Skip to main content

Advertisement

Log in

Seasonal nutrient retranslocation in reforested Pinus halepensis Mill. stands in Southeast Spain

  • Published:
New Forests Aims and scope Submit manuscript

Abstract

Retranslocation, resorption and relocation of nutrients are important adaptive mechanisms developed by plants to acquire the amount of the nutrients required for growth. They are usual mechanisms in deciduous and conifer trees that occur in Mediterranean regions where drought periods are usual. Soil factors, environmental characteristics and species factors are key drivers of nutrient retranslocation in conifers but is not well understood how soil fertility or intraspecific competition influences the process. We studied retranslocation in Pinus halepensis Mill. stands showing different site quality (differences in climate and intraspecific competition) occurring in Southeast Spain. We monitored reforested mature Aleppo pine forests in stands with differences in site quality, climate and intraspecific competition. Stands were characterised, the content of nutrients of soil and green samples (twigs and pine needles) were recorded, and seasonal nutrient retranslocation was obtained. Site characteristics were related to growth rate and nutrient content of foliage and soil. We evaluated whether the retranslocation of nutrients from older to younger foliage was related to the current-year growth rate and to the nutritional status of the plant as influenced by intraspecific competition. Foliar macronutrient concentrations and the amount of retranslocated macronutrients were seasonal, with differences related to site quality and tree density. As a general trend, nutrient concentrations increased after drought (autumn) and decreased during the growth period (spring). However, some micronutrients (mainly Na and Fe) decreased during both periods. The retranslocation pattern in Aleppo pine reinforced the hypothesis that pine adaptations to drought- and fire-prone habitats are linked to the resilience of these forest types. We developed scientific knowledge to assist decision making in adaptive forest management; e.g. fertilizer recommendations or reforestation programmes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • AEMET, Spanish National Meteorological Agency (2011). https://opendata.aemet.es. Accessed 16 Dec 2012

  • Agee JK (1998) Fire and pine ecosystems. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 193–218

    Google Scholar 

  • Ayari A, Moya D, Rejeb MN, Ben Mansoura A, Garchi S, de las Heras J, Hanchi B (2011) Alternative sampling methods to estimate structure and reproductive characteristics of Aleppo pine forest in Tunisia. For Syst 20(3):348–360

    Google Scholar 

  • Baquedano F, Valladares F, Castillo F (2008) Phenotypic plasticity blurs ecotypic divergence in the response of and to water stress. Eur J For Res 127(6):495–506

    Article  Google Scholar 

  • Blanco JA, Bosco Imbert J, Castillo FJ (2009) Thinning affects nutrient resorption and nutrient-use efficiency in two Pinus sylvestris stands in the Pyrenees. Ecol Appl 19(3):682–698

    Article  PubMed  Google Scholar 

  • Castro J, Zamora R, Hódar JA, Gómez JM, Gómez-Aparicio L (2004) Benefits of using shrubs as nurse plants for reforestation in Mediterranean mountains: a 4-year study. Rest Ecol 12:352–358

    Article  Google Scholar 

  • Chapin FS III, Schulze E, Mooney HA (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New York

    Google Scholar 

  • Corona P, Ferrara A (1989) Individual competition indices for conifer plantations. Agr Ecosyst Environ 27(1–4):429–437

    Article  Google Scholar 

  • de las Heras J, Moya D, López-Serrano FR, Rubio E (2013) Carbon sequestration and early thinning in Aleppo pine stands regenerated after fire in Southeastern Spain. New For 44(3):457–470

    Article  Google Scholar 

  • De Martonne E (1926) Aréisme et indice artidite. Compte Rendu L’Acad Sci Paris 182:1395–1398

    Google Scholar 

  • Del Arco JM, Escudero A, Garrido MV (1991) Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology 72:701–708

    Article  Google Scholar 

  • Del Campo A, Hermoso J, Ceacero C, Navarro Cerrillo RM (2011) Nursery location and potassium enrichment in Aleppo pine stock 1. Effect on nursery culture, growth, allometry and seedling quality. Forestry 84:221–234

