Fifty Years of Fertilization Experiments on Pinus pinaster in Southwest
France: The Importance of Phosphorus as a Fertilizer
Pierre Trichet, Mark R. Bakker, Laurent Augusto, Pierre Alazard, Dominique Merzeau, and
Etienne Saur
Abstract: Data from 50 years of fertilization trials on Maritime pine (Pinus pinaster) were compiled to
investigate how growth was affected by fertilization or improved nutrient availability. The results demonstrated
that only trees fertilized with phosphorus (P) fertilizers showed an overall improvement in productivity. The
effects were significant mainly at wetter sites and were less effective at drier sites. The form of P fertilizer does
not seem to be important, and a rate of about 17–35 kg of P ha⫺1 applied as a single dose at stand establishment
was found to be sufficient to obtain a significant improvement in growth. Foresters can expect an increase of
20 – 40% cumulative volume at rotation age or a reduction of 4 –5 years in rotation length due to fertilization with
P. The duration of the effect of P fertilization on the annual increment varied (up to 20 years after application
in the best cases). The high P-fixing capacity of these soils appears to be the most important factor in explaining
differential responsiveness to P fertilizers, but stand developmental stage or the appearance of other limitations
such as nitrogen may also explain the decline in the effectiveness of P fertilization with age. FOR. SCI. 55(5):
390 – 402.
Keywords: tree growth, fertilization, phosphorus, Pinus pinaster, podzol
T
LANDES OF GASCOGNE forest in southwest
France is the largest man-made forest area in Europe, and phosphorus (P) fertilizer is widely applied
to the Maritime pine (Pinus pinaster [Soland in Aït]) stands
of this forest range. Established trials showed promising tree
growth response to P application in the first few years after
the application (Guinaudeau et al. 1963), and this response
was of a magnitude similar to those obtained for various
pine species on other P-deficient soils in the southeastern
United States (Pritchett and Lewellyn 1966, Wells et al.
1986, Fox et al. 2006), South Africa (Donald and Glen
1974, Donald 1990), New Zealand (Weston 1956, Hunter
and Graham 1982, Payn et al. 2000), Australia (Gentle et al.
1965, Lewis and Harding 1963), and Morocco (Lepoutre
and Mandouri 1976). Although the application of P fertilizer at stand establishment has generated satisfactory results
for managers and land-owners in the Landes de Gascogne,
several questions remain regarding the complex relationship
between P fertilization, site quality, and tree growth. For
instance, P response was not observed at all sites and neither
the magnitude of response nor its intensity was the same in
the short and long term (Lemoine 1993, Vauchel 1996,
HE
Trichet et al. 1999, 2000). In addition, applications of nitrogen (N) or potassium (K), with or without P in trials from
the 1950s and 1960s (Saur 1989a, Bonneau 1995) were
reported to yield only limited short-term effects. However,
such applications may result in greater tree response in the
case of a changing environment or increased harvests. In
agreement with the latter hypothesis, annual optimum fertilizer inputs in a young P. pinaster stand showed that
complete fertilizer treatment (nitrogen, phosphorus, potassium, calcium, and magnesium [NPKCaMg]) increased tree
productivity (P ⬍ 0.05) more than P fertilization alone,
indicating that other elements besides P may limit tree
growth in the Landes of Gascogne forest area (Trichet et al.
2008).
Tree productivity generally declines with age of the tree
(Ryan et al. 1997, Binkley et al. 2002, Delzon and Loustau
2005, Delzon et al. 2005). It may thus be questionable
whether improved P availability because of the initial application of P fertilizers would maintain an increase in tree
productivity as trees grow older, or if older stands would
respond to P fertilization. Long-lasting P fertilizer effects
have been recorded for soil P levels and stand growth up to
Pierre Trichet, Institut National de la Recherche Agronomique, UR1263, Laboratory of Functional Ecology and Environmental Physics (EPHYSE), 69 Route
d’Arcachon, F-33612 Cestas, France—[email protected]. Mark R. Bakker, Université de Bordeaux, Unité Mixte de Recherche 1220 TCEM (Institut National
de la Recherche Agronomique-National Higher School of Agriculture of Bordeaux [ENITAB]), 71 Avenue E Bourlaux, BP 81, F-33883 Villenave d’Ornon,
France—[email protected] (corresponding author). Laurent Augusto, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1220
Transfert sol-plante et cycle des éléments minéraux dans les écosystèmes cultivés (TCEM) (Institut National de la Recherche Agronomique-National Higher School
of Agriculture of Bordeaux [ENITAB]), 71 Avenue E Bourlaux, BP 81, F-33883 Villenave d’Ornon, France—[email protected]. Pierre Alazard, Forêt,
Cellulose, Bois et Ameublement (FCBA), 128 Sivaillan, F-33480 Moulis-en-Médoc, France—[email protected]. Dominique Merzeau, Institut pour le
développement forestier–Centre de la Propriété Forestière d’Aquitaine (IDF-CPFA), 6 Parvis Chartrons, F-33075 Bordeaux, France— [email protected]. Etienne
Saur, Université de Bordeaux, Unité Mixte de Recherche 1220 TCEM (Institut National de la Recherche Agronomique-National Higher School of Agriculture of
Bordeaux [ENITAB]), 71 Avenue E Bourlaux, BP 81, F-33883 Villenave d’Ornon, France— [email protected].
