Nutrient efficiency and resorption in Quercus pyrenaica oak coppices under different rainfall regimes of the Sierra de Gata mountains (central western Spain)

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Nutrient efficiency and resorption in Quercus pyrenaica

oak coppices under different rainfall regimes of the

Sierra de Gata mountains (central western Spain)

Juan F. Gallardo, Alejandro Martín, Gerardo Moreno

To cite this version:

Original

article

Nutrient

_efficiency

and

_resorption

in

_{Quercus pyrenaica}

oak

_coppices

under

different rainfall

_regimes

of

the

Sierra de

Gata mountains

_(central

western

_Spain)

Juan F. Gallardo

a

_Alejandro

Martín

b

Gerardo Moreno

a

C.S.I.C.,

Aptdo

257, Salamanca 37071,

Spain

b

Area de

_Edafología,

Facultad _{of Farmacia,} Salamanca 37080,

_Spain

(Received 8 December _1997;

_accepted

8 January 1999)

Abstract - Nutrient

_uptake,

nutrient

_resorption

and nutrient use

_efficiency

_(NUE) were estimated in four _{Quercus pyrenaica} oak

_coppices

situated in the Sierra de Gata mountains

_(province

of Salamanca, central-western

_Spain).

The

_efficiency

_(NUE) with which a

_given

nutrient is used

_depends

on several factors. In the oak

_coppices

studied,

availability

of P, Ca and

_Mg

in the soil was one of the factors

_{governing efficiency.}

On the other hand, there was a certain

_independence

between soil N and K

_availability

and their

_{plant efficiency;}

in the case of N this occurred

_possibly

because it is a

_limiting

factor. There was a

_plant

nutritional

_Ca-Mg

imbalance due to soil

_acidity.

Leaf

_absorption

and/or

_leaching

at _{canopy level would also influence the N and K}

_efficiency.

The stand with the most

_dystrophic

soil was the least efficient

_{regarding Mg,}

and the

_plot

with the most

_eutrophic

soil

_regarding

Ca. All the oak

coppices

had low N

_efficiency.

Bioelement

_resorption

did not affect the NUE

_decisively

but it seemed to be influenced

_by

leaf

absorption

and

_{leaching occurring}

at _{the canopy level.}

_{Higher aboveground production suggested}

that the stands on

_granite

absorbed

greater

yearly

amounts of N, K and P than those on schist. _{(© Inra/Elsevier, Paris.)}

nutrient use

_efficiency

/

_resorption

/ root

_uptake

/ oak

_coppice

/ _Quercus

_pyrenaica

/

_{biogeochemical cycles}

Résumé - Efficience et

_{réabsorption}

d’éléments nutritifs dans _quatre taillis à

_{Quercus pyrenaica}

suivant un transect

pluvio-métrique

dans la Sierra de Gata (ouest de

_{l’Espagne). L’absorption}

d’éléments nutritifs, la

_{réabsorption}

et l’efficience d’utilisation d’éléments nutritifs _(NUE) ont été étudiés dans quatre chênaies _{(Quercus pyrenaica)} de la Sierra de Gatu

_(province

de

_Salamanque,

ouest de

_{l’Espagne).}

L’efficience d’utilisation de bioéléments (NUE) est

_dépendante

de différents facteurs. Dans les chênaies étu-diées la

_{disponibilité édaphique}

des éléments nutritifs influe sur l’efficience d’utilisation de P, Ca et

_Mg.

Au contraire, il

_n’y

a _{pas de}

relation entre l’efficience de N et K, et la

_{disponibilité édaphique}

de ces _{éléments, peut} être en raison des réserves

_édaphiques

impor-tantes de N total et de l’acidité du sol

_qui

entraîne une _{insuffisance pour Ca.}

_{L’absorption}

et le

_lessivage

_{des feuilles des arbres}

peu-vent aussi influencer l’efficience de N et K. La station avec le sol le

_{plus dystrophe correspond}

_{à la chênaie la moins efficiente pour}

Mg,

tandis que la station la moins

dystrophe

est _{la chênaie la moins efficiente pour le Ca.} En ce

_qui

concerne N, toutes les chênaies

ont une efficience très basse. La

_{réabsorption}

d’éléments

_biogènes

_{n’affecte pas la NUE des taillis} étudiés, parce

qu’elle

est influen-cée par les processus

d’absorption

et le

_lessivage

des bioéléments au niveau de la

_canopée

forestière. Les

_peuplements

sur

_granit

absorbent

_plus

d’N, K et P et

_{produisent plus}

de litière que les

peuplements

sur schistes. _(© Inra/Elsevier, Paris.)

efficience d’utilisation des bioéléments /

_{réabsorption}

/

_absorption

des racines / taillis de chêne /

_{Quercus pyrenaica}

/ cycles de

bioéléments

*

Correspondence

and

_reprints

1.

