Original article

Micronutrients in biomass fractions of holm oak, beech and fir forests of the massif (, NE Spain)

A Caritat J Terradas

CREAF, Facultat de Ciències, Universitat Autònoma de , 08193 Bellaterra, Barcelona, Spain (Received 24 July 1989; accepted 28 February 1990)

Summary - This study is part of a larger research programme on different forest ecosystems in the (Barcelona, NE Spain). The contents of 4 micronutrients (Mn, Fe, Zn and Cu) are given for some biomass fractions in individual monospecific stands of holm oak (Quercus ilex L), beech (Fagus sylvatica L) and fir (Abies alba). The behaviour of different micronutrients is related to relative mobility. Mn, Fe and Zn concentrations increase with leaf age. Nutrient levels of the Montseny stands are compared with those found in other forests of the same species. We have observed relatively high Mn concentrations in different biomass fractions of the holm oak forest studied. This can be related to the low soil pH values. Our 3 forests show different micronutrient allocational patterns. Total quantities of the micronu- trients in the biomass are only calculated for Q ilex forest. Values found are 33.6 kg Mn/ha, 15.0 kg Fe/ha, 2.8 kg Zn/ha and 0.17 kg Cu/ha. biomass fraction / micronutrient / Quercus ilex / Fagus sylvatica / Abies alba

Résumé - Éléments traces dans la biomasse de la chênaie, de la hêtraie et de la sapinière du massif de Montseny. Ce travail fait partie d’une étude sur les différents écosystèmes fo- restiers du massif de Montseny (Barcelone, NE, Espagne). La composition en Mn, Fe, Zn et Cu de différents compartiments de la biomasse est analysée pour des parcelles monospécifiques de chêne vert (Quercus ilex), de hêtre (Fagus sylvatica) et de sapin (Abies alba). Les concen- trations en Mn, Fe et Zn augmentent au cours du vieillissement de la feuille. Les niveaux de ces concentrations ont été comparés pour les espèces correspondant à celles d’autres forêts. Le niveau du Mn est relativement élevé dans les différents compartiments des arbres de l’espèce chêne vert. Cette différence est à mettre en relation avec la basse valeur du pH du sol. A chacune des 3 forêts étudiées correspond un type différent de répartition de ces éléments traces.

* Correspondence and reprints. Present address: Estudi General de , Laboratori del suro, C/ Hospital, 6 -17071- Girona, Spain L’immobilisation totale dans la biomasse de ces éléments traces n’a été calculée que pour le peuplement de chêne vert. Elle est évaluée pour le Mn, le Fe, le Zn et le Cu respectivement à 33,6, 15, 0, 2,8 et 0,17 kg/ha.

compartiment de la biomasse / élément trace / Quercus ilex / Fagus sylvatica / Abies alba

