Does carbon storage confer waterlogging tolerance? Evidence from four evergreen species of a temperate rainforest
M. Delgado A B C D , A. Zúñiga-Feest A D G and F. I. Piper E FA Laboratorio de Biología Vegetal, Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile (UACh), Valdivia, Chile.
B Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Temuco, Chile.
C Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias. Center of Plant, Soil Interaction, Universidad de la Frontera, Temuco, Chile.
D Centro de Investigaciones en Suelos Volcánicos (CISVo), UACh.
E Centro de Investigación en Ecosistemas de la Patagonia (CIEP), Moraleda 16, Coyhaique, Chile.
F Instituto de Ecología y Biodiversidad (IEB), Santiago, Chile.
G Corresponding author. Email: alejandrazunigafeest@gmail.com
Australian Journal of Botany 66(1) 74-84 https://doi.org/10.1071/BT17104
Submitted: 8 June 2017 Accepted: 13 December 2017 Published: 8 February 2018
Abstract
Deep shade and waterlogging are two common stressors affecting seedling performance in the understorey of evergreen rainforests. It has been hypothesised that high levels of carbon storage confer shade- and waterlogging tolerances by preventing carbon limitation under such stresses. Whether the tolerance to both stresses is positively or negatively related remains unclear. To explore the role of carbon storage in the relationships of waterlogging and shade tolerance, we investigated the responses to waterlogging and the levels of carbon storage in two species pairs with contrasting shade tolerance: Embothrium coccineum J.R.Forst. & G.Forst. and Gevuina avellana Mol. (Proteaceae) and Nothofagus dombeyi (Mirb.) Oerst. and Nothofagus nitida (Phil.) Krasser (Nothofagaceae). We subjected seedlings to waterlogging or control conditions for 30 days and evaluated survival, relative growth rate (RGR), biomass distribution, leaf chlorophyll fluorescence (Fv/Fm), and concentrations of total soluble sugars, starch and non-structural carbohydrates in different plant tissues. Waterlogging reduced survival, Fv/Fm and RGR in all species; however, the magnitude of reduction of Fv/Fm and RGR was significantly higher in the shade-intolerant species than in their shade-tolerant counterparts. In general, shade-intolerant species had significantly higher non-structural carbohydrate concentrations in waterlogging than in control conditions. By contrast, shade-tolerant species had similar non-structural carbohydrate concentrations under both conditions. Our results indicate that relatively shade-tolerant species performed better under waterlogging. A reduction in non-structural carbohydrates under waterlogging was not observed in any of studied species; rather, shade-intolerant species exhibited non-structural carbohydrate accumulation suggesting that carbon storage does not confer waterlogging tolerance in these species.
Additional keywords: carbon limitation, climate change, cluster roots, flooding, non-structural carbohydrates, swamp forests, Valdivian rainforest.
References
Alberdi M, Donoso C (2004) Variabilidad en Embothrium coccineum. In ‘Variación intraespecífica en las especies arbóreas de los bosques templados de Chile y Argentina’. pp. 345–356. (Editorial Universitaria: Santiago, Chile)Alberdi M, Reyes-Diaz M, Zúñiga R, Hess S, Bravo LA, Corcuera LJ (2009) Photochemical efficiency of PSII and photoprotective pigments in seedlings and adults of two Proteaceae with different shade tolerance from the Chilean temperate rain forest. Revista Chilena de Historia Natural 82, 387–402.
| Photochemical efficiency of PSII and photoprotective pigments in seedlings and adults of two Proteaceae with different shade tolerance from the Chilean temperate rain forest.Crossref | GoogleScholarGoogle Scholar |
Albrecht G, Biemelt S (1998) A comparative study on carbohydrate reserves and ethanolic fermentation in the roots of two wetland and non‐wetland species after commencement of hypoxia. Physiologia Plantarum 104, 81–86.
| A comparative study on carbohydrate reserves and ethanolic fermentation in the roots of two wetland and non‐wetland species after commencement of hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvFyrtLY%3D&md5=c3fb0c4199cbe89f725701fc093da037CAS |
Bailey-Serres J, Lee SC, Brinton E (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698–1709.
| Waterproofing crops: effective flooding survival strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmt73E&md5=1a74cb2dbd982d500568125559efef1bCAS |
Barrow N (1977) Phosphorus uptake and utilization by tree seedlings. Australian Journal of Botany 25, 571–584.
| Phosphorus uptake and utilization by tree seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXovVCjsQ%3D%3D&md5=c1ea92b1a78f9f74f38507b81a939683CAS |
Canham CD, Kobe RK, Latty EF, Chazdon RL (1999) Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121, 1–11.
| Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves.Crossref | GoogleScholarGoogle Scholar |
Colmer T, Atwell B, Ismail A, Pedersen O, Shabala S, Sorrell B, Voesenek L (2015) Waterlogging and submergence. In ‘Plants in action’. (Ed. T Colmer) pp. 1–44. (Australian Society of Plant Scientists: Canberra)
Coopman RE, Fuentes-Neira FP, Briceño VF, Cabrera HM, Corcuera LJ, Bravo LA (2010) Light energy partitioning in photosystems I and II during development of Nothofagus nitida growing under different light environments in the Chilean evergreen temperate rain forest. Trees 24, 247–259.
| Light energy partitioning in photosystems I and II during development of Nothofagus nitida growing under different light environments in the Chilean evergreen temperate rain forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtlGgu78%3D&md5=c26aaeb97bf729cde744dc43b45ebac7CAS |
Dale M, Causton D (1992) The ecophysiology of Veronica chamaedrys, V. montana and V. officinalis. II. The interaction of irradiance and water regime. Journal of Ecology 80, 493–504.
| The ecophysiology of Veronica chamaedrys, V. montana and V. officinalis. II. The interaction of irradiance and water regime.Crossref | GoogleScholarGoogle Scholar |
Delgado M, Suriyagoda L, Zúñiga-Feest A, Borie F, Lambers H, Field K (2014) Divergent functioning of Proteaceae species: the South American Embothrium coccineum displays a combination of adaptive traits to survive in high-phosphorus soils. Functional Ecology 28, 1356–1366.
| Divergent functioning of Proteaceae species: the South American Embothrium coccineum displays a combination of adaptive traits to survive in high-phosphorus soils.Crossref | GoogleScholarGoogle Scholar |
Delgado M, Zúñiga-Feest A, Almonacid L, Lambers H, Borie F (2015) Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil. Plant and Soil 395, 189–200.
| Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVamtrbF&md5=9fef0c6a77ee12700e106a8c3db3ca99CAS |
Díaz MF, Bigelow S, Armesto JJ (2007) Alteration of the hydrologic cycle due to forest clearing and its consequences for rainforest succession. Forest Ecology and Management 244, 32–40.
| Alteration of the hydrologic cycle due to forest clearing and its consequences for rainforest succession.Crossref | GoogleScholarGoogle Scholar |
Donoso C (2006) ‘Las especies arbóreas de los bosques templados de Chile y Argentina autoecología.’ (Marisa Cúneo Ediciones: Valdivia, Chile)
Donoso C, Escobar B (1986) Germinación de las Proteáceas arbóreas chilenas. Bosque 7, 85–94.
| Germinación de las Proteáceas arbóreas chilenas.Crossref | GoogleScholarGoogle Scholar |
Donoso-Ñanculao G, Castro M, Navarrete D, Bravo LA, Corcuera LJ (2010) Seasonal induction of cluster roots in Embothrium coccineum J.R.Forst. & G.Forst. in the field: factors that regulate their development. Chilean Journal of Agricultural Research 70, 559–566.
| Seasonal induction of cluster roots in Embothrium coccineum J.R.Forst. & G.Forst. in the field: factors that regulate their development.Crossref | GoogleScholarGoogle Scholar |
El-Shihaby OA, Younis ME, El-Bastawisy ZM, Nemat Alla MM (2002) Effect of kinetin on photosynthetic activity and carbohydrate content in waterlogged or seawater-treated Vigna sinensis and Zea mays plants. Plant Biosystems 136, 277–290.
| Effect of kinetin on photosynthetic activity and carbohydrate content in waterlogged or seawater-treated Vigna sinensis and Zea mays plants.Crossref | GoogleScholarGoogle Scholar |
Fajardo A, Piper FI (2015) High foliar nutrient concentrations and resorption efficiency in Embothrium coccineum (Proteaceae) in southern Chile. American Journal of Botany 102, 208–216.
| High foliar nutrient concentrations and resorption efficiency in Embothrium coccineum (Proteaceae) in southern Chile.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjsVOkt78%3D&md5=a9dd75518c7684b7674a168701ff1ed6CAS |
Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Functional Plant Biology 15, 63–92.