Introduction

Nutrient use

efficiency

_(NUE)

has been defined

by

Ferrés et al.

_[17]

as the biomass

_{production by}

_plants

_(in

terms of fixed

C)

per unit of nutrient

uptake.

NUE _appears

_mostly

in the literature with reference to

infertile

habitats,

such as marshes

[12],

peatlands

[7],

heathlands

_[2]

or semi-deserts

[33].

The

_efficiency

of

nutrient use

_{by plants}

to

_produce

_{biomass may} be an

important adaptation

to infertile habitats

_[7];

an increase in NUE in a

_{plant species}

should be a _response to the

decreasing

soil nutrient

_{availability,}

but this is not found in

_general

_{[1]. Furthermore,}

it is not clear whether the

greater NUE observed in

_oligotrophic

soils is a

charac-teristic of the

_{species inhabiting}

them or whether it is a

phenotypical

response of individual

specimens

to low nutrient

_availability

_[4].

In short-lived

_plants,

biomass

_production

_{per unit of} absorbed nutrient is

_simply

the inverse of the

concentra-tion of the nutrient in

_question

in the tissues of the

_plant.

However, in

_{long-lived plants}

some bioelements suffer

resorption

(i.e.

reabsorption by

young tissues of nutrients

retranslocated from senescent tissues as mature

_leaves),

which allows the

_plants

to use the same unit of absorbed

nutrient to

_produce

several

_vegetative

_organs

_[38],

increasing

the NUE.

_Resorption

is the

_repeated

use of the

same nutrient units and could therefore be a

_good

means

of

_estimating

the

_efficiency

of nutrient use; nevertheless

resorption

has not been found for all the

bioelements,

but is

_frequent

for N and P.

_Apart

from the

_probable

adap-tive value of efficient

_resorption,

_important

_interspecies

differences in

_resorption

indices have been observed.

Therefore nutrient concentrations

_only

afford a _very

approximate

idea of the

_efficiency

of nutrient use

_by

for-est

_species.

In these cases, it seems more

_appropriate

to

estimate

_{efficiency by measuring}

net

_{primary production}

(aerial

and

_underground)

_{per unit of nutrient}

_uptake

dur-ing

the _year. Under controlled

conditions,

such

measure-ments are

_possible;

_however,

_they

are not _very

_practical

under field conditions

_[4].

As an

_alternative,

Vitousek

_[38]

defined NUE

_(see

equation

later)

as the total amount of

_organic

matter return

(as

litterfall and root

return)

plus

that stored

per-manently

in the

_plant

_(in

the

_wood),

divided

_by

the

amount of nutrients lost

_{(as litterfall,}

_canopy

_leaching

or

by

root

return)

plus

the nutrients

_remaining

stored

_owing

to the

_growth

of the

_{vegetation (uptake according}

to Cole

and Rapp [ 10].

An easier method of

_calculating

the NUE

_{(specifically}

for

_forests)

was

_{proposed by}

Vitousek

_{[38, 39]}

as the inverse of the concentration of the nutrient

_{(that is,}

amount of

_dry

matter in litterfall per unit of the nutrient

contained in

_it).

Later,

Bridgham

et al.

_[7]

used the ratio of ’litterfall

_{production/litterfall}

nutrient’ as an index of

nutrient

_efficiency

(NUE;

production

per unit of resource

uptake), distinguishing

it from the resource _response

efficiency

(RRE),

defined as the

_production

_{per unit of}

available resource. In forests an additional

_problem

is the

exact measurement of the

_availability

of the resource

[24, 25].

Carceller et al.

[8]

reported

that under nutrient stress

conditions

_(either

due to soil

_oligotrophy

and/or to low

water

_{availability, giving}

rise to

_{deficiency symptoms)}

some

_{plants respond}

with increased

_efficiency.

Nevertheless,

parameters of both total and available soil nutrients are sometimes not correlated to

_plant

nutrient

uptake

(in

both fertile and _very unfertile

_soils),

_probably

because _{many factors affect} nutrient

_efficiency

in the

field.

Vitousek

_[38]

has

_pointed

out that the literature

con-tains _many references to litterfall and to the amounts of

N, P, Ca,

Mg

and K returned

_through

litterfall,

but little

information

_concerning

the amount of nutrients stored in wood

_{[14, 31]}

and even less about root return

_{[8, 30].}

Furthermore,

Cole and

_Rapp

[10]

and Gallardo et al.

[20]

have shown that N-, P- and Ca-return to the soil is

most-ly

achieved

_through

litterfall,

while K-return is

_mainly

due to _canopy

_{leaching; Mg}

is intermediate between these two

_{possibilities}

and varies

_according

to the

ecosystem

studied.

