Abstract
In forest ecosystems, gap formation changes the allocation of abiotic resources and thus affects the survival and growth of understory plants. However, how tree seedling survival and growth respond to low-temperature events and the influencing mechanisms remain unclear. To clarify how low-temperature event limits the survival and growth of tree seedlings in the montane regions of eastern Liaoning Province, northeast China, we investigated temperature and light intensity within secondary forest gaps, and the survival and growth of Juglans mandshurica seedlings after a low-temperature event in the spring of 2014. Damage to seedlings due to low temperature significantly varied in different aspects. Seedlings in gaps on southeast-facing slopes were the most seriously damaged, followed by those in gaps on northeast-facing slopes. In contrast, seedlings in west-facing gaps and in control plots without slope aspect were not damaged. The freezing injury index for seedlings was negatively correlated with minimum temperature (r = − 0.608, P < 0.01), but it was positively correlated with light intensity (r = 0.818, P < 0.01). In addition, height and root collar diameter of damaged seedlings were significantly lower than those of the undamaged seedlings (P < 0.01) during the early growing season (April–July), but no significant difference were observed during the late growing season (July–October) (P > 0.05). The extent of seedling damage was directly related to slope aspect. Low temperature and high light intensity were found to be the dominant factors affecting extent of damage to seedlings on southeast- and northeast-facing slopes.
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References
Awaya Y, Tanaka K, Kodani E, Nishizono T (2009) Responses of a beech (Fagus crenata Blume) stand to late spring frost damage in Morioka, Japan. For Ecol Manag 257(12):2359–2369
Blennow K (1998) Modelling minimum air temperature in partially and clear felled forests. Agric For Meteorol 91(3):223–235
Blennow K, Lindkvist L (2000) Models of low temperature and high irradiance and their application to explaining the risk of seedling mortality. For Ecol Manag 135(1–3):289–301
Blennow K, Lang ARG, Dunne P, Ball MC (1998) Cold-induced photoinhibition and growth of seedling snow gum (Eucalyptus pauciflora) under differing temperature and radiation regimes in fragmented forests. Plant Cell Environ 21(4):407–416
Cai ZQ, Cao KF, Feng YL, Feng ZL (2003) Acclimation of foliar photosynthetic apparatus of three tropical woody species to growth irradiance. Chin J Appl Ecol 14(4):493–496
Chen XW, Zhang Y, Ma HB (2000) Occurrence and control of frost in Tilia amurensis and Fraxinus mand shurica young plantations. Chin J Appl Ecol 11(6):809–813
Clark JS (1998) Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. Am Nat 152(2):204–224
De Grandpré L, Boucher D, Bergeron Y, Gagnon D (2011) Effects of small canopy gaps on boreal mixedwood understory vegetation dynamics. Commun Ecol 12(1):67–77
Diaci J, Adamic T, Rozman A (2012) Gap recruitment and partitioning in an old-growth beech forest of the Dinaric Mountains: influences of light regime, herb competition and browsing. For Ecol Manag 285(6):20–28
Dirks BOM, Van-Oijen M, Schapendonk AHCM, Goudriaan J, Wolf J (2002) Temperature sensitivity of photosynthesis in Lolium perenne swards: a comparison of two methods for deriving photosynthetic parameters from in vivo measurements. Photosynthetica 40(3):405–413
Dittmar C, Fricke W, Elling W (2006) Impact of late frost events on radial growth of common beech (Fagus sylvatica L.) in southern Germany. Eur J For Res 125(3):249–259
Duan WB, Li Y, Chen LX (2007) Microenvironmental heterogeneity of near surface layer illumination in the broad-leaved Pinus koraiensis forest gap. Sci Soil Water Conserv 5(6):82–86
Duan WB, Wang J, Li Y (2008) Microclimate characteristics of different size gaps in Pinus koraiensis-dominated broad leaved mixed forests. Chin J Appl Ecol 19(12):2561–2566
Egerton JJG, Banks JCG, Gibson A, Cunningham RB, Ball MC (2000) Facilitation of seedling establishment: reduction in irradiance enhances winter growth of Eucalyptus pauciflora. Ecology 81(5):1437–1449
Forrester JA, Lorimer CG, Dyer JH, Gower ST, Mladenoff DJ (2014) Response of tree regeneration to experimental gap creation and deer herbivory in north temperate forests. For Ecol Manag 329:137–147
Gray AN, Spies TA, Pabst RJ (2012) Canopy gaps affect long-term patterns of tree growth and mortality in mature and old-growth forests in the Pacific Northwest. For Ecol Manag 281(1):111–120
