Abstract
Nutrient resorption and relative allocation of nutrient to younger leaves are important mechanisms of resource conservation and utilization for perennial plants. However, it remains unclear how grazing and soil nutrient levels, particularly phosphorus (P) availability, affect nutrient resorption and allocation by perennial species. We investigated the impacts of long-term grazing (i.e., the legacy effect of grazing intensity) and soil P fertilization on nitrogen (N) and P resorption and allocation by two dominant perennial species, Stipa grandis and Carex korshinskyi, in a semiarid grassland. Foliar N and P concentrations of both species increased with grazing intensity under both low and high P availability, except P concentrations under high P conditions. For S. grandis, N and P resorption efficiencies (NRE, PRE) increased with grazing intensity under low P conditions, but PRE decreased with increasing grazing intensity under high P conditions. For C. korshinskyi, grazing decreased NRE under low P conditions but increased NRE under high P conditions. Relative P allocation to younger leaves by the two species increased with grazing intensity under low and high P conditions. For both species, the relationship between nutrient resorption and allocation shifted from synergistic under low P conditions to neutral or trade-off relationships under high P conditions. Our findings demonstrate that grazing has strong effects on foliar N and P concentrations and resorption and allocation, but these effects depend on soil P availability and species identity. High levels of grazing intensity exacerbate P limitation and alter N and P resorption and allocation in both dominant species, except P resorption of Carex korshinskyi. This study provides important insights into the mechanisms underlying grazing impacts on ecosystem N and P cycling.
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The data used in this study are available from the corresponding author or on reasonable request.
References
Achat DL, Pousse N, Nicolas M, Augusto L (2018) Nutrient remobilization in tree foliage as affected by soil nutrients and leaf life span. Ecol Monogr 88:408–428. https://doi.org/10.1002/ecm.1300/full
Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608. https://doi.org/10.2307/2261481
Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. In: Fitter AH, Raffaelli DG (eds) Advances in Ecological Research, vol 30. Elsevier Academic Press Inc, San Diego
Aoyagi R, Kitayama K (2016) Nutrient allocation among plant organs across 13 tree species in three Bornean rain forests with contrasting nutrient availabilities. J Plant Res 129:675–684. https://doi.org/10.1007/s10265-016-0826-z
Bai YF, Cotrufo MF (2022) Grassland soil carbon sequestration: current understanding, challenges, and solutions. Science 377:603–608. https://doi.org/10.1126/science.abo2380
Bai YF, Han XG, Wu JG, Chen ZZ, Li LH (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184. https://doi.org/10.1038/nature02850
Bai YF, Wu JG, Clark CM, Naeem S, Pan QM, Huang JH, Zhang LX, Han XG (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Glob Change Biol 16:358–372. https://doi.org/10.1111/j.1365-2486.2009.01950.x
Bai YF, Wu JG, Clark CM, Pan QM, Zhang LX, Chen SP, Wang QB, Han XG (2012) Grazing alters ecosystem functioning and C:N:P stoichiometry of grasslands along a regional precipitation gradient. J Appl Ecol 49:1204–1215. https://doi.org/10.1111/j.1365-2664.2012.02205.x
Bai YF, Wu JG, Xing Q, Pan QM, Huang JH, Yang DL, Han XG (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153. https://doi.org/10.1890/07-0992.1
Chapin FS, Kedrowski RA (1983) Seasonal-changes in nitrogen and phosphorus fractions and autumn retrospection in evergreen and deciduous taiga trees. Ecology 64:376–391. https://doi.org/10.2307/1937083