_{Consequently,}

it is difficult to

com-pare the results on NUE from different studies because

the data are obtained from different

_{calculations,}

depend-ing

on

_previous

definitions of NUE and the _ecosystems.

Blair

_[5]

affirmed that the definition of NUE

_depends

on

the _ecosystem in

_question

_{(annual, deciduous,}

_evergreen

plants,

etc.).

Aerts

_[3]

stated that

_efficiency

is also related to

nutri-ent

_{resorption by plants; reviewing}

the literature he

found that nutrient

_resorption

is close to 50 % for N and

P in some tree

_species.

Del Arco et al.

_[11]

_reported

that

N

_resorption

is a

_key

_process

_through

which

_plants

reach maximum

_efficiency

in their use of N.

Among

the factors assumed to exert some effect on

the above-mentioned differences in

_resorption

_[16]

are

soil

_fertility,

soil

_dryness

and those

_affecting

leaf

demog-raphy

(leaf

shedding period,

time of residence of nutrient

in

_leaves).

When

_requirements

are _greater than

_uptake,

the

_plant

must meet the rest of its needs for nutrients

_by

retranslocating

them from old _organs to new ones.

Following

this line of

_thought,

Carceller et al.

_[8]

Significant

relationships

between leaf nutrient

con-centration and soil nutrient

_availability

are

_reported

fre-quently,

but Aerts

_[3]

did not find _{any link} between leaf

nutrient

_resorption

and leaf nutrient

_{concentration,}

or soil

nutrient

_availability

and leaf nutrient

_resorption.

Regarding

the effect of soil

_fertility

on

_NUE,

several theories have been

_advanced;

it seems

_logical

that

species

found on the sites most

_impoverished

in soil P or

N would have

_higher

_resorption

indices because

_they

would be

_obliged

to retain these elements and reuse them

as much as

_possible,

thus

_favouring

more efficient

inter-nal

_recycling

_[34]

and

_affording

the

_plants

a certain

inde-pendence

from the

_supply

_coming

from the soil.

Paradoxically,

species living

in

_highly

fertile areas _may

have _very

_high

nutritional

_{requirements, leading}

them to use nutrients more

_efficiently

too

_[36].

However,

in

_general,

the

_majority

of autochthonous

European

forests are restricted to areas with poor soils.

For

_example,

Gallardo et al.

_[18]

have carried out

research on deciduous oak

_(Quercus

_pyrenaica

_Willd.)

coppices developed

on acid soils with low base and

available P contents

_[37].

Other _aspects related with the

biogeochemical cycles

of these forests

_{[23, 26, 27, 37]}

and their water balance

_{[28, 29]}

have also been studied.

It could thus be of interest to know the NUE and

resorption

values in four

well-studied,

oak-forest

ecosys-tems of the Sierra de Gata mountains

_following

a rainfall

gradient

[19]

and to see whether it is

_possible

to find dif-ferences between those values in relation to soil

charac-teristics,

especially

soil

_pH

and biochemical

_properties.

The aim of the _present work was first to estimate the

NUE

_(according

to Vitousek

[38])

and

_resorption

of macronutrients on

_plots

of these deciduous oak

_(Q.

pyre-naica)

coppices

and then to elucidate which factors

gov-ern these _processes,

_taking

into account the soil

avail-ability

of each macronutrient.

2. Materials and methods

2.1. Site

_description

and stand characteristics

The

_study

area is located in the El Rebollar district

(Sierra

de Gata

mountains,

province

of

Salamanca,

west-ern

_Spain).

The co-ordinates of the area are 40° 19’ N

and 6° 43’ W.

Four

_{experimental plots}

of

_{Quercus pyrenaica}

Willd.

coppices

were selected

_{(table I)}

with areas

_ranging

from

0.6 to 1 ha.

_They

were named

_{Fuenteguinaldo}

_(FG),

Villasrubias

_(VR),

El

_Payo

_(EP)

and Navasfrías

_(NF).

Stand ages range from 60 to about 80 _years

_{(table I).}

These

_coppices

were thinned for

_pasturing

_(cattle).

The climate of the area is classified as warm

Mediterranean,

characterised

_by

wet winters and

hot,

dry

summers

_[28],

with an _{average rainfall and}

_temperature

(table

I)

of

_{approximately}

1 580 L

m

-2

_year

_-1

and 10.4 °C for

_NF,

and 720 L

m

-2

_year

_-1

and 12.9 °C for FG.

The dominant soils are humic Cambisols

_developed

over schist and

_greywackes

at NF and VR, and over Ca-alkaline

_granite

at EP and FG

_[26].

