized root traits, including finer roots and mycorrhizal symbioses, facilitate P uptake in low-P soils. However, P addition may lead to competitive exclusion, with species adapted to P-rich conditions outcompeting low-P specialists. Some species may dominate early successional stages by rapidly utilizing available P, suppressing other species, and reducing biodiversity over time. Anthropogenic P additions, such as agricultural fertilization and erosion, can intensify this effect, further decreasing species diversity and altering community composition, including fauna and microbial components of the forest. Due to the complexity and variability of tropical environments, critical knowledge gaps remain in understanding how diverse forest components, soil organisms, and environmental conditions interact with P addition, particularly at local and regional scales. Long-term studies, especially in less accessible or underfunded tropical regions, are essential to improve understanding of species interactions, resource partitioning, and biodiversity functioning under P-limitation.

Keywords

Adaptive strategies / Biodiversity trade-offs / Functional diversity / Nutrient cycling / Nutrient limitation

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Ewuketu Linger, Richard T. Corlett, J. Aaron Hogan, Wenxing Long. How does biodiversity thrive in phosphorus-limited tropical forests. Journal of Forestry Research, 2026, 37(1): 77 DOI:10.1007/s11676-026-02018-x

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References

[1]

Aanderud ZT, Shuldman MI, Drenovsky RE, Richards JH. Shrub-interspace dynamics alter relationships between microbial community composition and belowground ecosystem characteristics. Soil Biol Biochem. 2008, 40(9): 2206-2216.

[2]

Aguirre-Gutiérrez J, Malhi Y, Lewis SL, Fauset S, Adu-Bredu S, Affum-Baffoe K, Baker TR, Gvozdevaite A, Hubau W, Moore S, Peprah T, Ziemińska K, Phillips OL, Oliveras I. Long-term droughts may drive drier tropical forests towards increased functional, taxonomic and phylogenetic homogeneity. Nat Commun. 2020, 11: 3346.

[3]

Allsup C, Marquardt S, Lankau R. Mycorrhizal driven positive feedbacks and forest resilience to reduced rainfall. Fungal Ecol. 2023, 65. 101280

[4]

Ao G, Feng JG, Han MG, Wang XD, Tang M, Ma SH, Zhu B. Responses of root and soil phosphatase activity to nutrient addition differ between primary and secondary tropical montane forests. Rhizosphere. 2022, 24. 100610

[5]

Aoyagi R, Kitayama K, Turner BL. How do tropical tree species maintain high growth rates on low-phosphorus soils?. Plant Soil. 2022, 480(1–2): 31-56.

[6]

Balandier P, Mårell A, Prévosto B, Vincenot L. Tamm review: forest understorey and overstorey interactions: so much more than just light interception by trees. Ecol Manag. 2022, 526. 120584

[7]

Baraloto C, Bonal D, Goldberg DE. Differential seedling growth response to soil resource availability among nine neotropical tree species. J Trop Ecol. 2006, 225487-497.

[8]

Basak BB, Sarkar B, Saha A, Sarkar A, Mandal S, Biswas JK, Wang HL, Bolan NS. Revamping highly weathered soils in the tropics with biochar application: what we know and what is needed. Sci Total Environ. 2022, 822. 153461

[9]

Beauregard MS, Hamel C, Atul-Nayyar S-A. Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol. 2010, 59(2): 379-389.

[10]

Benner JW, Vitousek PM. Development of a diverse epiphyte community in response to phosphorus fertilization. Ecol Lett. 2007, 10(7): 628-636.

[11]

Blubaugh CK, Carpenter-Boggs L, Reganold JP, Snyder WE. Herbivore-herbivore interactions complicate links between soil fertility and pest resistance. Basic Appl Ecol. 2021, 52: 57-67.

[12]

Bonan GB. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Sci. 2008, 320(5882): 1444-1449.

[13]

Buscot F, Munch JC, Charcosset JY, Gardes M, Nehls U, Hampp R. Recent advances in exploring physiology and biodiversity of ectomycorrhizas highlight the functioning of these symbioses in ecosystems. FEMS Microbiol Rev. 2000, 24(5): 601-614.

[14]

Coleman DC, Geisen S, Wall DH. Eldor A, Paul I, Serita D. Soil fauna: occurrence biodiversity and roles in ecosystem function. Frey soil microbiology ecology and biochemistry. 2024, Amsterdam, Elsevier131159.

[15]

Coley PD, Bryant JP, Chapin FSIII. Resource availability and plant antiherbivore defense. Sci. 1985, 230(4728): 895-899.

[16]

Condit R, Engelbrecht BMJ, Pino D, Pérez R, Turner BL. Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci. 2013, 110(13): 5064-5068.

[17]

Cope OL, Lindroth RL, Helm A, Keefover-Ring K, Kruger EL. Trait plasticity and trade-offs shape intra-specific variation in competitive response in a foundation tree species. New Phytol. 2021, 230(2): 710-719.

