Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest

Ana Quevedo-Rojas A F , Carlos García-Núñez B , Mauricio Jerez-Rico C , Ramón Jaimez D E and Teresa Schwarzkopf B
+ Author Affiliations
- Author Affiliations

A Facultad de Ciencias Forestales y Ambientales. Escuela Técnica Superior Forestal, Universidad de Los Andes, Mérida, 5101, Venezuela.

B Facultad de Ciencias, Instituto de Ciencias Ambientales y Ecológicas, Universidad de Los Andes, Mérida, 5101, Venezuela.

C Facultad de Ciencias Forestales y Ambientales, Centro de Estudios Forestales and Ambientales de Postgrado, Universidad de Los Andes, Mérida, 5101, Venezuela.

D Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Portoviejo, 130105, Ecuador.

E Facultad de Ciencias Forestales y Ambientales, Instituto de Investigaciones Agropecuarias, Universidad de Los Andes, Mérida, 5101, Venezuela.

F Corresponding author. Email: anamer2@gmail.com

Functional Plant Biology 45(9) 968-982 https://doi.org/10.1071/FP17308
Submitted: 3 November 2017  Accepted: 20 March 2018   Published: 9 May 2018

Abstract

To study the acclimation responses of the leaves of saplings of six tree species when changed to low or high levels of irradiance, we carried out a light exposure experiment. Species representative of contrasting shade tolerance groups were identified across a light gradient in the understorey of a Venezuelan Andean cloud forest. Measured traits included gas exchange, chlorophyll fluorescence, and morphoanatomical, biochemical and optical properties. Saplings were grown for 6 months in a shade-house receiving 20% photosynthetic photon flux (PPF) of full sunlight. Plant samples were then moved to shade-houses receiving low PPF (4%) or high PPF (65%). A factorial model (species × PPF), with repeated measurements (0, 15 and 120 days) was designed. Our results showed that morphological and anatomical traits were more plastic to PPF changes than photosynthetic traits. All species were susceptible to photoinhibition (15 days): shade-intolerant species showed dynamic photoinhibition (120 days), whereas shade-tolerant species presented chronic photoinhibition and the consequent inability to increase C assimilation rates under high PPF. The partially shade-tolerant species showed mixed responses; nonetheless, they exhibited larger adjustments in morphoanatomical and optical properties. Thus the acclimation responses of these species when subject to contrasting light conditions could help to explain their distribution along the light gradient in the understorey.

Additional keywords: chlorophyll fluorescence, gas exchange, leaf morphoanatomical properties, leaf optical properties, photoinhibition.


References

Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. Journal of Photochemistry and Photobiology. B, Biology 104, 1–8.
Recent progress in the studies of structure and function of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFWjsrY%3D&md5=d80ae0a3f4540802f0567745c5beb757CAS |

Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound. Biochemistry 36, 4149–4154.
Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVeht7Y%3D&md5=244509acb398baf18561ed0acce7f4edCAS |

Arnon DI (1949) Copper enzyme in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Copper enzyme in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH1MXhtFaqtg%3D%3D&md5=5c90b0c251acc14d947b0ad2c9441e9eCAS |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsL8%3D&md5=eea37a86aa6c49adebecb01da5cc5ad4CAS |

Barker MG, Press MC, Brown ND (1997) Photosynthetic characteristics of dipterocarp seedlings in three tropical rain forest light environments: a basis for niche partitioning? Oecologia 112, 453–463.
Photosynthetic characteristics of dipterocarp seedlings in three tropical rain forest light environments: a basis for niche partitioning?Crossref | GoogleScholarGoogle Scholar |

Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annual Review of Plant Biology 28, 355–377.
Comparative photosynthesis of sun and shade plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXksFSitr4%3D&md5=35870bdd9b02a65e9d02ab397424ecf5CAS |

Castro-Esau KL, Sanchez-Azofeifa GA, Rivard B, Wright SJ, Quesada M (2006) Variability in leaf optical properties of Mesoamerican trees and the potential for species classification. American Journal of Botany 93, 517–530.
Variability in leaf optical properties of Mesoamerican trees and the potential for species classification.Crossref | GoogleScholarGoogle Scholar |

