Sudden openings and gradual closures in canopy cover modulate acclimation, survival, and growth of a shade-tolerant rainforest tree species

Ana Paula Moretti1,2, Flavia Yesica Olguin1,2,4, Juan Marcelo Gauna1,2,3, Corina Graciano1,2,3()

PDF
Journal of Forestry Research ›› 2024, Vol. 35 ›› Issue (1) : 91. DOI: 10.1007/s11676-024-01736-4
Original Paper

Sudden openings and gradual closures in canopy cover modulate acclimation, survival, and growth of a shade-tolerant rainforest tree species

  • Ana Paula Moretti1,2, Flavia Yesica Olguin1,2,4, Juan Marcelo Gauna1,2,3, Corina Graciano1,2,3()
Author information +
History +

Abstract

Forest disturbances at gap levels are one of the most important events for the regeneration and establishment of intermediate tree species. Abrupt canopy openings expose plants to high light intensity and high evaporative demands that stress shade-acclimated plants. Later, the slow closure of gaps reduces light availability to plants established when the incident irradiation was higher. This work evaluated the morphological and physiological acclimation of Cabralea canjerana (Vell) Mart. regeneration to sudden and to gradual changes in canopy cover. A pot experiment was carried out with plants exposed to a sudden opening. A few days after the light shock, plants rapidly increased photosynthetic rates and decreased leaf water potential. After two months, plants activated physiological responses at leaf and whole plant levels to high light and water stresses, e.g., increased stomatal conductance, stomatal index and reduction of leaf: fine roots ratio and chlorophyll. After seven months, hydraulic conductivity of petioles and the whole leaf increased, and growth was much higher than plants that remained under the canopy. In a field experiment in gaps in the rainforest, plants acclimated to all canopy covers. Seven years after planting, growth was maximum in open environments within the gaps, even if the canopy closed during the first 20 months after planting. In conclusion, if this species is planted to enrich the rainforest, positions within gaps with lower canopy cover should be chosen and gap closure will not affect growth. To manage C. canjerana natural regeneration, the opening of gaps and removal of understory will increase survival and growth without the risk that the stress caused by these sudden openings could lead to the death of seedlings. Combining pot and field experiments helps to understand the autecology of trees with particular ecological interest, and to build sound restoration practices.

Keywords

Cabralea canjerana / Atlantic forest / Abiotic stress / Regeneration / Seedling

Cite this article

Download citation ▾
Ana Paula Moretti, Flavia Yesica Olguin, Juan Marcelo Gauna, Corina Graciano. Sudden openings and gradual closures in canopy cover modulate acclimation, survival, and growth of a shade-tolerant rainforest tree species. Journal of Forestry Research, 2024, 35(1): 91 https://doi.org/10.1007/s11676-024-01736-4