[18]

Cui EQ, Lu RL, Xu XN, Sun HF, Qiao Y, Ping JY, Qiu SY, Lin YH, Bao JH, Yong YT, Zheng ZM, Yan ER, Xia JY. Soil phosphorus drives plant trait variations in a mature subtropical forest. Glob Change Biol. 2022, 28(10): 3310-3320.

[19]

Cunha HFV, Andersen KM, Lugli LF, Santana FD, Aleixo IF, Moraes AM, Garcia S, Di Ponzio R, Mendoza EO, Brum B, Rosa JS, Cordeiro AL, Portela BTT, Ribeiro G, Coelho SD, de Souza ST, Silva LS, Antonieto F, Pires M, Salomão AC, Miron AC, de Assis RL, Domingues TF, Aragão LEOC, Meir P, Camargo JL, Manzi AO, Nagy L, Mercado LM, Hartley IP, Quesada CA. Direct evidence for phosphorus limitation on amazon forest productivity. Nat. 2022, 608(7923): 558-562.

[20]

Cusack DF, Addo-Danso SD, Agee EA, Andersen KM, Arnaud M, Batterman SA, Brearley FQ, Ciochina MI, Cordeiro AL, Dallstream C, Diaz-Toribio MH, Dietterich LH, Fisher JB, Fleischer K, Fortunel C, Fuchslueger L, Guerrero-Ramírez NR, Kotowska MM, Lugli LF, Marín C, McCulloch LA, Maeght JL, Metcalfe D, Norby RJ, Oliveira RS, Powers JS, Reichert T, Smith SW, Smith-Martin CM, Soper FM, Toro L, Umaña MN, Valverde-Barrantes O, Weemstra M, Werden LK, Wong M, Wright CL, Wright SJ, Yaffar D. Tradeoffs and synergies in tropical forest root traits and dynamics for nutrient and water acquisition: field and modeling advances. Front Glob Change. 2021, 4. 704469

[21]

Dai ZM, Liu GF, Chen HH, Chen CR, Wang JK, Ai SY, Wei D, Li DM, Ma B, Tang CX, Brookes PC, Xu JM. Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. ISME J. 2020, 14(3): 757-770.

[22]

Davidson EA, de Reis Carvalho CJ, Vieira ICG, de O Figueiredo R, Moutinho P, Yoko Ishida F, dos Primo Santos MT, Benito Guerrero J, Kalif K, Tuma Sabá R. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol Appl. 2004, 14(4): 150-163.

[23]

de Bang TC, Husted S, Laursen KH, Persson DP, Schjoerring JK. The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol. 2021, 229(5): 2446-2469.

[24]

de Britto Costa P, Staudinger C, Veneklaas EJ, Oliveira RS, Lambers H. Root positioning and trait shifts in hibbertia racemosa as dependent on its neighbour’s nutrient-acquisition strategy. Plant Cell Environ. 2021, 44(4): 1257-1267.

[25]

DeForest JL, Moorhead DL. Effects of elevated pH and phosphorus fertilizer on soil C, N and P enzyme stoichiometry in an acidic mixed mesophytic deciduous forest. Soil Biol Biochem. 2020, 150. 107996

[26]

Ding XX, Liu GL, Fu SL, Chen HYH. Tree species composition and nutrient availability affect soil microbial diversity and composition across forest types in subtropical China. CATENA. 2021, 201. 105224

[27]

Du EZ, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu XH, Jackson RB. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci. 2020, 13(3): 221-226.

[28]

Dueñas JF, Camenzind T, Roy J, Hempel S, Homeier J, Suárez JP, Rillig MC. Moderate phosphorus additions consistently affect community composition of arbuscular mycorrhizal fungi in tropical montane forests in southern ecuador. New Phytol. 2020, 227(5): 1505-1518.

[29]

Ellison D, Morris CE, Locatelli B, Sheil D, Cohen J, Murdiyarso D, Gutierrez V, van Noordwijk M, Creed IF, Pokorny J, Gaveau D, Spracklen DV, Tobella AB, Ilstedt U, Teuling AJ, Gebrehiwot SG, Sands DC, Muys B, Verbist B, Springgay E, Sugandi Y, Sullivan CA. Trees, forests and water: cool insights for a hot world. Glob Environ Change. 2017, 43: 51-61.

[30]

Elwood JW, Newbold JD, Trimble AF, Stark RW. The limiting role of phosphorus in a woodland stream ecosystem: effects of P enrichment on leaf decomposition and primary producers. Ecol. 1981, 62(1): 146-158.

[31]

Fang Z, Yu HL, Li CH, Wang B, Jiao F, Huang JY. Long-term phosphorus addition alters plant community composition but not ecosystem stability of a nitrogen-enriched desert steppe. Sci Total Environ. 2023, 879. 163033

[32]

Felzenberg ER, Yang GA, Hagenzieker JG, Poindexter JS. Physiologic, morphologic and behavioral responses of perpetual cultures of Caulobacter crescentus to carbon, nitrogen and phosphorus limitations. J Ind Microbiol Biotechnol. 1996, 17(3–4): 235-252.

[33]

Finlay RD. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot. 2008, 59(5): 1115-1126.