Cendrero-Mateo MP, Carmo-Silva AE, Porcar-Castell A, Hamerlynck EP, Papuga SA, Moran MS (2015) Dynamic response of plant chlorophyll fluorescence to light, water and nutrient availability. Functional Plant Biology 42, 746–757.
Dynamic response of plant chlorophyll fluorescence to light, water and nutrient availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFyru7nJ&md5=cc195e18d73af2134f26242d3ce1af55CAS |

Chazdon RL, Fetcher N (1984) Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. Journal of Ecology 72, 553–564.
Photosynthetic light environments in a lowland tropical rain forest in Costa Rica.Crossref | GoogleScholarGoogle Scholar |

Chazdon R, Pearcy W (1991) The importance of sunflecks for forest understory plants. Bioscience 41, 760–766.
The importance of sunflecks for forest understory plants.Crossref | GoogleScholarGoogle Scholar |

Chazdon R, Pearcy R, Lee D, Fetcher N (1996) Photosynthetic responses of tropical forest plants to contrasting light environments. In ‘Tropical forest plant ecophysiology’. (Eds SS Mulkey, RL Chazdon, AP Smith) pp. 5–55. (Springer: New York)

Chen J, Zhang Q, Li X, Cao K (2011) Steady and dynamic photosynthetic responses of seedling from contrasting successional groups under low-light growth conditions. Physiologia Plantarum 141, 84–95.
Steady and dynamic photosynthetic responses of seedling from contrasting successional groups under low-light growth conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1SgtA%3D%3D&md5=b4e693e032d3e470b3888d5fde2ec48bCAS |

Endler JA (1993) The color of light in forests and its implications. Ecological Monographs 63, 1–27.
The color of light in forests and its implications.Crossref | GoogleScholarGoogle Scholar |

Evans JR, 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 & Environment 24, 755–767.
Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsFCmurk%3D&md5=0fb61007f24009ea88d40c7da1d3ced4CAS |

García-Núñez C, Azócar A, Rada F (1995) Photosynthetic acclimation to light in juveniles of two cloud forest tree species. Trees 10, 114–124.
Photosynthetic acclimation to light in juveniles of two cloud forest tree species.Crossref | GoogleScholarGoogle Scholar |

Givnish TJ (1988) Adaptation to sun and shade: a whole plant perspective. Australian Journal of Plant Physiology 15, 63–92.
Adaptation to sun and shade: a whole plant perspective.Crossref | GoogleScholarGoogle Scholar |

Goldstein G, Santiago LS, Campanello PI, Avalos G, Zhang YJ, Villagra M (2016). Facing shortage or excessive light: how tropical and subtropical trees adjust their photosynthetic behavior and life history traits to a dynamic forest environment. In ‘Tropical tree physiology: adaptations and responses in a changing environment’. (Eds G Goldstein, LS Santiago) pp. 319–336. (Springer: Dordrecht, The Netherlands).

Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 63, 869–893.
Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs12ntrvF&md5=4258e8911b936c944fc16e2214a6a917CAS |

Griffin JJ, Ranney TG, Pharr DM (2004) Photosynthesis, chlorophyll fluorescence and carbohydrate content of Illicium taxa grown under varied irradiance. Journal of the American Society for Horticultural Science 129, 46–53.

Kitajima K (1994) Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98, 419–428.
Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees.Crossref | GoogleScholarGoogle Scholar |

Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum 86, 180–187.
Relationship between photosystem II activity and CO2 fixation in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSgsbg%3D&md5=78669bfaf1b7a834c7a0ed68b7fedef1CAS |

Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology 42, 313–349.
Chlorophyll fluorescence and photosynthesis: the basics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFSmsrc%3D&md5=2c653d591bf905cd3d4df9a6ddabb70eCAS |

Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant, Cell & Environment 24, 1345–1352.
Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFCltA%3D%3D&md5=d13cea1deb4f1ff9755b18f20d942c39CAS |