Acknowledgments: We express our gratitude to several generations of forest researchers, forest managers, and forest owners for providing the data used for
this analysis. We further thank the technical teams of the Institut National de la Recherche Agronomique-Pierroton experimental unit, of FCBA (formerly
AFOCEL) and of IDF-CPFA Aquitaine (and its predecessors) for the dendrometrical measurements. We also acknowledge Christian Morel for the soil testing
with the 32P isotopic dilution method of the soils from some contrasting trials. Financial support was obtained from the Région Aquitaine, the French Ministry
of Agriculture, and many partners of the forest, paper, and fiberwood sector for the installation, monitoring, and maintenance of this “Network of Fertilisation
Trials” throughout the last five decades.
Manuscript received December 14, 2006, accepted April 22, 2009
390
Forest Science 55(5) 2009
Copyright © 2009 by the Society of American Foresters
29 years after application in the United States (Pritchett and
Comerford 1982, Comerford et al. 2002, Fox et al. 2006),
for more than 19 years in South Africa (de Ronde and
Donald 1993), from 22 to 35 years in New Zealand (Mead
and Gadgil 1978, Lowell 1988, Comerford et al. 2002), and
up to 50 years in Australia (Turner et al. 2002). Although
most published results on the effects of fertilization in the
Landes of Gascogne region relate to short observation periods (5–10 years), results of long-term trials agree with the
long-term effects reported in the literature, which point to a
decline in the efficiency of P in relation to current growth
increments 20 years after application at stand establishment
(Gelpe and Lefrou 1986, Lemoine 1993, Vauchel 1996). In
this study we performed a metadata analysis on a compilation of 50 years of fertilization experiments with the objective of investigating the response of P. pinaster to nutrient
additions to examine how growth was affected by fertilizers.
We expected that such a compilation would make it possible
(1) to refine the existing responses of P fertilizers at individual sites and to establish how meaningful such a response is at the regional scale, (2) to detect nutrient limitations other than P, which are less evident from individual
experiments, in a metadata analysis including many sites,
(3) to compare short-term (incremental or yearly growth
effects) and medium-term effects (cumulative growth and
reductions in rotation length) of fertilization; and (4) to
investigate whether the age of the trees at the moment of
fertilization affects the fertilizer response or not.
Materials and Methods
Abbreviations and Definitions
Three groups of abbreviations and definitions were used
throughout this study and relate either to forestry, to fertilization, or to the evaluation of the fertilization effects. For
the forestry group, we used tree height (HT in m), tree
circumference at 130 cm height (C130 in m), stand basal area
(BA in m2 ha⫺1), stand bole volume (VOL in m3 ha⫺1), tree
bole volume (VOLtree in m3), gain in tree circumference by
fertilization relative to the controls (C130gain% in %), and
gain in tree height by fertilization relative to the controls
(HTgain% in %). For the fertilization group, we used the
amounts of fertilizers for a given nutritional element (e.g., P
rate in kg ha⫺1), the source of the fertilizer (i.e., three forms
were distinguished in the case of P fertilizers), all fertilizer
treatments containing P (P⫹), all fertilizer treatments without P (P⫺), site class (either dunes, humid, mesic, or dry
moorlands), the stand age at the time of fertilization (AGEF
in years), and the period of time since fertilization for the
last available measurement (TIMEF in years). Finally, for
the evaluation of fertilizer effects, we used the percentage
response in cumulative volume growth relative to controls
(cumulative percent growth response in %), the percentage
response in yearly increments of volume growth relative to
controls (incremental percent growth response in %), the
reduction in time to reach a certain average tree height due
to fertilization relative to controls (AGEshift in years), and
the annual AGEshift, i.e., the annual reduction in rotation
length due to fertilization relative to controls (AN-AGEshift
in yr yr⫺1).
