Blanco et al.

(2009) 1/45

Post-print of Ecological Applications 19(3) 2009, pp. 682-698.

DOI: DOI:10.1890/1051-0761-19.3.682

Running head: Thinning and resorption in Pinus sylvestris

Thinning affects Nutrient Resorption and Nutrient Use Efficiency in Two Pinus sylvestris

stands in the Pyrenees

JUAN A. BLANCO1, J. BOSCO IMBERT2 and FEDERICO J. CASTILLO 3

1
juan.blanco@ubc.ca

Dpto. Ciencias del Medio Natural, Universidad Pública de Navarra, Campus de Arrosadía s/n, Pamplona, 31006

Navarra, Spain.

Present address: Department of Forest Sciences, Forest Sciences Centre, The University of British Columbia, 3041-

2424 Main Mall, Vancouver, British Columbia , V6T 1Z4, Canada.

2
bosco.imbert@unavarra.es

Dpto. Ciencias del Medio Natural, Universidad Pública de Navarra, Campus de Arrosadía s/n, Pamplona, 31006

Navarra, Spain.

3
federico.castillo@unavarra.es

Author to whom correspondence should be addressed Dpto. Ciencias del Medio Natural, Universidad Pública de

Navarra, Campus de Arrosadía s/n, Pamplona, 31006 Navarra, Spain.

Tel. (34) 948 169 115

Fax (34) 948 168 930

 Blanco et al. 2007 2 / 45

Abstract

Needle chemical composition was measured and nutrient resorption, nutrient use efficiency

(NUE) and other indexes were estimated for 24 months in two contrasting natural Pinus sylvestris

L. forests in the western Pyrenees. For each location (Aspurz: 650 m elevation, 7% slope; Garde:

1335 m elevation, 40% slope), there were three reference plots (P0), three with 20 % of the basal

area removed (P20) and three with 30 % of the basal area removed (P30). Needle P, Ca and Mg

concentrations were higher in Garde but N concentration was higher for Aspurz, without

differences for K. Nutrient resorption efficiency of P was higher in Aspurz, of Mg higher in

Garde and there were no differences between sites in N and K. Nutrient resorption proficiency

was significantly higher in the site with lower soil nutrient availability, i.e., for P, Ca and Mg in

Aspurz but N in Garde (no differences in K); this may be an indicator of nutrient conservation

strategy. Annual nutrient productivity (A) was higher in all nutrients in Aspurz, whereas the

mean residence time (MRT) was higher in Garde in all nutrients but P. NUE was significantly

higher in Garde for all nutrients but P, which was more efficiently used in Aspurz. In both sites,

N, P and K concentrations were higher in 2002 cohort, Ca in 2000 cohort and maximum Mg was

found 2001 cohort. Thinning caused a reduction of Mg concentration in the 2001 cohort in

Aspurz, an increase of Ca resorption proficiency in Aspurz and Mg resorption at both sites, and

reduction of P, K and Mg nutrient response efficiency (NRE) in Garde. Thinning may have

caused an increase of the C:Mg ratio through facilitating the development of more biosynthesis

apparatus in a more illuminated canopy, but it seemed not to affect resorption in a significant

way. Changes in NRE in Garde after thinning show that forest management can affect how trees

use nutrients. Our results indicate that the strategy to optimize NUE is different in each stand. In

Aspurz (a Mediterranean ecosystem), pine trees carried out resorption more efficiently, while in

Blanco et al 2007 - 2 / 45 -
Blanco et al. (2009) 3/45

Garde (a continental forest), trees opted to use nutrients for longer periods of time, and reduced

their efficiency in using the available soil nutrients after reduced competition by thinning.

Key words: Mediterranean pine forest, nutrient cycling, nutrient uptake efficiency, nutrient use

efficiency, nutrient response efficiency, resorption efficiency, resorption proficiency, thinning,

forest management.

Introduction

Nutrient concentration in the leaves of plants results from a balance between nutrient uptake from

soil, reserve organs or atmospheric depositions, and outputs through resorption and leaching,

being the relative importance of these processes site-specific. At the ecosystem level, resorption

has an important influence on nutrient cycling, because it reduces tree dependence on nutrient

uptake from the soil and makes nutrients directly available for trees. By contrast, nutrients in

litterfall can be used by other organisms and even be immobilized in soil for long periods of time

before trees can use them again (Aerts and Chapin 2000). Plant adaptation to different levels of

nutrient availability is usually evaluated by taking nutrient use efficiency into consideration; this

is generally defined as the relationship between litterfall biomass and litterfall nutrient

concentration (Birk and Vitousek 1986). Other useful indexes to understand efficiency in the use

of resources are nutrient uptake efficiency (the ratio between the amount of nutrients in litterfall

and the amount of nutrients available in soil) and nutrient response efficiency (the ratio between

the amount of nutrients used for leaf or needle production and the amount of nutrients available

in soil) (Bridgham et al. 1995). There are clear differences in resorption capacity between tree

types (evergreen or deciduous) but it is still not clear which factors control resorption capacity.
 Blanco et al. 2007 4 / 45

Some authors have found that plants growing in nutrient-poor environments are more efficient

(Chapin 1980, Eckstein et al 1999), while others believe that resorption is independent of soil

fertility (Chapin and Kedrowski 1983, Birk and Vitousek 1986, Del Arco et al. 1991, Lal et al.

2001).

In addition to factors related to nutrient availability, other types of resorption controls have been

proposed, e.g., the capacity of plant organs to be a nutrient sink (Nambiar and Fife 1991), the

transport rate along phloem and xylem (Chapin and Molainen 1991), soil moisture (Del Arco et

al. 1991, Escudero et al. 1992, Pugnaire and Chapin 1993), or leaf longevity (Escudero et al.

