AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (2.3 MB)
Collect
AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Understory seedlings of Quercus mongolica survive by phenological escape

Shixiong WuYing LiuLulu HeWei ZengQijing Liu( )
College of Forestry, Beijing Forestry University, Beijing, 100083, China
Show Author Information

Abstract

Understanding understory seedling regeneration mechanisms is important for the sustainable development of temperate primary forests in the context of increasingly intense climate warming events. The poor regeneration of dominant tree species, however, is one of the biggest challenges it faces at the moment. Especially, the regeneration of the shade-intolerant Quercus mongolica seedling is difficult in primary forests, which contrasts with the extreme abundance of understory seedlings in secondary forests. The mechanism behind the interesting phenomenon is still unknown. This study used in-situ monitoring and nursery-controlled experiment to investigate the survival rate, growth performance, as well as nonstructural carbohydrate (NSC) concentrations and pools of various organ tissues of seedlings for two consecutive years, further analyze the understory light availability and simulate the foliage carbon (C) gain in the secondary and primary forest. Results suggested that seedlings in the secondary forest had greater biomass allocation aboveground, height and specific leaf area (SLA) in summer, which allowed the seedling to survive longer in the canopy closure period. High light availability and positive C gain in early spring and late autumn are key factors affecting the growth and survival of understory seedlings in the secondary forest, whereas seedlings in the primary forest had annual negative carbon gain. Through the growing season, the total NSC concentrations of seedlings gradually decreased, whereas those of seedlings in the secondary forest increased significantly in autumn, and were mainly stored in roots for winter consumption and the following year's summer shade period, which was verified by the nursery-controlled experiment that simulated autumn enhanced light availability improved seedling survival rate and NSC pools. In conclusion, our results revealed the survival trade-off strategies of Quercus mongolica seedlings and highlighted the necessity of high light availability during the spring and autumn phenological periods for shade-intolerant tree seedling recruitment.

References

 

Andivia, E., Villar-Salvador, P., Oliet, J.A., Puertolas, J., Dumroese, R.K., Ivetić, V., Molina-Venegas, R., Arellano, E.C., Li, G., Ovalle, J.F., 2021. Climate and species stress resistance modulate the higher survival of large seedlings in forest restorations worldwide. Ecol. Appl. 31, e02394. https://doi.org/10.1002/eap.2394.

 

Augspurger, C., Cheeseman, J., Salk, C., 2005. Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Funct. Ecol. 537-546. https://doi.org/10.1111/j.1365-2435.2005.01027.x.

 

Barrere, J., Petersson, L.K., Boulanger, V., Collet, C., Felton, A.M., Löf, M., Saïd, S., 2021. Canopy openness and exclusion of wild ungulates act synergistically to improve oak natural regeneration. For. Ecol. Manag. 487, 118976. https://doi.org/10.1016/j.foreco.2021.118976.

 

De Lombaerde, E., Baeten, L., Verheyen, K., Perring, M.P., Ma, S., Landuyt, D., 2021. Understorey removal effects on tree regeneration in temperate forests: a meta-analysis. J. Appl. Ecol. 58, 9-20. https://doi.org/10.1111/1365-2664.13792.

 

De Lombaerde, E., Blondeel, H., Baeten, L., Landuyt, D., Perring, M.P., Depauw, L., Maes, S.L., Wang, B., Verheyen, K., 2020. Light, temperature and understorey cover predominantly affect early life stages of tree seedlings in a multifactorial mesocosm experiment. For. Ecol. Manag. 461, 117907. https://doi.org/10.1016/j.foreco.2020.117907.

 

De Lombaerde, E., Verheyen, K., Van Calster, H., Baeten, L., 2019. Tree regeneration responds more to shade casting by the overstorey and competition in the understorey than to abundance per se. For. Ecol. Manag. 450, 117492. https://doi.org/10.1016/j.foreco.2019.117492.

 

De Pauw, K., Sanczuk, P., Meeussen, C., Depauw, L., De Lombaerde, E., Govaert, S., Vanneste, T., Brunet, J., Cousins, S.A.O., Gasperini, C., Hedwall, P., Iacopetti, G., Lenoir, J., Plue, J., Selvi, F., Spicher, F., Uria-Diez, J., Verheyen, K., Vangansbeke, P., De Frenne, P., 2022. Forest understorey communities respond strongly to light in interaction with forest structure, but not to microclimate warming. New Phytol. 233, 219-235. https://doi.org/10.1111/nph.17803.

 

Evans, J., Poorter, H., 2001. Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ. 24, 755-767. https://doi.org/10.1046/j.1365-3040.2001.00724.x.

