Abstract
Several studies have addressed the role of soil fertility on acorn N remobilization during seedling growth, but have focused on very early development stages or have assessed remobilization at a coarse grain ontogenetic scale making it difficult to know the precise time when seedlings switch from acorn N to soil N use. We cultivated Quercus variabilis seedlings under two distinct soil N fertility and assessed their growth, acorn N remobilization, and absorption of soil N at five distinct development stages, spanning from the incipient shoot emergence to the completion of the second flush of growth. Acorn N contributed more to seedling N content than soil N at all development stages. Seedlings began to uptake substantial amounts of soil N after the completion of leaf expansion during the first shoot flush of growth, coinciding with a fine root area that reached 50% of the maximum value observed at the end of the study. Roots became less dependent on acorn N before shoots. Soil fertility, rather than seedling growth rate, determined soil N uptake after the completion of leaf expansion in the first shoot flush of growth. We conclude that the acorn is the primary N source for Q. variabilis seedlings until the completion of the first shoot flush of growth. Soil fertility does not significantly affect either the amount of N remobilized from acorns or the switch from acorn N to massive soil N use, suggesting a minimal effect of forest microhabitat fertility on acorn N utilization by Q. variabilis seedlings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The data of this study are available upon reasonable request to the first author or the author for correspondence.
References
Aizen MA, Woodcock H (1996) Effects of acorn size on seedling survival and growth in Quercus rubra following simulated spring freeze. Can J Bot 74:308–314. https://doi.org/10.1139/b96-037
Barberis IM, Dalling JW (2008) The effect of light, seed size and biomass removal on cotyledon reserve use and root mass allocation in Gustavia superba seedlings. J Trop Ecol 24:607–617. https://doi.org/10.1017/s0266467408005440
Bartlow AW, Agosta SJ, Curtis R, Yi X, Steele MA (2018) Acorn size and tolerance to seed predators: the multiple roles of acorns as food for seed predators, fruit for dispersal and fuel for growth. Integr Zool 13:251–266. https://doi.org/10.1111/1749-4877.12287
Bewley JD, Black M (1978) Physiology and biochemistry of seeds in relation to germination. Springer, Berlin, Heidelberg
Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants – an economic analogy. Annu Rev Ecol Syst 16:363–392. https://doi.org/10.1146/annurev.es.16.110185.002051
Bonanomi G, Mogavero V, Rita A, Zotti M, Saulino L, Tesei G, Allegrezza M, Saracino A, Rossi S, Allevato E, Kikvidze Z (2021) Shrub facilitation promotes advancing of the Fagus sylvatica treeline across the Apennines (Italy). J Veg Sci 32:e13054. https://doi.org/10.1111/jvs.13054
Bonfil C (1998) The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae). Am J Bot 85:79. https://doi.org/10.2307/2446557
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth's nitrogen cycle. Science 330:192–196. https://doi.org/10.1126/science.1186120
Chen H, Zhao M, Qi L, Sun X, Li Q, Liu X, Wang N, Zwiazek JJ, Zhang W, Guo W, Wang R, Zhang F, Du N (2022) Shading reduced the compensation and enhancement effects of soil nutrition on the growth of cotyledon-damaged Quercus acutissima seedlings. Plant Soil 482:665–678. https://doi.org/10.1007/s11104-022-05719-4
Dickson RE, Tomlinson PT, Isebrands JG (2000) Allocation of current photosynthate and changes in tissue dry weight within northern red oak seedlings: individual leaf and flush carbon contribution during episodic growth. Can J for Res 30:1296–1307. https://doi.org/10.1139/x00-058
Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, Cambridge
Freschet GT, Violle C, Bourget MY, Scherer-Lorenzen M, Fort F (2018) Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress. New Phytol 219:1338–1352. https://doi.org/10.1111/nph.15225