1992). However, as it has been emphasized by Nambiar and Fife (1991), there is no single simple

explanation for variability in resorption efficiency. Resorption rates show changes in time due to

a number of factors, such as water availability (Escudero et al. 1992), abscission time (Del Arco

et al. 1991) or shade (Chapin and Molainen 1991). Therefore, at any particular point in time, the

measured resorption is not necessarily the potential resorption (the maximum nutrient withdrawal

that a tree species is able to carry out). Therefore, when comparing species or locations it is very

difficult to know if the maximum resorption or spatio-temporal variations in measured resorption

are being compared. In an attempt to solve these problems, Killingbeck (1996) developed a new

concept in nutrient resorption: resorption proficiency, defined as the minimum concentration

level to which a plant species is able to reduce a nutrient concentration before leaf fall. As a

consequence, resorption proficiency may be more informative when studying how individuals,

populations and communities can retain their leaf nutrients. Nevertheless, it is useful to analyze

nutrient use efficiency and resorption proficiency together because each variable provides a

different view of the same physiological process.

Blanco et al 2007 - 4 / 45 -
Blanco et al. (2009) 5/45

It is possible that not only natural factors are able to influence resorption capacity in plants, and

that human actions cause changes in this process as well. Although resorption has been studied in

a number of different types of forests (Aerts and Chapin 2000), studies dealing with the effects of

silvicultural practices on resorption are scarce. Furthermore, it seems that there are no general

trends in the results obtained so far. Understanding and estimating nutrient resorption can help to

plan more efficient forest management operations that directly affect nutrient availability, such as

fertilization, slash burning or thinning. With thinning of tree stands, reduction in stem density

could theoretically reduce nutrient competition and consequently increase nutrient availability.

However, although analyzing changes in this key process of nutrient cycling may be an important

issue when researching the effect of forest management on ecosystem function, the few published

studies about this subject do not provide conclusive results (Carlyle 1998, Herbohn and Congdon

1998, Piatek and Allen 2000). The use of a number of indexes of nutrient use efficiency can

provide insights into how forestry practices can affect tree growth by increasing or decreasing

tree efficiency and therefore nutrient requirements, and this also has important implications for

achieving effective forest management. In this work, we tested the following hypotheses: (1)

Thinning will reduce total nutrient uptake from soil and therefore soil nutrient availability for

remaining trees will increase, producing increases in nutrient concentrations in green needles. (2)

Trees will respond to this change by reducing nutrient use efficiency, nutrient uptake efficiency

and nutrient response efficiency.

Materials and methods

 Blanco et al. 2007 6 / 45

Study sites

Our experimental sites, Garde and Aspurz, are located in the western Pyrenees, in the province of

Navarre (northern Spain). The study site in Garde represents an example of medium-productive

Pinus sylvestris L. forests in Spain (Puertas 2001, Iriarte and Puertas 2003). The study location in

Aspurz is one of the most productive P. sylvestris forests in Spain (Puertas 2001, Iriarte and

Puertas 2003). Site characteristics are described in Table 1, and the most important soil properties

are shown in Table 2.

Experimental design

The Forest Service of the Government of Navarre set up nine experimental rectangular plots (30

m x 40 m) per location, following a complete randomized block design according to the

guidelines of the International Union of Forestry Research Organizations (IUFRO) (Andrew,

1986). To avoid edge effects, the silvicultural treatment corresponding to each plot was also

applied within a strip of 5–10 m adjacent to the plot. Thinning was carried out in August and

November 1999 in Garde and Aspurz, respectively. Three treatments with three replicates (one of

each treatment per block assigned at random) were established for each location (1) P0: reference

with no thinning; (2) P20: moderate thinning from below (20% of basal area removed) with

selection of crop trees, removing most of suppressed trees and some dominant or codominant

trees with malformed stems; (3) P30: heavy thinning from below (30% of basal area removed)

with selection of crop trees, removing all suppressed and some intermediate trees, as well as

some dominant or codominant trees with malformed stems. Logs and most branches from the

felled trees were left outside plot limits. Deciduous trees other than European beech (Fagus

sylvatica L.) were removed when necessary to facilitate thinning operations.

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Blanco et al. (2009) 7/45

Green needles collection and analysis

Green needles were collected every two months from December 2001 to October 2003. To

collect needles, three trees per plot were randomly selected and one green branch per tree was

cut. In Garde, green branches were cut between 3 and 5 m high and in Aspurz between 7 and 9 m.

Green needles collected from each branch were separated according to their age and were pooled

in the laboratory by plot and age. Dry, senesced needles were collected monthly over a two-year

period (October 2001 to October 2003) using the litter-trap technique described in Blanco et al.

(2005, 2006 a,b). Both green and senesced needles were dried at 70º C for about 72 hours, until

constant weight was reached, and then ground with an electric mill (Frisch, Pulverisette 14, Idar-

Oberstein, Germany). From each sample, 4.5 g were taken to analyze N, P, K, Ca and Mg. The

following methods were used to analyze the nutrients: N, using the Kjeldhal method (Harwitte

1980); P by spectrophotometry using the phosphomolibdo-vanadate method (Zasoski and Burau

1977, MAFF 1986), with a spectrophotometer UVICOM (Kontron Instruments) at 340 nm; Ca

and Mg by atomic absorption spectrophotometry (VARIAN, model SpectrAA-250 PLUS, SPS5);

and K by flame photometry.

Statistical analysis

Repeated measures analyses of variance (ANOVA) by cohort were used to analyze effect of site

(random effect), thinning intensity (fixed effect) and block on nutrient concentration in green

needles. Evaluation of residual plots and the Shapiro-Wilk test indicated the need to ln(x)

transform data to achieve an approximate homogeneity of variances and normal distribution.