Hansen J, Moller I (1975) Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Analytical Biochemistry 68, 87–94.
| Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXls1Siu7k%3D&md5=e2db21822d7a04036fd72dddf2289303CAS |
Huang B, Johnson JW, Nesmith S, Bridges DC (1994) Growth, physiological and anatomical responses of two wheat genotypes to waterlogging and nutrient supply. Journal of Experimental Botany 45, 193–202.
| Growth, physiological and anatomical responses of two wheat genotypes to waterlogging and nutrient supply.Crossref | GoogleScholarGoogle Scholar |
Irfan M, Hayat S, Hayat Q, Afroz S, Ahmad A (2010) Physiological and biochemical changes in plants under waterlogging. Protoplasma 241, 3–17.
| Physiological and biochemical changes in plants under waterlogging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltVWksrc%3D&md5=2e318cbecec85a958c9f96569b2c234fCAS |
Jaeger C, Gessler A, Biller S, Rennenberg H, Kreuzwieser J (2009) Differences in C metabolism of ash species and provenances as a consequence of root oxygen deprivation by waterlogging. Journal of Experimental Botany 60, 4335–4345.
| Differences in C metabolism of ash species and provenances as a consequence of root oxygen deprivation by waterlogging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGitL7L&md5=1bca1634f3e78e65e169208b86f4ba23CAS |
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 |
Kobe RK (1997) Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80, 226–233.
| Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth.Crossref | GoogleScholarGoogle Scholar |
Kogawara S, Yamanoshita T, Norisada M, Masumori M, Kojima K (2006) Photosynthesis and photoassimilate transport during root hypoxia in Melaleuca cajuputi, a flood-tolerant species, and in Eucalyptus camaldulensis, a moderately flood-tolerant species. Tree Physiology 26, 1413–1423.
| Photosynthesis and photoassimilate transport during root hypoxia in Melaleuca cajuputi, a flood-tolerant species, and in Eucalyptus camaldulensis, a moderately flood-tolerant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlSnur%2FI&md5=ae6e93a44156afd179543d7329246bebCAS |
Kozlowski T (1997) Responses of woody plants to flooding and salinity. Tree Physiology 17, 490
| Responses of woody plants to flooding and salinity.Crossref | GoogleScholarGoogle Scholar |
Kunstler G, Coomes DA, Canham CD (2009) Size‐dependence of growth and mortality influence the shade tolerance of trees in a lowland temperate rain forest. Journal of Ecology 97, 685–695.
| Size‐dependence of growth and mortality influence the shade tolerance of trees in a lowland temperate rain forest.Crossref | GoogleScholarGoogle Scholar |
Laanisto L, Niinemets Ü (2015) Polytolerance to abiotic stresses: how universal is the shade–drought tolerance trade‐off in woody species? Global Ecology and Biogeography 24, 571–580.
| Polytolerance to abiotic stresses: how universal is the shade–drought tolerance trade‐off in woody species?Crossref | GoogleScholarGoogle Scholar |
Lambers H, Bishop JG, Hopper SD, Laliberte E, Zuniga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Annals of Botany 110, 329–348.
| Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOjurnP&md5=cc25bb687a7608a87ae8fcb5031991fdCAS |
Lenssen J, Menting F, Van der Putten W (2003) Plant responses to simultaneous stress of waterlogging and shade: amplified or hierarchical effects? New Phytologist 157, 281–290.
| Plant responses to simultaneous stress of waterlogging and shade: amplified or hierarchical effects?Crossref | GoogleScholarGoogle Scholar |
Li M, López R, Venturas M, Pita P, Gordaliza GG, Gil L, Rodríguez-Calcerrada J (2015) Greater resistance to flooding of seedlings of Ulmus laevis than Ulmus minor is related to the maintenance of a more positive carbon balance. Trees 29, 835–848.
| Greater resistance to flooding of seedlings of Ulmus laevis than Ulmus minor is related to the maintenance of a more positive carbon balance.Crossref | GoogleScholarGoogle Scholar |
Lusk CH, Contreras O (1999) Foliage area and crown nitrogen turnover in temperate rain forest juvenile trees of differing shade tolerance. Journal of Ecology 87, 973–983.
| Foliage area and crown nitrogen turnover in temperate rain forest juvenile trees of differing shade tolerance.Crossref | GoogleScholarGoogle Scholar |
Lusk C, Piper FI (2007) Seedling size influences relationships of shade tolerance with carbohydrate‐storage patterns in a temperate rainforest. Functional Ecology 21, 78–86.