 

Fischer, S., Hanf, S., Frosch, T., Gleixner, G., Popp, J., Trumbore, S., Hartmann, H., 2015. Pinus sylvestris switches respiration substrates under shading but not during drought. New Phytol. 207, 542-550. https://doi.org/10.1111/nph.13452.

 

Frey, B., Ashton, M., 2018. Growth, survival and sunfleck response of underplanted red oaks (Quercus spp., section Erythrobalanus) along a topographic gradient in southern New England. For. Ecol. Manag. 419, 179-186. https://doi.org/10.1016/j.foreco.2018.03.030.

 

Fridley, J.D., 2012. Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485, 359-362. https://doi.org/10.1038/nature11056.

 

Furze, M.E., Huggett, B.A., Aubrecht, D.M., Stolz, C.D., Carbone, M.S., Richardson, A.D., 2019. Whole-tree nonstructural carbohydrate storage and seasonal dynamics in five temperate species. New Phytol. 221, 1466-1477. https://doi.org/10.1111/nph.15462.

 

Gandin, A., Gutjahr, S., Dizengremel, P., Lapointe, L., 2011. Source–sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum. J. Exp. Bot. 62, 3467-3479. https://doi.org/10.1093/jxb/err020.

 

Gaucher, C., Gougeon, S., Mauffette, Y., Messier, C., 2005. Seasonal variation in biomass and carbohydrate partitioning of understory sugar maple (Acer saccharum) and yellow birch (Betula alleghaniensis) seedlings. Tree Physiol. 25, 93-100. https://doi.org/10.1093/treephys/25.1.93.

 

Ge, X., Zhu, J., Lu, D., Zhu, C., Gao, P., Yang, X., 2021. Effects of Korean Pine basal area in mixed broadleaved–Korean pine forest stands on its natural regeneration in northeast China. For. Sci. 67, 179-191. https://doi.org/10.1093/forsci/fxaa045.

 

Gruber, A., Pirkebner, D., Oberhuber, W., 2013. Seasonal dynamics of mobile carbohydrate pools in phloem and xylem of two alpine timberline conifers. Tree Physiol. 33, 1076-1083. https://doi.org/10.1093/treephys/tpt088.

 

Hao, Z., Zhang, J., Song, B., Ye, J., Li, B., 2007. Vertical structure and spatial associations of dominant tree species in an old-growth temperate forest. For. Ecol. Manag. 252, 1-11. https://doi.org/10.1016/j.foreco.2007.06.026.

 

Hartmann, H., Adams, H.D., Hammond, W.M., Hoch, G., Landhäusser, S.M., Wiley, E., Zaehle, S., 2018. Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environ. Exp. Bot. 152, 7-18. https://doi.org/10.1016/j.envexpbot.2018.03.011.

 

Heberling, J.M., Cassidy, S.T., Fridley, J.D., Kalisz, S., 2019a. Carbon gain phenologies of spring-flowering perennials in a deciduous forest indicate a novel niche for a widespread invader. New Phytol. 221, 778-788. https://doi.org/10.1111/nph.15404.

 

Heberling, J.M., MacKenzie, C.M., Fridley, J.D., Kalisz, S., Primack, R.B., 2019b. Phenological mismatch with trees reduces wildflower carbon budgets. Ecol. Lett. 22, 616-623. https://doi.org/10.1111/ele.13224.

 

Hoch, G., Richter, A., Körner, C., 2003. Non-structural carbon compounds in temperate forest trees. Plant Cell Environ. 26, 1067-1081. https://doi.org/10.1046/j.0016-8025.2003.01032.x.

 

Huang, L., Koubek, T., Weiser, M., Herben, T., 2018. Environmental drivers and phylogenetic constraints of growth phenologies across a large set of herbaceous species. J. Ecol. 106, 1621-1633. https://doi.org/10.1111/1365-2745.12927.

 

Imada, S., Tako, Y., 2022. Seasonal accumulation of photoassimilated carbon relates to growth rate and use for new aboveground organs of young apple trees in following spring. Tree Physiol. 42, 2294-2305. https://doi.org/10.1093/treephys/tpac072.

 

Kenzo, T., Yoneda, R., Ninomiya, I., 2018. Seasonal changes in photosynthesis and starch content in Japanese fir (Abies firma Sieb. et Zucc.) saplings under different levels of irradiance. Trees (Berl.) 32, 429-439. https://doi.org/10.1007/s00468-017-1640-5.

 

Klein, T., Vitasse, Y., Hoch, G., 2016. Coordination between growth, phenology and carbon storage in three coexisting deciduous tree species in a temperate forest. Tree Physiol. 36, 847-855. https://doi.org/10.1093/treephys/tpw030.