References

[1]
Aimi SC, Araujo MM, Tabaldi LA, Tonetto TD, Zavistanovicz TC, Berghetti áL (2020) Shading as a determinant factor for the survival and growth of Cabralea canjerana in Southern Brazil. Cerne 26:349–355. https://doi.org/10.1590/01047760202026032743
[2]
Amir AA (2012) Canopy gaps and the natural regeneration of Matang Mangroves. For Ecol Manag 269(1):60–67. https://doi.org/10.1016/j.foreco.2011.12.040
[3]
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II. inactivation, protein damage and turnover. BBA-Bioenerg 1143:113–134
[4]
Berghetti áLP, Araujo MM, Tabaldi LA, Turchetto F, Aimi SC, Rorato DG, Marchezan C, Griebeler AM, Barbosa FM, Brunetto G (2020) Morphological, physiological and biochemical traits of Cordia trichotoma under phosphorous application and a water-retaining polymer. J for Res 32:855–865. https://doi.org/10.1007/s11676-020-01132-8
[5]
Calzavara AK, Bianchini E, Mazzanatti T, Oliveira HC, Stolf-Moreira R, Pimenta JA (2015) Morphoanatomy and ecophysiology of tree seedlings in semideciduous forest during high-light acclimation in nursery. Photosynthetica 53(4):597–608. https://doi.org/10.1007/s11099-015-0151-0
[6]
Campanello PI, Genoveva Gatti M, Ares A, Montti L, Goldstein G (2007) Tree regeneration and microclimate in a liana and bamboo-dominated semideciduous Atlantic forest. For Ecol Manag 252(1–3):108–117. https://doi.org/10.1016/j.foreco.2007.06.032
[7]
Campanello PI, Villagra M, Garibaldi JF, Ritter LJ, Araujo JJ, Goldstein G (2012) Liana abundance, tree crown infestation, and tree regeneration ten years after liana cutting in a subtropical forest. For Ecol Manag 284:213–221. https://doi.org/10.1016/j.foreco.2012.07.043
[8]
Campoe OC, Iannelli C, Stape JL, Cook RL, Mendes JCT, Vivian R (2014) Atlantic forest tree species responses to silvicultural practices in a degraded pasture restoration plantation: from leaf physiology to survival and initial growth. For Ecol Manag 313:233–242. https://doi.org/10.1016/j.foreco.2013.11.016
[9]
Campoe OC, Stape JL, Mendes JCT (2010) Can intensive management accelerate the restoration of Brazil’s Atlantic forests? For Ecol Manag 259(9):1808–1814. https://doi.org/10.1016/j.foreco.2009.06.026
[10]
Caquet B, Barigah TS, Cochard H, Montpied P, Collet C, Dreyer E, Epron D (2009) Hydraulic properties of naturally regenerated beech saplings respond to canopy opening. Tree Physiol 29(11):1395–1405. https://doi.org/10.1093/treephys/tpp067
[11]
Carter JL, White DA (2009) Plasticity in the Huber value contributes to homeostasis in leaf water relations of a mallee Eucalypt with variation to groundwater depth. Tree Physiol 29(11):1407–1418. https://doi.org/10.1093/treephys/tpp076
[12]
Crawford AJ, McLachlan DH, Hetherington AM, Franklin KA (2012) High temperature exposure increases plant cooling capacity. Curr Biol 22(10):R396–R397. https://doi.org/10.1016/j.cub.2012.03.044
[13]
Denslow JS (1987) Tropical rainforest gaps and tree species diversity. Annu Rev Ecol Syst 18:431–451. https://doi.org/10.1146/annurev.es.18.110187.002243
[14]
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2020) InfoStat versión 2020. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar
[15]
Duan H, Wang D, Zhao N, Huang G, de Dios VR (2022) Tissue DT limited hydraulic recovery in seedlings of six tree species with contrasting leaf habits in subtropical China. Front Plant Sci 13:967187. https://doi.org/10.3389/fpls.2022.967187
[16]
Felton A, Felton AM, Wood J, Lindenmayer DB (2006) Vegetation structure, phenology, and regeneration in the natural and anthropogenic tree-fall gaps of a reduced-impact logged subtropical Bolivian forest. For Ecol Manag 235(1–3):186–193. https://doi.org/10.1016/j.foreco.2006.08.011
[17]
Fracheboud Y, Leipner J (2003) The application of chlorophyll fluorescence to study light, temperature, and drought stress. In: DeEll JR, Toivonen PMA (eds) Practical applications of chlorophyll fluorescence in plant biology. Springer, US, pp 125–150
[18]
Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: Seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30(1):19–30. https://doi.org/10.1111/j.1365-3040.2006.01600.x
[19]
Gálhidy L, Mihók B, Hagyó A, Rajkai K, Standovár T (2006) Effects of gap size and associated changes in light and soil moisture on the understorey vegetation of a Hungarian beech forest. Plant Ecol 183:133–145. https://doi.org/10.1007/s11258-005-9012-4
[20]
Gandolfi S, Joly CA, Leit?o Filho HDF (2009) “Gaps of deciduousness”: cyclical gaps in tropical forests. Sci Agric 66(2):280–284. https://doi.org/10.1590/S0103-90162009000200020
[21]
Garbarino M, Mondino EB, Lingua E, Nagel TA, Duki? V, Govedar Z, Motta R (2012) Gap disturbances and regeneration patterns in a Bosnian old-growth forest: a multispectral remote sensing and ground-based approach. Ann for Sci 69:617–625. https://doi.org/10.1007/s13595-011-0177-9
[22]
Haworth M, Elliott-Kingston C, McElwain JC (2011) The stomatal CO2 proxy does not saturate at high atmospheric CO2 concentrations: evidence from stomatal index responses of Araucariaceae conifers. Oecologia 167:11–19. https://doi.org/10.1007/s00442-011-1969-1
[23]
