Photosynthetica 2015, 53(4):537-546 | DOI: 10.1007/s11099-015-0141-2

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

H. El Aou-Ouad1,2, I. Florez-Sarasa1, M. Ribas-Carbó1, J. Flexas1, H. Medrano1, J. Gulías1,*
1 Research Group on Plant Biology under Mediterranean Conditions, Department of Biology, Ctra Valldemossa, Palma de Mallorca, Spain
2 Département de Biologie, Université Abdelmalek Essaadi, Faculté des Sciences, Tetouan, Morocco

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.

Keywords: chilling temperature; leaf area ratio; seedling survival; specific leaf area

Received: July 8, 2014; Accepted: February 13, 2015; Published: December 1, 2015Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Aou-Ouad, H., Florez-Sarasa, I., Ribas-Carbó, M., Flexas, J., Medrano, H., & Gulías, J. (2015). Trade-offs between seedling growth, plant respiration and water-use efficiency in two Mediterranean shrubs Rhamnus alaternus and Rhamnus ludovici-salvatoris. Photosynthetica53(4), 537-546. doi: 10.1007/s11099-015-0141-2.
Download citation

References

  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  4. Boyer J.S., Westgate M.E.: Grain yields with limited water. - J. Exp. Bot. 55: 2385-2394, 2004. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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.
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  14. Garnier E.: Growth analysis of congeneric annual and perennial grass species. - J. Ecol. 80: 665-675, 1992. Go to original source...
  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. Go to original source...
  16. Gratani L., Varone L., Catoni R.: Relationship between net photosynthesis and leaf respiration in Mediterranean evergreen species. - Photosynthetica 46: 567-573, 2008. Go to original source...
  17. Gratani L., Varone L.: Adaptative photosynthetic strategies of the Mediterranean maquis species according to their origin. - Photosynthetica 42: 551-558, 2004. Go to original source...
  18. Guijarro J.A.: [Contribution to the Balearic Bioclimatology.] - PhD Thesis. Universitat de les Illes Balears, Palma de Mallorca 1986. [In Spanish]
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  24. Hou J., Romo J.T.: Seed weight and germination time affect growth of two shrubs. - J. Range Manage. 51: 699-703, 1998. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  32. Lambers H., Chapin F.S. III., Pons T.L.: Plant Physiological Ecology. Pp. 540. Springer, New York 1998. Go to original source...
  33. Larcher W.: Temperature stress and survival ability of Mediterranean sclerophyllous plants. - Plant Biosyst. 134: 279-295, 2000. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  48. Myers J.A., Kitajima K.: Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. - J. Ecol. 95: 383-395, 2007. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...