[34]

Fisher JL, Veneklaas EJ, Lambers H, Loneragan WA. Enhanced soil and leaf nutrient status of a Western Australian Banksia woodland community invaded by Ehrharta calycina and Pelargonium capitatum. Plant Soil. 2006, 284(1–2): 253-264.

[35]

Fleming PA, Wentzel JJ, Dundas SJ, Kreplins TL, Craig MD, Hardy GE. Global meta-analysis of tree decline impacts on fauna. Biol Rev. 2021, 96(5): 1744-1768.

[36]

Fortier R, Wright SJ. Nutrient limitation of plant reproduction in a tropical moist forest. Ecol. 2021, 102(10. e03469

[37]

Freire . The origins of photosynthetic systems: clues from the phosphorus and sulphur chemical scenarios. Biosyst. 2023, 226. 104873

[38]

Gao C, Xu L, Montoya L, Madera M, Hollingsworth J, Chen L, Purdom E, Singan V, Vogel J, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG, Taylor JW. Co-occurrence networks reveal more complexity than community composition in resistance and resilience of microbial communities. Nat Commun. 2022, 13. 3867

[39]

Georg Joergensen R, Scheu S. Response of soil microorganisms to the addition of carbon, nitrogen and phosphorus in a forest Rendzina. Soil Biol Biochem. 1999, 316): 859-866.

[40]

Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJA, Laurance WF, Lovejoy TE, Sodhi NS. Primary forests are irreplaceable for sustaining tropical biodiversity. Nat. 2011, 478(7369): 378-381.

[41]

Gómez-Aparicio L, Domínguez-Begines J, Villa-Sanabria E, García LV, Muñoz-Pajares AJ. Tree decline and mortality following pathogen invasion alters the diversity, composition and network structure of the soil microbiome. Soil Biol Biochem. 2022, 166. 108560

[42]

Gough L, Osenberg CW, Gross KL, Collins SL. Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos. 2000, 89(3): 428-439.

[43]

Gu HJ, Wang H, Liu M, Shangguan ZJ, Shi HJ, Xu W, Ren F, Zhu JX, He JS. Leaf N: P stoichiometry overrides the effect of individual nutrient content on insect herbivore population dynamics in a Tibetan Alpine grassland. Agric Ecosyst Environ. 2022, 336. 108032

[44]

Guilbeault-Mayers X, Laliberté E. Root phosphatase activity is coordinated with the root conservation gradient across a phosphorus gradient in a lowland tropical forest. New Phytol. 2024, 243(2): 636-647.

[45]

Han XJ, Zhao YQ, Chen YJ, Xu J, Jiang C, Wang XQ, Zhuo RY, Lu MZ, Zhang J. Lignin biosynthesis and accumulation in response to abiotic stresses in woody plants. Res. 2022, 2. 9

[46]

Harvey MG, Bravo GA, Claramunt S, Cuervo AM, Derryberry GE, Battilana J, Seeholzer GF, McKay JS, O’Meara BC, Faircloth BC, Edwards SV, Pérez-Emán J, Moyle RG, Sheldon FH, Aleixo A, Smith BT, Chesser RT, Silveira LF, Cracraft J, Brumfield RT, Derryberry EP. The evolution of a tropical biodiversity hotspot. Sci. 2020, 370(6522): 1343-1348.

[47]

Hernández-Blanco M, Costanza R, Chen HJ, de Groot D, Jarvis D, Kubiszewski I, Montoya J, Sangha K, Stoeckl N, Turner K, van ‘t Hoff V. Ecosystem health, ecosystem services, and the well-being of humans and the rest of nature. Glob Change Biol. 2022, 28(17): 5027-5040.

[48]

Hölzl G, Dörmann P. Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res. 2007, 46(5): 225-243.

[49]

Hong PB, Schmid B, De Laender F, Eisenhauer N, Zhang XW, Chen HZ, Craven D, De Boeck HJ, Hautier Y, Petchey OL, Reich PB, Steudel B, Striebel M, Thakur MP, Wang SP. Biodiversity promotes ecosystem functioning despite environmental change. Ecol Lett. 2022, 25(2): 555-569.

[50]

Hu DD, Wang MT, Zheng Y, Lv M, Zhu GJ, Zhong QL, Cheng DL. Leaf litter phosphorus regulates the soil meso- and micro-faunal contribution to home-field advantage effects on litter decomposition along elevation gradients. CATENA. 2021, 207. 105673

[51]

Huang J, Liu L, Liu JX, Zhang W, Wang SH, Ye Q, Mo JM, Zheng MH. Seven years phosphorus addition has no effect on soil acidity in two tropical plantations. Ecol Manag. 2023, 532. 120822

[52]

Huston M. A general hypothesis of species diversity. Am Nat. 1979, 113(1): 81-101.

[53]

Iqbal Z, Iqbal MS, Hashem A, AbdAllah EF, Ansari MI. Plant defense responses to biotic stress and its interplay with fluctuating dark/light conditions. Front Plant Sci. 2021, 12. 631810

[54]

Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M. High plant diversity is needed to maintain ecosystem services. Nat. 2011, 477(7363): 199-202.