The

_physical,

physic-ochemical,

and biochemical

_properties

of the four forest soils are shown in table

_II;

soil

_samples

were taken from the selected modal soil

_profile

at each

_plot

[37].

Tree

_density

_{(table I)}

_ranges between 1 043 trees

ha

-1

at the VR

_plot

and 406 trees

ha

-1

at the EP

_plot

_{[22, 28].}

The

_plot

with the lowest tree

_density

_(EP)

has the

_highest

mean trunk diameter

_{(25 cm),}

the _greatest

_height

(17 m)

and biomass

(131

Mg

ha

-1

);

the lowest values of these

parameters

correspond

to the VR

_plot

_{(11 cm,}

8.5 m and

63.8

_Mg

_ha

_-1

_,

_{respectively).}

_{Aboveground production}

ranged

from 4.1 to 2.6

_Mg

ha

-1

_year

_-1

in FG and

_NF,

respectively

[20].

Methodological

aspects

and data of soil

_analysis,

aboveground

biomass,

litterfall

_production

_(from

February

1990 to

_February

1993),

foliar

_analysis,

rainfall

distribution,

throughfall,

water concentrations of bioele-ments, canopy N

absorption,

annual

potential

return of bioelements

_(total

nutrients returned to the soil

_through

the

litterfall,

assuming complete

mineralization),

etc., have been

_given

_by

_Gallego

et al.

_{[22, 23],}

Martin et al.

[26],

Moreno et al.

_{[28, 29]}

and Gallardo et al.

_{[19, 20].}

Owing

to

_{methodological}

difficulties,

no data on root

biomass and below

_{ground production}

of oak

_coppices

have been obtained. Annual nutrient immobilisation in wood has also been estimated

_[18].

_Exchangeable

cations were determined

_following

the neutral

ammoni-um-acetate method

[26];

available Ca and K

_using

1 N

ammonium acetate as

_extracting

solution

_[37];

and avail-able P

_using

to the

_Bray-Kurtz

_[6]

_procedure.

Some of the

_important

soil characteristics of the

stands are shown in table II.

2.2. Methods

Each

_plot

was divided into three

_parts,

and in each of the three

_subplots

the same

_experiments

were

_performed.

As a

_result,

data refer in

_general

to a mean of three

repli-cates. Standard deviations were

_only

calculated where

2.2.1. Estimation

_{of tree uptake}

_(TU)

An estimation of the

annual,

soil nutrient

_{uptake by}

plants

was made. The tree nutrient

_uptake

from the soil

was calculated

_according

to the

_{following equation}

_(units

in

_kg

ha

-1

_year

_-1

_):

where TU is tree

_uptake

of the nutrient

considered; LF,

litterfall; SG,

stem

_growth;

and

_TF,

_throughfall

_(nutrients

retained in small branches and bark are difficult to

deter-mine).

2.2.2. Calculation

_{of efficiency}

indices

Two

_efficiency

indices,

involving

different

factors,

were determined.

The first was defined

_by

Vitousek

[38]

as

_dry

matter

of litterfall per unit of nutrient content in

litterfall;

this

index is

_frequently

used for N and P

(we

also use it for

K,

for

_{comparative purposes)}

and is shown in table III as

NEI

(nutrient

efficiency

index).

The second index

determined,

GEI

_(general

_efficiency

index),

contains all the terms

_{given by}

Vitousek

[38]

except the contribution from roots

_(not

determined in this

_study)

and can therefore be defined

_by

the

_following

formula:

where LF is litterfall

(referred

to as

_{kg dry}

matter

_ha

_-1

_);

SG,

stem

_{growth (referred}

to as

_{kg dry}

matter

_ha

_-1

_);

_NR,

nutrient returned

_by

litterfall

(in

kg

ha

-1

);

NI, nutrient immobilised

_by

stems

_(in

_kg

ha

-1

);

and TF,

_throughfall

of the nutrient considered

_{(in kg}

ha

-1

).

The amount of nutrients absorbed

_by

the leaves at the canopy level

[29]

is subtracted since these nutrients are

of external

_origin

and are not absorbed

_{directly by}

the

roots.

2.2.3. Estimation

_{of the resorption}

index

_(Re)

Taking

into account the theoretical considerations

expressed

above,

and in an _attempt to overcome the

drawbacks involved in the calculation of

_resorption,

the

resorption

index

_(Re)

was estimated

_using

the

_following

expression

(units

in

_kg

_ha

_-1

_):

where MM is leaf mineral mass

_(sum

of the masses of the nutrient

_considered)

calculated

_{by harvesting}

trees of

different diameter

classes;

NR is nutrient return

_by

leaf

litter;

and CL is nutrient canopy

leaching

(sensu

stricto).