Description of the Forest Region Studied
The Landes of Gascogne in the southwest of France
consist mainly of poorly drained plains with moorland vegetation. Nearly 1 million ha are currently under forest and
90% of the forest area is privately owned (Inventaire Forestier National 2003). The main cultivated species is P.
pinaster, which is present on more than 85% of the total
forest area. Most of the stands are intensively managed as
mono-specific, even-aged stands generally with rotation
lengths from 35 to 65 years. Soils have developed from a
coarse sandy Aeolian parent material deposited in the Pleistocene and are of low fertility, acidic, and highly organic
(Saur 1989b, Augusto et al. 2006). They can be classified as
Entic to Albic Podzols (Food and Agriculture Organization
(FAO)/International Union of Soil Sciences 2006), depending on the depth of the water table, and lenses of a cemented
spodic horizon can occur between depths of 40 and 100 cm
in the soil (Trichet et al. 1999). In the inland plains of the
forest area, three main site classes can be distinguished in
relation to the depth of the water table: dry moorland, mesic
(or mesophylous) moorland, and humid moorland. Humid
moorland is the most frequent class. On the coastal fringe,
forests have been established on dunes (from the Holocene
period), forming a fourth site class. The mean annual temperature ranges from 10 to 15°C (from west to east), and
precipitation ranges from 750 to 1,250 mm yr⫺1 (from north
to south) and is distributed irregularly over the year.
Construction of the Fertilization Database
Local literature resources, such as collections of the
periodicals Revue Forestière Française, Annales des Sciences Forestières, Annales de Recherches Sylvicoles AFOCEL, Rapports Annuels AFOCEL, and Informations-Forêt
AFOCEL-ARMEF, for the relevant period (1955–2005)
were examined for published results and descriptions of
fertilization trials. Other literature available in local libraries
of relevant research institutes provided further valuable
information. Additional information was added from personal archives, mostly concerning ongoing fertilizer trials.
Based on this extensive review of the literature, a preliminary “fertilization” database was built containing a list of
103 fertilizer trials. After data quality checks the data from
48 trials were analyzed in the present study. To perform a
meta-analysis on these data, the recommendations and considerations of Gurevitch and Hedges (1999) were followed.
Different forms, rates, and combinations of fertilizers were
incorporated into the database as separate treatments to
enable the effects of each treatment or combination of
treatments to be tested (Ostonen et al. 2007). An equal
weight was attributed to each fertilization treatment (1 observation ⫽ 1 value per experimental treatment). When
consecutive measurements were available for a given fertilization treatment, only the last measurement for each
treatment was included. This was done to guarantee the
assumption of meta-analysis that data must be independent
and to allow the full growth response to a given treatment to
be expressed. As many sources did not report the variance
of the results, we were not able to weight mean values by
their variances as proposed by Gurevitch and Hedges
Forest Science 55(5) 2009
391
(1999). However, because these authors concluded that a
meta-analysis can be carried out even without variance
weighting, we assumed that the validity of our tests was not
severely compromised.
Data Set Characteristics
The summary characteristics of the 48 experimental trials included in the present study are listed in Table 1. This
table shows that for the majority of trials, the results came
from the gray literature or had not been published previously. All original publications were in French. Initial stand
characteristics such as tree height, circumference, stand
volume, and basal area were either zero for stands that had
received an application of fertilizer at stand establishment or
were not reported for the older sites that had been fertilized
(and are consequently not referenced in Table 1). Likewise,
data on soil and foliage were scarce or were only available
at the time of trial initiation or a few years later. Thus, we
could not proceed to a general evaluation of foliar or soil
data, but some published results have been used in the
Discussion. Generally, in the trials considered, sites had
undergone standard preparation, i.e., plowing of the top
20 – 40 cm of soil before fertilization with subsequent mechanical weed control every 3–5 years. The “humid moorland” site class represented 56% (n ⫽ 27 trials) of the
database, the “mesic moorlands” 19% (n ⫽ 9), the “dry
moorlands” 23% (n ⫽ 11), and the “dunes” 2% (n ⫽ 1). The
stand age in years at the time of fertilization ranged from 0
to 55 years. The period of time since fertilization for the last
available measurement varied from 1 to 41 years. Three
forms of P fertilizers were identified: P slags, rock phosphates, and superphosphates. Rates of applied P ranged
from 5 to 131 kg of P ha⫺1, and several trials included N
and/or K (Table 1).