Gao L, Hill PW, Jones DL, Guo Y, Gao F, Cui X (2020) Seasonality is more important than forest type in regulating the pool size and composition of soil soluble N in temperate forests. Biogeochemistry 150:279–295. https://doi.org/10.1007/s10533-020-00698-z
García-Cebrián F, Esteso-Martínez J, Gil-Pelegrín E (2003) Influence of cotyledon removal on early seedling growth in Quercus robur L. Ann for Sci 60:69–73. https://doi.org/10.1051/forest:2002075
Gomez JM, Schupp EW, Jordano P (2019) Synzoochory: the ecological and evolutionary relevance of a dual interaction. Biol Rev Camb Philos Soc 94:874–902. https://doi.org/10.1111/brv.12481
Kabeya D, Sakai S (2003) The role of roots and cotyledons as storage organs in early stages of establishment in Quercus crispula: a quantitative analysis of the nonstructural carbohydrate in cotyledons and roots. Ann Bot 92:537–545. https://doi.org/10.1093/aob/mcg165
Kitajima K (2002) Do shade-tolerant tropical tree seedlings depend longer on seed reserves? Functional growth analysis of three Bignoniaceae species. Funct Ecol 16:433–444. https://doi.org/10.1046/j.1365-2435.2002.00641.x
Kleczewski NM, Herms DA, Bonello P (2010) Effects of soil type, fertilization and drought on carbon allocation to root growth and partitioning between secondary metabolism and ectomycorrhizae of Betula papyrifera. Tree Physiol 30:807–817. https://doi.org/10.1093/treephys/tpq032
Kobe RK, Iyer M, Walters MB (2010) Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology 91:166–179. https://doi.org/10.1890/09-0027.1
Lehmeier CA, Schaufele R, Schnyder H (2005) Allocation of reserve-derived and currently assimilated carbon and nitrogen in seedlings of Helianthus annuus under sub-ambient and elevated CO2 growth conditions. New Phytol 168:613–621. https://doi.org/10.1111/j.1469-8137.2005.01531.x
Li G, Zhu Y, Liu Y, Wang J, Liu J, Dumroese RK (2014) Combined effects of pre-hardening and fall fertilization on nitrogen translocation and storage in Quercus variabilis seedlings. Eur J Forest Res 133:983–992. https://doi.org/10.1007/s10342-014-0816-4
Luo N, Villar-Salvador P, Li GL, Wang JX (2021) The dark side of nursery photoperiod reduction on summer plantation performance of a temperate conifer: high winter mortality mediated by reduced seedling carbohydrate and nitrogen storage. For Ecol Manag 491:119171. https://doi.org/10.1016/j.foreco.2021.119171
Luo N, Wei N, Li G (2023) Growth versus storage: response of Pinus tabuliformis and Quercus mongolica seedlings to variation in nutrient supply and its associated effect on field performance. New for. https://doi.org/10.1007/s11056-023-09966-w
Maillard P, Deléens E, Daudet FA, Lacointe A, Frossad JS (1994) Carbon and nitrogen partitioning in walnut seedlings during the acquisition of autotrophy through simultaneous 13CO2 and 15NO3 long-term labelling. J Exp Bot 45:203–210. https://doi.org/10.1093/jxb/45.2.203
Maillard P, Guehl JM, Muller JF, Gross P (2001) Interactive effects of elevated CO2 concentration and nitrogen supply on partitioning of newly fixed 13C and 15N between shoot and roots of pedunculate oak seedlings (Quercus robur). Tree Physiol 21:163–172. https://doi.org/10.1093/treephys/21.2-3.163
Mancilla-Leytón JM, Cambrollé J, Figueroa ME, Martín Vicente Á (2013) Growth and survival of cork oak (Quercus suber) seedlings after simulated partial cotyledon consumption under different soil nutrient contents. Plant Soil 370:381–392. https://doi.org/10.1007/s11104-013-1646-8
Martínez-Baroja L, Pérez-Camacho L, Villar-Salvador P, Rebollo S, Leverkus AB, Pesendorfer MB, Molina-Morales M, Castro J, Rey-Benayas JM, Matlack G (2021) Caching territoriality and site preferences by a scatter-hoarder drive the spatial pattern of seed dispersal and affect seedling emergence. J Ecol 109:2342–2353. https://doi.org/10.1111/1365-2745.13642
McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593. https://doi.org/10.1890/0012-9658(1999)080[2581:Baipoo]2.0.Co;2
McCormack ML, Guo D, Iversen CM, Chen W, Eissenstat DM, Fernandez CW, Li L, Ma C, Ma Z, Poorter H, Reich PB, Zadworny M, Zanne A (2017) Building a better foundation: improving root-trait measurements to understand and model plant and ecosystem processes. New Phytol 215:27–37. https://doi.org/10.1111/nph.14459