[55]

Kang HB, Xue Y, Cui YX, Moorhead DL, Lambers H, Wang DX. Nutrient limitation mediates soil microbial community structure and stability in forest restoration. Sci Total Environ. 2024, 935. 173266

[56]

Lambers H. Phosphorus acquisition and utilization in plants. Annu Rev Plant Biol. 2022, 73: 17-42.

[57]

Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible WR, Stitt M, Teste F, Turner BL. Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol. 2012, 196(4): 1098-1108.

[58]

Lambers H, Albornoz F, Kotula L, Laliberté E, Ranathunge K, Teste FP, Zemunik G. How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil. 2018, 424(1–2): 11-33.

[59]

Lewis SL. Tropical forests and the changing earth system. Philos Trans R Soc Lond B Biol Sci. 2006, 361(1465): 195-210.

[60]

Lewis SL, Malhi Y, Phillips OL. Fingerprinting the impacts of global change on tropical forests. Philos Trans R Soc Lond B Biol Sci. 2004, 359(1443): 437-462.

[61]

Lewis SL, Edwards DP, Galbraith D. Increasing human dominance of tropical forests. Sci. 2015, 349(6250): 827-832.

[62]

Li J, Li ZA, Wang FM, Zou B, Chen Y, Zhao J, Mo QF, Li YW, Li XB, Xia HP. Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fertil Soils. 2015, 51(2): 207-215.

[63]

Li Y, Schuldt A, Ebeling A, Eisenhauer N, Huang YY, Albert G, Albracht C, Amyntas A, Bonkowski M, Bruelheide H, Bröcher M, Chesters D, Chen J, Chen YN, Chen JT, Ciobanu M, Deng XL, Fornoff F, Gleixner G, Guo LD, Guo PF, Heintz-Buschart A, Klein AM, Lange M, Li S, Li Q, Li YB, Luo AR, Meyer ST, von Oheimb G, Rutten G, Scholten T, Solbach MD, Staab M, Wang MQ, Zhang NL, Zhu CD, Schmid B, Ma KP, Liu XJ. Plant diversity enhances ecosystem multifunctionality via multitrophic diversity. Nat Ecol Evol. 2024, 8(11): 2037-2047.

[64]

Liang GH, Butler OM, Warren CR. Lipid profiles of plants and soil microbial communities are shaped by soil parent material in Australian sclerophyll forests. Plant Soil. 2024, 498(1–2): 39-55.

[65]

Liu D. Root developmental responses to phosphorus nutrition. J Integr Plant Biol. 2021, 63(6): 1065-1090.

[66]

Liu L, Gundersen P, Zhang T, Mo JM. Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem. 2012, 44(1): 31-38.

[67]

Liu XJ, Tan ND, Zhou GY, Zhang DQ, Zhang QM, Liu SZ, Chu GW, Liu JX. Plant diversity and species turnover co-regulate soil nitrogen and phosphorus availability in Dinghushan forests, Southern China. Plant Soil. 2021, 464(1–2): 257-272.

[68]

Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA. Biodiversity and ecosystem functioning: current knowledge and future challenges. Sci. 2001, 294(5543): 804-808.

[69]

Løvdal T, Skjoldal EF, Heldal M, Norland S, Thingstad TF. Changes in morphology and elemental composition of Vibrio splendidus along a gradient from carbon-limited to phosphate-limited growth. Microb Ecol. 2008, 55(1): 152-161.

[70]

Lugli LF, Rosa JS, Andersen KM, Di Ponzio R, Almeida RV, Pires M, Cordeiro AL, Cunha HFV, Martins NP, Assis RL, Moraes ACM, Souza ST, Aragão LEOC, Camargo JL, Fuchslueger L, Schaap KJ, Valverde-Barrantes OJ, Meir P, Quesada CA, Mercado LM, Hartley IP. Rapid responses of root traits and productivity to phosphorus and cation additions in a tropical lowland forest in Amazonia. New Phytol. 2021, 230(1): 116-128.

[71]

Lum MR, Hirsch AM. Roots and their symbiotic microbes: strategies to obtain nitrogen and phosphorus in a nutrient-limiting environment. J Plant Growth Regul. 2002, 21(4): 368-382.

[72]

Luo RY, Kuzyakov Y, Zhu B, Qiang W, Zhang Y, Pang XY. Phosphorus addition decreases plant lignin but increases microbial necromass contribution to soil organic carbon in a subalpine forest. Glob Change Biol. 2022, 28(13): 4194-4210.

[73]

Luo XZ, Elrys AS, Zhang LL, Ibrahim MM, Liu Y, Fu SL, Yan JH, Ye Q, Wen DZ, Hou EQ. The global fate of inorganic phosphorus fertilizers added to terrestrial ecosystems. One Earth. 2024, 7(8): 1402-1413.

[74]

Ma SH, Chen GP, Tian D, Du EZ, Xiao W, Jiang L, Zhou Z, Zhu JL, He HB, Zhu B, Fang JY. Effects of seven-year nitrogen and phosphorus additions on soil microbial community structures and residues in a tropical forest in Hainan Island, China. Geoderma. 2020, 361. 114034

[75]

Ma XC, Geng QH, Zhang HG, Bian CY, Chen HYH, Jiang DL, Xu X. Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality. New Phytol. 2021, 229(5): 2957-2969.