Chen H, Reed SC, Lu XT, Xiao KC, Wang KL, Li DJ (2021) Coexistence of multiple leaf nutrient resorption strategies in a single ecosystem. Sci Total Environ 772:144951. https://doi.org/10.1016/j.scitotenv.2021.144951
Dale MP, Causton DR (1992) The ecophysiology of veronica-chamaedrys, v-montana and v-officinalis .4. Effects of shading on nutrient allocations - a field experiment. J Ecol 80:517–526. https://doi.org/10.2307/2260695
de Tombeur F, Laliberte E, Lambers H, Faucon M-P, Zemunik G, Turner BL, Cornelis J-T, Mahy G (2021) A shift from phenol to silica-based leaf defences during long-term soil and ecosystem development. Ecol Lett 24:984–995. https://doi.org/10.1111/ele.13713
Diaz C, Lemaitre T, Christ A, Azzopardi M, Kato Y, Sato F, Morot-Gaudry JF, Le Dily F, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147:1437–1449. https://doi.org/10.1104/pp.108.119040
Díaz S, Lavorel S, McIntyre S, Falczuk V, Casanoves F, Milchunas DG, Skarpe C, Rusch G, Sternberg M, Noy-Meir I, Landsberg J, Zhang W, Clark H, Campbell BD (2007) Plant trait responses to grazing - a global synthesis. Glob Change Biol 13:313–341. https://doi.org/10.1111/j.1365-2486.2006.01288.x
Diehl P, Mazzarino MJ, Funes F, Fontenla S, Gobbi M, Ferrari J (2003) Nutrient conservation strategies in native Andean-Patagonian forests. J Veg Sci 14:63–70. https://doi.org/10.1111/j.1654-1103.2003.tb02128.x
Eckstein RL, Karlsson PS, Weih M (1999) Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytol 143:177–189. https://doi.org/10.1046/j.1469-8137.1999.00429.x
Elser JJ, Hamilton A (2007) Stoichiometry and the new biology - the future is now. Plos Biol 5:1403–1405. https://doi.org/10.1371/journal.pbio.0050181
Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398. https://doi.org/10.1111/j.1365-2435.2010.01803.x
Estiarte M, Peñuelas J (2015) Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob Change Biol 21:1005–1017. https://doi.org/10.1111/gcb.12804
Fitter AH, Setters NL (1988) Vegetative and reproductive allocation of phosphorus and potassium in relation to biomass in 6 species of viola. J Ecol 76:617–636. https://doi.org/10.2307/2260563
Frank DA (2008) Ungulate and topographic control of nitrogen: phosphorus stoichiometry in a temperate grassland; soils, plants and mineralization rates. Oikos 117:591–601. https://doi.org/10.1111/j.0030-1299.2008.16220.x
Giese M, Brueck H, Gao YZ, Lin S, Steffens M, Kogel-Knabner I, Glindemann T, Susenbeth A, Taube F, Butterbach-Bahl K, Zheng XH, Hoffmann C, Bai YF, Han XG (2013) N balance and cycling of Inner Mongolia typical steppe: a comprehensive case study of grazing effects. Ecol Monogr 83:195–219. https://doi.org/10.1890/12-0114.1
Gleason SM, Read J, Ares A, Metcalfe DJ (2009) Phosphorus economics of tropical rainforest species and stands across soil contrasts in Queensland, Australia: understanding the effects of soil specialization and trait plasticity. Funct Ecol 23:1157–1166. https://doi.org/10.1111/j.1365-2435.2009.01575.x
Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. J Ecol 97:984–991. https://doi.org/10.1111/j.1365-2745.2009.01540.x
Hidaka A, Kitayama K (2011) Allocation of foliar phosphorus fractions and leaf traits of tropical tree species in response to decreased soil phosphorus availability on Mount Kinabalu, Borneo. J Ecol 99:849–857. https://doi.org/10.1111/j.1365-2745.2011.01805.x
Jia RY, Tang B, Sun Q, Song WJ, Wang Y, Bai YF (2023) Grazing intensity mediates effects of plant arbuscular mycorrhizal symbiosis on nitrogen and phosphorus resorption in semiarid grasslands. Plant Soil. https://doi.org/10.1007/s11104-023-06080-w
Killingbeck KT (1996) Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727. https://doi.org/10.2307/2265777
Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792. https://doi.org/10.1890/04-1830
Lambers H, Plaxton WC (2015) Phosphorus: back to the roots. Ann Plant Rev 48
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. https://doi.org/10.1016/j.tree.2007.10.008
