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N resorption efficiency and proficiency in response to winter cold in three evergreen species

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Abstract

Background and aims

Along temperature gradients, changes in leaf nutrient status have been reported by different authors, which suggest the existence of differences in nutrient availability and in the patterns of nutrient use. However, the effects of temperature on nutrient resorption efficiency within a species have rarely been studied. Our aim here is to analyze the effects of the differences in winter temperatures on the nitrogen resorption of the leaves of three evergreen tree species.

Methods

Green and senescent leaves were sampled from mature specimens of the three species at 11 sites with contrasting winter temperatures. N resorption efficiencies were calculated from the differences between N contents in green and shed leaves collected from the same tree individuals. Minimum N concentrations in leaf litter were used as an estimation of resorption proficiency. Leaf mass per unit area (LMA) and concentrations of hemicellulose and cellulose were also determined in green leaves.

Results

N contents in green leaves did not show any response to temperature gradients. By contrast, N contents in leaf litter increased with decreasing temperature. As a consequence, N resorption efficiency and proficiency declined with decreasing temperature. LMA and the concentrations of structural carbohydrates increased with declining temperature.

Conclusions

The species studied have a lower potential for N resorption in environments with lower winter temperatures. The main reason for this lower efficiency seems to be the higher amounts of N immobilized in the greater amount of cell wall needed to cope with lower winter temperatures. The evergreen habit would thus be associated with higher costs at cooler sites, because the cold resistance traits imply reduced N resorption efficiency and increased dependence on soil N.

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References

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  CAS  Google Scholar 

  • Aerts R, Cornelissen JHC, Van Logtestijn RSP, Callaghan TV (2007) Climate change has only a minor impact on nutrient resorption parameters in a high-latitude peatland. Oecologia 151:132–139

    Article  CAS  PubMed  Google Scholar 

  • Ball MC, Wolfe J, Canny M, Hofmann M, Nicotra AB, Hughes D (2002) Space and time dependence of temperature and freezing in evergreen leaves. Funct Plant Biol 29:1259–1272

    Article  Google Scholar 

  • Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Chapin FS III, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64:376–391

    Article  CAS  Google Scholar 

  • Chapin FS III, Moilanen L (1991) Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72:709–715

    Article  Google Scholar 

  • Chapin FS III, Matson PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology, 2nd edn. Springer, New York

    Google Scholar 

  • Chapmann HD, Pratt PF (1973) Methods of analysis for soils, plants and water. University of California, Riverside

    Google Scholar 

  • Chen Y, Han W, Tang L, Tang Z, Fang J (2013) Leaf nitrogen and phosphorus concentrations of woody plants differ in responses to climate, soil and plant growth form. Ecography 36:178–184

    Article  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 

  • Diehl P, Mazzarino MJ, Funes F, Fontenla S, Gobbi M, Ferrari J (2003) Nutrient conservation strategies in native Andean-Patagonian forests. J Veg Sci 14:63–70

    Article  Google Scholar 

  • Eckstein RL, Karlsson PS, Weih (1998) The significance of resorption of leaf resources for shoot growth in evergreen and deciduous woody plants from a subarctic environment. Oikos 81:567–575

    Article  Google Scholar 

  • Eckstein RL, Karlsson PS, Weih M (1999) Research review. Leaf life span and nutrient resorption as determinant of plant nutrient conservation in temperate-artic regions. New Phytol 143:177–189

    Article  Google Scholar 

  • Emberger L (1930) La végétation de la région méditerranéenne. Essai d’une classification des groupements végétaux. Rev Gen Bot 43:641–662, et 705–729

    Google Scholar 

  • Enoki T, Kawaguchi H (1999) Nitrogen resorption from needles of Pinus thunbergii Parl. growing along a topographic gradient of soil nutrient availability. Ecol Res 14:1–8

    Article  Google Scholar 

  • Escudero A, Del Arco JM (1987) Ecological significance of the phenology of leaf abscission. Oikos 49:11–14

    Article  Google Scholar 

  • Escudero A, Del Arco JM, Garrido MV (1992) The efficiency of nitrogen retranslocation from leaf biomass in Quercus ilex ecosystems. Vegetatio 99–100:225–237