INTRODUCTION monospecific forest canopies, in 3 different stands of the Montseny range in northern Spain, and also to look for Studies on mineral element in cycling differences related to the life forest have focused cycles ecosystems mainly and leaf morphology in these 3 species on the major nutrients. Data on micro- by comparing the micronutrient con- nutrients are and relatively scarce, tents of the various biomass fractions. most aspects of the role of micro- nutrients in ecosystems’ components are understood. poorly We know that THE STUDY AREA micronutrients accumulate in highly me- tabolically active parts of the plant, like leaves and twigs, because of their in- The experimental plots are located in volvement in enzymatic reactions within the Montseny massif, about 40 km NNE coenzyme molecules (Kramer and Koz- of Barcelona. lowski, 1979). Concentrations of the The evergreen oak plot (41° 16’ N, relatively immobile elements increase 2° 21’ E, 665 m asl) measures 0.23 ha with the age of leaves, probably due and lies within La Castanya Biological to a passive accumulation in the tran- Experimental Station, at the foot of a spiration flow and to relatively low ab- rough mountain slope (30°). The slope sorption rates (Larcher, 1977). The in the plot is slight, varying from 7 to lowest concentrations are found in 23°, and the orientation is W and NW. wood; nevertheless, wood is the bio- The bedrock consists of a metamorphic mass fraction containing the greatest schist, and the soil is a ranker (U 2 b/c, quantity of micronutrients, simply be- gravelly phase) associated with a dys- cause it is the largest one. Concentra- tric cambisol (Bd). Mean annual pre- tions usually decrease as the stem cipitation is around 900 mm and mean diameter increases. Bark is an area of annual air temperature is 9 - 10 °C. accumulation and usually has high mi- The tree layer is dense and formed ex- cronutrient concentrations (Denaeyer clusively of Quercus ilex. The basal De Smet, 1971). area was 26.6 m2/ha in 1979. There As occurs frequently with major were 2 100 stems/ha with a DBH > 5 nutrients, rates of change and total cm and 536 stems with DBH > 15 cm. content of oligoelements vary greatly The dominant trees were 9-12 m in among species. The aim of this study height and had an estimated age of was to determine the levels of 4 micro- 60 - 90 years. nutrients (Mn, Fe, Zn and Cu) in the The beech plot (41° 46’ N, 2° 28’ E, different biomass fractions of holm oak 1 165 m asl) measures 0.12 ha and is (Quercus ilex), beech (Fagus sylvatica) located in the Santa Fe Valley. The and silver fir (Abies alba), growing in slope is gentle (5°). The bedrock is a In deep altered granodiorite, and the soil wood from 10 trees (September 1983). the fir forest (Passavets) we collected samples is a cambisol Bh, dystric-humic (Bd - of leaves, 1-5 branches and wood is about yr-old 1 a). Mean annual precipitation boles belonging to 3 fir trees. air 1 200 mm (Rod, 1983) and average Bulked samples of each biomass fraction temperature is 8 - 9 °C. The canopy is from the different trees in each plot were dense and consists of Fagus sylvatica analysed. They were dried to constant were with some isolated individuals of Ilex weight at 80 °C. Mn, Fe, Zn and Cu atomic absorption with a PYE aquifolium as subdominants. The basal analysed by UNICAM Sp-1900 (Spectroscopy Service, was 26.7 in 1980. There are area m2/ha Barcelona University) after acid digestion, 1 460 stems/ha with a DBH > 5 cm and following the methods described by Allen et 625 stems/ha with DBH > 15 cm. The al (1974) for Mn, Fe and Zn. For Cu, due to dominant trees are 16 -20 m in height the low concentrations, it was necessary to the and 50-60 years old. The last tree thin- adopt a different procedure: samples were with HNO3 and HClO4 on a was carried out between 15 to 30 digested ning hot plate, gradually increasing the tempera- years ago. ture to 210 °C and maintaining it at this level The fir plot (41° 47’ N, 2° 27’ E, to the end of the digestion. These Cu ana- of 1 355 m asl) is in the Passavets fir for- lyses were carried out in the Department of the of Aberdeen. est. It measures 0.12 ha and is situated Soil Science University The micronutrient concentrations were on a NNW slope. The bedrock is a in order to determine individual hornfels and the soil is a ranker (U 2 d, analysed tree variability in the different biomass frac- stony phase) associated with dystric tions of 11 holm oaks. The variability of the lithosols. The mean annual precipitation different elements is less than 12% in all the is 1200 mm and the mean temperature biomass fractions except in the stem wood is 7-8 °C. The tree layer is dense and where it is between 12 and 22%. Total mi- have been calculated is entirely of Abies alba Mill. cronutrient quantities composed from the biomass values obtained by dimen- The basal area was 42.4 in 1980. m2/ha sional analysis (Ferres, 1984) and micro- There were 567 stems/ha with a DBH > nutrient concentrations. 5 cm and 467 stems/ha with DBH > 15 cm. The dominant trees were 21-25 m in and from 120-160 old. height years RESULTS AND DISCUSSION