| Seedling size influences relationships of shade tolerance with carbohydrate‐storage patterns in a temperate rainforest.Crossref | GoogleScholarGoogle Scholar |
Maxwell K, Johnson GN (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=67b717491b366aa26499b8d93bbcd62bCAS |
Mielke MS, Schaffer B (2010) Photosynthetic and growth responses of Eugenia uniflora L. seedlings to soil flooding and light intensity. Environmental and Experimental Botany 68, 113–121.
| Photosynthetic and growth responses of Eugenia uniflora L. seedlings to soil flooding and light intensity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCnu70%3D&md5=b56f1f2cb1efbd31a85e4fd8a495f9d0CAS |
Myers JA, Kitajima K (2007) Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. Journal of Ecology 95, 383–395.
| Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVeitb4%3D&md5=2228af43bdfcbb32630c974ba5fe6e9cCAS |
Naidoo G, Naidoo S (1992) Waterlogging responses of Sporobolus virginicus (L.) Kunth. Oecologia 90, 445–450.
| Waterlogging responses of Sporobolus virginicus (L.) Kunth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1czot1SnsQ%3D%3D&md5=e8ff0d56de020f0d78bc6334d4bde3f2CAS |
Neuenschwander A (2010) ‘El cambio climático en el sector silvoagropecuario de Chile.’ (Salviat Impresores S.A. edn) (Fundación para la innovación agraria: Santiago, Chile)
Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. Forest Ecology and Management 260, 1623–1639.
| Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation.Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs. Ecological Monographs 76, 521–547.
| Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs.Crossref | GoogleScholarGoogle Scholar |
Parent C, Capelli N, Berger A, Crèvecoeur M, Dat JF (2008) An overview of plant responses to soil waterlogging. Plant Stress 2, 20–27.
Piper FI (2015) Patterns of carbon storage in relation to shade tolerance in southern South American species. American Journal of Botany 102, 1442–1452.
| Patterns of carbon storage in relation to shade tolerance in southern South American species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlWitbnJ&md5=a6cf1604a60f313a6488290bacc507d7CAS |
Piper FI, Zuniga-Feest A, Rojas P, Alberdi M, Corcuera LJ, Lusk CH (2008) Responses of two temperate evergreen Nothofagus species to sudden and gradual waterlogging: relationships with distribution patterns. Revista Chilena de Historia Natural 81, 257–266.
| Responses of two temperate evergreen Nothofagus species to sudden and gradual waterlogging: relationships with distribution patterns.Crossref | GoogleScholarGoogle Scholar |
Piper FI, Reyes-Díaz M, Corcuera LJ, Lusk CH (2009) Carbohydrate storage, survival, and growth of two evergreen Nothofagus species in two contrasting light environments. Ecological Research 24, 1233–1241.
| Carbohydrate storage, survival, and growth of two evergreen Nothofagus species in two contrasting light environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Knt7vF&md5=88c92598f00f484fce6058d88b92e345CAS |
Piper FI, Sepúlveda P, Bustos-Salazar A, Zúñiga-Feest A (2017) Carbon allocation to growth and storage in two evergreen species of contrasting successional status. American Journal of Botany 104, 654–662.
| Carbon allocation to growth and storage in two evergreen species of contrasting successional status.Crossref | GoogleScholarGoogle Scholar |
Poot P, Lambers H (2003) Growth responses to waterlogging and drainage of woody Hakea (Proteaceae) seedlings, originating from contrasting habitats in south-western Australia. Plant and Soil 253, 57–70.
| Growth responses to waterlogging and drainage of woody Hakea (Proteaceae) seedlings, originating from contrasting habitats in south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsLY%3D&md5=d970a9a1b7aa863c5a9f2ac69f6ae8faCAS |
Pryor RJ, Davidson NJ, Close DC (2006) Waterlogging duration: Interspecific comparison of Leptospermum scoparium (Forst et Forst.f.), Acacia melanoxylon (R.Br.), Nothofagus cunninghamii (Hook.) and Eucalyptus obliqua (L’Herit). Austral Ecology 31, 408–416.
| Waterlogging duration: Interspecific comparison of Leptospermum scoparium (Forst et Forst.f.), Acacia melanoxylon (R.Br.), Nothofagus cunninghamii (Hook.) and Eucalyptus obliqua (L’Herit).Crossref | GoogleScholarGoogle Scholar |
Purnell HM (1960) Studies of the family Proteaceae. I. Anatomy and morphology of the roots of some Victorian species. Australian Journal of Botany 8, 38–50.
| Studies of the family Proteaceae. I. Anatomy and morphology of the roots of some Victorian species.Crossref | GoogleScholarGoogle Scholar |
Roe JH (1934) A colorimetric method for the determination of fructose in blood and urine. Journal of Biological Chemistry 107, 15–22.