Letts MG, Mulligan M (2005) The impact of light quality and leaf wetness on photosynthesis in north-west Andean tropical montane cloud forest. Journal of Tropical Ecology 21, 549–557.
The impact of light quality and leaf wetness on photosynthesis in north-west Andean tropical montane cloud forest.Crossref | GoogleScholarGoogle Scholar |

Liang KM, Lin ZF, Liu N, Zhang QM, Wang J, Wang ZF, Guan LL (2010) Characteristics of sun- and shade-adapted populations of an endangered plant Primulina tabacum Hance. Photosynthetica 48, 494–506.
Characteristics of sun- and shade-adapted populations of an endangered plant Primulina tabacum Hance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1Gmsw%3D%3D&md5=66d800bc4d3bbbd7358cd3bca5606ce1CAS |

Márquez O (1990) Génesis de una secuencia de suelos en el Bosque Experimental San Eusebio, La Carbonera, Estado Mérida. Revista Forestal Venezolana 32, 133–150.

Matthew EG, Pou A, Zwieniecki MA, Holbrook NM (2012) On measuring the response of mesophyll conductance to carbon dioxide with the variable J method. Journal of Experimental Botany 63, 413–425.
On measuring the response of mesophyll conductance to carbon dioxide with the variable J method.Crossref | GoogleScholarGoogle Scholar |

Maxwell K, Johnson G (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=9e83b12b5b0047c2d8ec3840387ee7aaCAS |

Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves – relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant & Cell Physiology 46, 629–637.
CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves – relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslGrtLY%3D&md5=eda67a30f44c978753a734b6bf784f65CAS |

Mulkey SS, Pearcy RW (1992) Interactions between acclimation and photoinhibition of photosynthesis of a tropical forest understory herb, Alocasia macrorrhiza, during simulated canopy gap formation. Functional Ecology 6, 719–729.
Interactions between acclimation and photoinhibition of photosynthesis of a tropical forest understory herb, Alocasia macrorrhiza, during simulated canopy gap formation.Crossref | GoogleScholarGoogle Scholar |

Müller L (1961) Un aparato de micro Kjeldahl simple para análisis rutinarios rápidos de materiales vegetales. Turrialba 11, 17–25.

Oberbauer SF, Strain BR (1986) Effects of canopy position and irradiance on leaf physiology and morphology of Pentaclethra macroloba (Mimosaceae). American Journal of Botany 73, 409–416.
Effects of canopy position and irradiance on leaf physiology and morphology of Pentaclethra macroloba (Mimosaceae).Crossref | GoogleScholarGoogle Scholar |

Poorter L, Kwant R, Hernández R, Medina E, Werger MJA (2000) Leaf optical properties in Venezuelan cloud forest trees. Tree Physiology 20, 519–526.
Leaf optical properties in Venezuelan cloud forest trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs1Wqu7c%3D&md5=a6f94af2311beeface7fbe236a6dfe8fCAS |

Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research 73, 149–156.
The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVGltb8%3D&md5=0e279a93a711d82901aa8b16b113d891CAS |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvent: verification of the concentration of chorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvent: verification of the concentration of chorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=14f84141eddcb544e9e58c981c910743CAS |

Quevedo A, Jerez M, Schwarzkopf T, García C (2015) Distribution of juveniles of tree species along a canopy closure gradient in a tropical cloud forest of the Venezuelan Andes. iForest-Biogeosciences and Forestry 9, 353

Quevedo A, Schwarzkopf T, García C, Jerez M (2016) Ambiente de luz del sotobosque de una selva nublada andina: estructura del dosel y estacionalidad climática. Revista de Biología Tropical 64, 1699–1707.