Hernandez Velasco M, Mattsson A (2020) Light shock stress after outdoor sunlight exposure in seedlings of Picea abies (L.) Karst and Pinus sylvestris L. pre-cultivated under LEDs—possible mitigation treatments and their energy consumption. Forests 11(3):354. https://doi.org/10.3390/f11030354
[24]
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485
[25]
Kraj W, ?lepaczuk A (2022) Morphophysiological acclimation of developed and senescing beech leaves to different light conditions. Forests 13(8):1333. https://doi.org/10.3390/f13081333
[26]
Lavinsky AO, Gomes FP, Mielke MS, Fran?a S (2014) Photosynthetic acclimation in shade-developed leaves of Euterpe edulis Mart (Arecaceae) after long-term exposure to high light. Photosynthetica 52(3):351–357. https://doi.org/10.1007/s11099-014-0038-5
[27]
Li XN, Wang YH, Yang ZH, Liu T, Mu CC (2022) Photosynthesis adaption in Korean pine to gap size and position within Populus davidiana forests in Xiaoxing’anling, China. J for Res 33:1517–1527. https://doi.org/10.1007/s11676-021-01439-0
[28]
Melcher PJ, Holbrook MN, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol Evol 3(4):685–694. https://doi.org/10.1111/j.2041-210X.2012.00204.x
[29]
Mohammed GH, Zarco-Tejada P, Miller JR (2003) Applications of chlorophyll fluorescence in forestry and ecophysiology. Practical applications of chlorophyll fluorescence in plant biology. Springer, US, pp 79–124
[30]
Montgomery RA, Chazdon RL (2002) Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131:165–174. https://doi.org/10.1007/s00442-002-0872-1
[31]
Moretti AP, Olguin FY, Pinazo MA, Graciano C (2019) Water and light stresses drive acclimation during the establishment of a timber tree under different intensities of rainforest canopy coverage. Cerne 25(1):93–104. https://doi.org/10.1590/01047760201925012616
[32]
Murphy MRC, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant Cell Environ 35:1407–1418. https://doi.org/10.1111/j.1365-3040.2012.02498.x
[33]
Olguin FY, Moretti AP, Pinazo MA, Graciano C (2019) Morpho-physiological acclimation to canopy coverage of Araucaria angustifolia during the establishment in the Atlantic forest Argentina. Bosque 40(3):323–333. https://doi.org/10.4067/S0717-92002019000300323
[34]
Prado K, Maurel C (2013) Regulation of leaf hydraulics: from molecular to whole plant levels. Front Plant Sci 4:51890. https://doi.org/10.3389/fpls.2013.00255
[35]
Quevedo-Rojas A, García-Nú?ez C, Jerez-Rico M, Jaimez R, Schwarzkopf T (2018) Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest. Funct Plant Biol 45(9):968–982. https://doi.org/10.1071/FP17308
[36]
Rungwattana K, Hietz P (2018) Radial variation of wood functional traits reflect size-related adaptations of tree mechanics and hydraulics. Funct Ecol 32(2):260–272. https://doi.org/10.1111/1365-2435.12970
[37]
Sanches MC, Marzinek J, Bragiola NG, Terra Nascimento AR (2017) Morpho-physiological responses in Cedrela fissilis Vell. submitted to changes in natural light conditions: implications for biomass accumulation. Trees-Struct Funct 31:215–227. https://doi.org/10.1007/s00468-016-1474-6
[38]
Smith WK, Berry ZC (2013) Sunflecks? Tree Physiol 33(3):233–237. https://doi.org/10.1093/treephys/tpt005
[39]
Szymańska R, ?lesak I, Orzechowska A, Kruk J (2017) Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot 139:165–177. https://doi.org/10.1016/j.envexpbot.2017.05.002
[40]
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16(1):53–60. https://doi.org/10.1016/j.tplants.2010.10.001
[41]
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
[42]
Tozzi ES, Easlon HM, Richards JH (2013) Interactive effects of water, light and heat stress on photosynthesis in Fremont cottonwood. Plant Cell Environ 36(8):1423–1434. https://doi.org/10.1111/pce.12070
[43]
Turchetto F, Araujo MM, Tabaldi LA, Griebeler AM, Rorato DG, Aimi SC, Berghetti áLP, Gomes DR (2016) Can transplantation of forest seedlings be a strategy to enrich seedling production in plant nurseries? For Ecol Manag 375:96–104. https://doi.org/10.1016/j.foreco.2016.05.029
[44]
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin
[45]
Valladares F, Niinemets ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol, Evol Syst 39:237–257. https://doi.org/10.1146/annurev.ecolsys.39.110707.173506
[46]
Vilhar U, Simon?i? P (2012) Water status and drought stress in experimental gaps in managed and semi-natural silver fir-beech forests. Euro J for Res 131:1381–1397. https://doi.org/10.1007/s10342-012-0605-x
[47]
Wright JS, Muller-Landau HC, Condit R, Hubbell SP (2003) Gap-dependent recruitment, realized vital rates, and size distributions of tropical trees. Ecology 84(12):3174–3185. https://doi.org/10.1890/02-0038
[48]
Wyka TP, Robakowski P, ?ytkowiak R, Oleksyn J (2022) Anatomical acclimation of mature leaves to increased irradiance in sycamore maple (Acer pseudoplatanus L.). Photosynth Res 154:41–55. https://doi.org/10.1007/s11120-022-00953-4
[49]
Zimmermann AP, Fleig FD, Tabaldi LA (2019) Aimi SC Morphological and physiological plasticity of saplings of Cabralea canjerana (Vell.) Mart in different light conditions. Revista árvore 43:e430103. https://doi.org/10.1590/1806-90882019000100003
PDF

Accesses

Citations

Detail

Sections
Recommended

/