Guan YY, Fei F, Guan QW, Chen B (2016) Advances in studies of forest gap ecology. Sci Silvae Sin 52(4):91–99
Guo R, Zeng R, Zhang JX, Zhang XL, Sun GY (2015) Effects of different light intensities on reactive oxygen species metabolism and chlorophyll fluorescence parameters in leaves of flue-curing tobacco seedlings after chilling stress. Acta Agric Boreali-sin 30:225–230
Han YZ, Wang ZQ (2002) Spatial heterogeneity and forest regeneration. Chin J Appl Ecol 13(5):615–619
Hu WH, Yan XH, Yuan LF, Yang Q, Wu ZY (2011) The role of light intensity in the recovery of photosynthesis in tomato leaves after chilling under low light. B Bot Res 31(2):164–168
Hubbell SP, Foster RB, O′Brien ST, Harms KE, Condit R, Wechsler B, Wright SJ, Loo de Lao S (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283:554–557
James G, Landis RM, Ashton MS, Galvão J (2005) Growth response by big-leaf mahogany (Swietenia macrophylla) advance seedling regeneration to overhead canopy release in southeast Pará, Brazil. For Ecol Manag 204:399–412
Jie JM, Yu JH, Huang GB, Jie MH (2008) Effects of light intensity on photoinhibition in pepper seedlings treated under low temperature and poor irradiance. Trans Chin Soc Agric Eng 24(5):231–234
Jin GZ, Liu YY, Liu S, Kim JH (2007) Effect of gaps on species diversity in the naturally regenerated mixed broadleaved-Korean pine forest of the Xiaoxing’an mountains, China. J Ecol Environ 30(4):325–330
Jing X, Duan WB, Chen LX, Wang T, Du S, Zhang YS, Chen QM (2015) Spatial distribution pattern of main populations and gap makers in Picea koraiensis and Abies nephrolepis forest of Xiaoxing′an Mountains, Northeast China. Chin J Appl Ecol 26(10):2928–2936
Jönsson AM, Linderson ML, Stjernquist I, Schlyter P, Bäring L (2004) Climate change and the effect of temperature backlashes causing frost damage in Picea abies. Glob Planet Change 44(1–4):195–207
Laughlin GP, Kalma JD (1990) Frost risk mapping for landscape planning: a methodology. Theor Appl Climatol 42(1):41–51
Li DL, Jin YQ, Xiang QB (2005) Survey of the freezing injury of phoebe chekiangensis seedlings around Nanjing. J Jiangsu For Sci Technol 32(4):12–14
Li M, Duan WB, Chen LX, Liu Y, Gao ZQ (2012) Geostatistical analysis of extreme soil surface temperature of forest gap in Pinus koraiensis dominated broadleaved mixed forest. J Nat Resour 27(10):1688–1695
Li XF, Zhu JJ, Wang QL, Zhang JX, Zhu CY, Liu XF, Liu LM (2013) Research on the disturbance of frost damage to forests. Acta Ecol Sin 33(12):3563–3574
Lindkvist L, Chen D (1999) Air and soil frost indices in relation to plant mortality in elevated complex clear-felled terrain. Clim Res 12(1):65–75
Liu YY, Jin GZ, Li FR (2014) Influence of forest gaps on seedling establishment in a mixed broadleaved-Korean pine (Pinus koraiensis) forest in Xiao Xing′an Mountains. Chin Sci Bull 59(24):2396–2406
Luo Y, Tang HR, Zhang Y (2007) Effect of low temperature stress on activities of SOD and enzymes of ascorbate–glutathione cycle. Acta Hortic Sin 34(6):1405–1410
Muhamed H, Touzard B, Bagousse-Pinguet YL, Michalet R (2013) The role of biotic interactions for the early establishment of oak seedlings in coastal dune forest communities. For Ecol Manag 297(3):67–74
Nagel TA, Svoboda M, Rugani T, Diaci J (2010) Gap regeneration and replacement patterns in an old-growth Fagus–Abies forest of Bosnia–Herzegovina. Plant Ecol 208(2):307–318
Nordlander G, Hellqvist C, Johansson K, Nordenhem H (2011) Regeneration of European boreal forests: effectiveness of measures against seedling mortality caused by the pine weevil Hylobius abietis. For Ecol Manag 262(12):2354–2363
Nunez M, Bowman DMJS (1986) Nocturnal cooling in a high altitude stand of Eucalyptus delegatensis as related to stand density. Aust For Res 16(2):185–197
Rambo TR, North MP (2009) Canopy microclimate response to pattern and density of thinning in a Sierra Nevada forest. For Ecol Manag 257(2):435–442
Ramming A, Jönsson AM, Hickler T, Smith B, Bärring L, Sykes MT (2010) Impacts of changing frost regimes on Swedish forests: incorporating cold hardiness in a regional ecosystem model. Ecol Model 221(2):303–313
Romell E, Hallsby G, Karlsson A (2009) Forest floor light conditions in a secondary tropical rain forest after artificial gap creation in northern Borneo. Agric For Meteorol 149(6–7):929–937
Sane PV, Lvanov AG, Hurry V, Huner NP, Öquist G (2003) Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Physiol 132(4):2144–2151
Song Y, Zhang YX, Guo N, Sun GY (2013) Effects of lights on chlorophyll fluorescence characteristics and energy allocation pathways in leaves of Populus simonii × P. nigra seedlings after chilling stress. J Anhui Agric Sci 41(10):4421–4423
