Abstract
Phenotypic plasticity occurs when plants acclimatize to contrasting conditions. Herein, we test the hypothesis that seedlings of a light-demanding species have greater phenotypic plasticity compared to seedlings of a shade-tolerant species under high irradiance. Thus, we investigate the growth, anatomical, and leaf gas exchange responses of Citharexylum myrianthum, a light-demanding species, and Poecilanthe parviflora, a shade-tolerant species, under full light and 60% shading. Under full light, the seedlings of both species were shorter, showed lower photosynthetic rates and specific leaf area, and thicker palisade parenchyma. In the same conditions, C. myrianthum showed increased number of leaves, and P. parviflora reduced leaf area and increased number of stomata and allocation of phloem and cortical parenchyma. Lower photosynthetic rates may negatively affect biomass allocation and growth, although C. myrianthum seems to show a higher tolerance to irradiance since it produced more leaves. P. parviflora seems to optimize heat dissipation, reduce water loss, and improve the allocation of photoassimilate transport and storage, which could increase performance during establishment in field conditions. The plasticity index of both species was similar. Thus, generalizations about the species plasticity and ecological group to which they belong should be avoided. Species-related responses of growth, anatomical, and gas exchange parameters were found, indicating that generalizations about the performance of functional groups should also be avoided. These findings may contribute to the success of forest restoration projects.
Similar content being viewed by others
References
Bragg JG, Westoby M (2002) Leaf size and foraging for light in a sclerophyll woodland. Funct Ecol 16:633–639. https://doi.org/10.1046/j.1365-2435.2002.00661.x
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 53:597–608. https://doi.org/10.1007/s11099-015-0151-0
Campoe OC, Stape JL, Mendes JCT (2010) Can intensive management accelerate the restoration of Brazil’s atlantic forests? For Ecol Manag 259:1808–1814. https://doi.org/10.1016/j.foreco.2009.06.026
Carvalho PER (2003) Espécies arbóreas brasileiras. Embrapa Informação Tecnológica, Colombo
Castro EM, Pereira FJ, Paiva R (2009) Histologia vegetal: estrutura e função de órgãos vegetativos. UFLA, Lavras
Chapin FS III (1980) The mineral nutrition of wild plants. Annu Ver Ecol Syst 11:233–260. https://doi.org/10.1146/annurev.es.11.110180.001313
DeLucia EH, Nelson K, Vogelmann TC, Smith WK (1996) Contribution of internal reflectance to light absorption and photosynthesis of shade leaves. Plant Cell Environ 19:159–170. https://doi.org/10.1111/j.1365-3040.1996.tb00237.x
DeWitt TJ, Scheiner SM (2004) Phenotypic variation from single genotypes: a primer. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, USA, pp 1–9
Dickson A, Leaf AL, Hosner JF (1960) Quality appraisal of white spruce and white pine seedling stock in nurseries. For Chron 36:10–13. https://doi.org/10.5558/tfc36010-1
Duryea ML (1984) Nursery cultural practices: impacts on seedling quality. In: Duryea ML, Landis TD, Perry CR (eds) Forestry nursery manual: production of bareroot seedlings, forestry sciences. Springer, Dordrecht, pp 143–164
Evans JE, 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
Fagundes MC, Dalmolin AC, Lobo LS, Schilling AC, Santos MS, Mielke MS (2021) Growth and phenotypic plasticity of two tropical tree species under low light availability. J Plant Ecol 14:270–279. https://doi.org/10.1093/jpe/rtaa095
Favaretto VF, Martinez CA, Soriani HH, Furriel RPM (2011) Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions. Environ Exp Bot 70:20–28. https://doi.org/10.1016/j.envexpbot.2010.06.003
Ferreira OGL, Rossi FD, Vaz RZ, Fluck AC, Costa OAD, Farias PP (2017) Leaf area determination by digital image analysis. Arch Zootec 66:593–597
Firmino TP, Souza LA, Barbeiro C, Marcílio T, Romagnolo MB, Pastorini LG (2021) Influence of the light on the morphophysiological responses of native trees species of the semidecidual stational forest. Braz J Bot 44:963–976. https://doi.org/10.1007/s40415-021-00754-4
Gaburro TA, Zanetti LV, Gama VN, Milanez CRD, Cuzzuol GRF (2015) Physiological variables related to photosynthesis are more plastic than the morphological and biochemistry in non-pioneer tropical trees under contrasting irradiance. Braz J Bot 38:39–49. https://doi.org/10.1007/s40415-014-0113-y
Gates DM (1980) Biophysical ecology. Springer-Verlag, New York
Gebauer R, Urban J, Volaˇrík D, Matouˇsková M, Vitásek R, Houˇsková K, Hurt V, Pantová P, Polívková T, Plichta R (2022) Does leaf gas exchange correlate with petiole xylem structural traits in Ulmus laevis seedlings under well-watered and drought stress conditions? Tree Physiol 42:2534–2545. https://doi.org/10.1093/treephys/tpac082