    Article  Google Scholar 

  • Delgado-Baquerizo M, Covelo F, Gallardo A (2011) Dissolved organic nitrogen in Mediterranean ecosystems. Pedosphere 21:309–318

    Article  CAS  Google Scholar 

  • Doblas-Miranda E, Martínez-Vilalta J, Lloret F, Álvarez A, Ávila A, Bonet FJ, Brotons L, Castro J, Curiel Yuste J, Díaz M, Ferrandis P, García-Hurtado E, Iriondo JM, Keenan TF, Latron J, Llusià J, Loepfe L, Mayol M, Moré G, Moya D, Peñuelas J, Pons X, Poyatos R, Sardans J, Sus O, Vallejo VR, Vayreda J, Retana J (2015) Reassessing global change research priorities in Mediterranean terrestrial ecosystems: how far have we come and where do we go from here? Global Ecol Biogeogr 24:25–43

    Article  Google Scholar 

  • Doblas-Miranda E, Alonso R, Arnan X, Bermejo V, Brotons L, de las Heras J, Estiarte M, Hodar JA, Llorens P, Lloret F, Lopez-Serrano FR, Martinez-Vilalta J, Moya D, Peñuelas J, Pino J, Rodrigo A, Roura-Pascual N, Valladares F, Vila M, Zamora R, Retana J (2017) A review of the combination among global change factors in forests, shrublands and pastures of the Mediterranean Region: beyond drought effects. Glob Planet Change 148:42–54

    Article  Google Scholar 

  • Fife DN, Nambiar EKS, Saur E (2008) Retranslocation of foliar nutrients in evergreen tree species planted in a Mediterranean environment. Tree Physiol 28:187–196

    Article  CAS  PubMed  Google Scholar 

  • Hedo J, Lucas-Borja ME, Wic C, Andrés-Abellán M, de las Heras J (2015) Soil microbiological properties and enzymatic activities of long-term post-fire recovery in dry and semiarid Aleppo pine (Pinus halepensis M.) forest stands. Solid Earth 6:243–252

    Article  Google Scholar 

  • Helmisaari HS (1992) Nutrient retranslocation within the foliage of Pinus sylvestris. Tree Physiol 10(1):45–58

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Tecles E, Osem Y, Alfaro-Sanchez R, de las Heras J (2015) Vegetation structure of planted versus natural Aleppo pine stands along a climatic gradient in Spain. Ann For Sci 72(5):641–650

    Article  Google Scholar 

  • IGN (2006) Mapa de suelos de España. Instituto Geográfico Nacional, Madrid, Spain

    Google Scholar 

  • Jacobs DF, Oliet JA, Aronson J, Bolte A, Bullock JM, Donoso PJ, Landhäusser SM, Madsen P, Peng S, Rey-Benayas JM, Weber JC (2015) Restoring forests: what constitutes success in the twenty-first century? New For 46(5):601–614

    Article  Google Scholar 

  • López-Serrano FR, de las Heras J, González-Ochoa AI, García-Morote FA (2005) Effects of silvicultural treatments and seasonal patterns on foliar nutrients in young post-fire Pinus halepensis forest stands. For Ecol Manag 210:321–336

    Article  Google Scholar 

  • Maestre FT, Cortina J, Bautista S (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas? For Ecol Manag 198:303–317

    Article  Google Scholar 

  • MAFF (1986) The analysis of agricultural material. Ministry of Agriculture Fisheries and Food, Reference book 427, HMSO, London, UK, pp 156–157

  • Merchant A (2016) The importance of storage and redistribution in vascular plants. Tree Physiol 36(5):533–535

    Article  PubMed  Google Scholar 

  • Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30(9):1083–1095

    Article  CAS  PubMed  Google Scholar 

  • Millett J, Millard P, Hester AJ, McDonald AJS (2005) Do competition and herbivory alter the internal nitrogen dynamics of birch saplings? New Phytol 168:413–422

