, Volume 53, Issue 4, pp 537–546 | Cite as

Trade-offs between seedling growth, plant respiration and water-use efficiency in two Mediterranean shrubs Rhamnus alaternus and Rhamnus ludovici-salvatoris

  • H. El Aou-Ouad
  • I. Florez-Sarasa
  • M. Ribas-Carbó
  • J. Flexas
  • H. Medrano
  • J. Gulías
Original Papers


Seedling recruitment is a critical developmental stage in regeneration of plant populations under Mediterranean conditions that strongly depends on water availability. Seed mass and relative growth rate (RGR) may affect the early establishment of seedlings through different physiological processes. Here, we examined the effects of the seed mass and carbon balance on seedling growth under two water regimes in Rhamnus alaternus L. and Rhamnus ludovici-salvatoris, two Mediterranean shrubs, showing a different ability to recruit seedlings. Plant water consumption and biomass accumulation (ΔB) were measured during three periods of the growth in order to estimate water use efficiency (WUE), RGR, and its components. Additionally, net photosynthesis and leaf, stem, and root respiration were measured in plants grown in pots well watered and under progressive drought. Rhamnus alaternus showed the higher seed mass, ΔB, and plant WUE than that of R. ludovici-salvatoris in all periods and water regimes. The higher RGR of R. alaternus was observed during the first and the second period, but the reverse trend was registered during the third period as a consequence of the higher initial biomass of R. alaternus. Also, R. alaternus showed a higher specific leaf area and estimated carbon balance than that of R. ludovicisalvatoris. The observed differences in ΔB, estimated carbon balance, seed mass, and WUE between both species could explain their different distribution and ability to recruit seedlings under natural conditions.

Additional key words

chilling temperature leaf area ratio seedling survival specific leaf area 



dry mass


transpiration rate


stomatal conductance


leaf area


leaf area ratio


leaf mass ratio


net photosynthetic rate


net carbon assimilation to dark respiration ratio on a mass basis


respiration rate


relative growth rate


root:shoot ratio


specific leaf area


soil water content


vapor pressure deficit


intrinsic water-use efficiency (= P N/g s)


