, Volume 32, Issue 6, pp 1547–1558 | Cite as

Water-use efficiency is higher in green stems than in leaves of a tropical tree species

  • Eleinis Ávila-LoveraEmail author
  • Wilmer Tezara
Original Article


Key message

Stems have similar photosynthetic rates as leaves but higher water-use efficiency.


Plants with green photosynthetic stems are common in sub-tropical and tropical dry woodlands worldwide, yet the benefits of photosynthetic stems in tropical species have not been studied before. Parkinsonia praecox (Ruiz & Pav. ex Hook.) Hawkins (Fabaceae) is a small tree found in the arid and semi-arid regions of northern Venezuela and has green stems. We evaluated ecophysiological traits and the role of the photosynthetic stem in the carbon gain of P. praecox in a tropical dry forest, by measuring seasonal changes in water status, gas exchange, water-use efficiency (WUE), photochemical activity of PSII, and biochemical, morphometric and functional traits of leaves and green stems. We found stem net photosynthesis with a rate of 17 µmol m−2 s−1, indicating that the stem contribution to the carbon balance of the species is positive. We also found 1.6 and 2.5 times higher instantaneous and intrinsic WUE, respectively, in green stems than in leaves during the rainy season, which has important implications for water balance. Drought had a negative effect on water potential, leaf PN and photochemical activity of the stem. A similar contribution to the daily whole-plant carbon gain by each photosynthetic organ was found during both seasons; however, when leaf loss is complete during the dry season, the stem contribution would increase up to 100%.


Carbon balance Carbon isotope composition Drought Gas exchange Stem net photosynthesis Water loss 



We want to thank Jenny De Almeida, Rosa Urich, Ilsa Coronel, Oranys Marín and Carolina Kalinhoff for help provided in the field. Special thanks to Luis Hermoso for his help with the anatomical sections, and Miquel Gonzalez-Meler for his help with the carbon isotope data. We also thank Ana Herrera for helpful discussions that improved this manuscript.


This study was funded by Universidad Central de Venezuela Consejo de Desarrollo Científico y Humanístico (PI 03-7458-2009 and PG 03-7635-2009 to WT).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights statement

This research did not involve human participants and animals.