When any of the interactions of thinning intensity by site were significant, ANOVAs were carried

out separately by site. Linear contrasts were used to compare among different treatments when

thinning intensity had a significant effect on nutrient concentration. Nutrient resorption efficiency
 Blanco et al. 2007 8 / 45

was calculated at stand-level to avoid underestimation, following Aerts (1996) as (N-L)/N where

N is the average percentage of nutrient concentration in each set of green needles collected in

each sampling time before abscission and L is the average percentage of nutrients concentration

in abscised needles collected from litter traps at the same time. Dry needle mean nutrient

concentration was also used to calculate resorption proficiency (Killingbeck 1996). Needle level

nutrient use efficiency (NUE) was calculated as

aboveground biomass ( g ha 1 )
NUE 
nutrient content in aboveground biomass ( g ha 1 ) (Chapin 1980)

To include a temporal dimension, we decomposed NUE in annual nutrient productivity (A) and

mean residence time (MRT), being NUE = A x MRT, as in Escarré et al. (1999).

aboveground biomass produced every year ( g ha 1 y 1 )

A
aboveground nutrient mass ( g ha 1 )

aboveground nutrient mass ( g ha 1 )

MRT 
aboveground nutrient mass produced every year ( g ha 1 y 1 )

Two-way ANOVAs (site and thinning intensity) were used to analyze these data. We also

determined nutrient-response, nutrient-use and nutrient-uptake efficiencies following Bridgham

et al. (1995). Nutrient-response efficiency (NRE) was defined as leaf production per unit of

available nutrient in soil; NUE as leaf production per unit of acquired nutrient, and nutrient-

uptake efficiency (NUpE) as acquired nutrient by trees (calculated as the nutrients required to

support estimated annual aboveground biomass production) per unit of available nutrient in soil

(estimated as soil nutrient pools, Table 2). NRE is consequently NUE times NUpE. We used the

Blanco et al 2007 - 8 / 45 -
Blanco et al. (2009) 9/45

methods reported in Blanco (2004) and Blanco et al. (2005, 2006 a,b) to calculate nutrient pools

in litterfall and soil and annual production.

Results

Nutrient concentrations in green needles

Nutrient status was different depending on the site and needle cohort. Differences between sites

followed the same pattern in the four cohorts, with the highest N concentrations in Aspurz, but P,

Ca and Mg highest in Garde and no differences between sites in K for P, Ca and Mg (Table 3).

Maximum nitrogen concentration was reached in the 2001 cohort in Aspurz and in the 2002

cohort in Garde. In general, Garde N and P concentrations showed similar temporal dynamics,

and oscillations were smaller (Figures 1 and 2). Potassium showed a decrease in nutrient

concentration at both sites in spring (Figure 3). Calcium concentration increased with needle age,

with maximum concentrations in the 1999 cohort at both sites (Figure 4), but P and K showed the

highest concentrations in the 2002 cohort in both Aspurz and Garde, with no clear changes with

needle age for N (Figures 1, 2 and 3). Finally, no clear seasonality in Mg concentration was

found (Figure 5).

A significant effect of thinning was only found in Mg in Aspurz in the 2001 cohort: the average

Mg concentration in P30 (0.72 ± 0.02 mg-1 g) was lower than in P0 (0.92 ± 0.02 mg-1 g,

F1,5=7.71, P=0.04), but no different from P20 (0.86 ± 0.03 mg-1 g, F1,9=4.23, P=0.10). In 2001

cohort in Aspurz, concentrations of P appeared higher in P20 (0.99 ± 0.02 mg-1 g) than in P30
 Blanco et al. 2007 10 / 45

(0.87± 0.02 mg-1 g), but these differences were not significant (F1,5=5.83, P=0.07), and there

were no differences between control and thinned plots (F1,5=9.01, P=0.39).

Resorption efficiency and indexes of nutrient use efficiency

No differences between sites were found for N, K and Ca resorption efficiencies but for P

resorption efficiency was higher in Aspurz and for Mg it was higher in Garde (Table 4).

Resorption efficiency showed maxima in autumn for N and P at both sites, and for K in Garde,

with no clear patterns for other nutrients. In the case of Ca, negative resorption indicated this

nutrient was accumulated in senesced needles, especially in Aspurz (Figure 6). Linear contrast

showed significantly higher Mg resorption at control plots in both sites (F1,182=5.46, P=0.02), but

there were no differences between P20 and P30 (F1,182=0.01, P=0.97).

Nitrogen mean resorption proficiency was higher in Garde, but it was higher in Aspurz for P, Ca

and Mg (Table 4). There were no differences between sites for K. In Aspurz, thinning affected

mean resorption proficiency for Ca (with the highest proficiency in P20) and Mg (highest

proficiency in P30), while in Garde P20 showed the highest proficiency for Mg, with P30 in an

intermediate position between P0 and P20 (Table 3).

Annual nutrient productivity was higher in Aspurz for all nutrients, whereas MRT was higher in

Garde for all nutrients except P, which did not show differences between sites. NUE was

significantly higher for P in Aspurz, but for the rest of the measured nutrients NUE was higher in

Garde. NUpE was higher for N and P in Garde and for K and Mg in Aspurz, with no differences

for Ca. NRE was higher for P in Garde and for K in Aspurz, with no differences for other

nutrients (Table 5, Figure 7).

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Blanco et al. (2009) 11/45

Differences among thinning intensities were only found for NUpE K and NUpEMg (Table 4), but

those differences disappeared when analyzed separately by site. Finally, differences among

thinning intensities in NRE were found only in Garde for P, K and Mg, with NRE always higher

in the control plots compared to the thinned ones, and without differences among thinning

intensities (Table 5, Figure 7).

Discussion

Nutrient concentration in green needles

Our results showed differences in needle nutrient concentration between sites; these are likely

caused by differences in the edaphic material (Chapin 1980, Herbohn and Congdon 1998). Thus,

the higher soil concentrations of Ca and Mg measured in Garde (Table 2; Blanco et al. 2003) may

cause higher concentrations of these elements in green needles. In the same way, the higher N

concentration in soil at Aspurz (horizon A, Table 2) may have a direct influence on the higher N

concentration in green needles at this site. However, differences between sites in P and K

concentrations did not follow this pattern. For example, soil K concentration in Aspurz was lower

than in Garde (Blanco 2004) but needle K concentration was higher in Aspurz. At Aspurz, a high

initial value of N was measured in the youngest needles, which may be caused by a high mitotic

activity in the cells of the new cohort. These cells are typically a primary sink of N (Chapin 1980,

Fife and Nambiar 1982).

On the other hand, N concentration was lower in the older cohorts, in agreement with the

observations by Fife and Nambiar (1982) for P. radiata D.Don. This may be an indicator that N
 Blanco et al. 2007 12 / 45

is being transferred from older cohorts to new ones. This use of the oldest cohorts as reservoirs

has previously been described (De Lillis and Fontanella 1992, Sabaté et al. 1995, Amponsa et al.