plant water-use efficiency


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anyia A.O., Slaski J.J., Nyachiro J.M. et al.: Relationship of carbon isotope discrimination to water use efficiency and productivity of barley under field and greenhouse conditions. — J. Agron. Crop Sci. 193: 313–323, 2007.CrossRefGoogle Scholar
  2. Atkin O.K., Bruhn D., Hurry V.M., Tjoelker M.G.: The hot and the cold: unravelling the variable response of plant respiration to temperature. — Funct. Plant. Biol. 32: 87–105, 2005.CrossRefGoogle Scholar
  3. Barbour M.M., Warren C.R., Farquhar G.D. et al.: Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. — Plant Cell Environ. 33: 1176–1185, 2010.PubMedGoogle Scholar
  4. Boyer J.S., Westgate M.E.: Grain yields with limited water. — J. Exp. Bot. 55: 2385–2394, 2004.CrossRefPubMedGoogle Scholar
  5. Castro J., Reich P.B., Sánchez-Miranda A., Guerrero J.D.: Evidence that the negative relationship between seed mass and relative growth rate is not physiological but linked to species identity: a within-family analysis of Scots pine. — Tree Physiol. 28: 1077–1082, 2008.CrossRefPubMedGoogle Scholar
  6. Castro-Díez P., Montserrat-Martí G., Cornelissen J.H.C.: Tradeoffs between phenology, relative growth rate, life form and seed mass among 22 Mediterranean woody species. — Plant Ecol. 166: 117–129, 2003.CrossRefGoogle Scholar
  7. Duncan D.S., Sperry J.S.: Coordination between water transport capacity, biomass growth, metabolic scaling and species stature in co-occuring shrub and tree species. — Plant Cell Environ. 37: 2679–2690, 2014.CrossRefGoogle Scholar
  8. Dutilleul C., Driscoll S., Cornic G. et al.: Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. — Plant Physiol. 131: 264–275, 2003.PubMedCentralCrossRefPubMedGoogle Scholar
  9. El Aou-ouad H., Medrano H., Lamarti A., Gulías J.: Seed germination at different temperatures and seedling emergence at different depths of Rhamnus sp. — Cent. Eur. J. Biol. 9: 569–578, 2014.Google Scholar
  10. Flexas J., Galmés J., Ribas-Carbó M., Medrano H.: The effects of drought in plant respiration. — In: Lambers H., Ribas-Carbó M. (ed.): Plant Respiration: From Cell to Ecosystem. Advances in Photosynthesis and Respiration, Vol 18. Pp. 177–194. Springer, Dordrecht 2005.CrossRefGoogle Scholar
  11. Galmés J., Cifre J., Medrano H., Flexas J.: Modulation of relative growth rate and its components by water stress in Mediterranean species with different growth forms. — Oecologia 145: 21–31, 2005.CrossRefPubMedGoogle Scholar
  12. Galmés J., Conesa M.A., Ochogavía J.M. et al.: Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. — Plant Cell Environ. 34: 245–260, 2011.CrossRefPubMedGoogle Scholar
  13. Galmés J., Ribas-Carbó M., Medrano H., Flexas J.: Response of leaf respiration to water stress in Mediterranean species with different growth forms. — J. Arid. Environ. 68: 206–222, 2007.CrossRefGoogle Scholar
  14. Garnier E.: Growth analysis of congeneric annual and perennial grass species. — J. Ecol. 80: 665–675, 1992.CrossRefGoogle Scholar
  15. Gratani L., Catoni R., Varone L.: Morphological, anatomica and physiological leaf traits of Q. ilex, P. latifolia, P. lentiscus and M. communis and their response to Mediterranean climate stress factors. — Bot. Stud. 54: 35–46, 2013.CrossRefGoogle Scholar
  16. Gratani L., Varone L., Catoni R.: Relationship between net photosynthesis and leaf respiration in Mediterranean evergreen species. — Photosynthetica 46: 567–573, 2008.CrossRefGoogle Scholar
  17. Gratani L., Varone L.: Adaptative photosynthetic strategies of the Mediterranean maquis species according to their origin. — Photosynthetica 42: 551–558, 2004.CrossRefGoogle Scholar
  18. Guijarro J.A.: [Contribution to the Balearic Bioclimatology.] — PhD Thesis. Universitat de les Illes Balears, Palma de Mallorca 1986. [In Spanish]Google Scholar
  19. Gulías J., Cifre J., Jonasson S. et al.: Seasonal and inter-annual variations of gas exchange in thirteen woody species along a climatic gradient in the Mediterranean island of Mallorca. — Flora 204: 169–181, 2009.CrossRefGoogle Scholar
  20. Gulías J., Flexas J., Abadía A., Medrano H.: Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species. — Tree Physiol. 22: 687–697, 2002.CrossRefPubMedGoogle Scholar
  21. Gulías J., Traveset A., Riera N., Mus M.: Critical stages in the Recruitment Process of Rhamnus alaternus L. — Ann. Bot.-London 93: 723–731, 2004.CrossRefGoogle Scholar
  22. Gulías. J., Seddaiu. G., Cifre. J. et al.: Leaf and plant water use efficiency in cocksfoot and tall fescue accessions under differing soil water availability. — Crop Sci. 52: 2321–2331, 2012.CrossRefGoogle Scholar