 

Kunstler, G., Coomes, D.A., Canham, C.D., 2009. Size-dependence of growth and mortality influence the shade tolerance of trees in a lowland temperate rain forest. J. Ecol. 97, 685-695. https://doi.org/10.1111/j.1365-2745.2009.01482.x.

 

Leakey, A., Scholes, J., Press, M., 2005. Physiological and ecological significance of sunflecks for dipterocarp seedlings. J. Exp. Bot. 56, 469-482. https://doi.org/10.1093/jxb/eri055.

 

Lee, B.R., Ibáñez, I., 2021. Spring phenological escape is critical for the survival of temperate tree seedlings. Funct. Ecol. 35, 1848-1861. https://doi.org/10.1111/1365-2435.13821.

 

Lee, B.R., Ibáñez, I., 2021. Improved phenological escape can help temperate tree seedlings maintain demographic performance under climate change conditions. Global Change Biol. 27, 3883-3897. https://doi.org/10.1111/gcb.15678.

 

Lee, B.R., Miller, T.K., Rosche, C., Yang, Y., Heberling, J.M., Kuebbing, S.E., Primack, R.B., 2022. Wildflower phenological escape differs by continent and spring temperature. Nat. Commun. 13, 7157. https://doi.org/10.1038/s41467-022-34936-9.

 

Lu, D., Wang, G.G., Yan, Q., Gao, T., Zhu, J., 2018a. Effects of gap size and within-gap position on seedling growth and biomass allocation: is the gap partitioning hypothesis applicable to the temperate secondary forest ecosystems in Northeast China? For. Ecol. Manag. 429, 351-362. https://doi.org/10.1016/j.foreco.2018.07.031.

 

Lu, D., Wang, G.G., Zhang, J., Fang, Y., Zhu, C., Zhu, J., 2018b. Converting larch plantations to mixed stands: effects of canopy treatment on the survival and growth of planted seedlings with contrasting shade tolerance. For. Ecol. Manag. 409, 19-28. https://doi.org/10.1016/j.foreco.2017.10.058.

 

Lu, D., Zhang, G., Zhu, J., Wang, G.G., Zhu, C., Yan, Q., Zhang, J., 2019. Early natural regeneration patterns of woody species within gaps in a temperate secondary forest. Eur. J. For. Res. 138, 991-1003. https://doi.org/10.1007/s10342-019-01219-w.

 

Maes, S.L., Perring, M.P., Depauw, L., Bernhardt-Römermann, M., Blondeel, H., Brūmelis, G., Brunet, J., Decocq, G., Den Ouden, J., Govaert, S., Härdtle, W., Hédl, R., Heinken, T., Heinrichs, S., Hertzog, L., Jaroszewicz, B., Kirby, K., Kopecký, M., Landuyt, D., Máliš, F., Vanneste, T., Wulf, M., Verheyen, K., 2020. Plant functional trait response to environmental drivers across European temperate forest understorey communities. Plant Biol. 22, 410-424. https://doi.org/10.1111/plb.13082.

 

Markesteijn, L., Poorter, L., 2009. Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought-and shade-tolerance. J. Ecol. 97, 311-325. https://doi.org/10.1111/j.1365-2745.2008.01466.x.

 

Mei, L., Xiong, Y., Gu, J., Wang, Z., Guo, D., 2015. Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees. Oecologia 177, 333-344. https://doi.org/10.1007/s00442-014-3186-1.

 

Montague, M.S., Landhäusser, S.M., McNickle, G.G., Jacobs, D.F., 2022. Preferential allocation of carbohydrate reserves belowground supports disturbance-based management of American chestnut (Castanea dentata). For. Ecol. Manag. 509, 120078. https://doi.org/10.1016/j.foreco.2022.120078.

 

Myers, J.A., Kitajima, K., 2007. Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J. Ecol. 95, 383-395. https://doi.org/10.1111/j.1365-2745.2006.01207.x.

 

Piper, F.I., Fajardo, A., 2016. Carbon dynamics of Acer pseudoplatanus seedlings under drought and complete darkness. Tree Physiol. 36, 1400-1408.

 

Regier, N., Streb, S., Zeeman, S.C., Frey, B., 2010. Seasonal changes in starch and sugar content of poplar (Populus deltoides × nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiol. 30, 979-987. https://doi.org/10.1093/treephys/tpq047.

 
Richardson, A.D., O'Keefe, J., 2009. Phenological differences between understory and overstory: a case study using the long-term Harvard Forest records. In: Noormets, A. (Ed.), Phenology of Ecosystem Processes. Applications in Global Change Research. Springer New York, NY, pp. 87–117. https://doi.org/10.1007/978-1-4419-0026-5_4.
 