Milberg PER, Lamont BB (1997) Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient-poor soils. New Phytol 137:665–672. https://doi.org/10.1046/j.1469-8137.1997.00870.x
Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095. https://doi.org/10.1093/treephys/tpq042
Miller AJ, Cramer MD (2005) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36. https://doi.org/10.1007/s11104-004-0965-1
Miransari M, Smith DL (2014) Plant hormones and seed germination. Environ Exp Bot 99:110–121. https://doi.org/10.1016/j.envexpbot.2013.11.005
Nadeem M, Mollier A, Morel C, Shahid M, Aslam M, Zia-ur-Rehman M, Wahid MA, Pellerin S (2013) Maize seedling phosphorus nutrition: allocation of remobilized seed phosphorus reserves and external phosphorus uptake to seedling roots and shoots during early growth stages. Plant Soil 371:327–338. https://doi.org/10.1007/s11104-013-1689-x
Newton AC, Pigott CD (1991) Mineral nutrition and mycorrhizal infection of seedling oak and birch. I. Nutrient uptake and the development of mycorrhizal infection during seedling establishment. New Phytol 117:37–44. https://doi.org/10.1111/j.1469-8137.1991.tb00942.x
Oliet JA, Puértolas J, Planelles R, Jacobs DF (2013) Nutrient loading of forest tree seedlings to promote stress resistance and field performance: a Mediterranean perspective. New for 44:649–669. https://doi.org/10.1007/s11056-013-9382-8
Pemán J, Chirino E, Espelta JM, Jacobs DF, Martín-Gómez P, Navarro-Cerrillo R, Oliet JA, Vilagrosa A, Villar-Salvador P, Gil-Pelegrín E (2017) Physiological keys for katural and artificial regeneration of oaks. In: Gil-Pelegrín E, Peguero-Pina JJ, Sancho-Knapik D (eds) Oaks physiological ecology exploring the functional diversity of genus Quercus L. Springer, Cham, pp 453–511
Peng Y, Niu J, Peng Z, Zhang F, Li C (2010) Shoot growth potential drives N uptake in maize plants and correlates with root growth in the soil. Field Crops Res 115:85–93. https://doi.org/10.1016/j.fcr.2009.10.006
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x
Reich PB, Teskey RO, Johnson PS, Hinckley TM (1980) Periodic root and shoot growth in oak. For Sci 26:590–598. https://doi.org/10.1093/forestscience/26.4.590
Ruzicka DR, Barrios-Masias FH, Hausmann NT, Jackson LE, Schachtman DP (2010) Tomato root transcriptome response to a nitrogen-enriched soil patch. BMC Plant Biol 10:75. https://doi.org/10.1186/1471-2229-10-75
Shi W, Bloomberg M, Li G, Su S, Jia L (2017) Combined effects of cotyledon excision and nursery fertilization on root growth, nutrient status and outplanting performance of Quercus variabilis container seedlings. PLoS ONE 12:e0177002. https://doi.org/10.1371/journal.pone.0177002
Shi W, Villar-Salvador P, Li G, Jiang X (2019) Acorn size is more important than nursery fertilization for outplanting performance of Quercus variabilis container seedlings. Ann for Sci 76:22. https://doi.org/10.1007/s13595-018-0785-8
Silla F, Escudero A (2003) Uptake, demand and internal cycling of nitrogen in saplings of Mediterranean Quercus species. Oecologia 136:28–36. https://doi.org/10.1007/s00442-003-1232-5
Sun ZC, Ma TY, Xu SQ, Guo HR, Hu CC, Chen CJ, Song W, Liu XY (2022) Levels and variations of soil bioavailable nitrogen among forests under high atmospheric nitrogen deposition. Sci Total Environ 838:156405. https://doi.org/10.1016/j.scitotenv.2022.156405
Tilki F (2010) Influence of acorn size and storage duration on moisture content, germination and survival of Quercus petraea (Mattuschka). J Environ Biol 31:325–328. https://doi.org/10.2112/JCOASTRES-D-09-00120.1
Toca A, Moler E, Nelson A, Jacobs DF (2022) Environmental conditions in the nursery regulate root system development and architecture of forest tree seedlings: a systematic review. New for 53:1113–1143. https://doi.org/10.1007/s11056-022-09944-8
Urza AK, Weisberg PJ, Chambers JC, Sullivan BW (2019) Shrub facilitation of tree establishment varies with ontogenetic stage across environmental gradients. New Phytol 223:1795–1808. https://doi.org/10.1111/nph.15957
Uscola M, Salifu KF, Oliet JA, Jacobs DF (2015a) An exponential fertilization dose–response model to promote restoration of the Mediterranean oak Quercus ilex. New for 46:795–812. https://doi.org/10.1007/s11056-015-9493-5