Grossnickle SC, MacDonald JE (2018) Seedling quality: history, application, and plant attributes. Forests 9:283. https://doi.org/10.3390/f9050283
Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manag 148:185–206. https://doi.org/10.1016/S0378-1127(00)00535-1
Hanba YT, Kogami H, Terashima I (2002) The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant Cell Environ 25:1021–1030. https://doi.org/10.1046/j.1365-3040.2002.00881.x
Höhl M, Ahimbisibwe V, Stanturf JÁ, Elsasser P, Kleine M, Bolte A (2020) Forest landscape restoration—what generates failure and success? Forests 11:938. https://doi.org/10.3390/f11090938
Jacobs DF, Salifu KF, Seifert J (2005) Relative contribution of initial root and shoot morphology in predicting field performance of hardwood seedlings. New For 30:235–251. https://doi.org/10.1007/s11056-005-5419-y
Jaenicke H (1999) Seedling quality. In: Jaenicke H (ed) Good tree nursery practices: practical guidelines for research nurseries. ICRAF, Nairobi, pp 7–21
Johansen DA (1940) Plant microtechnique. McGraw Hill, New York
Kraus JE, Souza HC, Rezende MH, Castro NM, Vecchi C, Luque R (1998) Astra blue and basic fuchsin double staining of plant materials. Biotech Histochem 73:235–243. https://doi.org/10.3109/10520299809141117
Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional groups. Springer, Berlin
Lovelock CE, Jebb M, Osmond CB (1994) Photoinhibition and recovery in tropical plant species: response to disturbance. Oecologia 97:297–307. https://doi.org/10.1007/BF00317318
Mathur S, Jain L, Jajoo A (2018) Photosynthetic efficiency in sun and shade plants. Photosynthetica 56:354–365. https://doi.org/10.1007/s11099-018-0767-y
Mazzanatti T, Calzavara AK, Pimenta JA, Oliveira HC, Stolf-Moreira R, Bianchini E (2016) Light acclimation in nursery: morphoanatomy and ecophysiology of seedlings of three light-demanding neotropical tree species. Braz J Bot 39:19–28. https://doi.org/10.1007/s40415-015-0203-5
McAusland L, Vialet-Chabrand S, Davey P, Baker NR, Brendel O, Lawson T (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211:1209–1220. https://doi.org/10.1111/nph.14000
Mengarda LGH, Milanez CRD, Silva DM, Aguilar MAG, Cuzzuol GRF (2012) Morphological and physiological adjustments of Brazilwood (Caesalpinia echinata Lam.) To direct solar radiation. Braz J Plant Physiol 24:161–172. https://doi.org/10.1590/S1677-04202012000300003
Molin PG, Chazdon R, de Barros Ferraz SF, Brancalion PHS (2018) A landscape approach for cost-effective large-scale forest restoration. J Appl Ecol 55:2767–2778. https://doi.org/10.1111/1365-2664.13263
Morais Junior VTM, Jacovine LAG, Torres CMME, Alvesa EBBM, Paiva HN, Alcántara-de la Cruz R, Zanuncio JC (2019) Early assessment of tree species with potential for carbon offset plantations in degraded area from the Southeastern Brazil. Ecol Indic 98:854–860. https://doi.org/10.1016/j.ecolind.2018.12.004
Moura CJR, Nunes MFSQC, Abreu RCR (2022) A novel monitoring protocol to evaluate large–scale forest restoration projects in the tropics. Trop Ecol 63:113–121. https://doi.org/10.1007/s42965-021-00194-x
Nave AG, Rodrigues RR (2007) Combination of species into filling and diversity groups as forest restoration methodology. In: Rodrigues RR et al (eds) High diversity forest restoration in degraded areas: methods and projects in Brazil. Nova Science Publishers, Inc, New York, pp 103–126
Niinemets Ü, Lukjanova A, Turnbull MH, Sparrow AD (2007) Plasticity in mesophyll volume fraction modulates light-acclimation in needle photosynthesis in two pines. Tree Physiol 27:1137–1151. https://doi.org/10.1093/treephys/27.8.1137
Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–927. https://doi.org/10.1111/j.1365-3040.2005.01344.x
Õunapuu-Pikas E, Venisse JS, Label P, Sellin A (2022) Leaf and branch hydraulic plasticity of two light-demanding broadleaved tree species differing in water-use strategy. Forests 13:594. https://doi.org/10.3390/f13040594
Paraná IDR (2022) Médias Históricas—Período 1976/2019. https://www.idrparana.pr.gov.br/Pagina/Dados-Meteorologicos-Historicos-e-Atuais. Accessed 22 Oct 2022
Poorter L, McDonald I, Alarco A, Fichtler E, Licona JC, Penã-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492. https://doi.org/10.1111/j.1469-8137.2009.03092.x
Poorter H, Niinemets U, Ntagkas N, Siebenkäs A, Mäenpää M, Matsubara S, Pons TL (2019) A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytol 223:1073–1105. https://doi.org/10.1111/nph.15754
Portela FSC, Macieira BPB, Zanetti LV, Gama VN, Silva DM, Milanez CRD, Cuzzuol GRF (2019) How does Cariniana estrellensis respond to different irradiance levels? J For Res 30:31–44. https://doi.org/10.1007/s11676-017-0578-1
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Phvsiol 35:15–44.