Li WH, Xu FW, Zheng SX, Taube F, Bai YF (2017) Patterns and thresholds of grazing-induced changes in community structure and ecosystem functioning: species-level responses and the critical role of species traits. J Appl Ecol 54:963–975. https://doi.org/10.1111/1365-2664.12806
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316
Liu L, Cheng JH, Li YW, Lan ZC, Bai YF (2021) N-enrichment induced biodiversity loss can be explained by reductions in competitive intransitivity: evidence from a decade-long grassland experiment. Environ Exp Bot 184:10. https://doi.org/10.1016/j.envexpbot.2021.104372
Lu XM, Zhao XZ, Tachibana T, Uchida K, Sasaki T, Bai YF (2021) Plant quantity and quality regulate the diversity of arthropod communities in a semi-arid grassland. Funct Ecol 35:601–613. https://doi.org/10.1111/1365-2435.13742
Lü XT, Freschet GT, Flynn DFB, Han XG (2012) Plasticity in leaf and stem nutrient resorption proficiency potentially reinforces plant-soil feedbacks and microscale heterogeneity in a semi-arid grassland. J Ecol 100:144–150. https://doi.org/10.1111/j.1365-2745.2011.01881.x
Lü XT, Freschet GT, Kazakou E, Wang ZW, Zhou LS, Han XG (2015) Contrasting responses in leaf nutrient-use strategies of two dominant grass species along a 30-yr temperate steppe grazing exclusion chronosequence. Plant Soil 387:69–79. https://doi.org/10.1007/s11104-014-2282-7
Lü XT, Han XG (2010) Nutrient resorption responses to water and nitrogen amendment in semi-arid grassland of Inner Mongolia, China. Plant Soil 327:481–491. https://doi.org/10.1007/s11104-009-0078-y
Lü XT, Reed S, Yu Q, He NP, Wang ZW, Han XG (2013) Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland. Glob Change Biol 19:2775–2784. https://doi.org/10.1111/gcb.12235
McNaughton SJ (1979) Grazing as an optimization process - grass ungulate relationships in the serengeti. Am Nat 113:691–703. https://doi.org/10.1086/283426
McNaughton SJ (1985) Ecology of a grazing ecosystem - the serengeti. Ecol Monogr 55:259–294. https://doi.org/10.2307/1942578
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5
Niu KC, He JS, Lechowicz MJ (2016) Grazing-induced shifts in community functional composition and soil nutrient availability in Tibetan alpine meadows. J Appl Ecol 53:1554–1564. https://doi.org/10.1111/1365-2664.12727
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture Circular No. 939, Washington D. C
Rennenberg H, Schmidt S (2010) Perennial lifestyle-an adaptation to nutrient limitation? Tree Physiol 30:1047–1049. https://doi.org/10.1093/treephys/tpq076
Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177. https://doi.org/10.1890/0012-9658(1998)079[0165:Heopan]2.0.Co;2
Schönbach P, Wan HW, Gierus M, Bai YF, Muller K, Lin LJ, Susenbeth A, Taube F (2011) Grassland responses to grazing: effects of grazing intensity and management system in an Inner Mongolian steppe ecosystem. Plant Soil 340:103–115. https://doi.org/10.1007/s11104-010-0366-6
Shan YM, Chen DM, Guan XX, Zheng SX, Chen HJ, Wang MJ, Bai YF (2011) Seasonally dependent impacts of grazing on soil nitrogen mineralization and linkages to ecosystem functioning in Inner Mongolia grassland. Soil Biol Biochem 43:1943–1954. https://doi.org/10.1016/j.soilbio.2011.06.002
Shen JB, Yuan LX, Zhang JL, Li HG, Bai ZH, Chen XP, Zhang WF, Zhang FS (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005. https://doi.org/10.1104/pp.111.175232
Sokolov AP, Kicklighter DW, Melillo JM, Felzer BS, Schlosser CA, Cronin TW (2008) Consequences of considering carbon-nitrogen interactions on the feedbacks between climate and the terrestrial carbon cycle. J Clim 21:3776–3796. https://doi.org/10.1175/2008jcli2038.1
Tang B, Man J, Bai YF (2020) Leaf nitrogen acquisition of Leymus chinensis varies with leaf age and land use change in a semiarid grassland. Environ Exp Bot 175:104051. https://doi.org/10.1016/j.envexpbot.2020.104051