Uscola M, Villar-Salvador P, Gross P, Maillard P (2015b) Fast growth involves high dependence on stored resources in seedlings of Mediterranean evergreen trees. Ann Bot 115:1001–1013. https://doi.org/10.1093/aob/mcv019
Villar R, Ruiz-Benito P, de la Riva EG, Poorter H, Cornelissen JHC, Quero JL (2017) Growth and growth-related traits for a range of Quercus species grown as seedlings under controlled conditions and for adult plants from the field. In: Gil-Pelegrin E, Peguero-Pina JJ, Sancho-Knapik D (eds) Oaks physiological ecology exploring the functional diversity of genus Quercus L. Springer, Cham, pp 393–417
Villar-Salvador P, Planelles R, Enriquez E, Rubira JP (2004) Nursery cultivation regimes, plant functional attributes, and field performance relationships in the Mediterranean oak Quercus ilex L. For Ecol Manag 196:257–266. https://doi.org/10.1016/j.foreco.2004.02.061
Villar-Salvador P, Heredia N, Millard P (2010) Remobilization of acorn nitrogen for seedling growth in holm oak (Quercus ilex), cultivated with contrasting nutrient availability. Tree Physiol 30:257–263. https://doi.org/10.1093/treephys/tpp115
von Wirén N, Gazzarrini S, Frommer WB (1997) Regulation of mineral nitrogen uptake in plants. Plant Soil 196:191–199. https://doi.org/10.1023/A:1004241722172
White AC, Rogers A, Rees M, Osborne CP (2016) How can we make plants grow faster? A source-sink perspective on growth rate. J Exp Bot 67:31–45. https://doi.org/10.1093/jxb/erv447
Willaume M, Pages L (2006) How periodic growth pattern and source/sink relations affect root growth in oak tree seedlings. J Exp Bot 57:815–826. https://doi.org/10.1093/jxb/erj059
Yi X, Ju M (2020) Soil nitrogen assimilation of 1-year oak seedlings: implication for forest fertilization and management. For Ecol Manag 456. https://doi.org/10.1016/j.foreco.2019.117703
Yi X, Wang Z (2016) The importance of cotyledons for early-stage oak seedlings under different nutrient levels: a multi-species study. J Plant Growth Regul 35:183–189. https://doi.org/10.1007/s00344-015-9516-7
Yi X, Wang Z, Liu C, Liu G, Zhang M (2015) Acorn cotyledons are larger than their seedlings’ need: evidence from artificial cutting experiments. Sci Rep 5:8112. https://doi.org/10.1038/srep08112
Yi X, Bartlow AW, Curtis R, Agosta SJ, Steele MA, Heard M (2019) Responses of seedling growth and survival to post-germination cotyledon removal: an investigation among seven oak species. J Ecol 107:1817–1827. https://doi.org/10.1111/1365-2745.13153
Acknowledgements
We would like to express our gratitude to Jinfeng Guo who assisted us in cultivating the seedlings, as well as to Na Wang and Leng Han for their contributions to complete the laboratory work. We also acknowledge the constructive comments of two anonymous reviewers that contributed to improve the manuscript.
Funding
The study was funded by the National Natural Science Foundation of China (No.32171764, No.32101503), the project QueVADIS (PID2022-141762OB-I00) from the Spanish Government, and the REMEDINAL network of the Comunidad de Madrid (S2018/EMT-4338). Kaifen Zhao was supported by a fellowship of the China Scholarship Council (2022).
Author information
Authors and Affiliations
Contributions
KZ: experiment design and execution, data curation, formal analysis, software, visualization, writing—original draft, writing—review and editing. PV-S: writing—review and editing. GL: conceptualization, experiment design, methodology, review and editing, funding acquisition, and project administration.
Corresponding author
Ethics declarations
Conflict of interest
All authors have no conflict of interest.
Additional information
Communicated by L. Kalcsits .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhao, K., Villar-Salvador, P. & Li, G. The contribution of acorn and soil N to early development of Chinese cork oak (Quercus variabilis Blume) seedlings under contrasting soil fertility conditions. Trees 38, 251–261 (2024). https://doi.org/10.1007/s00468-023-02481-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-023-02481-7