2005). It is possible that requirements of new organs (especially inflorescences rich in K) caused

high levels of K resorption from needles (Milla et al. 2005), a phenomenon observed in Garde in

Winter 2002/2003. The fluctuation of K resorption was obvious at Garde (as were N and P

variations) but was much less so at Aspurz (Figure 6); this may be related to a higher K demand

in the continental site. Furthermore, K is usually present in plant cells in ionic and free form

(Fisher and Binkley 2000), and thus this element is highly mobile and easily leached. Its tendency

to be leached away could explain the observed concentration decrease in the oldest needles

(observed as well by Bockheim and Leide (1991) for P. banksiana Lamb.), which have been

exposed longer to rainfall, and this may be the case in Garde, the site with the higher annual

rainfall (see Figure 3). For Ca the pattern was the opposite, with it showing an increase in

concentration through needle life. Calcium is an element mostly joined to structural compounds,

and as a consequence, Ca concentration increases with tissue lignification in young cohorts

(Bockheim and Leide 1991, Ralhan and Singh 1987). Regarding Mg, the lack of clear temporal

patterns may be related to the fact that apoplastic and vacuolar Mg is believed to be unavailable

for resorption (Slovik 1997).

Thinning effects were only detected in Aspurz, resulting in a reduction in needle Mg

concentrations in the 2001 cohort (Figure 5). Similar concentration decreases have been reported

by other authors after human interventions (Aerts 1996, Santa Regina and Tarazona 1999). The

decrease in Mg concentration could be caused by an increase in the C:Mg ratio caused by the

increased development of tree crows to occupy the empty crown space created by thinning. As a

consequence, more carbon compounds are allocated to branches and needles, diluting needle

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Blanco et al. (2009) 13/45

nutrients and creating significant differences for Mg, the nutrient with the lowest concentrations

and nearly significant differences for P, the nutrient with the second lowest concentrations.

Finally, Mg differences among thinning intensities may be a consequence of adaptation to new

light conditions, which, because of an increase in performance of photosynthetic pigments, allow

maintenance of similar photosynthetic activity with lower pigment concentrations (Kozlowski et

al. 1991). Given our non-conclusive results on this nutrient, however, these speculative ideas

need more data to be supported.

Resorption efficiency and proficiency

Mean N resorption (Aspurz 42.8 ± 1.92%; Garde 41.9 ± 2.13%) was lower than that recorded by

Fife and Nambiar (1982) for P. radiata (48%) or by Pugnaire and Chapin (1993) for P. sabiniana

Dougl. (55%). However, it was close to the value reported by Escudero et al. (1992) for P.

halepensis Mill. (40.7%). Maximum resorption was reached in October 2002 and it was below

80%, the maximum level proposed by several authors (Escudero et al. 1992, Pugnaire and Chapin

1993, Aerts and Chapin 2000). Between-site differences in N resorption did not follow the same

pattern of between-site differences reported for soil N by Blanco (2004) at these same sites. This

fact supports the suggestion by Aerts and Chapin (2000) that resorption rates depend not only on

soil fertility, but on other factors such as water availability (Aerts 1996), length of resorption

period (Del Arco et al. 1991, Killingbeck 1996), or light availability (Covelo and Gallardo 2002).

Furthermore, it must be taken into account that resorption efficiency may be not only an

adaptation to low nutrient availability, but also a phenotypic response to nutrient status (Pugnaire

and Chapin 1993).

 Blanco et al. 2007 14 / 45

In the case of P, its resorption efficiency (Aspurz 54.0 ± 3.75%; Garde 49.6 ± 4.23%) was in the

range reported by other authors (Aerts 1996, Escudero et al. 1992), although it was lower than the

value reported by Fife and Nambiar (1982) for P. radiata (85.8%). Maximum resorption

efficiency was measured in October 2002 in both sites, and reached nearly 90%, which is the

maximum level proposed by Aerts and Chapin (2000) and Pugnaire and Chapin (1993).

Differences between study sites for P resorption were not related to soil P concentration, which

was similar at both sites (Blanco 2004).

Our K resorption results must be analyzed cautiously, because our methodology does not take

into account K losses to leaching (Bockheim and Leide 1991). However, our observations were

similar to those of Ralhan and Singh (1987) in P. roxburghii Sarg. Both our study sites showed

similar maximum resorption values for K (Aspurz 88.0%, Garde 91.7%), thus not following the

pattern of higher resorption in less fertile sites found in other studies (Kimmins 2004, Vitousek

1982).

For Ca, the negative values were due to the immobilization of this nutrient in structural

compounds with age: Ca concentration increases in senesced needles when the relative content of

other nutrients decrease (Chapin 1980). Finally, Mg resorption values were lower than those for

other elements (without considering Ca, which was not resorbed but immobilized), an expected

result given that Mg is an almost non-mobile nutrient with little susceptibility to leaching (Feger

1997). Uptake could be enough to cover Mg demand (Whittaker et al. 1979, Feger 1997, Slovik,

1997). As a consequence, senescence caused little change in Mg concentration, with almost non-

existent Mg resorption (Aspurz) or even an increase with age (Garde).

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Blanco et al. (2009) 15/45

At our study sites, mean resorption proficiency levels were at an intermediate level, as defined by

Killingbeck (1996). However, maximum proficiency values were close to a complete resorption

of foliar N (Table 3) and approached Killingbeck’s (1996) maximum potential resorption

proficiency. This fact might indicate that resorption proficiency is a phenotypic response that

depends on tree nutritional status (Pugnaire and Chapin 2003).

For P, pines in Aspurz were undergoing complete resorption, leaving very low concentrations in

needles; these were similar to the limits proposed by Killingbeck (1996) and by Aerts and Chapin

(2000). Although, trees in Garde were less proficient, in autumn they also reached the values that

Killingbeck (1996) has described as indicating high proficiency (see Table 3). These differences

likely indicated between-site differences in nutrient requirement, rather than a capacity to use

nutrients in a more efficient way. This hypothesis is supported by the likelihood of low genetic

difference between the two P. sylvestris populations, given the relatively short distance between

them (less than 25 km), although we lack genetic data. It is possible that the trees at Garde are

able to reduce P concentration to levels similar to those of Aspurz, but because they have lower

nutrient requirements, the trees at Garde are not reaching their full potential. Although to our

knowledge there are no other values reported for Mg, the high Mg resorption proficiency of P.

sylvestris could be an indicator of its adaptation to recycle this nutrient. However, the fact that the

lowest concentrations of Mg in needles and soil were found at the same site (Aspurz) could also

indicate that differences between sites are an important factor in determining resorption

proficiency (Killingbeck 1996).