Stan AB, Daniels LD (2014) Growth releases across a natural canopy gap-forest gradient in old-growth forests. For Ecol Manag 313:98–103
Tan JJ (2013) Physiological and biochemical responses of Pinus massoniana superior provenance seedlings under artificial low temperature stress. Sci Silvae Sin 49(3):51–55
Tang JM, Zhai MP (2006) Morphological response and biomass allocation of Schima superb seedlings at different habitats in gap. J Huazhong Agric Univ 25(5):559–563
Tian Y, Zheng GY, Zhang HH, Xu N, Wang J, Sun GY (2013) Effects of light intensity and temperature on chlorophyll fluorescence in leaves of basil seedlings. Pratac Sci 30(10):1561–1568
Verduin JJ, Seidlitz A, Keulen MV, Paling EI (2013) Maximising establishment success of Amphibolis antarctica seedlings. J Exp Mar Biol Ecol 449(1770):57–60
Wang BY, Feng YL (2005) Effects of growth light intensities on photosynthesis in seedlings of two tropical rain forest species. Acta Ecol Sin 25(1):23–30
Wang N, Wu J, Xia PY, Su JL (2011) Physiological responses of Ilex latifolia to low temperature and its cold tolerance. J South China Agric Univ 32(3):82–86
Wang Y, Liu J, Zhang JX, Li XF, Zhu CY, Zhao TB, Yue Y, Zhan SY (2015) Spatial distribution characteristics of photosynthetic photon flux density and air temperature in gaps at two different slope directions of secondary forest ecosystem in montane area of eastern Liaoning Province. Chin J Ecol 34(4):933–940
Wu J, Wang ZQ, Liu XF (2002) Frost injury to young Tilia amurensis plantation. J Northeast For Univ 30(6):6–10
Yan T, Lü XT, Yang K, Zhu JJ (2016) Leaf nutrient dynamics and nutrient resorption: a comparison between larch plantations and adjacent secondary forests in Northeast China. J Plant Ecol 9:165–173
Yang K, Shi W, Zhu JJ (2013) The impact of secondary forests conversion into larch plantations on soil chemical and microbiological properties. Plant Soil 368(1–2):535–546
Zenner EK, Sagheb-Talebi K, Akhavan R, Peck JLE (2015) Integration of small-scale canopy dynamics smoothes live-tree structural complexity across development stages in old-growth Oriental beech (Fagus orientalis Lipsky) forests at the multi-gap scale. For Ecol Manag 335(2):26–36
Zhang YD (1992) Liaodong area meteorological disasters and disaster mitigation strategies. Meteorological Press, Beijing, pp 83–98
Zhang YP, Wang JX, Ma YX, Liu YH, Li YR (2002) The temporal-spatial distribution of temperature on the surface roughness of the tropical secondary forest gap in Xishuangbanna, Yunnan Province. Sci Silvae Sin 38(6):1–5
Zhou Q, Wang JZ, Chen XH (2010) Effect of durative low temperature on morphological and physiological characteristics of cucumber seedling. North Hortic 16:1–3
Zhu JJ, Mao ZH, Hu LL, Zhang JX (2007) Plant diversity of secondary forests in response to anthropogenic disturbance levels in montane regions of northeastern China. J For Res 12(6):403–416
Zhu JJ, Tan H, Li FQ, Chen M, Hu LL (2009) Comparison of near-ground air temperature and soil temperature of summer within three gaps of different sizes at secondary forests in Eastern Montane Regions of Liaoning Province. Sci Silvae Sin 45(8):161–165
Zhu JJ, Zhang GQ, Wang GF, Yan QL, Lu DL, Li XF, Zheng X (2015) On the size of forest gaps: can their lower and upper limits be objectively defined? Agric For Meteorol 213(2):64–76
Zhu CY, Wang Y, Li XF, Liu J, Zhang JX, Wang T (2016) Spatiotemporal distribution of the minimum temperature during autumn at different slope directions of secondary forest gap in montane zone of eastern Liaoning Province. Chin J Ecol 35(6):1411–1419
Acknowledgements
This work was supported by the National Key Research and Development Program of China (2016YFC0500302) and the National Nature Scientific Foundation Project of China (31200432). We thank Dr. Li-ning Song, Dr. Qiao-ling Yan, Dr. Kai-Yang and Ming-cai Li for their helpful suggestions on the earlier versions of this manuscript.
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Project funding: This work was supported by the National Key Research and Development Program of China(2016YFC0500302)and the National Nature Scientific Foundation Project of China (31200432).
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Corresponding editor: Chai Ruihai.
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Li, X., Wen, Y., Zhang, J. et al. The effect of low-temperature event on the survival and growth of Juglans mandshurica seedlings within forest gaps. J. For. Res. 29, 943–951 (2018). https://doi.org/10.1007/s11676-017-0520-6
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DOI: https://doi.org/10.1007/s11676-017-0520-6