  1. Adams M, Strain B (1968) Photosynthesis in stems and leaves of Cercidium floridum—spring and summer diurnal field response and relation to temperature. Oecol Plant 3:285–297Google Scholar
  2. Aschan G, Pfanz H (2003) Non-foliar photosynthesis—a strategy of additional carbon acquisition. Flora Morphol Distrib Funct Ecol Plants 198:81–97. CrossRefGoogle Scholar
  3. Ávila E, De Almeida J, Tezara W (2014a) Comparación ecofisiológica y anatómica de los tejidos fotosintéticos de Cercidium praecox (Ruiz & Pav. ex Hook.) Harms (Fabaceae, Caesalpinioideae). Acta Bot Venezuelica 37:59–76Google Scholar
  4. Ávila E, Herrera A, Tezara W (2014b) Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. Photosynthetica 52:3–15. CrossRefGoogle Scholar
  5. Ávila-Lovera E, Ezcurra E (2016) Stem-succulent trees from the Old and New World tropics. In: Goldstein G, Santiago LS (eds) Tropical tree physiology. Springer International Publishing, Switzerland, pp 45–65CrossRefGoogle Scholar
  6. Ávila-Lovera E, Zerpa AJ, Santiago LS (2017) Stem photosynthesis and hydraulics are coordinated in desert plant species. New Phytol. CrossRefPubMedGoogle Scholar
  7. Berveiller D, Kierzkowski D, Damesin C (2007) Interspecific variability of stem photosynthesis among tree species. Tree Physiol 27:53–61CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  9. Bruinsma J (1963) The quantitative analysis of chlorophylls a and b in plant extracts. Photochem Photobiol 2:241–249. CrossRefGoogle Scholar
  10. Cernusak LA, Cheesman AW (2015) The benefits of recycling: how photosynthetic bark can increase drought tolerance. New Phytol 208:995–997. CrossRefPubMedGoogle Scholar
  11. Cernusak LA, Tcherkez G, Keitel C et al (2009) Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Funct Plant Biol 36:199–213. CrossRefGoogle Scholar
  12. Chaves MM, Pereira JS (1992) Water stress, CO2 and climate change. J Exp Bot 43:1131–1139. CrossRefGoogle Scholar
  13. Comstock JP, Ehleringer JR (1988) Contrasting photosynthetic behavior in leaves and twigs of Hymenoclea salsola, a green-twigged warm desert shrub. Am J Bot 75:1360–1370. CrossRefGoogle Scholar
  14. Comstock JP, Cooper TA, Ehleringer JR (1988) Seasonal patterns of canopy development and carbon gain in nineteen warm desert shrub species. Oecologia 75:327–335. CrossRefPubMedGoogle Scholar
  15. Cornic G, Briantais J-M (1991) Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183:178–184. CrossRefPubMedGoogle Scholar
  16. Damesin C (2003) Respiration and photosynthesis characteristics of current-year stems of Fagus sylvatica: from the seasonal pattern to an annual balance. New Phytol 158:465–475. CrossRefGoogle Scholar
  17. Demmig B, Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 171:171–184. CrossRefPubMedGoogle Scholar
  18. Díaz M, Granadillo E (2005) The significance of episodic rains for reproductive phenology and productivity of trees in semiarid regions of northwestern Venezuela. Trees 19:336–348. CrossRefGoogle Scholar
  19. Ehleringer J (1983) Ecophysiology of Amaranthus palmeri, a Sonoran Desert summer annual. Oecologia 57:107–112CrossRefGoogle Scholar
  20. Ehleringer JR, Cook CS (1984) Photosynthesis in Encelia farinosa Gray in response to decreasing leaf water potential. Plant Physiol 75:688–693CrossRefGoogle Scholar
  21. Ehleringer JR, Comstock JP, Cooper TA (1987) Leaf-twig carbon isotope ratio differences in photosynthetic-twig desert shrubs. Oecologia 71:318–320CrossRefGoogle Scholar
  22. Ehleringer JR, Phillips SL, Comstock JP (1992) Seasonal variation in the carbon isotopic composition of desert plants. Funct Ecol 6:396–404. CrossRefGoogle Scholar
  23. Fajardo L, Rodríguez JP, González V, Briceño-Linares JM (2013) Restoration of a degraded tropical dry forest in Macanao, Venezuela. J Arid Environ 88:236–243. CrossRefGoogle Scholar
  24. Farquhar G, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552Google Scholar
  25. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345. CrossRefGoogle Scholar
  26. Farquhar GD, von Caemmerer S (1982) Modelling of Photosynthetic Response to Environmental Conditions. In: Lange PDOL, Nobel PPS, Osmond PCB, Ziegler PDH (eds) Physiological plant ecology II. Springer, Berlin, pp 549–587CrossRefGoogle Scholar
  27. Farquhar GD, O’leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct Plant Biol 9:121–137Google Scholar
  28. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40:503–537CrossRefGoogle Scholar
  29. Filippou M, Fasseas C, Karabourniotis G (2007) Photosynthetic characteristics of olive tree (Olea europaea) bark. Tree Physiol 27:977–984CrossRefGoogle Scholar
  30. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA 990:87–92. CrossRefGoogle Scholar
  31. Gibson AC (1983) Anatomy of photosynthetic old stems of nonsucculent dicotyledons from North American deserts. Bot Gaz 144:347–362CrossRefGoogle Scholar
  32. Herrera A (2013) Crassulacean acid metabolism-cycling in Euphorbia milii. AoB Plants 5:plt014. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Herrera A, Cuberos M (1990) Stomatal size, density and conductance in leaves of some xerophytes from a thorn scrub in Venezuela differing in carbon fixation pathway. Ecotropicos 3:67–76Google Scholar