In this estimation

_only

the soil losses

_brought

about

_by

root

_absorption

_(without

_considering

the increase in root

biomass)

and the soil

_{gains through}

leaf litter and

throughfall

are considered

[19]. Thus,

the nutrient

leach-ing

has also been taken into account in this

_resorption

The

_greatest

_problem

involved in

_calculating

the

resorption

index for N is the leaf

_absorption

of N at the

canopy level

[29].

Escudero et al.

[16]

have shown that the maximum N contents of leaves of

_Q.

_pyrenaica

are

reached

_only

2 bor 3 months after

_sprouting,

the stabili-sation

_phase

_being

_prolonged

until leaf fall

[23].

Since it is not

_possible

to know the exact moment at which leaf

N

_absorption

at _{the canopy level takes}

_place,

it has been

assumed that leaf

_absorption

of N would occur

_during

the initial

_stages

of leaf

_growth

and

_development

_owing

to the _greater demand for N

_during

this _stage

_(afterwards

rainfall decreases

_[28]).

Accordingly,

it is assumed that the amount of leaf

absorbed N would

_already

be included in the

mineral-mass value

_(values

estimated

_during

the

_phase

when

con-centrations become stabilised

_{[23]). Thus,}

to estimate the

resorption

of N

_(ReN),

the

_{following expression}

is used

in this case:

where NR TU, and MM are as above.

3. Results and

discussion

The results are

_given

in table III.

3.1. Leaf and leaf-litter

_composition

Table III

_gives

the mean nutrient

_composition

of tree

lower values of N and P concentrations in leaves than

those found in the schist

_plots

(NF

and

VR);

knowing

that leaf and litter

_{production (table}

_I)

are

_higher

in the

first two

_plots

than in the latter two

stands,

these lower N

and P concentrations _may reflect a dilution effect

_[19].

The _poorest soil

(VR)

had the

_highest

values of

_Mg

and K concentrations and the lowest of

Ca,

demonstrating

a

nutrient imbalance

[27].

Theoretically,

the Ca and

_Mg

_composition

of leaf

lit-ter is increased

_compared

to leaf contents because of the loss of

_organic

C

_during

the

_{decomposition}

_process; but

for elements

_{undergoing leaching}

_(K)

or

_resorption

_(N

and

_P),

the nutrient concentration is lower in the

leaf-lit-ter than in the tree leaf

_{[27]. Thus,}

_Gallego

et al.

_[23]

stated that the chemical

_composition

of the tree leaf

changes during

the _year in these

_coppices.

3.2. Tree nutrient

_uptake

_(TU)

Root nutrient

_uptake

is shown in table III.

The sum of return

_(LF

+

_TF)

was

_previously

deter-mined

_by

Gallardo et al.

_[19]

and the annual retention in

the trunk and branch biomass

_{by Gallego}

et al.

_[23].

Net

foliar

_absorption

of N from

_atmospheric

contributions

[19, 29]

was estimated to be

5.4,

6.6,

10.2 and 5.4

_kg

ha

-1

_year

_-1

at NF, EP,

VR and

_FG,

_{respectively;}

note the

high

leaf

_absorption

of the stand

(VR)

with more

dys-trophic

soil. 3.2.1.

_Nitrogen

The total tree N

_uptake

_(root

_{uptake plus}

leaf

absorp-tion)

was

51, 59, 42

and 78

_kg

ha

-1

_year

_-1

at

NF, EP,

VR and

_FG,

_{respectively.}

The stands

_developed

on

_granite

(FG

and

EP)

take _up more total N

_(they

also have a

high-er N root

_uptake;

table

_III)

and the

_highest

_aboveground

production

(table I).

The

_supply

of N

_throughout

the mineralisation of abundant soil humus does not seem to

be limited

_[27]

_except

_by

summer soil

_dryness

_[37].

3.2.2.

_Phosphorus

The stands

_developed

on

_granite

_(FG

and

_EP)

also take _up more P

_{(table III)}

than those on schist

_(NF

and

VR).

They require

more available soil P to maintain the

higher

aboveground production

(table

I).

In this case,

soil P is not a

_limiting

factor

_[37].

3.2.3. Calcium

The _greater amount of soil Ca at FG

_(table

_II)

leads to a much

_higher

root

_uptake

₍₁₃₉

_kg

ha

-1

_year

_-1

₎

than that observed in the other

_plots.

3.2.4.

_Magnesium

The

_plots

at VR and FG

_displayed

the most intense

Mg

uptake

(table III).

This

_{higher Mg}

root

_uptake

in VR

is

_possibly

due to

_Ca/Mg

nutritional imbalance

_[27].

In any case,

Mg

reserves in soil should contribute to tree

nutrition

[29].

3.2.5. Potassium

FG also has the

_highest

K root

_uptake

_{(table III).}

Owing

to the

_solubility

and ease of K

_leaching

_[29],

a

high

quantity

of K must be

_{supplied by}

the soil K

_pool.