METHODS Micronutrient concentrations

For the holm oak forest (La Castanya stand) in the different frac- we used the field samples of the biomass The concentrations fractions collected previously by Ferres tions agree with the general trends dis- (1984). These samples, obtained from 15 cussed in the introduction, as can be were trees from even stem diameter class, seen in table I. divided into: leaves (separated into age In the holm we can combine our classes); 1 or 2 year-old twigs of 0-1 cm dia- oak, meter (bark included); wood from the data with those of Ferres (1984) for branches (divided into 1 cm diameter major nutrients to obtain the following and bark classes); wood from the boles, nutrient ranking: Ca > N > K > Mg - from the branches and boles. We took ad- P > Mn > Fe > Na > Zn > Cu. In the ditional bole wood samples from 10 trees cases of the beech and fir stands, we with a Pressler borer. data on the nutrients, In the beech stand (Santa Fe) we col- lack similar major lected samples of leaves, twigs and thin but the micronutrient ranking is identi- cal. Concentrations in the individual bi- (table II). Montseny beech leaves show omass components are as follows. Fe levels similar to other beech forests (Guha and Mitchell, 1966; Heinrichs and Leaves Mayer, 1980), but for Mn we observed rela- tively low values. Fir has low Mn concen- In the holm oak, Fe concentrations in the trations. As expected, at Montseny the leaves are similar to these found in the beech leaves are richer in Fe than the Rouquet (Rapp, 1971) and Zn concentra- leaves of the holm oak or the fir. tions are close to those found in Prades The Mn requires further comment. We (Escarre et al, 1983). Mn levels are higher know that micronutrients are, in general, than those at either Rouquet or Prades more available in areas with a slightly acid pH (Sutcliffe and Baker, 1979). This is Thus, the Mn concentrations in the reflected in the biomass content of Montseny holm oak could be a con- these nutrients. Nihlgård and Lindgren sequence of the relatively high amounts (1977) studied 3 beech forests growing of Mn in the soil and the low pH values with on different soil types and found that when compared with the other sites Mn oxidizes and precipitates, becom- holm oak forests studied by Lossaint and ing unavailable to plants at a pH higher Rapp (1971) and Escarré et al (1983). than 6. As a result, the concentrations Incidentally, the beech and fir stands and contents of this element in plant studied here have relatively less acidic tissues are higher in beech forests soils than at the other European sites been growing on acid soils where production where the same species have is also low. Olsen (1948) observed that, studied, and this may explain why Mn on calcareous soils, beech leaves show levels are lower in Montseny. concentrations of Fe higher than those of Mn, while on acid soils, the reverse is true. Passama (1970) analysed Mn, Twigs, branches and stems Fe and Zn in the leaves of holm oaks growing on acid and calcareous soils The twigs in the holm oak stands have and found that there was a general ten- Mn and Zn concentrations similar to dency for the levels to increase with acid- those found in Prades (Escarre et al, ity, especially for Mn. 1983) and higher concentrations of Fe. The concentration of Cu in the twigs Other fractions is higher than that of the leaves for holm oak and fir, but for beech the reverse is We have considered the bark, inflores- true. In general, fir branches are rela- cences and fruits for the holm oak alone tively rich in micronutrients. The obser- (table I). Our results do not require much vations of micronutrient accumulation, comment. It is worth noting, however, that and especially of Fe, in relation to the Fe and Zn are present in relatively low age of the twigs, made by Heinrichs and concentrations in acorns, showing a pat- Mayer (1980) for Picea abies forests, tern similar to that observed for Na suggest a storage function. Our results (Ferres, 1984) in the same stand. Mn for fir could also be the result of the and, especially, Zn have quite high storage of the less mobile elements in values in the inflorescences. that biomass fraction. The stem wood is poor in micro- Micronutrient levels in the biomass nutrients in the 3 species, except for Cu in the beech (table I). The micronutrient levels in the biomass Using the data collected by Rodin and obviously depend on the quantity of the Bazilevich (1967) on temperate forests, biomass. In figure 1 we show the dis- holm oak leaves contain, in general, tribution of Mn, Fe and Zn in the holm lower concentrations than are found in oak. Table III shows data from the differ- the leaves of deciduous trees and are ent types of forests. Note that the 3 holm closer to the concentrations found in con- oak forests are rather poor in Mn and Fe ifers; however, the holm oak wood is when compared with the F sylvatica and richer than that of deciduous trees. This P abies stands. However, they are rela- pattern is not observed clearly in our tively rich in Mn when compared with Montseny data. stands of Mediterranean pines. CONCLUSION quantities of Mn and Ca are found in the bark. As for the the foliar The concentration ranking of the micro- macronutrients, micronutrient levels an nutrients studied in the Montseny