Thinning seemed to have no effect on resorption efficiency, in accordance with Piatek and Allen

(2000). Although thinning and the consequent reduction in stem density could have caused
 Blanco et al. 2007 16 / 45

changes in resorption rates by increasing nutrient availability (Kimmins 2004), our results lead us

to think that those changes are too small or too slow to affect the resorption process. However, it

is difficult to reach clear general conclusions because of the scarcity of studies on the effects of

thinning on resorption, and the lack of strong and conclusive results in the studies that do exist

(Carlyle 1998, Piatek and Allen 2000). The lack of conclusive results may also be linked to a

possible underestimation of this parameter (Van Heewaarden et al. 2003), or to changes in LAI

after thinning. Clearly, more research is needed on thinning effects.

Indexes of nutrient use efficiency

The fact that A was higher for all nutrients at Aspurz while MRT was longer at Garde indicates

that trees were using site-specific strategies for soil nutrient use. On one hand, faster growth at

Aspurz caused higher nutritional requirements and as a consequence, more efficient use of

nutrients to produce aboveground biomass (Vitousek 1982, Birk and Vitousek 1986). On the

other hand, the higher MRT at Garde could be caused by lower rates of nutrient circulation

through needle fall in this forest. As a consequence, nutrient renovation in aboveground biomass

was slower at Garde than at Aspurz (Blanco et al. 2006 a,b). Escarré et al. (1999) have also stated

that higher soil nutrient concentrations and lower needle nutrient dilution by slower growth could

be a cause of increasing MRT. However, Aerts (1990) and Aerts and Chapin (2000) have shown

that in sites with low nutrient availability, the usual plant strategy to optimize the use of nutrients

is to increase MRT and to reduce A. Nevertheless, the negative relationship between A and MRT

has not been conclusively verified.

In our study, NUEN and NUEP values were similar to these proposed by Aerts and Chapin (2000),

whereas NUECa values were similar to those described by Vitousek (1982). The tendency of K

Blanco et al 2007 - 16 / 45 -
Blanco et al. (2009) 17/45

and Mg to move primarily in the ecosystem as throughfall makes it difficult to calculate an

appropriate NUE and the results shown here must be treated with caution. In our study, the most

important determinant of NUE could be MRT. This is supported by the fact that NUE was higher

for all nutrients at Garde (except P), despite the higher A for all nutrients at Aspurz. Interestingly,

when NRE is taken into account, differences between sites were found only for P (with Garde

being more efficient) and K (with Aspurz being more efficient). Garde’s soil can be classified as

highly deficient in P and Aspurz’s soil close to be deficient in K (Cobertera 1993), and this may

be a first explanation for these differences. However, our results do not support the hypothesis of

a relationship between NUE and soil nutrient availability because there were three different

behaviors depending on the nutrient involved. Firstly, Garde’s NUE N was the highest but N

concentration in soil was lower than at Aspurz. Secondly, Aspurz’s NUEP was higher than

Garde’s, but there were no differences between sites in P concentration in soil. Finally, NUE K,

NUECa and NUEMg were higher in Garde, the site with the highest soil concentrations of those

nutrients (Blanco 2004). These three different patterns support the opinions of Aerts et al. (1999)

and Aerts and Chapin (2000), who state that a high NUE is not an advantage in itself on

nutritionally poor sits if it is not also accompanied by other strategies to reduce nutrient losses

from plants.

A final explanation for differences between sites may be a link between NUE and other factors,

such as water supply (Binkley et al. 2004, Stape et al. 2004, 2006). Garde has a wetter climate

with shorter periods of water stress (Table 1) and a soil with higher percentage of clay and cation

exchange capacity than that of Aspurz (see Table 2), and these characteristics may help plants to

use the nutrients more efficiently. A last clue about the different strategies in soil nutrient use at

both sites was provided by the differences in NUpE for N and P, whose values were higher at
 Blanco et al. 2007 18 / 45

Garde, and NREP, higher also in Garde. This means that for every unit of N and P taken from the

soil, trees at Garde returned more N and P through litterfall, with an opposite situation for K and

Mg at Aspurz. This may be related to the lower soil temperature at Garde, that may be causing a

lower root uptake and therefore forcing to trees at Garde to do a better use of up-taken nutrients.

The difference between sites is also an indication that trees in Aspurz optimized the use of P by

retaining it for a longer period of time, while trees at Garde showed a greater tendency to increase

N use efficiency. Garde trees did this through a combination of using N for a longer period of

time, and producing more needle mass per unit of N in soil (perhaps because this nutrient is less

available there; Table 2), whereas trees at Aspurz produced more needle mass per unit of N in

green needles. It seems that as a consequence of localized optimization of N use efficiency, trees

in Garde must optimize P use by producing more needle mass per unit of P in soil. Trees at

Aspurz also appear to use this strategy, but for K; this is likely related to the lower availability of

K in Aspurz (Table 2).

The lack of thinning intensity effect on NUE, NUpE and NRE at Aspurz could be a consequence

of the limited change in nutrient availability caused by thinning from below. This type of

thinning primarily eliminates dead, ill and suppressed trees, which demand few nutrients and are

relatively more abundant at the Mediterranean site (Aspurz); therefore, the global effect at this

site would be smaller. Given that NRE is the ratio between needle mass produced and mass of

available nutrients in soil, and that thinning did not change the latter, our results for Aspurz mean

that there was no change in the amount of needle mass produced per unit of soil nutrient. This can

be interpreted as an indication that trees in Aspurz may have already been highly efficient in the

use of nutrients, and light or medium thinning from below is not sufficient to cause changes in

nutrient use efficiency. However, at the continental site of Garde, NRE after thinning decreased

Blanco et al 2007 - 18 / 45 -
Blanco et al. (2009) 19/45

for P, K and Mg, which may be interpreted as a reduction of needle mass produced by unit of soil

nutrient. When trees face higher nutrient availability (as at Garde compared to Aspurz; Table 2)

they may not exploit their full potential to use nutrients efficiently; therefore they are able to

respond to a small change in nutrient availability (e.g., as a consequence of thinning) by relaxing

their mechanisms of nutrient use efficiency. Yuan et al. (2006) also described a decrease in NRE

when increasing available resources and noticed that only when trees have an adequate

availability of one resource may they take advantage of increased availability of another.