3.3.

_Resorption

It is assumed that the leaves shed before the normal

period

of abscission have not

_{undergone resorption}

of

nutrients,

according

to Carceller et al.

_[8];

this

assump-tion is difficult to _accept if severe defoliation has

occurred

_(e.g.

EP).

As a

_result,

the inclusion of

_damaged

leaves in the calculation would lead to an

underestima-tion of the

_resorption

index. 3.3.1. N

_resorption

The absolute values of N

_resorption

_(table

_III)

are

similar for all the _{stands, except} NF

_(the

stand with the

highest

rainfall;

table

_I),

where the N

_resorption

is much

higher

than for other stands. Since the

_lengths

of the

abscission

_periods

are _very similar because all the

_plots

contain the same

_species

and are

_subject

to almost identi-cal climatic conditions

_(except

_rainfall),

the calculated

values of the

_resorption

index were similar

_(except

for

NF with

_highest

_{precipitation, implying}

a

_higher

leaf N

leaching

and more

_resorption).

There seems to be no

relation between

_resorption

indices and soil characteris-tics.

The relative values of the three drier stands

_{(EP, VR,}

FG)

are lower than those

_{reported by}

Escudero et al.

_[16]

for

_{Q. pyrenaica}

_{(46 %)}

and for most deciduous

_species

(values

between 69 % for Betula

_pubescens

and 37 % for

Crataegus

monogyna);

the value of NF is also lower than those

_{reported by}

Carceller et al.

_[8]

for

_Fagus

syl-vatica

₍₆₃

_%)

and

_by

_Chapin

and Moilanen

[9]

for B.

papyrifera

(between

58 and 65

_%).

Our results can be

those

_appearing

in the

literature;

this could be a

conse-quence of the different methods used to calculate the indices

considered,

but the same trend is observed when

our results are

_compared

with those of Carceller et al.

[8],

who used identical calculations. This could indicate

that there is not a severe limitation of N in the

_coppices

studied. The low N

_{resorption might}

also be due to leaf

absorption

of N

_by

the _canopy

_[29]

and it can be

assumed that the energy cost for the tree is lower than for

_{high resorption.}

One can

_speculate

about the idea that

the

_{species only}

_display

_resorption

when

_they

are able to

derive additional benefits from the use of their

_strategy

and do not become involved in excessive costs (as, for

example,

when nutrients stored in old leaves can be used

more

_efficiently

in other _parts of the

_plant).

In view of

the low

_production

of fruits

_[20],

this does not seem to

occur in the forests studied.

3.3.2. P

_resorption

Concerning

the relative values of P

_resorption

(table

III),

stands on schist

_(NF

and

_VR)

with low available P-reserves show values around 50 % and those

_developed

on

_granitic

substrates

(FG

and

_EP)

with

_higher

available

P-reserves have values close to 20 %. Turrión et al.

_[37]

also observed differences in available P

_depending

on

the nature of the _parent material. However, within each

group, the differences between P

resorption

values are

minimal in

_spite

of the fact that there is four times as

much available soil P at FG than at EP

_(table

_II).

The

usual clear

_relationship

between available soil P

_(in

Ah

horizon)

and P

_resorption

does not exist _any more when

threshold values of soil

_availability

or

_plant

_organs are

exceeded; therefore,

the nature of the

_underlying

sub-strate does seem to have some effect on the P

_resorption.

Furthermore,

it is _necessary to take the

_general

abun-dance of micorrhizal

_fungi

into account

_(Schneider,

_pers.

comm.)

in these oak

_coppices.

The levels of P

_resorption

_vary

_{considerably, being}

greater overall in deciduous

_species

_[35]

than in

ever-green

species.

For a

_{single species,}

in most cases these levels remain almost constant,

regardless

of the different

habitats

_occupied.

The P

_resorption

values recorded are

similar to those

_{reported by}

Sanz

_[32]

for

_Q.

_pyrenaica

(between

33 and 65

_%),

for Betula

_pubescens

_{(76 %)}

and Fraxinus

_angustifolia

_{(27 %);}

_by

Carceller et al.

_[8])

for

Fagus

sylvatica

(50 %);

and

_{by Chapin,}

Moilanen

[9]

for

B.

_papyrifera

_(between

27 and 45

%).

Stands with

_high

N

_{resorption efficiency}

also showed

greater

efficiency

in P

_resorption

_{(table III).}

Sanz

_[32]

reported

a

_{significant relationship}

between both indices

for different deciduous

_species

and she found the

follow-ing expression:

ReP = 5.49 ₊ 0.98 _x ReN r = 0.70 (P <

_0.01)

where ReP and ReN are the

_resorption

indices of P and

N,

respectively.