Saldaña A, Parra MJ, Flores-Bavestrello A, Corcuera LJ, Bravo LA (2014) Effects of forest successional status on microenvironmental conditions, diversity, and distribution of filmy fern species in a temperate rainforest. Plant Species Biology 29, 253–262.
| Effects of forest successional status on microenvironmental conditions, diversity, and distribution of filmy fern species in a temperate rainforest.Crossref | GoogleScholarGoogle Scholar |
Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant and Soil 274, 101–125.
| Cluster roots: a curiosity in context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiurfK&md5=8c9e723ce3d4f137ca88c2ae926c5c01CAS |
Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiology 135, 549–560.
| Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12ms78%3D&md5=1b841d66a827f2ef68a37780d88a889dCAS |
Smethurst CF, Shabala S (2003) Screening methods for waterlogging tolerance in lucerne: comparative analysis of waterlogging effects on chlorophyll fluorescence, photosynthesis, biomass and chlorophyll content. Functional Plant Biology 30, 335–343.
| Screening methods for waterlogging tolerance in lucerne: comparative analysis of waterlogging effects on chlorophyll fluorescence, photosynthesis, biomass and chlorophyll content.Crossref | GoogleScholarGoogle Scholar |
Sokal RR, Rohlf FJ (1995) ‘Biometry: the principles and practice of statistics in biological research.’ (State University of New York at Stony Brook: New York)
Steffens D, Hutsch B, Eschholz T, Losak T, Schubert S (2005) Water logging may inhibit plant growth primarily by nutrient deficiency rather than nutrient toxicity. Plant, Soil and Environment 51, 545–552.
Steubing L, Alberdi M, Wenzel H (1983) Seasonal changes of cold resistance of Proteaceae of the South Chilean laurel forest. Plant Ecology 52, 35–44.
Sun OJ, Sweet GB, Whitehead D, Buchan GD (1995) Physiological responses to water stress and waterlogging in Nothofagus species. Tree Physiology 15, 629–638.
| Physiological responses to water stress and waterlogging in Nothofagus species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FnslentQ%3D%3D&md5=5c2119769c8afb0075558aed901b42d6CAS |
Sutton B, Ting IP, Sutton R (1981) Carbohydrate metabolism of cactus in a desert environment. Plant Physiology 68, 784–787.
| Carbohydrate metabolism of cactus in a desert environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsVOhtLw%3D&md5=f63aa82a55550781352eb253b15f7ed3CAS |
Valladares F, Laanisto L, Niinemets Ü, Zavala MA (2016) Shedding light on shade: ecological perspectives of understorey plant life. Plant Ecology & Diversity 9, 237–251.
| Shedding light on shade: ecological perspectives of understorey plant life.Crossref | GoogleScholarGoogle Scholar |
Veblen T, Donoso C, Kitzberger T, Rebertus A (1996) Ecology of southern Chilean and Argentinean Nothofagus forests. In ‘The ecology and biogeography of Nothofagus forests’. (Eds TT Veblen, RS Hill, J Read) pp. 293–353. (Yale University Press: New Haven, CT, USA)
Visser E, Voesenek L, Vartapetian B, Jackson M (2003) Flooding and plant growth. Annals of Botany 91, 107–109.
| Flooding and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVCks7k%3D&md5=9ebb3dbd7d63751998a39b19145bb713CAS |
Walters MB, Reich PB (1999) Low‐light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad‐leaved evergreen species differ? New Phytologist 143, 143–154.
| Low‐light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad‐leaved evergreen species differ?Crossref | GoogleScholarGoogle Scholar |
Zúñiga R, Alberdi M, Reyes-Diaz M, Olivares E, Hess S, Bravo LA, Corcuera LJ (2006) Seasonal changes in the photosynthetic performance of two evergreen Nothofagus species in south central Chile. Revista Chilena de Historia Natural 79, 489–504.
| Seasonal changes in the photosynthetic performance of two evergreen Nothofagus species in south central Chile.Crossref | GoogleScholarGoogle Scholar |
Zúñiga-Feest A, Bustos-Salazar A, Alves F, Martinez V, Smith-Ramírez C (2017) Physiological and morphological responses to permanent and intermittent waterlogging in seedlings of four evergreen trees of temperate swamp forests. Tree Physiology 37, 779–789.
| Physiological and morphological responses to permanent and intermittent waterlogging in seedlings of four evergreen trees of temperate swamp forests.Crossref | GoogleScholarGoogle Scholar |