represent impor- tant percentage of the total amount of stands is the same for all 3 types of these elements if we bear in mind that forest: Mn > Fe > Zn > Cu. The holm the leaf biomass is 3.8% of the oak shows values similar to those found only total biomass of this forest. The per- at other sites with the same species, of Mn located in leaves is except for Mn. The high levels of Mn centage especially high and is greater than the in Montseny are probably due to low percentage of N. Leaf nutrients have a soil pH and the resulting high concen- turnover rate than the nutrients trations of soluble Mn in the soils. higher stored in other biomass fractions. micronutrient concen- Usually, high Our 3 forests show different micro- trations are found in the most metabo- nutrient allocational and this lically active tissues: the leaves and patterns, is related to their different The levels in fir branches are the probably twigs. modes of life exception. Mn, Fe and Zn levels in- (deciduous, evergreen conifers, broad-leaved evergreens). crease with leaf age as do the other Beech tends to have concentra- elements such as Ca and higher accumulating tions of Mn and Fe in the leaves. Holm Na (Ferres, 1984). On the other hand, oak has a even distribution N and P are translocated more relatively easily. for the levels of Mn in Concentrations of these metals in the (except high Fir, as other conifers, shows wood decrease as the diameter in- leaves). micronutrient levels in the creases, as do the marcronutrients, be- high branches. cause of a dilution phenomenon. The wood and bark of the holm oak forest contain a large proportion of the ACKNOWLEDGMENTS nutrient content, as is usual in forest ecosystems, because of their great work the The main part of the Fe, Zn This was supported financially by quantity. CAICYT. We thank Estació Biològica de la and Cu is found in the wood, bark, Castanya de la Generalitat de Catalunya and leaves and twigs. Mg, Na, N and K the Servei de Parcs Naturals de la Diputació show the same pattern. The highest de Barcelona. We also thank Dr Miller and Dr Killham for their advice and facilities gi- Kramer JK, Koslowski TT (1979) Physiology ven to some of our analytical work done in of Woody Plants. Academic Press, New their laboratories (Forestry and Soil Science York, 811 p Departments, Aberdeen University) and M Larcher W (1977) Ecofisiologia vegetal. Compte and M Gumbao for the revision of Omega, Barcelona, 305 p the version. English Lossaint P, Rapp M (1971) Répartition de la matière organique, productivité et cycles des éléments minéraux dans des écosys- RÉFÉRENCES tèmes forestiers. Actes Coll. Bruxelles: Ecologie et Conservation, 4 UNESCO Plant bio- Allan NDA, Rencz AN Concentration, Nihlgård B, Lindgren L (1977), (1982) and bioele- mass and distribution of nutrients in a mass, primary production in subarctic Picea mariana-Cladonia al- ments of three mature beech forests pestris ecosystem. Can J For Res 12, South Sweden. Oikos 28, 95-104 947-968 Olsen C (1948) The mineral, nitrogen and Allen SE, Grimshaw HM, Parkinson JA (1974) sugar content of beech leaves and beech Chemical Analysis of Ecological Materi- leaf sap at various times. CR Lab Carls- als. Blackwell, Oxford berg Sér Chim 26, 197-230 Denaeyer de Smet S (1971) Teneurs en élé- Passama L (1970) Composition minérale de ments biogènes des tapis végétaux dans diverses espèces calcicoles et calcifuges les forêts caducifolièes d’Europe. In: Pro- de la région méditerranéenne française. ductivité des écosystèmes forestiers. Oecol Plant 5, 225-246 Actes Coll Bruxelles (Écologie et Conser- Rapp M (1971) Cycle de la matière or- vation 4), (Duvigneaud P, ed) Unesco, ganique et des éléments minéraux dans 515-526 quelques écosystèmes méditerranéens. Escarre A, Gracia C, Terradas J (1983) Editions du CNRS, Paris, 184 p Structure and of dynamics evergreen-oak Rapp M (1978) El cicio biogeoquimico en forest In: of Forest ecosystems. Dynamics un bosque de pino carrasco. In: Ecologia Ecosystems. European Science Founda- forestal (P Pesson, ed) Ediciones Mundi- tion. Uppsala 21-24 Prensa, 97-118 Ferres LL Biomasa, (1984) producción y Cabanettes A Biomasse, mineralomasas del enzinar montano de Rapp M, (1980) minéralomasse et productivité d’un La Castanya (Montseny). Doctoral Thesis Universitat Autònoma de écosystème à pins pignons (Pinus pinea, Dept, Ecologia, L) du littoral méditerranéen. Acta Barcelona, Bellaterra Ecolog- ica. Oecol Plant 15, 151-164 Guha MM, Mitchell RL (1966) The trace and major element composition of the leaves Rodin LE, Bazilevich NI (1967) Production in Terrestrial of some deciduous trees. II. Seasonal and Mineral Cycling Vegeta- changes- Plant Soil 24, 90-112 tion. Oliver and Boyd, Edinburgh and 228 Heinrichs H, Mayer R (1980) The role of for- London, p est vegetation in the biogeochemical Sutcliffe JF, Baker DA (1979) Las plantas y cycle of heavy metals. J Environ Qual 9, las sales minerales. Cuadermos Biologia. 111-118 Omega, Barcelona, 67 p Johnson FL, Risser PG (1974) Biomass, an- Whittaker RH, Likens GE, Bormann FH, nual net primary production, and dynam- Eaton JS, Siccama TG (1979) The Hub- ics of six mineral elements in a post bard Brook ecosystem study: forest Oak-Blackjack oak forest. Ecology 55, nutrient cycling and element behaviour. 1246-1258 Ecology 60, 203-220