[76]

Mahmoud SS, Croteau RB. Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci. 2002, 7(8): 366-373.

[77]

Maitra P, Zheng Y, Wang YL, Mandal D, PP, Gao C, Babalola BJ, Ji NN, Li XC, Guo LD. Phosphorus fertilization rather than nitrogen fertilization, growing season and plant successional stage structures arbuscular mycorrhizal fungal community in a subtropical forest. Biol Fertil Soils. 2021, 57(5): 685-697.

[78]

Malhi Y, Roberts JT, Betts RA, Killeen TJ, Li WH, Nobre CA. Climate change, deforestation, and the fate of the Amazon. Sci. 2008, 319(5860): 169-172.

[79]

Manu R, Corre MD, Aleeje A, Mwanjalolo MJG, Babweteera F, Veldkamp E, van Straaten O. Responses of tree growth and biomass production to nutrient addition in a semi-deciduous tropical forest in Africa. Ecol. 2022, 103(6. e3659

[80]

Mao QG, Chen H, Gurmesa GA, Gundersen P, Ellsworth DS, Gilliam FS, Wang C, Zhu F, Ye Q, Mo JM, Lu XK. Negative effects of long-term phosphorus additions on understory plants in a primary tropical forest. Sci Total Environ. 2021, 798. 149306

[81]

Massmann A, Cavaleri MA, Oberbauer SF, Olivas PC, Porder S. Foliar stoichiometry is marginally sensitive to soil phosphorus across a lowland tropical rainforest. Ecosyst. 2022, 251): 61-74.

[82]

Mayor JR, Wright SJ, Turner BL. Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol. 2014, 102(1): 36-44.

[83]

McLaughlin SB, Wimmer R. Tansley review no. 104: calcium physiology and terrestrial ecosystem processes. New Phytol. 1999, 142(3): 373-417.

[84]

Menge DNL, Hedin LO, Pacala SW. Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. PLoS ONE. 2012, 7(8. e42045

[85]

Mo QF, Li ZA, Sayer EJ, Lambers H, Li YW, Zou B, Tang JW, Heskel M, Ding YZ, Wang FM. Foliar phosphorus fractions reveal how tropical plants maintain photosynthetic rates despite low soil phosphorus availability. Funct Ecol. 2019, 333): 503-513.

[86]

Mo QF, Wang WJ, Lambers H, Chen YQ, Yu SQ, Wu CS, Fan YX, Zhou Q, Li ZA, Wang FM. Response of foliar mineral nutrients to long-term nitrogen and phosphorus addition in a tropical forest. Funct Ecol. 2021, 35(10): 2329-2341.

[87]

Moeneclaey I, Schelfhout S, Vanhellemont M, DeCock E, Van Coillie F, Verheyen K, Baeten L. Species ecological strategy and soil phosphorus supply interactively affect plant biomass and phosphorus concentration. Basic Appl Ecol. 2022, 62: 1-11.

[88]

Mouquet N, Gravel D, Massol F, Calcagno V. Extending the concept of keystone species to communities and ecosystems. Ecol Lett. 2013, 16(1): 1-8.

[89]

Nohrstedt . Response of coniferous forest ecosystems on mineral soils to nutrient additions: a review of Swedish experiences. Scand J Res. 2001, 16(6): 555-573.

[90]

Ostertag R, Verville JH. Fertilization with nitrogen and phosphorus increases abundance of non-native species in Hawaiian montane forests. Plant Ecol. 2002, 162(1): 77-90.

[91]

Ouchi T, Ibrahim AK, Latham GV. Seismicity and crustal structure in the orozco fracture zone: project rose phase II. J Geophys Res. 1982, 87(B10): 8501-8507.

[92]

Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao SL, Rautiainen A, Sitch S, Hayes D. A large and persistent carbon sink in the world’s forests. Sci. 2011, 333(6045): 988-993.

[93]

Pan YJ, Song YP, Zhao L, Chen PF, Bu CH, Liu P, Zhang DQ. The genetic basis of phosphorus utilization efficiency in plants provide new insight into woody perennial plants improvement. Int J Mol Sci. 2022, 23(4): 2353.

[94]

Pillay R, Venter M, Aragon-Osejo J, González-del-Pliego P, Hansen AJ, Watson JE, Venter O. Tropical forests are home to over half of the world’s vertebrate species. Front Ecol Environ. 2022, 20110-15.

[95]

Pirttilä AM, Brusila V, Koskimäki JJ, Wäli PR, Ruotsalainen AL, Mutanen M, Markkola AM. Exchange of microbiomes in plant-insect herbivore interactions. Mbio. 2023, 14(2): e03210-e03222.

[96]

Poudyal S, Owen JS, Sharkey TD, Fernandez RT, Cregg B. Phosphorus requirement for biomass accumulation is higher compared to photosynthetic biochemistry for three ornamental shrubs. Sci Hortic. 2021, 275. 109719

[97]

Rapport DJ, Costanza R, McMichael AJ. Assessing ecosystem health. Trends Ecol Evol. 1998, 13(10): 397-402.

