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

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Photosynthetica

Abstract

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.

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Abbreviations

DM:

dry mass

E :

transpiration rate

g s :

stomatal conductance

LA:

leaf area

LAR:

leaf area ratio

LMR:

leaf mass ratio

P N :

net photosynthetic rate

P Nm/R Dm :

net carbon assimilation to dark respiration ratio on a mass basis

R D :

respiration rate

RGR:

relative growth rate

R/S:

root:shoot ratio

SLA:

specific leaf area

SWC:

soil water content

VPD:

vapor pressure deficit

WUEi :

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

WUEWP :

plant water-use efficiency

References

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Boyer J.S., Westgate M.E.: Grain yields with limited water. — J. Exp. Bot. 55: 2385–2394, 2004.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Garnier E.: Growth analysis of congeneric annual and perennial grass species. — J. Ecol. 80: 665–675, 1992.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gratani L., Varone L., Catoni R.: Relationship between net photosynthesis and leaf respiration in Mediterranean evergreen species. — Photosynthetica 46: 567–573, 2008.

    Article  Google Scholar 

  • Gratani L., Varone L.: Adaptative photosynthetic strategies of the Mediterranean maquis species according to their origin. — Photosynthetica 42: 551–558, 2004.

    Article  Google Scholar 

  • Guijarro J.A.: [Contribution to the Balearic Bioclimatology.] — PhD Thesis. Universitat de les Illes Balears, Palma de Mallorca 1986. [In Spanish]

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hou J., Romo J.T.: Seed weight and germination time affect growth of two shrubs. — J. Range Manage. 51: 699–703, 1998.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Lambers H., Chapin F.S. III., Pons T.L.: Plant Physiological Ecology. Pp. 540. Springer, New York 1998.

    Book  Google Scholar 

  • Larcher W.: Temperature stress and survival ability of Mediterranean sclerophyllous plants. — Plant Biosyst. 134: 279–295, 2000.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Myers J.A., Kitajima K.: Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. — J. Ecol. 95: 383–395, 2007.

    Article  CAS  Google Scholar 

  • Pattison R.R., Goldstein G., Ares A.: Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. — Oecologia 117: 449–459, 1998.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Research Group on Plant Biology under Mediterranean Conditions, Department of Biology, Ctra Valldemossa, km 7.5. 07122, Palma de Mallorca, Spain

    H. El Aou-Ouad, I. Florez-Sarasa, M. Ribas-Carbó, J. Flexas, H. Medrano & J. Gulías

  2. Département de Biologie, Université Abdelmalek Essaadi, Faculté des Sciences, B.P. 2121, 93002, Tetouan, Morocco

    H. El Aou-Ouad

Authors
  1. H. El Aou-Ouad
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  2. I. Florez-Sarasa
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  3. M. Ribas-Carbó
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  4. J. Flexas
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  5. H. Medrano
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  6. J. Gulías
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Correspondence to J. Gulías.

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Acknowledgements: This research was supported by AVERROES grant (Erasmus MUNDUS, European Commission).

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El Aou-Ouad, H., Florez-Sarasa, I., Ribas-Carbó, M. et al. Trade-offs between seedling growth, plant respiration and water-use efficiency in two Mediterranean shrubs Rhamnus alaternus and Rhamnus ludovici-salvatoris . Photosynthetica 53, 537–546 (2015). https://doi.org/10.1007/s11099-015-0141-2

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