Our results do not support our first hypothesis (increase in nutrient concentration after thinning)

but partially support the second hypothesis (reduction of nutrient use efficiency after thinning).

This means that thinning from below is a forestry practice that has a low impact on the use of

nutrients by remaining trees, and therefore other management practices (such as thinning from

above) should be tested if forest managers want to change trees’ nutrient use efficiency.

Nevertheless, an effect of thinning on nutrient availability at the continental site (Garde) was

found, which indicates that tree sensitivity to thinning varies by site. Studies in this area are

generally lacking, and research under different conditions is required in order to conclusively

establish the influence of thinning on tree nutrient use efficiency.

As a final consideration, we should not forget the limitations of using these indexes to estimate

NUE. In the first place, it should be noticed that leaf-level NUE ignores the carbon that is fixed

by the leaf and supports production or respiration elsewhere in the plant (Aerts and Chapin

2000).The methodology used to calculate nutrient uptake and NUpE can be somewhat misleading

because other storage pools than needles, in particular storage in the roots, are not considered. In

addition, an exact accounting of NUE requires accurate belowground estimates of production and
 Blanco et al. 2007 20 / 45

uptake, but this is expensive and time-consuming to measure (Bridgham et al. 1995). In this study

we have used green and senesced litterfall to estimate nutrient resorption from leaves and their

turnover time (Chapin 1980, Vitousek 1982). However, a mechanistic understanding of

adaptations of perennial plants to maximize NUE must not only consider tissue nutrient

concentrations but also allocation of production to various tissues, the kinetics of root uptake,

carbon fixation per unit plant nutrient and mobilization of stores nutrient reserves (Miller 1979,

Pastor and Bockheim 1984, Birk and Vitousek 1986, Bridgham et al. 1995). One more potential

source of error in our study was that to calculate available soil N we used total organic N as a

surrogate for net N mineralization, given the direct relationship between them (Schlesinger

1997). If thinning caused changes in percentages of labile N pools and/or if differences in labile

pools among plots already existed before thinning, this might have affected our NRE estimates.

However, soil temperature and soil moisture (the main controlling factors of ammonification,

Chapin et al. 2002), together with total organic N, did not exhibit significant differences among

thinning intensities suggesting that differences in N mineralization rates probably did not occur.

Finally, availability for other soil nutrients was estimated using standard extraction techniques

and assuming that trees absorbed the extracted nutrient pools; also mycorrhizal associations

might have been affected by thinning resulting in changes in nutrient availability.

Conclusions and management implications

Nitrogen, P and K concentrations were lower in older needle cohorts, probably due to a transfer

of nutrients to young cohorts, whereas Ca and Mg concentrations were higher in older cohorts,

probably as a consequence of the union between those nutrients and structural compounds.

Resorption efficiency of N, P and K were higher at the Mediterranean site of Aspurz, though

these differences are difficult to explain if only nutrient availability is considered, and we suggest

Blanco et al 2007 - 20 / 45 -
Blanco et al. (2009) 21/45

that resorption efficiency may be linked to a number of factors in addition to soil nutrients. For

all nutrients, resorption proficiency was higher at the site with lower nutrient availability,

indicating site specific nutrient conservation strategies, with trees reducing nutrient

concentrations in senescent needles to lower values when nutrient availability was also low.

However, this same pattern was not found for resorption efficiency, which was higher in Aspurz

for P (but with no differences between sites in availability of this nutrient), higher in Garde for

Mg (the site with the highest Mg availability) and which showed no differences between sites for

N, K and Ca (despite their differences in availability). This is proof that the relative amount of

nutrients resorbed from needles over a given period is driven not only by nutrient availability, but

also by factors such as water availability, needle age and phenological events. The higher MRT at

the continental site led to higher NUE for all nutrients except P. This could indicate that

improving NUE by using the same nutrients over a greater period (as seen in the trees at Aspurz)

is more effective than producing more biomass per nutrient unit. NUE was not related to nutrient

availability, because the highest NUEN was found at the site with the lowest N concentration in

soil, NUECa, NUEMg and NUEK were higher in the site with the highest concentration of those

nutrients and NUEP was different at each site while P concentration in soil was similar in both

forests. Finally, thinning only reduced Mg concentration in Aspurz, and produced no changes in

nutrient-use-efficiency indexes. This fact shows that at nutrient-limited sites, thinning from below

may not be an effective way for improving nutrient availability for remaining trees because it

only removes trees with small demands for nutrients (dead, sick, occluded, highly dominated

trees). Therefore, if forest managers are trying to increase tree growth rates and tree production

by increasing nutrient availability for selected trees, other strategies may be more suitable, such

as increasing thinning intensity by removing more than 30% of basal area, or using thinning from

above or fertilization. However, NREP, NREk and NREMg decreased after thinning in Garde (the
 Blanco et al. 2007 22 / 45

continental site with higher nutrient availability) due to a reduction of needle mass production,

indicating the possibility of influencing tree use efficiency by forest management. This result is

an indication that thinning from below, although it only removes dead and suppressed trees, may

be an effective way of increasing nutrient availability in stands with only moderate nutrient

limitation.