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rezende CL, Scarano FR, Assadd ED, Joly CA, Metzger JP, Strassburg BBN, Tabarelli M, Fonseca GA, Mittermeier RA (2018) From hotspot to hopespot: an opportunity for the Brazilian atlantic forest. Perspect Ecol Conserv 16:208–214. https://doi.org/10.1016/j.pecon.2018.10.002
Rodrigues RR, Gandolfi S, Nave AG, Aronson J, Barreto TE, Vidal CY, Brancalion PHS (2011) Large-scale ecological restoration of high-diversity tropical forests in SE Brazil. For Ecol Manag 261:1605–1613. https://doi.org/10.1016/j.foreco.2010.07.005
Rozendaal DMA, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light: relationships with demand and adult stature. Funct Ecol 20:207–216. https://doi.org/10.1111/j.1365-2435.2006.01105.x
Smith WK, Vogelmann TC, DeLucia EH, Bell DT, Shepherd KA (1997) Leaf form and photosynthesis—do leaf structure and orientation interact to regulate internal light and carbon dioxide? Bioscience 47:785–793. https://doi.org/10.2307/1313100
SOS Mata Atlântica Foundation, INPE (2021) Atlas dos remanescentes florestais da mata Atlântica: período 2019/2020, relatório técnico. Fundação SOS Mata Atlântica, São Paulo, p 73
Souza GM, Sato AM, Ribeiro RV, Prado CHBA (2010) Photosynthetic responses of four tropical tree species grown under gap and understorey conditions in a semi-deciduous forest. Braz J Bot 33:529–538. https://doi.org/10.1590/S0100-84042010000400002
Terashima I, Miyazawa SI, Hanba Y (2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105. https://doi.org/10.1007/PL00013972
Tserej O, Feeley KJ (2021) Variation in leaf temperatures of tropical and subtropical trees are related to leaf thermoregulatory traits and not geographic distributions. Biotropica 53:868–878. https://doi.org/10.1111/btp.12919
Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequence. Annu Rev Ecol Evol Syst 39:237–257. https://doi.org/10.1146/annurev.ecolsys.39.110707.173506
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116. https://doi.org/10.1111/j.1365-2745.2006.01176.x
Vogelmann TC (1993) Plant tissue optics. Annu Rev Plant Physiol 44:231–251. https://doi.org/10.1146/annurev.pp.44.060193.001311
Vogelmann TC, Martin G (1993) The functional significance of palisade tissue: penetration of directional versus diffuse light. Plant Cell Environ 16:65–72. https://doi.org/10.1111/j.1365-3040.1993.tb00845.x
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Yamashita N, Ishida A, Kushima H, Tanaka N (2000) Acclimation to sudden increase in light favoring an invasive over native trees in subtropical Islands. Jpn Oecol 125:412–419. https://doi.org/10.1007/s004420000475
Zanon JA, Silva FAM, Silva RB, de Paula RC, Mariano LF (2021) Impact of sand mining: a case study of initial growth of forest species for recovery of degraded areas. Bosque 42:111–120. https://doi.org/10.4067/S0717-92002021000100111
Zhong M, Cerabolini BEL, Castro-Díez P, Puyravaud JP, Cornelissen JHC (2020) Allometric co-variation of xylem and stomata across diverse woody seedlings. Plant Cell Environ 43:2301–2310. https://doi.org/10.1111/pce.13826
Acknowledgements
We acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a scholarship awarded to T.V.D. and the Fundação Araucária (FAPPR) for scholarships awarded to A.C.S.O. and D.N.B.
Author information
Authors and Affiliations
Contributions
EB, HCO, JAP and RSM designed the study. TVD, ACSO, DNB and AKC conducted the experiment, collected the biological material, and performed the measurements. TVD, ACSO, DNB, AKC, CM, and MB performed the analysis and interpreted the results. All authors contributed to writing the article and have approved the final version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare the absence of any commercial or financial relationships that could be indicated a potential conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Debiasi, T.V., Ornelas, A.C.S., Brauco, D.N. et al. Irradiance triggers different morphophysiological responses in two neotropical tree seedlings with contrasting light demands. Theor. Exp. Plant Physiol. 36, 33–50 (2024). https://doi.org/10.1007/s40626-023-00303-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-023-00303-2