    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 

  • Franklin O, Ågren GI (2002) Leaf senescence and resorption as mechanisms of maximizing photosynthetic production during canopy development at N limitation. Funct Ecol 16:727–733

    Article  Google Scholar 

  • Gleason SM, Ares A (2007) Foliar resorption in tree species. In: Scarggs AK (ed) New research on forest ecology. Nova, New York, pp 1–32

    Google Scholar 

  • Goering HK, Van Soest PJ (1970) Forage fibre analysis (apparatus, reagents, procedures and some applications). Agricultural Handbook no. 379. ARS-USDA, Washington, pp 1–20

    Google Scholar 

  • Han WX, Fang JY, Reich PB, Woodward F, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796

    Article  CAS  PubMed  Google Scholar 

  • Han W, Tang L, Chen Y, Fang J (2013) Relationship between the relative limitation and resorption efficiency of nitrogen vs phosphorus in woody plants. PLoS One 8(12):e83366

    Article  PubMed Central  PubMed  Google Scholar 

  • Hikosaka K (2004) Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494

    Article  PubMed  Google Scholar 

  • Holub P, Tuma I (2010) The effects of enhanced nitrogen on aboveground biomass allocation and nutrient resorption in the fern Athyrium distentifolium. Plant Ecol 207:373–380

    Article  Google Scholar 

  • Huang J, Wang X, Yan E (2007) Leaf nutrient concentration, nutrient resorption and litter decomposition in an evergreen broad-leaved forest in eastern China. For Ecol Manag 239:150–158

    Article  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123:32–40

    Article  Google Scholar 

  • IPCC (ed) (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Jian Q, Keming M, Yuxin Z (2009) Leaf-trait relationships of Quercus liaotungensis along an altitudinal gradient in Dongling Mountain, Beijing. Ecol Res 24:1243–1250

    Article  Google Scholar 

  • Karlsson PS (1994) The significance of internal nutrient cycling in branches for growth and reproduction of Rhododendron lapponicum. Oikos 70:191–200

    Article  Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792

    Article  Google Scholar 

  • Kunstler G, Thuiller W, Curt T, Bouchaud M, Jouvie R, Deruette F, Lepart J (2007) Fagus sylvatica L. recruitment across a fragmented Mediterranean Landscape, importance of long distance effective dispersal, abiotic conditions and biotic interactions. Divers Distrib 13:799–807

    Article  Google Scholar 

  • Lovelock CE, Feller IC, Ball MC, Ellis J, Sorrell B (2007) Testing the growth rate vs geochemical hypothesis for latitudinal variation in plant nutrients. Ecol Lett 10:1154–1163

    Article  CAS  PubMed  Google Scholar 

  • Manzoni S, Jackson RB, Trofymow JA, Porporato A (2008) The global stoichiometry of litter nitrogen mineralization. Science 321:684–686

    Article  CAS  PubMed  Google Scholar 

  • Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106

    Article  Google Scholar 

  • May JD, Killingbeck KT (1992) Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology 73:1868–1878

    Article  Google Scholar 

  • Mediavilla S, Escudero A (2003) Photosynthetic capacity, integrated over the lifetime of a leaf, is predicted to be independent of leaf longevity in some tree species. New Phytol 159:203–211

    Article  Google Scholar 

  • Mediavilla S, Gallardo-López V, González-Zurdo P, Escudero A (2012) Patterns of leaf morphology and leaf N content in relation to winter temperatures in three evergreen tree species. Int J Biometeorol 56:915–926

    Article  PubMed  Google Scholar 

  • Milla R, Castro-Díez P, Maestro-Martínez M, Montserrat-Martí G (2005) Relationships between phenology and the remobilization of nitrogen, phosphorus and potassium in branches of eight Mediterranean evergreens. New Phytol 168:167–178

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Niinemets U, Tamm U (2005) Species differences in timing of leaf fall and foliage chemistry modify nutrient resorption efficiency in deciduous temperate forest stands. Tree Physiol 25:1001–1014

    Article  PubMed  Google Scholar 

  • Oleksyn J, Reich PB, Zytkowiak R, Karolewski P, Tjoelker MG (2003) Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations. Oecologia 136:220–235