Acknowledgements

The authors wish to thank the Departamento de Educación y Cultura, Government of Navarre, for

financial support and the Departamento de Medio Ambiente for the experimental setting of

silvicultural treatments and financial support. In particular, we acknowledge Fernando Puertas,

Carmen Traver and Ana Iriarte for assistance at several stages of this work. We also thank Louise

K. Blight for her English language review.

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Table 1. Site characteristics (mean  SE). Stand descriptors from Puertas (2001) and Iriarte and
Puertas (2003).
Site Aspurz Garde

Latitude 42º48’50’’ N 42º42’31’’ N

Longitude 52’30’’ W 1º8’40’’ W

Altitude (m) 625 1335

Slope (%) 7 40

Soil Haplic Alisol Dystric Cambisol

Mean air temperature (°C) 12.01 (11.8)2 8.21 (7.8)2

Mear soil temperature (°C) 11.22 7.62

Mean precipitation (mm) 9121 12681

Climate type (Papadakis 1970) Cold wet Mediterranean Cold wet continental

Other overstory tree species 2 Fagus sylvatica L. Fagus sylvatica L.

Quercus humilis Mill.

Dominant understory species 3 Pteridium aquilinum (L.) Kuhn Deschampsia flexuosa L.

Rubus ulmifolius Schott Pteridium aquilinum (L.) Kuhn

Stands before thinning

Site Index at age 80 y (m) 29 23

Age (y) 32 37

Density (stems ha-1) 4 4040  326 3230  162

Dominant height (m) 5 15.1  0.4 14.3  0.2

Mean DBH (cm) 6 11.7  0.5 13.8  0.3

Volume (m3 ha-1) 270.7  11.9 290.1  10.5

Fraction of green crown (%) 7 40 54

Stands after thinning 8 P20 P30 P20 P30

Density (stems ha-1) 9 2186  245 1295  136 1697  156 1478  113

Blanco et al 2007 - 30 / 45 -
Blanco et al. (2009) 31/45

Mean DBH (cm) 6 13.7  0.3 13.1  0.4 17.0  0.4 16.7  0.3

Volume (m3 ha-1) 234.2  10.7 207.8  9.4 246.4  8.8 213.0  9.8

1
Thirty-five years average of daily average temperature and accumulated rainfall (Ministry of

Environment, Spain).
2
Study period average of monthly temperature (May 2000 to August 2003).
3
Eighteen and ten tree species identified in Aspurz and Garde, respectively.
4
Sixty-six and fifty-two shrub and herb species identified in Aspurz and Garde, respectively.
5
Trees with DBH > 7.5 cm.
6
Measured averaging (n = 100) the height of the thickest dominant trees per hectare.
7
Measured by double cross measurement.
8
Percentage of tree height that supports live branches.
9
P20: moderate thinning from below (20% of basal area removed); P30: heavy thinning from

below (30% of basal area removed).

 Blanco et al. 2007 32 / 45

Table 2. Soil chemical and physical properties at the study sites. Comparisons between sites in horizon A are shown for organic matter (OM), organic C

(defined as in Walkley and Black (1934)), Kjeldahl N, available P (defined as in Bray and Kurtz (1945)), exchangeable K, exchangeable Ca, exchangeable Mg

and C/N ratio. Horizon A data are averages of bimonthly samples taken from April 2001 to Aprils 2003 (n = 13), as described in Huarte (2003) and Blanco

(2004).

Site/ Depth Clay Silt Sand pH Density a CEC b OM C N P K Ca Mg

1:2.5 C/N

Horizon cm % % % H2O g cm3 meq 100 g-1 % mg g-1 mg g-1 mg g-1 mg g-1 mg g-1 mg g-1

ASPURZ

Ac 0 –10 7.2 50.5 42.3 5.45 0.96 14.2 11.69 67.8** 3.05** 0.029 0.098*** 1.94** 0.213*** 22.6

B 10 – 45 14.2 33.3 55.5 5.55 1.31 7.2 1.14 6.6 1.503 0.011 0.043 0.980 0.142 4.4

GARDE

A 0 – 10 23.3 30.8 45.8 5.48 0.76 23.3 9.88 57.3 2.67 0.026 0.145 2.20 0.273 22.0

B 10 – 45 25.7 34.5 39.4 6.00 1.26 19.7 3.05 17.7 2.310 0.007 0.055 2.872 0.170 7.7

C 45 – 60 26.5 31.7 41.8 6.40 0.71 22.6 1.88 10.9 1.602 0.014 0.043 3.732 0.212 6.8

a
Density: apparent density
b
CEC: cation exchange capacity
c
* P < 0.05 ** P < 0.01, *** P < 0.001

Blanco et al 2007 - 32 / 45 -
Blanco et al. (2009) 33/45

Table 3. Partial results from repeated measures ANOVA showing effect of site on three different

variables. The letter in the Site row stands for the site with the highest value of the given variable (A:

Aspurz, G: Garde, =: no significant differences between sites). Results for resorption efficiency and

proficiency were calculated by using data for each plot and sampling date (efficiency: collection of

green needles from Dec 2001 to Oct 2003; proficiency: collection of dry needles from May 2000 to

Aug 2003 as described in Blanco et al. 2006a). Results for sampling date effects are not shown.

Nutrient Concentration in green needles by cohorts Resorption Resorption

efficiency proficiency

1999 2000 2001 2002

D.f. 1,8 1,10 1,9 1,9 1,182 1,580

N Site -1 A A A = G

F - 22.452 75.368 62.577 0.276 14.296

P - 0.002 <0.001 <0.001 0.6 <0.001

P Site G G G G A A

F 330.903 62.233 82.807 6.201 4.674 192.537

P <0.001 <0.001 <0.001 <0.034 0.032 <0.001

K Site = = = = = =

F 1.334 3.828 0.809 17.95 0.429 3.229

P 0.282 0.079 0.392 0.002 0.628 0.073

Ca Site G G G G = A

F 8.667 17.827 16.288 6.201 0.059 45.009

P 0.019 0.002 0.003 0.034 0.809 <0.001

Mg Site G G G G G A

F 31.077 33.951 32.225 61.989 4.974 429.559

P <0.001 <0.001 <0.001 <0.001 0.027 <0.001

1
Due to lost samples, there were not enough data to compare N concentrations in cohort 1999.
 Blanco et al. 2007 34 / 45

Table 4. Mean (± SE) and maximum resorption proficiency in senesced needles (minimum concentrations) in mg g -1. Different letters stand for significant

Tukey’s HSD among thinning intensities.