Reich PB, Ellsworth D, Uhl C (1995) Leaf carbon and nutrient assimilation and conservation in species of differing successional status in an oligotrophic Amazon forest. Functional Ecology 9, 65–76.
Leaf carbon and nutrient assimilation and conservation in species of differing successional status in an oligotrophic Amazon forest.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M (2003) The evolution of plant functional variation: traits, spectra and strategies. International Journal of Plant Sciences 164, S143–S164.
The evolution of plant functional variation: traits, spectra and strategies.Crossref | GoogleScholarGoogle Scholar |

Ribeiro R, Souza G, Oliveira R, Machado E (2005) Photosynthetic responses of tropical tree species from different successional groups under contrasting irradiance conditions. Revista Brasileira de Botanica. Brazilian Journal of Botany 28, 149–161.
Photosynthetic responses of tropical tree species from different successional groups under contrasting irradiance conditions.Crossref | GoogleScholarGoogle Scholar |

Rozendaal DM, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Functional Ecology 20, 207–216.
Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature.Crossref | GoogleScholarGoogle Scholar |

SAS (2004) ‘SAS/STAT 9.1 user’s guide.’ (SAS. Institute Inc., Cary, NC)

Schabenberger O, Pierce F (2002) ‘Contemporary statistical models for the plant and soil sciences.’ (CRC Press, Boca Raton, FL)

Schwarzkopf T, Riha SJ, Fahey TJ, Degloria S (2011) Are cloud forest tree structure and environment related in the Venezuela Andes? Austral Ecology 36, 280–289.
Are cloud forest tree structure and environment related in the Venezuela Andes?Crossref | GoogleScholarGoogle Scholar |

Sterck F, Duursma RA, Pearcy R, Valladares F, Cieslak M, Weemstra M (2013) Plasticity influencing the light compensation point offsets the specialization for light niches across shrub species in a tropical forest understorey. Journal of Ecology 101, 971–980.
Plasticity influencing the light compensation point offsets the specialization for light niches across shrub species in a tropical forest understorey.Crossref | GoogleScholarGoogle Scholar |

Sukhov V, Surova L, Sherstneva O, Katicheva L, Vodeneev V (2015) Variation potential in fluence on photosynthetic cyclic electron flow in pea. Frontiers in Plant Science 5, 766
Variation potential in fluence on photosynthetic cyclic electron flow in pea.Crossref | GoogleScholarGoogle Scholar |

Sukhova E, Mudrilov M, Vodeneev V, Sukhov V (2017) Influence of the variation potential on photosynthetic flows of light energy and electrons in pea. Photosynthesis Research
Influence of the variation potential on photosynthetic flows of light energy and electrons in pea.Crossref | GoogleScholarGoogle Scholar |

Takahashi S, Badger M (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16, 53–60.
Photoprotection in plants: a new light on photosystem II damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvFOgtw%3D%3D&md5=1e82c8012b07f6427815ccc0b8d0d796CAS |

Thimijan RW, Heins RD (1983) Photometric, radiometric and quantum light units of measure: a review of procedures for interconversion. HortScience 18, 818–822.

Walters RG (2005) Towards an understanding the photosynthetic acclimation. Journal of Experimental Botany 56, 435–447.
Towards an understanding the photosynthetic acclimation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovVylsg%3D%3D&md5=98552d66aeb9cdc5b7ad510f8eeda3d9CAS |

Way D, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiology 30, 669–688.
Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data.Crossref | GoogleScholarGoogle Scholar |

Yamashita N, Ishida A, Kushima H, Tanaka N (2000) Acclimation to sudden increase in light favoring an invasive over native trees in subtropical islands, Japan. Oecologia 125, 412–419.
Acclimation to sudden increase in light favoring an invasive over native trees in subtropical islands, Japan.Crossref | GoogleScholarGoogle Scholar |

Zhang Q, Zhang TJ, Chow WS, Xie X, Chen YJ, Peng CL (2015) Photosynthetic characteristics and light energy conversions under different light environments in five tree species occupying dominant status at different stages of subtropical forest succession. Functional Plant Biology 42, 609–619.
Photosynthetic characteristics and light energy conversions under different light environments in five tree species occupying dominant status at different stages of subtropical forest succession.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXps1Okurc%3D&md5=9f4a2a25e87a0f9eb7eec2c9d2e07e0aCAS |