[98]

Raven PH, Gereau RE, Phillipson PB, Chatelain C, Jenkins CN, Ulloa Ulloa C. The distribution of biodiversity richness in the tropics. Sci Adv. 2020, 6(37. eabc6228

[99]

Reichert T, Rammig A, Fuchslueger L, Lugli LF, Quesada CA, Fleischer K. Plant phosphorus-use and-acquisition strategies in Amazonia. New Phytol. 2022, 2344): 1126-1143.

[100]

Roberts P, Hamilton R, Piperno DR. Tropical forests as key sites of the “Anthropocene”: past and present perspectives. Proc Natl Acad Sci. 2021, 118(40. e2109243118

[101]

Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL. Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol. 2012, 1002): 309-316.

[102]

Sarmiento G, Goldstein G, Meinzer F. Adaptive strategies of woody species in neotropical savannas. Biol Rev. 1985, 60(3): 315-355.

[103]

Schmid KM, Ohlrogge JB. Vance DE, Vance JE. Chapter 14 lipid metabolism in plants. New compr biochem. 1996, Amsterdam, Elsevier363389

[104]

Seabloom EW, Adler PB, Alberti J, Biederman L, Buckley YM, Cadotte MW, Collins SL, Dee L, Fay PA, Firn J, Hagenah N, Harpole WS, Hautier Y, Hector A, Hobbie SE, Isbell F, Knops JMH, Komatsu KJ, Laungani R, MacDougall A, McCulley RL, Moore JL, Morgan JW, Ohlert T, Prober SM, Risch AC, Schuetz M, Stevens CJ, Borer ET. Increasing effects of chronic nutrient enrichment on plant diversity loss and ecosystem productivity over time. Ecol. 2021, 102(2. e03218

[105]

Segar J, Pereira HM, Baeten L, Bernhardt-Römermann M, De Frenne P, Fernández N, Gilliam FS, Lenoir J, Ortmann-Ajkai A, Verheyen K, Waller D, Teleki B, Brunet J, Chudomelová M, Decocq G, Dirnböck T, Hédl R, Heinken T, Jaroszewicz B, Kopecký M, Macek M, Máliš F, Naaf T, Orczewska A, Reczynska K, Schmidt W, Šebesta J, Stachurska-Swakoń A, Standovár T, Swierkosz K, Vild O, Wulf M, Staude IR. Divergent roles of herbivory in eutrophying forests. Nat Commun. 2022, 13. 7837

[106]

Sengupta U, Krishna S. More is not always better: impact of nutrient-addition on floral traits important for buzz pollination. Acta Oecol. 2023, 121. 103957

[107]

Shao XL, Zhang Q, Yang XT. Spatial patterns of insect herbivory within a forest landscape: the role of soil type and forest stratum. Ecosyst. 2021, 8. 69

[108]

Siebers M, Dörmann P, Hölzl G. Membrane remodelling in phosphorus-deficient plants. Phosphorus Metab Plants. 2015, 48: 237-264.

[109]

Sitters J, Wubs ERJ, Bakker ES, Crowther TW, Adler PB, Bagchi S, Bakker JD, Biederman L, Borer ET, Cleland EE, Eisenhauer N, Firn J, Gherardi L, Hagenah N, Hautier Y, Hobbie SE, Knops JMH, MacDougall AS, McCulley RL, Moore JL, Mortensen B, Peri PL, Prober SM, Riggs C, Risch AC, Schütz M, Seabloom EW, Siebert J, Stevens CJ, Veen GFC. Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands. Glob Change Biol. 2020, 264): 2060-2071.

[110]

Sun F, Song CJ, Wang M, Lai DYF, Tariq A, Zeng FJ, Zhong QP, Wang FM, Li ZA, Peng CL. Long-term increase in rainfall decreases soil organic phosphorus decomposition in tropical forests. Soil Biol Biochem. 2020, 151. 108056

[111]

Tao Y, Zhou XB, Li YG, Liu HL, Zhang YM. Short-term N and P additions differentially alter the multiple functional traits and trait associations of a desert ephemeral plant in China. Environ Exp Bot. 2022, 200. 104932

[112]

Teste FP, Lambers H, Enowashu EE, Laliberté E, Marhan S, Kandeler E. Soil microbial communities are driven by the declining availability of cations and phosphorus during ecosystem retrogression. Soil Biol Biochem. 2021, 163. 108430

[113]

Thuma JA, Duff C, Pitera M, Januario N, Orians CM, Starks PT. Nutrient enrichment and rainfall affect plant phenology and floral resource availability for pollinators. Front Ecol Evol. 2023, 11. 1150736

[114]

Treseder KK, Allen MF. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol. 2002, 155(3): 507-515.

[115]

Turner BL, Brenes-Arguedas T, Condit R. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nat. 2018, 555(7696): 367-370.