The

_slope

of the

_straight

line is almost

equal

to

_{unity, demonstrating}

the

_{proportionality}

between both variables.

Obviously, availability

of N and P are

_dependent

on

the mineralisation rate of soil

_organic

matter

(and

mycor-rhizal

_{fungi; Duchaufour}

_[13]);

but

_using

the

decomposi-tion constants obtained

_by

Martin et al.

_[27]

a

non-signif-icant

_relationship

was obtained between these constants

and the

_resorption

indices. 3.3.3. K

_resorption

The

_highest

K

_resorption

is obtained at VR

(table III),

which is

_precisely

the

_plot

with the lowest soil available

K concentration.

_However,

this factor does not seem to

affect the

_resorption

of this element to _{any considerable}

extent, because the other

_plot

_developed

over schist

_(NF)

has a lower content of soil available K than EP

(table II)

and,

in contrast, it has the lowest

resorption.

Therefore,

the differences between

_plots

are masked

_by

the

partici-pation

of two factors

_(leaf

litter return and

_throughfall)

of similar

_importance.

The relative K

_resorption

indices

_{(table III)}

are much lower than the 59 % obtained

_by

Carceller et al.

_[8]

for

Fagus

sylvatica

forests;

it should be stressed that these

authors did not consider

_throughfall,

_{which is very}

important

[29].

It is therefore difficult to establish a

com-parison

between these values.

3.4.

_Efficiency

indices 3.4.1.

_Nitrogen

Based on the

_efficiency

indices

described,

the stands

at

_EP,

NF and FG used N in the least efficient _way

_(table

III),

VR

_being

the most efficient one.

Calculated NEI values

(between

71 and

98)

were

lower than those determined

_by

Ferrés et al.

_[17]

for

Quercus

ilex

_(152),

Abies _sp.

₍₁₅₇₎

and

_Fagus

_sylvatica

(179),

and

_by

Nú&ntilde;ez et al.

_[30]

for Cistus

_laudaniferus

(225),

but similar to those determined

_by

Carceller et al.

[8]

for F.

_sylvatica

₍₉₉₎

and those

_{reported by}

Vitousek

[38]

for _temperate deciduous forests

_(ranging

from 30 to

92).

In the case of

N,

Birk and Vitousek

_[4]

found that

efficiency

decreased with the increase in available N.

Likewise,

Ferrés et al.

_[17]

attributed _greater

_efficiency

to reduced N

_availability

in the

soil,

caused

_{by delayed}

drought

in Mediterranean areas. In our

_work,

the soils

(EP

and

_NF)

with the

_highest

_percentage

of total N

_(table

II)

appear to make less efficient use of this nutrient. Turrión et al.

_[37]

found that,

_{theoretically,}

soil N is not a

_limiting

_factor,

because of the

_high

amount of total soil

N and the

_{relatively high decomposition}

rate of soil

organic

matter

_[27],

but

_they

also

_pointed

out that

sum-mer

_drought

can

_hamper

the nitrification and nitrate

transport towards the roots

[37].

Accordingly,

the

mod-erate or even low

_efficiency

values of N in the forests

studied can be said to

_correspond

to moderate or

_high

total soil N

levels,

respectively.

It could be

_expected

that the leaf N

_resorption

does

not affect the

_efficiency

of the overall use of this nutrient

decisively,

because leaf N

_leaching

and

_drought

also

have an influence on N

_efficiency.

In summary, there are favourable conditions for the

loss of N in these forests

(litterfall

coincides with the

period

of maximum

rainfall,

as

_pointed

out

_by

Moreno et

al.

_[29],

a

_rapid

colonisation of floor litter

_by

micro-organisms

that slow down the release of N

_[27]

and leaf

absorption

of this nutrient

_by

_{the canopy}

_[29];

these

fac-tors lead to a low

_efficiency

of this element.

3.4.2.

_Phosphorus

P was used more

_efficiently

in oak

_coppices

located

on schist

_(NF

and

_VR)

than in those

_developed

on

gran-ites

(table

III). Turrión et al.

[37]

found more available P in soils on

_granite

(FG

and

_EP)

than in soils on schist.

The

_efficiency

indices at VR and NF are _very

_similar;

in

fact there are no differences in available soil P contents

in these two oak

_coppices

_{(table II),}

in contrast to the

values found in the other two stands.

FG had the lowest

_efficiency

index,

corresponding

to

a

_higher

content of available P in the

_epipedon

_{(table II).}

The calculated

_efficiency

indices are lower than those

reported by

Ferrés et al.

_[17]

_{for Fagus}

_sylvatica

_{(2 416)}

but similar to those estimated

_by

the same authors for

Abies _sp.