  34. Huang J, Ji M, Xie Y et al (2016) Global semi-arid climate change over last 60 years. Clim Dyn 46:1131–1150. CrossRefGoogle Scholar
  35. Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J Exp Bot 42:1003–1011. CrossRefGoogle Scholar
  36. Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187. CrossRefGoogle Scholar
  37. Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer, New YorkCrossRefGoogle Scholar
  38. Lawlor DW (1995) The effects of water deficit on photosynthesis. In: Smirnoff R (ed) Environment and plant metabolism: flexibility and acclimation. BIOS Scientific Publishers, Oxford, pp 129–160Google Scholar
  39. Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:871–885. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Levizou E, Manetas Y (2008) Maximum and effective PSII yields in the cortex of the main stem of young Prunus cerasus trees: effects of seasons and exposure. Trees 22:159–164. CrossRefGoogle Scholar
  42. Lindorf H, de Parisca L, Rodríguez P (2006) Botanica. Clasificación, estructura, reproducción, 2nd edn. Ediciones de la Biblioteca de la Universidad Central de Venezuela, VenezuelaGoogle Scholar
  43. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nilsen ET (1995) Stem photosynthesis: extent, patterns, and role in plant carbon economy. In: Gartner BL (ed) Plant stems: physiology and functional morphology. Academic Press, San Diego, pp 223–240CrossRefGoogle Scholar
  45. Nilsen ET, Bao Y (1990) The influence of water stress on stem and leaf photosynthesis in Glycine max and Sparteum junceum (Leguminosae). Am J Bot 77:1007–1015. CrossRefGoogle Scholar
  46. Nilsen E, Sharifi M (1997) Carbon isotopic composition of legumes with photosynthetic stems from mediterranean and desert habitats. Am J Bot 84:1707–1713CrossRefGoogle Scholar
  47. Nilsen ET, Meinzer FC, Rundel PW (1989) Stem photosynthesis in Psorothamnus spinosus (smoke tree) in the Sonoran desert of California. Oecologia 79:193–197CrossRefGoogle Scholar
  48. Osmond CB, Smith SD, Gui-Ying B, Sharkey TD (1987) Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Characterization of leaf and stem CO2 fixation and H2O vapor exchange under controlled conditions. Oecologia 72:542–549CrossRefGoogle Scholar
  49. Pivovaroff AL, Pasquini SC, De Guzman ME et al (2016) Multiple strategies for drought survival among woody plant species. Funct Ecol 30:517–526. CrossRefGoogle Scholar
  50. Sanchez-Bragado R, Molero G, Reynolds MP, Araus JL (2016) Photosynthetic contribution of the ear to grain filling in wheat: a comparison of different methodologies for evaluation. J Exp Bot 67:2787–2798. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Schulze E-D, Hall AE (1982) Stomatal responses, water loss and CO2 assimilation rates of plants in contrasting environments. In: Lange PDOL, Nobel PPS, Osmond PCB, Ziegler PDH (eds) Physiological plant ecology II. Springer, Berlin, pp 181–230CrossRefGoogle Scholar
  52. Smith SD, Osmond CB (1987) Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Morphology, stomatal conductance and water-use efficiency in field populations. Oecologia 72:533–541CrossRefGoogle Scholar
  53. Tezara W, Martínez D, Rengifo E, Herrera A (2003) Photosynthetic responses of the tropical spiny shrub Lycium nodosum (Solanaceae) to drought, soil salinity and saline spray. Ann Bot 92:757–765. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Tezara W, Marín O, Rengifo E et al (2005) Photosynthesis and photoinhibition in two xerophytic shrubs during drought. Photosynthetica 43:37–45. CrossRefGoogle Scholar
  55. Tezara W, Urich R, Coronel I et al (2010) Asimilación de carbono, eficiencia de uso de agua y actividad fotoquímica en xerófitas de ecosistemas semiáridos de Venezuela. Ecosistemas 19:67–78Google Scholar
  56. Tezara W, Colombo R, Coronel I, Marín O (2011) Water relations and photosynthetic capacity of two species of Calotropis in a tropical semi-arid ecosystem. Ann Bot 107:397–405. CrossRefPubMedGoogle Scholar
  57. Tinoco-Ojanguren C (2008) Diurnal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert. J Arid Environ 72:127–140. CrossRefGoogle Scholar
  58. Vandegehuchte MW, Bloemen J, Vergeynst LL, Steppe K (2015) Woody tissue photosynthesis in trees: salve on the wounds of drought? New Phytol 204:998–1002CrossRefGoogle Scholar
  59. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. CrossRefGoogle Scholar
  60. Wittmann C, Aschan G, Pfanz H (2001) Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regime. Basic Appl Ecol 2:145–154. CrossRefGoogle Scholar
  61. Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefGoogle Scholar
  62. Yiotis C, Psaras GK, Manetas Y (2008) Seasonal photosynthetic changes in the green-stemmed Mediterranean shrub Calicotome villosa: a comparison with leaves. Photosynthetica 46:262–267CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centro de Botánica Tropical, Instituto de Biología ExperimentalUniversidad Central de VenezuelaCaracasVenezuela
  2. 2.Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA

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