[116]

Umaña MN, Condit R, Pérez R, Turner BL, Wright SJ, Comita LS. Shifts in taxonomic and functional composition of trees along rainfall and phosphorus gradients in central Panama. J Ecol. 2021, 109(1): 51-61.

[117]

Usman M, Ho-Plágaro T, Frank HER, Calvo-Polanco M, Gaillard I, Garcia K, Zimmermann SD. Mycorrhizal symbiosis for better adaptation of trees to abiotic stress caused by climate change in temperate and boreal forests. Front Glob Change. 2021, 4. 742392

[118]

Valencia E, de Bello F, Galland T, Adler PB, Lepš J, E-Vojtkó A, van Klink R, Carmona CP, Danihelka J, Dengler J, Eldridge DJ, Estiarte M, García-González R, Garnier E, Gómez-García D, Harrison SP, Herben T, Ibáñez R, Jentsch A, Juergens N, Kertész M, Klumpp K, Louault F, Marrs RH, Ogaya R, Ónodi G, Pakeman RJ, Pardo I, Pärtel M, Peco B, Peñuelas J, Pywell RF, Rueda M, Schmidt W, Schmiedel U, Schuetz M, Skálová H, Šmilauer P, Šmilauerová M, Smit C, Song MH, Stock M, Val J, Vandvik V, Ward D, Wesche K, Wiser SK, Woodcock BA, Young TP, Yu FH, Zobel M, Götzenberger L. Synchrony matters more than species richness in plant community stability at a global scale. Proc Natl Acad Sci. 2020, 117(39): 24345-24351.

[119]

Van Langenhove L, Janssens IA, Verryckt L, Brechet L, Hartley IP, Stahl C, Courtois E, Urbina I, Grau O, Sardans J, Peguero G, Gargallo-Garriga A, Peñuelas J, Vicca S. Rapid root assimilation of added phosphorus in a lowland tropical rainforest of French Guiana. Soil Biol Biochem. 2020, 140. 107646

[120]

Vitousek PM, Porder S, Houlton BZ, Chadwick OA. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl. 2010, 20(1): 5-15.

[121]

Wahab A, Muhammad M, Munir A, Abdi G, Zaman W, Ayaz A, Khizar C, Reddy SPP. Role of arbuscular mycorrhizal fungi in regulating growth, enhancing productivity, and potentially influencing ecosystems under abiotic and biotic stresses. Plants. 2023, 12(17): 3102.

[122]

Wan NF, Zheng XR, Fu LW, Kiær LP, Zhang ZJ, Chaplin-Kramer R, Dainese M, Tan JQ, Qiu SY, Hu YQ, Tian WD, Nie M, Ju RT, Deng JY, Jiang JX, Cai YM, Li B. Global synthesis of effects of plant species diversity on trophic groups and interactions. Nat Plants. 2020, 65503-510.

[123]

Wang C, Mori T, Mao QG, Zhou KJ, Wang ZH, Zhang YQ, Mo H, Lu XK, Mo JM. Long-term phosphorus addition downregulates microbial investments on enzyme productions in a mature tropical forest. J Soils Sediments. 2020, 20(2): 921-930.

[124]

Wang LL, Ren F, Zhang C, Huang XJ, Zhang ZH, He JS, Yang YP, Duan YW. The effects of changes in flowering plant composition caused by nitrogen and phosphorus enrichment on plant–pollinator interactions in a Tibetan Alpine grassland. Front Plant Sci. 2022, 13. 964109

[125]

Wardle DA, Zackrisson O (2005) Effects of species and functional group loss on island ecosystem properties. Nature 435:806–810. https://doi.org/10.1038/nature03611

[126]

Wardle DA, Barker GM, Yeates GW, Bonner KI, Ghani A. Introduced browsing mammals in New Zealand natural forests: aboveground and belowground consequences. Ecol Monogr. 2001, 71(4): 587-614.

[127]

Wassen MJ, Schrader J, van Dijk J, Eppinga MB. Phosphorus fertilization is eradicating the niche of northern Eurasia’s threatened plant species. Nat Ecol Evol. 2021, 5(1): 67-73.

[128]

Wei SZ, Tie LH, Liao J, Liu X, Du ML, Lan SX, Li XR, Li CS, Zhan HC, Huang CD. Nitrogen and phosphorus co-addition stimulates soil respiration in a subtropical evergreen broad-leaved forest. Plant Soil. 2020, 450(1–2): 171-182.

[129]

Woodrow IE, Berry JA. Enzymatic regulation of photosynthetic CO2, fixation in C3 plants. Annu Rev Plant Physiol Plant Mol Biol. 1988, 39: 533-594.

[130]

Wright SJ (2019) Plant responses to nutrient addition experiments conducted in tropical forests. Ecol Monogr 89:e01382. https://doi.org/10.1002/ecm.1382

[131]

Wright SJ, Turner BL, Yavitt JB et al (2018) Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology 99:1129–1138. https://doi.org/10.1002/ecy.2193

[132]

Xia Y, Peñuelas J, Sardans J, Zhong XJ, Xu LL, Yang ZJ, Yang YS, Yang LM, Yue K, Fan YX. Phosphorus addition accelerates soil organic carbon mineralization by desorbing organic carbon and increasing microbial activity in subtropical forest soils. Appl Soil Ecol. 2024, 193. 105166

[133]

Xiao RX, Zou YR, Guo XR, Li H, Lu H. Fatty acid desaturases (FADs) modulate multiple lipid metabolism pathways to improve plant resistance. Mol Biol Rep. 2022, 49(10): 9997-10011.