Calculation of Growth Responses
The growth response due to fertilization relative to controls was expressed either as a percentage value for cumulative volume growth, or as an incremental volume growth,
or as a difference in years to obtain a given tree height, the
so-called age-shift (South et al. 2006). To build cumulative
percent growth and incremental percent growth response
values when volume data were not directly available, the
available data on other dendrometrical variables were used
to calculate total stand bole volume. Briefly, we used the
following procedure for estimating stand volume:
1. When the average HT and average C130 values of the
trees of the stand were available, the bole volume of the tree
was estimated as
VOLtree ⫽
1
䡠 C2130 䡠 HT 䡠 f,
4␲
(1)
where f is the form factor (unitless, derived from Vallet et
al. 2006). Equation 1 was tested with the data from sites
where VOLtree, HT, and C130 were available. The estimated
values of VOLtree were validated (r2 ⫽ 0.97; n ⫽ 15)
against the measured values of VOLtree, and so we concluded that this equation was reliable in our context. The
VOLtree values were multiplied by stand density to estimate
392
Forest Science 55(5) 2009
the stand volume (VOL). In a few cases stand density was
not available. However, all of the stands of the same trial
were managed in the same way, and when this information
was available, they had a similar density. Therefore, for the
calculation of the percent value relative to controls for
volume growth, VOLtree values were used when stand density was unknown.
2. When only C130, HT, or BA was available, percent
values relative to controls for volume growth were calculated based on the proportionality between gains in C130,
HT, and VOLtree, respectively, gains in BA and VOL. The
relationships were validated on a set of measured values of
our database when VOL and either C130, HT, or BA was
available (r2 ⫽ 0.96 – 0.98; n ⫽ 37).
When HT data were available, we also used the approach
described by South et al. (2006) to calculate an AGEshift
value, i.e., the reduction in time to reach a certain average
tree height due to better conditions, in our case, fertilization.
The first stage was to calculate a predicted age for control
trees to reach the HT of fertilized trees based on calibrated
height growth curves from Alvarez-Gonzalez et al. (2005)
using their “Interior” parameter set. These curves were valid
in the Landes forest context for each of the five fertility
classes published by the French national forest office (Office National des Forêts) (site index at age 35 ranging from
18.3 to 25.1 m), and the error of prediction was ⬍2%. Then
we calculated a value for AGEshift as the difference between
the predicted age for control trees to reach the HT of the
fertilized trees minus the actual age of the control treatments, i.e., the reduction in age (in years) as a result of
fertilization (see South et al. 2006 for more information).
This value was also investigated on a yearly basis by dividing the AGEshift value by the number of years considered
(annual reduction in rotation length, AN-AGEshift). The
number of observations used to evaluate the effect of fertilization treatment for each type of variable (cumulative
percent growth response, AGEshift, and incremental percent
growth response) is given in Table 2.
Variable Selection and Statistics
Fertilizer effects were evaluated on cumulative and incremental percent growth responses relative to controls (expressed as a percentage of controls) and AGEshift values (in
years gained relative to the controls) using SAS software
(version 8.1; SAS Institute, Inc. 1999). To meet model
assumptions, log-transformed values of cumulative and incremental growth and of (AGEshift ⫹ 2) were used for the
calculations. For reasons of presentation and for comparison
with the literature, mean values in tables and figures are
nontransformed values. For each of the three variables, we
first tested a generalized linear model in which all of the
following variables were tested: TIMEF, AGEF, site class, P
rate, P form, and interactions AGEF ⫻ TIMEF, P rate ⫻ N
rate, P rate ⫻ K rate, and P rate ⫻ site class. Effects of N
or K rate alone could not be tested (N alone was generally
restricted to dry sites, and K was always applied with P)
(Table 2). Then, depending on the outcome of the generalized linear model, only variables with a P level of ⬍ 0.10
were selected for further examination of specific fertilizer
Forest Science 55(5) 2009
393
Andrauts
Baron III
Berganton
Betria
Blagon
Boe
Bouheyre
Bourideys I
Bourideys II
Bray
Castillonville I
Castillonville II
Caudos
Clochettes
Condom
Grand Ludee
Hermitage PZ
Hermitage R
Jauge
Lagnereau
Lue
Luxey I
Luxey II
Magescq
Marcheprime
Mimizan
Peytejoux
Pierroton 76
Pierroton 79
Pigeon
Pomarez
Pont des A.