_{(1 518)}

or

_Quercus

ilex

_{(1 246),}

and similar to

the values

_{reported by}

Carceller et al.

_[8]

for F.

_sylvatica

(1 438)

and those found

_by

Vitousek

_[38]

for

_temperate

deciduous forests or Mediterranean ecosystems.

However,

if

_only

the NEI is considered, the FG

_plot

(which

has a

_high

content of soil available

P;

table

II)

would be less efficient in the utilization of P than the other oak stands

and,

also, less efficient than a

_jaral

(Cistus

laudaniferus)

ecosystem of western

_Spain

_[30].

3.4.3. Calcium

The

_highest

NEI for Ca occurs in the stand with the

lowest concentration of

_{soil-exchangeable}

Ca

2+

and a

relatively

acid soil

(VR;

table III), while the FG stand

has the lowest indices

_(NEI

and

GEI)

and a

_higher

con-tent of both

_exchangeable

and available Ca

_(higher

_pH

of

the

_epipedon)

in the soil.

For this

nutrient,

GEI seems to be more related to the soil

_exchangeable

Ca than to available Ca

_{(Ah horizon).}

The

_efficiency

of Ca for the four oak stands studied here lies within the values

_{given by}

Vitousek

_[38]

for

temperate deciduous forests and is

_slightly

_higher

than those

_{given by}

Ferrés et al.

_[17]

for

_{F. sylvatica}

(113)

or

Q. ilex (111).

Because no

_{deep drainage}

was observed at FG

[28]

there is no loss of bases from the soil

_profile

and this

explains

the much

_higher

_pH

and base saturation values of the

_superficial

horizon

_(Ah),

_compared

the other sites

(table

II; [20, 26])

with the

_highest

_aboveground

produc-tivity

(table I).

3.4.4.

Magnesium

In the case of this

_element,

_only

the GEI was

estimat-ed since the return of this nutrient to the soil is

_governed

to a

_large

extent

_by

_throughfall

_[29].

_Application

of this index shows that in the

_plots

studied the order of

effi-ciency

for

_Mg

is

_directly

the

_opposite

to that observed for Ca

_{(table III);}

i.e. VR would be the least efficient

plot

for

_Mg

utilization,

_perhaps

because of a

_possible

nutrient imbalance between Ca and

_Mg

[26];

i.e. an

increase in

_{Mg uptake}

in Ca-deficient forest soils. The

lowest leaf

_Ca/Mg

ratio occurs in VR

_(2.3)

and this ratio is close to 4 in NF and FG. FG showed the

_highest

_Mg

efficiency

and litter

_production

_{(table I).}

3.4.5. Potassium

The

_plot

at NF had the

_highest

GEI for K

_{(table III);}

there is

_obviously

an inverse

_relationship

between this index and leaf

_leaching

(the

quantitative importance

of

throughfall

differs

_considerably

_{among the} stands

_{[ 19].}

The

_plot

at VR has the

_highest

NEI and the lowest K

leaching;

this index has a limited value in the other

_plots

in this case

_owing

to the intense K

_leaching

_(high

solu-bility

of

K).

4.

Conclusions

As a result of the _present

findings,

we can conclude

that: stands

_developed

on

_{granite annually}

absorbed

greater amounts of

N,

K and P

_annually

than stands

developed

on

_schist,

related to their

_{higher aboveground}

Bioelement

resorption

does not affect the NUE of these oak

_{coppices decisively,}

but is influenced

_by

processes of leaf

absorption

and

_leaching

_occurring

in the canopy.

Rainfall

differences between sites do not seem to

influence

the NUE nor the

_resorption

of the stands

(except

N

_resorption

in

_NF).

_Obviously

other factors

(besides

pluviometry)

also influence the

NUE,

as

deduced from

_the

definition of GEI.

In the oak

stands studied,

the soil nutrient

_availability

governs

efficiency

in the case of P and

Ca,

but not in the

case of N and K.

_Concerning

N this occurred

_possibly

because the nitrate

_supply

was limited

_{by drought.}

Leaf

absorption

and/or

_leaching

at _{the canopy level would}

also influence the N and K

_efficiency.

_{Nevertheless,}

all

the oak

_coppices

showed low N

_{efficiency, indicating}

that there was no severe N

_deficiency.

FG

_(with

the

_highest

litter

_production

and the least

dys-trophic

soil)

is the least efficient

_coppice

_regarding

Ca.

Acknowledgements:

The

_present

work was

_possible

thanks to

_support

from the ’Junta de Castilla _y León’ and finances from the MEDCOP/AIR

_Project

_(General

Division

XII,

E.

_U.)

and the

_Spanish

C.I.C.Y.T. Funds. The

_English

version was revised

_by

N. Skinner and the final version

by

G. Aussenac.

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