[134]

Yan H, Freschet GT, Wang HM, Hogan JA, Li SG, Valverde-Barrantes OJ, Fu XL, Wang RL, Dai XQ, Jiang L, Meng SW, Yang FT, Zhang MM, Kou L. Mycorrhizal symbiosis pathway and edaphic fertility frame root economics space among tree species. New Phytol. 2022, 234(5): 1639-1653.

[135]

Yan L, Tang D, Pang JY, Lambers H. Root carboxylate release is common in phosphorus-limited forest ecosystems in China: using leaf manganese concentration as a proxy. Plant Soil. 2025, 508(1–2): 143-158.

[136]

Yang LM, Yang ZJ, Zhong XJ, Xu C, Lin YY, Fan YX, Wang MH, Chen GS, Yang YS. Decreases in soil P availability are associated with soil organic P declines following forest conversion in subtropical China. CATENA. 2021, 205. 105459

[137]

Yang XL, Wang XT, Xiao S, Liu ZY, Zhou XH, Du GZ, Liu K, Wang YJ, Chen SY, Nielsen UN. Dominant plants affect litter decomposition mainly through modifications of the soil microbial community. Soil Biol Biochem. 2021, 161. 108399

[138]

Yang XG, Shen KP, Xia TT, He YJ, Guo Y, Wu BL, Han X, Yan JW, Jiao M. Invasive and native plants differentially respond to exogenous phosphorus addition in root growth and nutrition regulated by arbuscular mycorrhizal fungi. Plants. 2023, 12(11. 2195

[139]

Yang SY, Lin WY, Hsiao YM, Chiou TJ. Milestones in understanding transport, sensing, and signaling of the plant nutrient phosphorus. Plant Cell. 2024, 365): 1504-1523.

[140]

Yetgin A. Exploring the dynamic nature of root plasticity and morphology in the face of changing environments. Ecol Front. 2024, 44(1): 112-119.

[141]

Yu RP, Li XX, Xiao ZH, Lambers H, Li L. Phosphorus facilitation and covariation of root traits in steppe species. New Phytol. 2020, 226(5): 1285-1298.

[142]

Yu QS, Ma SH, Ni XF, Ni XL, Guo ZM, Tan XP, Zhong MY, Abu Hanif M, Zhu JL, Ji CJ, Zhu B, Fang JY. Long-term phosphorus addition inhibits phosphorus transformations involved in soil arbuscular mycorrhizal fungi and acid phosphatase in two tropical rainforests. Geoderma. 2022, 425. 116076

[143]

Yu QS, Ni XF, Cheng XL, Ma SH, Tian D, Zhu B, Zhu JL, Ji CJ, Tang ZY, Fang JY. Foliar phosphorus allocation and photosynthesis reveal plants’ adaptative strategies to phosphorus limitation in tropical forests at different successional stages. Sci Total Environ. 2022, 846. 157456

[144]

Yuan Y, Li Y, Mou ZJ, Kuang LH, Wu WJ, Zhang J, Wang FM, Hui DF, Peñuelas J, Sardans J, Lambers H, Wang J, Kuang YW, Li ZA, Liu ZF. Phosphorus addition decreases microbial residual contribution to soil organic carbon pool in a tropical coastal forest. Glob Change Biol. 2021, 27(2): 454-466.

[145]

Zaret M, Kinkel L, Borer ET, Seabloom EW. Soil nutrients cause threefold increase in pathogen and herbivore impacts on grassland plant biomass. J Ecol. 2023, 111(8): 1629-1640.

[146]

Zhang JF, Li J, Fan YX, Mo QF, Li YW, Li YX, Li ZA, Wang FM. Effect of nitrogen and phosphorus addition on litter decomposition and nutrients release in a tropical forest. Plant Soil. 2020, 454(1–2): 139-153.

[147]

Zhang J, Zheng MH, Zhang YJ, Wang J, Shen H, Lin YB, Tang XL, Hui DF, Lambers H, Sardans J, Peñuelas J, Liu ZF. Soil phosphorus availability affects diazotroph communities during vegetation succession in lowland subtropical forests. Appl Soil Ecol. 2021, 166. 104009

[148]

Zhang JF, Zhou JG, Lambers H, Li YW, Li YX, Qin GM, Wang M, Wang J, Li ZA, Wang FM. Nitrogen and phosphorus addition exerted different influences on litter and soil carbon release in a tropical forest. Sci Total Environ. 2022, 832. 155049

[149]

Zhang GL, Bai JH, Zhai YJ, Jia J, Zhao QQ, Wang W, Hu XY. Microbial diversity and functions in saline soils: a review from a biogeochemical perspective. J Adv Res. 2024, 59: 129-140.

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