    Article  CAS  PubMed  Google Scholar 

  • Oyarzabal M, Paruelo JM, Federico P, Oesterheld M, Laurenroth WK (2008) Trait differences between grass species along a climatic gradient in South and North America. J Veg Sci 19:183–192

    Article  Google Scholar 

  • Premoli AC, Brewer CA (2007) Environmental vs genetically driven variation in ecophysiological traits of Nothofagus pumilo from contrasting elevations. Aust J Bot 55:585–591

    Article  Google Scholar 

  • Pugnaire FI, Chapin FS III (1992) Environmental and physiological factors governing nutrient resorption efficiency in barley. Oecologia 90:1120–1126

    Article  Google Scholar 

  • Pugnaire FI, Chapin FS III (1993) Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology 74:124–129

    Article  Google Scholar 

  • Rajashekar CB, Lafta A (1996) Cell-wall changes and cell tension in response to cold acclimation and exogenous abscisic acid in leaves and cell cultures. Plant Physiol 111:605–612

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reiter WD (1998) The molecular analysis of cell wall components. Trends Plant Sci 3:27–32

    Google Scholar 

  • Silla F, Escudero A (2003) Uptake, demand and internal cycling of nitrogen in saplings of Mediterranean Quercus species. Oecologia 136:28–36

    Article  PubMed  Google Scholar 

  • Tang L, Han W, Chen Y, Fang J (2013) Resorption proficiency and efficiency of leaf nutrients in woody plants in eastern China. J Plant Ecol 6:408–417

    Article  Google Scholar 

  • Van Heerwaarden LM, Toet S, Aerts R (2003) Nitrogen and phosphorus resorption efficiency and proficiency in six subarctic bog species after 4 years of nitrogen fertilization. J Ecol 91:1060–1070

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Novais RF, 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 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    Article  CAS  Google Scholar 

  • Weih M, Karlsson PS (2001) Growth response of Mountain birch to air and soil temperature: is increasing leaf-nitrogen content an acclimation to lower air temperature? New Phytol 150:147–155

    Article  Google Scholar 

  • Welker JM, Fahnestock JT, Sullivan PF, Chimner RA (2005) Leaf mineral nutrition of Arctic plants in response to warming and deeper snow in northern Alaska. Oikos 109:167–177

    Article  Google Scholar 

  • Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19

    Article  Google Scholar 

  • Yasumura Y, Ishida A (2011) Temporal variation in leaf nitrogen partitioning of a broad-leaved evergreen tree, Quercus myrsinaefolia. J Plant Res 124:115–123

    Article  CAS  PubMed  Google Scholar 

  • Yuan ZY, Chen HY (2009) Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Glob Ecol Biogeogr 18:11–18

    Article  Google Scholar 

  • Yuan ZY, Li LH, Han XG, Huang JH, Wan SQ (2005) Foliar nitrogen dynamics and nitrogen resorption of a sandy shrub Salix gordejevii in northern China. Plant Soil 278:183–193

    Article  CAS  Google Scholar 

  • Zhang SB, Zhang JL, Slik JW, Cao KF (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr 21:809–818

    Article  Google Scholar 

Download references

Acknowledgments

This paper has received financial support from the Spanish Ministerio de Ciencia e Innovación—EU-FEDER (Project No. CGL2006-04281 and CGL2010-21187), the Regional Government of Castilla-León (Project No. SA126A08) and Miguel Casado S José Foundation.

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Authors and Affiliations

  1. Departamento de Ecología, Facultad de Biología, Universidad de Salamanca, 37071, Salamanca, Spain

    Patricia González-Zurdo, Alfonso Escudero & Sonia Mediavilla

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  1. Patricia González-Zurdo
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  2. Alfonso Escudero
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  3. Sonia Mediavilla
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Correspondence to Sonia Mediavilla.

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Responsible Editor: Jeffrey Walck.

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González-Zurdo, P., Escudero, A. & Mediavilla, S. N resorption efficiency and proficiency in response to winter cold in three evergreen species. Plant Soil 394, 87–98 (2015). https://doi.org/10.1007/s11104-015-2509-2

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