Sangsupan, H.A., Hibbs, D.E., Withrow-Robinson, B.A., Elliott, S., 2021. Effect of microsite light on survival and growth of understory natural regeneration during restoration of seasonally dry tropical forest in upland northern Thailand. For. Ecol. Manag. 489, 119061. https://doi.org/10.1016/j.foreco.2021.119061.

 

Schuster, M.J., Wragg, P.D., Reich, P.B., 2021. Phenological niche overlap between invasive buckthorn (Rhamnus cathartica) and native woody species. For. Ecol. Manag. 498, 119568. https://doi.org/10.1016/j.foreco.2021.119568.

 

Schuster, M.J., Wragg, P.D., Williams, L.J., Butler, E.E., Stefanski, A., Reich, P.B., 2020. Phenology matters: extended spring and autumn canopy cover increases biotic resistance of forests to invasion by common buckthorn (Rhamnus cathartica). For. Ecol. Manag. 464, 118067. https://doi.org/10.1016/j.foreco.2020.118067.

 

Sevanto, S., Mcdowell, N.G., Dickman, L.T., Pangle, R., Pockman, W.T., 2014. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37, 153-161. https://doi.org/10.1111/pce.12141.

 

Sun, Y., Zhu, J., Sun, O.J., Yan, Q., 2016. Photosynthetic and growth responses of Pinus koraiensis seedlings to canopy openness: implications for the restoration of mixed-broadleaved Korean pine forests. Environ. Exp. Bot. 129, 118-126. https://doi.org/10.1016/j.envexpbot.2016.02.005.

 

Tripathi, S., Bhadouria, R., Srivastava, P., Devi, R.S., Chaturvedi, R., Raghubanshi, A., 2020. Effects of light availability on leaf attributes and seedling growth of four tree species in tropical dry forest. Ecol. Process. 9, 1-16. https://doi.org/10.1186/s13717-019-0206-4.

 

Vitasse, Y., 2013. Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol. 198, 149-155. https://doi.org/10.1111/nph.12130.

 

Walters, M.B., Reich, P.B., 1999. Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytol. 143, 143-154. https://doi.org/10.1046/j.1469-8137.1999.00425.x.

 

Weber, R., Schwendener, A., Schmid, S., Lambert, S., Wiley, E., Landhäusser, S.M., Hartmann, H., Hoch, G., 2018. Living on next to nothing: tree seedlings can survive weeks with very low carbohydrate concentrations. New Phytol. 218, 107-118. https://doi.org/10.1111/nph.14987.

 

Wiley, E., Casper, B.B., Helliker, B.R., 2017. Recovery following defoliation involves shifts in allocation that favour storage and reproduction over radial growth in black oak. J. Ecol. 105, 412-424. https://doi.org/10.1111/1365-2745.12672.

 

Ye, Z.-P., Suggett, D.J., Robakowski, P., Kang, H.-J., 2013. A mechanistic model for the photosynthesis–light response based on the photosynthetic electron transport of photosystem II in C3 and C4 species. New Phytol. 199, 110-120. https://doi.org/10.1111/nph.12242.

 

Yemm, E., Willis, A., 1954. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57, 508. https://doi.org/10.1042/bj0570508.

 

Zhang, M., Zhu, J., Li, M., Zhang, G., Yan, Q., 2013. Different light acclimation strategies of two coexisting tree species seedlings in a temperate secondary forest along five natural light levels. For. Ecol. Manag. 306, 234-242. https://doi.org/10.1016/j.foreco.2013.06.031.

 

Zhang, T., Yan, Q., Wang, J., Zhu, J., 2018. Restoring temperate secondary forests by promoting sprout regeneration: effects of gap size and within-gap position on the photosynthesis and growth of stump sprouts with contrasting shade tolerance. For. Ecol. Manag. 429, 267-277. https://doi.org/10.1016/j.foreco.2018.07.025.

 

Zhou, G., Liu, Q., Xu, Z., Du, W., Yu, J., Meng, S., Zhou, H., Qin, L., Shah, S., 2020. How can the shade intolerant Korean pine survive under dense deciduous canopy? For. Ecol. Manag. 457, 117735. https://doi.org/10.1016/j.foreco.2019.117735.

Forest Ecosystems
Article number: 100185
Cite this article:
Wu S, Liu Y, He L, et al. Understory seedlings of Quercus mongolica survive by phenological escape. Forest Ecosystems, 2024, 11(2): 100185. https://doi.org/10.1016/j.fecs.2024.100185

108

Views

0

Downloads

1

Crossref

1

Web of Science

1

Scopus

0

CSCD

Altmetrics

Received: 11 December 2023
Revised: 17 February 2024
Accepted: 12 March 2024
Published: 21 March 2024
© 2024 The Authors.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return