    Article  CAS  PubMed  Google Scholar 

  • Misson L, Rathgeber C, Guiot J (2004) Dendroecological analysis of climatic effects on Quercus petraea and Pinus halepensis radial growth using the process-based MAIDEN model. Can J For Res 34:888–898

    Article  Google Scholar 

  • Moreno-Gutiérrez C, Battipaglia G, Cherubini P, Saurer M, Nicolás E, Contreras S, Querejeta JI (2012) Stand structure modulates the long-term vulnerability of Pinus halepensis to climatic drought in a semiarid Mediterranean ecosystem. Plant Cell Environ 35:1026–1039

    Article  PubMed  Google Scholar 

  • Moya D, de las Heras J, López-Serrano FR, Leone V (2008) Optimal intensity and age of management in young Aleppo pine stands for post-fire resilience. For Ecol Manag 255(8–9):3270–3280

    Article  Google Scholar 

  • Moya D, de las Heras J, López-Serrano FR, Ferrandis P (2015) Post-fire seedling recruitment and morpho-ecophysiological responses to induced drought and salvage logging in Pinus halepensis Mill. stands. Forests 6(6):1858–1877

    Article  Google Scholar 

  • Munson AD, Margolis HA, Brand DG (1995) Seasonal nutrient dynamics in white pine and white spruce in response to environmental manipulation. Tree Physiol 15(3):141–149

    Article  CAS  PubMed  Google Scholar 

  • Muukkonen P (2005) Needle biomass turnover rates of Scots pine (Pinus sylvestris L.) derived from the needle-shed dynamics. Trees 19(3):273–279

    Article  Google Scholar 

  • Nambiar EK, Fife DN (1991) Nutrient retranslocation in temperate conifers. Tree Physiol 9:185–207

    Article  CAS  Google Scholar 

  • Newton AC, Cantarello E (2015) Restoration of forest resilience: an achievable goal? New For 46(5):645–668

    Article  Google Scholar 

  • Oliet JA, Puertolas J, Planelles R, Jacobs DF (2013) Nutrient loading of forest tree seedlings to promote stress resistance and field performance: a Mediterranean perspective. New For 44(5):649–669

    Article  Google Scholar 

  • Parraga-Aguado I, Querejeta JI, Gonzalez-Alcaraz MN, Concesa HM (2014) Metal(loid) allocation and nutrient retranslocation in Pinus halepensis trees growing on semiarid mine tailings. Sci Tot Environ 485–486:406–414

    Article  Google Scholar 

  • Piñeiro G, Perelman S, Guerschman JP, Paruelo JM (2008) Evaluating models: observed vs. predicted or predicted vs. observed? Ecol Model 216:316–322

    Article  Google Scholar 

  • Pommerening A (2006) Evaluating structural indices by reversing forest structural analysis. For Ecol Manag 224:266–277

    Article  Google Scholar 

  • Proe MF, Midwood AJ, Craig J (2000) Use of stable isotopes to quantify nitrogen, potassium and magnesium dynamics in young Scots pine (Pinus sylvestris). New Phytol 146:461–469

    Article  CAS  Google Scholar 

  • Querejeta JI, Barberá GG, Granados A, Castillo VM (2008) Afforestation method affects the isotopic composition of planted Pinus halepensis in a semiarid region of Spain. For Ecol Manag 254(1):56–64

    Article  Google Scholar 

  • Quezel P (2000) Taxonomy and biogeography of Mediterranean pines (Pinus halepensis and Pinus brutia). In: Ne’eman G, Trabaud L (eds) Ecology, biogeography and management of Pinus halepensis and Pinus brutia forest ecosystems in the Mediterranean Basin. Backhuys Publisher, Leiden, pp 1–12

    Google Scholar 

  • Reich PB, Grigal DF, Aber JD, Gower ST (1997) Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78(2):335–347