Porge
Rasson
Reaup
Retis
Retjons
Sabres
Saint Alban
Saucats
Saumejan
Sore 7
Sore Bis
Sore Verrerie
Tabarton
Trensacq
Vieille St G.
Ychoux
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
Gray
Unpubl.
Gray
Unpubl.
Unpubl.
Gray
Unpubl.
Gray
Gray
Gray
Unpubl.
Gray
Unpubl.
Unpubl.
Gray
Unpubl.
Unpubl.
JCR
Gray
Gray
Unpubl.
Gray
Unpubl.
Gray
JCR
JCR
Unpubl.
Gray
Gray
Gray
Gray
Gray
Gray
JCR
Unpubl.
Gray
Unpubl.
Gray
Unpubl.
Gray
Unpubl.
Gray
JCR
Gray
Gray
Gray
Gray
Gray
Source
Humid
Humid
Humid
Humid
Humid
Mesic
Humid
Dry
Dry
Mesic
Humid
Humid
Humid
Humid
Mesic
Humid
Humid
Humid
Mesic
Mesic
Humid
Humid
Mesic
Dry
Mesic
Humid
Dry
Humid
Humid
Humid
Humid
Mesic
Dune
Humid
Dry
Humid
Humid
Dry
Mesic
Humid
Dry
Humid
Dry
Dry
Humid
Dry
Dry
Humid
Class
0
50
0
16
0
53
44
10
10
12
0
0
0
0
25
0
0
14
23
25
0
17
0
21
39
0
0
0
0
20
55
0
8
11
0
0
0
0
0
0
0
10
11
2
0
22
10
38
AGEF
15
4
34
9
8
12
6
3
3
8
7
8
3
5
8
6
17
9
1
6
7
10
3
7
12
41
8
19
16
3
21
11
⬍1
11
2
12
5
11
17
13
2
5
3
3
8
5
2
8
TIMEF
—
52
0, 28, 55
0, 55
—
87, 131
—
—
—
0, 55
—
0, 52
—
—
—
—
—
65
—
—
—
87
—
22
87
0, 55
—
0, 52
—
—
131
35, 70
—
0, 55
—
0, 33, 55, 87
—
—
—
5, 11, 22, 44
—
—
0, 55
—
—
0, 42
0, 55
—
P_Slag
44
—
0, 49
—
—
—
33
52
52
—
—
0, 52
—
35
33
52
—
52
87
0, 33, 65
—
—
6, 17, 26
—
79
—
0, 52
0, 52
52
—
—
—
—
—
—
—
—
0, 65,131
—
5, 11, 22,44
—
0, 87
—
—
44
0, 42
0, 55
44
P_Rphos
—
—
—
0, 55
17, 35, 52, 70, 88, 105
—
—
—
—
—
26, 52
0, 26, 52
17, 35, 52
—
—
—
28, 55
—
—
—
17, 35, 52
—
—
—
—
—
0, 52
—
—
0, 55
—
—
0, 20
—
17, 35, 52
—
17, 35, 52
—
28, 55
5,11, 22, 44
17, 35, 52
—
—
—
—
—
0, 55
—
P_Sphos
120
—
0, 60
0, 160
—
—
25
47
47
0, 80
—
—
—
—
25
—
—
0, 240
50
0, 220
—
165
—
75
0, 280
0, 78
—
—
—
0, 150
50
0, 15
0, 45
0, 130, 142
—
—
—
50
—
2.5, 5, 10, 20
—
0, 100
0, 80
0, 60
120
0, 36
0, 100
—
N
135
—
0, 60
0, 125
—
—
35
—
—
0, 125
—
—
—
—
34
—
—
220
200
—
—
140
—
50
212
0, 130
—
—
—
0, 125
—
80, 160
0, 45
0, 125
—
—
—
80
—
0, 12.5, 25, 50, 100
—
—
0, 125
—
135
0, 96
0, 125
—
K
C130, HT, VOL
—
C130, HT, VOL
C130, HT, BA, VOL
C130, HT
C130, VOL
C130, HT, VOL
C130
C130
C130, HT
C130, HT, VOL
C130, HT, VOL
HT
HT
—
HT
C130
HT, BA, VOL
—
—
HT
C130, HT, VOL
HT
BA
HT, BA
C130, HT, BA, VOL
C130, HT
C130, HT
C130, HT, VOL
—
C130, VOL
HT, VOL
—
C130, HT, BA, VOL
HT
HT, BA, VOL
HT
HT, VOL
C130
C130, HT, VOL
HT
C130, HT, VOL
—
C130, HT
HT
—
—
C130
CUMUL
—
C130
—
VOL
—
—
C130, HT, VOL
C130
C130
—
—
—
HT
HT
C130
HT
C130
BA, VOL
BA
BA, VOL
HT
VOL
HT
C130
BA
C130
—
C130
VOL
BA
—
—
HT
VOL
—
HT, BA, VOL
HT
VOL
C130
—
—
C130, VOL
HT
C130, HT
—
BA
HT
C130, VOL
INCREM
Source, referenced in Journal of Citations Reports (JCR), unpublished (Unpubl.), or gray literature; Class, site class is either Humid, Mesic, or Dry moorland or dunes; AGEF, age in years of the stand at time of fertilizer
application; TIMEF, years since fertilizer application; P_Slag, rate in kg P ha⫺1 applied as P slags; P_Rphos, rate in kg P ha⫺1 applied as rock phosphate; P_Sphos, rate in kg P ha⫺1 applied as superphosphates; N, N