  23. Herrera C.M., Jordano P., López-Soria L., Amat J.: Recruitment of a mastfruiting, bird-dispersed tree: bridging frugivory activity and seedling establishment. — Ecol. Monogr. 64: 315–344, 1994.CrossRefGoogle Scholar
  24. Hou J., Romo J.T.: Seed weight and germination time affect growth of two shrubs. — J. Range Manage. 51: 699–703, 1998.CrossRefGoogle Scholar
  25. Houghton J., Thompson K., Rees M.: Does seed mass drive the differences in relative growth rate between growth forms? — Proc. Biol. Sci. 280: 9–21, 2013.CrossRefGoogle Scholar
  26. Hurry V., Igamberdiev A.U., Keerberg O. et al.: Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. — In: Lambers H., Ribas-Carbo M. (ed.): Plant Respiration: from Cell to Ecosystem, Vol. 18. Pp. 43–61. Adv. Photos. Resp. Ser. Springer, Dordrecht 2005.CrossRefGoogle Scholar
  27. Chaves M.M., Pereira J.S., Maroco J. et al.: How plants cope with water stress in the field? Photosynthesis and growth. — Ann. Bot.-London 89: 907–916, 2002.CrossRefGoogle Scholar
  28. Impa S.M., Nadaradjan S., Boominathan P. et al.: Carbon isotope discrimination accurately reflects variability in WUE measured at a whole plant level in rice. — Crop Sci. 45: 2517–2522, 2005.CrossRefGoogle Scholar
  29. Ismail A.M., Hall A.E.: Correlation between water-use efficiency and carbon isotope discrimination in diverse cowpea genotypes and isogenic lines. — Crop Sci. 32: 7–12, 1992.CrossRefGoogle Scholar
  30. Kennedy P.G., Hausmann N.J., Wenk E.H., Dawson T.E.: The importance of seed reserves for seedling performance: an integrated approach using morphological, physiological, and stable isotope techniques. — Oecologia. 141: 547–554, 2004.CrossRefPubMedGoogle Scholar
  31. Lambers H., Freijsen N., Poorter H. et al.: Analyses of growth based on net assimilation rate and nitrogen productivity: their physiological background. — In: Lambers H., Cambridge M.L., Konings H., Pons T.L. (ed.): Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. Pp. 101–123. SPB Academic Publishing, The Hague 1989.Google Scholar
  32. Lambers H., Chapin F.S. III., Pons T.L.: Plant Physiological Ecology. Pp. 540. Springer, New York 1998.CrossRefGoogle Scholar
  33. Larcher W.: Temperature stress and survival ability of Mediterranean sclerophyllous plants. — Plant Biosyst. 134: 279–295, 2000.CrossRefGoogle Scholar
  34. Lázaro-Nogal A., Forner A., Traveset A., Valladares F.: Contrasting water strategies of two Mediterranean shrubs of limited distribution: uncertain future under a drier climate. — Tree Physiol. 33: 1284–1295, 2013.CrossRefPubMedGoogle Scholar
  35. Lelièvre F., Seddaiu G., Ledda L. et al.: Water use efficiency and drought survival in Mediterranean perennial forage grasses. — Field Crop. Res. 121: 333–342, 2011.CrossRefGoogle Scholar
  36. Lloret F., Peñuelas J., Ogaya R.: Establishment of co-existing Mediterranean tree species under a varying soil moisture regime. — J. Veg. Sci. 15: 237–244, 2004.CrossRefGoogle Scholar
  37. Long S.P., Bernacchi C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. — J. Exp. Bot. 54: 2393–2401, 2003.CrossRefPubMedGoogle Scholar
  38. Ma X.W., Ma F.W., Li C.Y. et al.: Biomass accumulation, allocation, and water-use efficiency in 10 Malus rootstocks under two watering regimes. — Agroforest Syst. 80: 283–294, 2010.CrossRefGoogle Scholar
  39. Marañón T., Grubb P.J.: Physiological Basis and Ecological Significance of the Seed Size and Relative Growth Rate Relationship in Mediterranean Annuals. — Funct. Ecol. 7: 591–599, 1993.CrossRefGoogle Scholar
  40. Martim S.A., Santos M.P., Peçanha A.L. et al.: Photosynthesis and cell respiration modulated by water deficit in grapevine (Vitis Vinifera L.) CV. Cabernet Sauvignon. — Braz. J. Plant Physiol. 21: 95–102, 2009.CrossRefGoogle Scholar
  41. McDowell N., Pockman W.T., Allen C.D. et al.: Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? — New Phytol. 178: 719–739, 2008.CrossRefPubMedGoogle Scholar
  42. Mediavilla S., Escudero A.: Differences in biomass allocation patterns between saplings of two co-occurring Mediterranean oaks as reflecting different strategies in the use of light and water. — Eur. J. Forest. Res. 129: 697–706, 2010.CrossRefGoogle Scholar
  43. Medrano H., Flexas J., Galmés J.: Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms. — Plant Soil 317: 17–29, 2009.CrossRefGoogle Scholar
  44. Meinzer F.C., Saliendra N.Z., Crisosto C.H.: Carbon isotope discrimination and gas exchange in Coffee arabica during adjustment to different soil moisture regimes. — Aust. J. Plant Physiol. 19: 171–184, 1992.CrossRefGoogle Scholar
  45. Moles A.T., Westoby M.: What do seedlings die from, and what are the implications for evolution of seed size? — Oikos 106: 193–199, 2004.CrossRefGoogle Scholar
  46. Moreno-Gutiérrez C., Battipaglia G., Cherubini P. et al.: Stand structure modulates the longterm vulnerability of Pinus halepensis to climatic drought in a semiarid Mediterranean ecosystem. — Plant Cell Environ. 35: 1026–1039, 2012.CrossRefPubMedGoogle Scholar