    Article  Google Scholar 

  • Ruiz-Navarro A, Barberá GG, Navarro-Cano JA, Albaladejo J, Castillo VM (2009) Soil dynamics in Pinus halepensis reforestation: effect of microenvironments and previous land use. Geoderma 153:353–361

    Article  CAS  Google Scholar 

  • Sardans J, Peñuelas J, Roda F (2005) Changes in nutrient use efficiency, status and retranslocation in young post-fire regeneration Pinus halepensis in response to sudden N and P input, irrigation and removal of competing vegetation. Trees 19:233–250

    Article  CAS  Google Scholar 

  • Saur E, Ranger J, Lemoine B, Gelpe J (1992) Micronutrient distribution in 16 year old maritime pine. Tree Physiol 10:307–316

    Article  CAS  PubMed  Google Scholar 

  • Saur E, Nambiar EKS, Fife DN (2000) Foliar nutrient retranslocation in Eucalyptus globulus. Tree Physiol 20:1105–1112

    Article  CAS  PubMed  Google Scholar 

  • Schulze E-D, Chapin FS III (1987) Plant specialization to environments of different resource availability. In: Schulze E-D, Zwolfer H (eds) Potentials and limitations of ecosystem analysis. Ecological studies 61. Springer, Berlin, pp 120–148

    Chapter  Google Scholar 

  • Soil Survey Staff (2010) Keys to soil taxonomy, 11th edn. USDA-Natural Resources Conservation Service, Washington, DC

  • Stanturf J (2015) Future landscapes: opportunities and challenges. New For. doi:10.1007/s11056-015-9500-x

    Google Scholar 

  • Stefan K, Raitio H, Bartels U, Furst A (2000) Manual on methods and criteria for harmonized sampling, assessment, monitoring and analysis of the effects of air pollution on forest. Part IV. Sampling and analysis of needles and leaves. UN/ECE, Austrian Federal Forest Research Centre, Vienna

  • Tsitsoni T, Karagiannakidou V (2000) Site quality and stand structure in Pinus halepensis forests of north Greece. Forestry 72(1):51–64

    Article  Google Scholar 

  • Uscola M, Villar-Salvador P, Gross P, Maillard P (2015a) Fast growth involves high dependence on stored resources in seedlings of Mediterranean evergreen trees. Ann Bot 115:1001–1013

    Article  PubMed  PubMed Central  Google Scholar 

  • Uscola M, Salifu KF, Oliet JA, Jacobs DF (2015b) An exponential fertilization dose–response model to promote restoration of the Mediterranean oak Quercus ilex. New For 46(5):795–812

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Ferreira Novais R, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Villar-Salvador P, Puertolas Simon J, Cuesta B, Penuelas JL, Uscola M, Heredia-Guerrero N, Rey Benayas JM (2012) Increase in size and nitrogen concentration enhances seedling survival in Mediterranean plantations: insights from an ecophysiological conceptual model of plant survival. New For 43(5–6):755–770

    Article  Google Scholar 

  • Villar-Salvador P, Uscola M, Jacobs DF (2015) The role of stored carbohydrates and nitrogen in the growth and stress tolerance of planted forest trees. New For 46:813–839

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the Spanish Institute for Agricultural and Food Research and Technology (INIA) for the funding awarded through National Research Projects GEPRIF (RTA2014-00011-C06). We would like to thank Helen Warburton for reviewing the English. We also thank the Regional Forestry Services of Junta de Comunidades de Castilla-La Mancha and Comunidad Autónoma Región de Murcia for field assistance and experimental forest management.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Moya.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 357 kb)

Supplementary material 2 (DOC 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de las Heras, J., Hernández-Tecles, E.J. & Moya, D. Seasonal nutrient retranslocation in reforested Pinus halepensis Mill. stands in Southeast Spain. New Forests 48, 397–413 (2017). https://doi.org/10.1007/s11056-016-9564-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11056-016-9564-2

Keywords

Navigation