Tsujii Y, Aiba S, Kitayama K (2020) Phosphorus allocation to and resorption from leaves regulate the residence time of phosphorus in above-ground forest biomass on Mount Kinabalu, Borneo. Funct Ecol 34:1702–1712. https://doi.org/10.1111/1365-2435.13574
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15. https://doi.org/10.1890/08-0127.1
Wan HW, Bai YF, Schonbach P, Gierus M, Taube F (2011) Effects of grazing management system on plant community structure and functioning in a semiarid steppe: scaling from species to community. Plant Soil 340:215–226. https://doi.org/10.1007/s11104-010-0661-2
Yang H, Auerswald K, Bai YF, Wittmer MHOM, Schnyder H (2011) Variation in carbon isotope discrimination in Cleistogenes squarrosa (Trin.) Keng: patterns and drivers at tiller, local, catchment, and regional scales. J Exp Bot 62:4143–4152. https://doi.org/10.1093/jxb/err102
Yu Q, Chen QS, Elser JJ, He NP, Wu HH, Zhang GM, Wu JG, Bai YF, Han XG (2010) Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol Lett 13:1390–1399. https://doi.org/10.1111/j.1461-0248.2010.01532.x
Yu RP, Zhang WP, Yu YC, Yu SB, Lambers H, Li L (2020) Linking shifts in species composition induced by grazing with root traits for phosphorus acquisition in a typical steppe in Inner Mongolia. Sci Total Environ 712:136495. https://doi.org/10.1016/j.scitotenv.2020.136495
Zhan SX, Wang Y, Zhu ZC, Li WH, Bai YF (2017) Nitrogen enrichment alters plant N: P stoichiometry and intensifies phosphorus limitation in a steppe ecosystem. Environ Exp Bot 134:21–32. https://doi.org/10.1016/j.envexpbot.2016.10.014
Zhang TR, Li FY, Li YL, Shi CJ, Wang H, Wu L, Bai Z, Suri G, Wang ZY (2022) Disentangling the effects of animal defoliation, trampling, and excretion deposition on plant nutrient resorption in a semi-arid steppe: the predominant role of defoliation. Agric Ecosyst Environ 337:10. https://doi.org/10.1016/j.agee.2022.108068
Zhang TR, Li FY, Shi CJ, Li YL, Tang SM, Baoyin TGT (2020) Enhancement of nutrient resorption efficiency increases plant production and helps maintain soil nutrients under summer grazing in a semi-arid steppe. Agric Ecosyst Environ 292:106840. https://doi.org/10.1016/j.agee.2020.106840
Zheng SX, Chi YG, Yang XJ, Li WH, Lan ZC, Bai YF (2022) Direct and indirect effects of nitrogen enrichment and grazing on grassland productivity through intraspecific trait variability. J Appl Ecol 59:598–610. https://doi.org/10.1111/1365-2664.14078
Zheng SX, Ren HY, Lan ZC, Li WH, Wang KB, Bai YF (2010) Effects of grazing on leaf traits and ecosystem functioning in Inner Mongolia grasslands: scaling from species to community. Biogeosciences 7:1117–1132. https://doi.org/10.5194/bg-7-1117-2010
Acknowledgements
We are grateful to the staff at the Inner Mongolia Grassland Ecosystem Research Station (IMGERS), Chinese Academy of Sciences, for their help with the fieldwork. We appreciate the anonymous reviewers and editor for their valuable comments and suggestions that have greatly improved the quality of our manuscript.
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This study was supported by the National Natural Science Foundation of China (32192461 and 32192464) and the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA23080000).
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YB designed the research. RJ, BT, WC, and XL performed the experiments and collected the data. RJ, WC, BT, XL, YW, and YB conducted the data analysis and wrote the manuscript. All authors contributed to the revision of the manuscript, and YB edited the manuscript.
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Jia, R., Chen, W., Tang, B. et al. Phosphorus Availability Mediates Grazing Impacts on Resorption and Allocation of Foliar Nitrogen and Phosphorus by Dominant Species in Semiarid Grasslands. J Soil Sci Plant Nutr 23, 5482–5494 (2023). https://doi.org/10.1007/s42729-023-01415-z
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DOI: https://doi.org/10.1007/s42729-023-01415-z