  47. Morison J.I.L., Baker N.R., Mullineaux P.M., Davies W.J.: Improving water use in crop production. — Philos. T. Roy. Soc. B 363: 639–658, 2008.CrossRefGoogle Scholar
  48. Myers J.A., Kitajima K.: Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. — J. Ecol. 95: 383–395, 2007.CrossRefGoogle Scholar
  49. Pattison R.R., Goldstein G., Ares A.: Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. — Oecologia 117: 449–459, 1998.CrossRefGoogle Scholar
  50. Pérez-Ramos I.M., Gómez-Aparicio L., Villar R. et al.: Seedling growth and morphology of three oak species along field resource gradients and seed mass variation: a seedling agedependent response. — J. Veg. Sci. 21: 419–437, 2010.CrossRefGoogle Scholar
  51. Ponton S., Dupouey J.L., Bréda N., Dreyer E.: Comparison of water-use efficiency of seedlings from two sympatric oak species: genotype × environment interactions. — Tree Physiol. 22: 413–422, 2002.CrossRefPubMedGoogle Scholar
  52. Poorter H., Gifford R.M., Kriedemann P.E., Wong S.C.: A quantitative analysis of dark respiration and carbon content as factors in the growth response of plants to elevated CO2. — Aust. J. Bot. 40: 501–513, 1992.CrossRefGoogle Scholar
  53. Poorter H., Remkes C.: Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. — Oecologia 83: 553–559, 1990.CrossRefGoogle Scholar
  54. Poorter H., Van der Werf A., Atkin O.K., Lambers H.: Respiratory energy requirements of roots vary with the potential growth rate of a plant species. — Physiol. Plantarum 83: 469–475, 1991.CrossRefGoogle Scholar
  55. Reich P.: Variation among plant species in leaf turnover rates and associated traits: implications for growth at all life stages. — In: Lambers H., Porter H., Van Vuuren M.M.I. (ed.): Inherent Variation in Plant Growth: Physiological Mechanisms and Ecological Consequences. Pp. 309–336. Backhuys Publishers, Leiden 1998.Google Scholar
  56. Rey P.J., Alcantara J.: Recruitment dynamics of a fleshy-fruited plant (Olea europea): connecting patterns of seed dispersal to seedling establishment. — J. Ecol. 88: 622–633, 2000.CrossRefGoogle Scholar
  57. Smith D.D., Sperry J.S.: Coordination between water transport capacity, biomass growth, metabolic scaling and species stature in co-occurring shrub and tree species. — Plant Cell Environ. 37: 2679–2690, 2014.CrossRefPubMedGoogle Scholar
  58. Traveset A., Gulias J., Riera N., Mus M.: Transition probabilities from pollination to establishment in a rare dioecious shrub species (Rhamnus ludovici-salvatoris) in two habitats. — J. Ecol. 91: 427–437, 2003.CrossRefGoogle Scholar
  59. Tomás M., Medrano H., Pou A. et al.: Water use efficiency in grapevine cultivars grown under controlled conditions: effects of water stress at the leaf and whole plant level. — Aust. J. Grape Wine Res. 18: 164–172, 2012.CrossRefGoogle Scholar
  60. Urbieta I.R., Pérez-Ramos I.M., Zavala M.A. et al.: Soil water heterogeneity and emergence time control seedling establishment in three co-occurring oak species. — Can. J. Forest Res. 38: 2382–2393, 2008.CrossRefGoogle Scholar
  61. Valladares F., Zaragoza-Castells J., Sánchez-Gomez D. et al.: Is shade beneficial for Mediterranean shrubs experiencing periods of extreme drought and late-winter Frosts? — Ann. Bot.-London 102: 923–933, 2008.CrossRefGoogle Scholar
  62. Van der Werf A., Kooijman A., Welschen R., Lambers H.: Respiratory costs for maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex acutiformis. — Physiol. Plantarum 72: 483–491, 1988.CrossRefGoogle Scholar
  63. Villar-Salvador P., Heredia N., Millar P.: Remobilization of acorn nitrogen for seedling growth in holm oak (Quercus ilex), cultivated with contrasting nutrient availability. — Tree Physiol. 30: 257–263, 2010.CrossRefPubMedGoogle Scholar
  64. Virgona J.M., Farquhar G.D.: Genotypic variation in relative growth rate and carbon isotope discrimination in sunflower is related to photosynthetic capacity. — Aust. J. Plant Phys. 23: 227–236, 1996.CrossRefGoogle Scholar
  65. Wildy D.T., Pate J.S., Sefcik L.T.: Water use efficiency of a mallee eucalypt growing naturally and in short-rotation coppice cultivation. — Plant Soil 262: 111–128, 2004.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2015

Authors and Affiliations

  • H. El Aou-Ouad
    • 1
    • 2
  • I. Florez-Sarasa
    • 1
  • M. Ribas-Carbó
    • 1
  • J. Flexas
    • 1
  • H. Medrano
    • 1
  • J. Gulías
    • 1
  1. 1.Research Group on Plant Biology under Mediterranean Conditions, Department of BiologyCtra ValldemossaPalma de MallorcaSpain
  2. 2.Département de BiologieUniversité Abdelmalek Essaadi, Faculté des SciencesTetouanMorocco

Personalised recommendations