Site Parameter Thinning intensity N P K Ca Mg

Aspurz Mean Proficiency 0% 8.16 ±0.25 a 0.46 ±0.02 b 2.74 ±0.08 a 6.33 ±0.11 b 0.77 ±0.01 d

20% 8.62 ±0.24 a 0.41 ±0.02 b 2.72 ±0.07 a 5.78 ±0.11 c 0.77 ±0.01 d

30% 8.70 ±0.24 a 0.44 ±0.02 b 2.86 ±0.09 a 5.82 ±0.12 b 0.70 ±0.01 e

Mean 8.49 ±0.19 0.44 ±0.01 2.78 ±0.05 5.98 ±0.07 0.75 ±0.01

Maximum proficiency 0% 4.10 0.15 1.30 3.78 0.57

20% 4.00 0.14 1.55 1.08 0.43

30% 4.63 0.18 1.19 1.07 0.45

Mean 4.02 0.14 1.19 1.07 0.43

Garde Mean Proficiency 0% 7.74 ±0.25 b 0.72 ±0.03 a 3.25 ±0.15 a 6.97 ±0.16 a 1.00 ±0.01 a

20% 7.78 ±0.25 b 0.69 ±0.03 a 3.18 ±0.13 a 6.54 ±0.14 a 0.93 ±0.02 b

30% 7.73 ±0.25 b 0.69 ±0.03 a 3.10 ±0.14 a 6.80 ±0.14 a 0.96 ±0.02 ab

Mean 7.75 ±0.16 0.70 ±0.02 3.17 ±0.08 6.77 ±0.09 0.96 ±0.01

Maximum proficiency 0% 3.70 0.21 0.67 3.72 0.49

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Blanco et al. (2009) 35/45

20% 4.03 0.22 0.58 3.48 0.65

30% 3.81 0.25 0.69 4.14 0.59

Mean 3.74 0.21 0.58 3.48 0.49

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Table 5. Results from two-way ANOVAs for Annual Efficiency (A), Mean Residence Time (MRT),

Nutrient Use Efficiency (NUE), Nutrient Uptake Efficiency (NUpE) and Nutrient Response Efficiency

(NRE) Significant differences in bold case.

Variability source d.f. N P K Ca Mg

F P F P F P F P F P

Site 1 32.298 <0.001 6.083 0.039 17.316 0.003 16.974 0.003 10.150 0.013

Block (Site) 4 0.399 0.804 0.388 0.812 0.389 0.811 0.433 0.782 0.420 0.790

Thinning intensity 2 1.048 0.394 0.990 0.413 1.009 0.407 1.130 0.370 1.086 0.383

Site x Thinning intensity 2 0.053 0.949 0.070 0.933 0.065 0.938 0.065 0.938 0.064 0.939

Error 12

MRT

Site 1 38.702 <0.001 0.128 0.664 15.191 0.005 16.797 0.003 10.728 0.011

Block (Site) 4 0.752 0.584 0.070 0.933 0.417 0.792 0.299 0.871 0.314 0.861

Thinning intensity 2 0.785 0.489 0.962 0.410 0.938 0.431 0.981 0.416 1.504 0.279

Site x Thinning intensity 2 0.330 0.728 0.168 0.847 0.277 0.765 0.174 0.843 0.488 0.631

Error 12

NUE

Site 1 9.009 0.017 28.828 <0.001 6.017 0.045 5.294 0.050 5.463 0.073

Block (Site) 4 0.956 0.481 3.051 0.084 0.504 0.735 0.261 0.895 0.179 0.943

Thinning intensity 2 0.003 0.997 0.215 0.811 0.552 0.597 0.545 0.600 1.713 0.240

Site x Thinning intensity 2 0.992 0.412 1.688 0.245 2.005 0.197 0.681 0.533 2.382 0.154

Error 12

NUpE

Site 1 19.129 0.002 30.171 <0.001 66.951 <0.001 0.822 0.382 7.491 0.026

Block (Site) 4 1.648 0.254 1.888 0.206 1.592 0.267 1.504 0.252 1.295 0.349

Thinning intensity 2 2.252 0.168 4.639 0.046 5.952 0.026 2.001 0.178 8.447 0.011

Site x Thinning intensity 2 2.415 0.151 0.142 0.870 0.284 0.760 0.673 0.529 0.719 0.516

Error 12

NRE

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 Blanco et al. (2009) 37/45

Site 1 67.154 <0.001 5.396 0.049 95.392 <0.001 1..645 0.236 0.041 0.845

Block (Site) 4 3.009 0.087 3.832 0.056 3.377 0.071 1.223 0.373 1.304 0.346

Thinning intensity 2 2.227 0.170 10.370 0.006 9.791 0.007 1.644 0.252 5.658 0.029

Site x Thinning intensity 2 2.856 0.116 1.471 0.286 3.487 0.063 0.911 0.440 4.678 0.051

Error 12
 Blanco et al. 2007 38 / 45

Figure Legends

Figure 1. Temporal evolution of N concentration from December 2001 to October 2003. Data points

represent mean  SE (n=3).

Figure 2. Temporal evolution of P concentration from December 2001 to October 2003. Data points

represent mean  standard error (n=3).

Figure 3. Temporal evolution of K concentration from December 2001 to October 2003. Data points

represent mean  standard error (n=3).

Figure 4. Temporal evolution of Ca concentration from December 2001 to October 2003. Data points

represent mean  standard error (n=3).

Figure 5. Temporal evolution of Mg concentration from December 2001 to October 2003. Data points

represent mean  standard error (n=3).

Figure 6. Mean percentage of nutrient concentration in green needles resorbed before abscission. Data

points represent mean  standard error (n=3).

Figure 7. Nutrient use efficiency and its components. a) Annual Productivity (A). b) Mean Residence

Time (MRT). c) Global Nutrient Use Efficiency (NUE). d) Nutrient Uptake Efficiency (NUpE). e)

Nutrient Response Efficiency (NRE). Columns with different letters have significantly different values

and columns without a letter have similar values (Tukey’s HSD).

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Figure 1.
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Figure 2.

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Figure 3.
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Figure 4.

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Figure 5.
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Figure 6.

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Figure 7.