added or not, if added then values indicate modalities without N (0) or with N (kg ha⫺1 added); K, K added or not, if added then values indicate modalities without K (0) or with K (kg ha⫺1 added); CUMUL, type of
cumulative information used, i.e., circumference at 130 cm (C130), height (HT), volume (VOL), or basal area (BA); INCREM, type of incremental information used. Controls exist for each of the sites (not indicated
separately).
Name of site
Description of sites and information used in the analyses
No.
Table 1.
Table 2. Number of observations exploited for fertilization on cumulative growth (% gain), AGEshift (years gained), and
incremental growth (% gain) compared with control treatments
Composition
Variable
C
P
PK
PN
PNK
P⫹
N
NK
K
P⫺
Total
Cumulative
AGEshift
Incremental
38
31
34
53
46
32
6
5
8
11
9
17
26
24
27
96
84
84
3
3
6
4
4
7
0
0
0
7
7
13
141
122
131
P form
Cumulative
AGEshift
Incremental
Site class
P_Slag
P_Rphos
P_Sphos
Du
Dr
M
H
Total
36
31
32
29
26
27
31
27
25
0
0
7
23
19
32
23
15
21
95
88
71
141
122
131
The number of observations for fertilizer composition, for the type of phosphorus form and type of site class are presented for each of the three variables.
For composition the numbers of observations refer to Control (C), to P, N, or K only treatments (P, N, and K, respectively), or to combinations of treatments
(PK, PN, PNK, and NK), adding up to the total number in the right column. P⫹ refers to all treatments having P and P⫺ refers to all treatments without
P. The number of observations for the P⫹ treatments are given separately for each phosphorus form, i.e., P slags (P_slag, rock phosphates (P_Rphos), or
superphosphates (P_Sphos) (cf. Table 1; see text for further information). The total number of observations for each of the three variables is also presented
per site class: dunes (Du), dry moorland (Dr), mesic moorland (M), and humid moorlands (H).
effects. For this we used two different tests. To identify
significant contrasts between a given fertilizer treatment and
controls, the Dunnett test was applied. For the evaluation of
different mean fertilizer effects for different TIMEF, AGEF,
form of fertilizer, composition of fertilizer, or site class
groups we used the Bonferroni t test. The two tests for
examining fertilizer effects were applied either on the entire
data set or on a subset of a given fertilizer composition (P⫹
or P⫺), a given range of TIMEF or AGEF classes (i.e., 0 – 4,
5– 8, 9 –16, 17–25, and 26 – 45 years for TIMEF and 0 –5,
6 –20, and 21–55 years for AGEF) or given site classes (i.e.,
humic and mesic moorlands). In this second stage of the
analysis of fertilizer effects on the AGEshift value, ANAGEshift was also investigated (annual reduction in rotation
length in yr yr⫺1).
Results
Cumulative Percent Growth Response
The summary statistics for cumulative percent growth
response are presented in Table 3 and show that site class
had the strongest effect on cumulative growth (P ⫽ 0.0007).
The effects of TIMEF (P ⫽ 0.054), AGEF (P ⫽ 0.058), and
P rate ⫻ site class interaction (P ⫽ 0.065) also contributed
to the explanation of observed differences in cumulative
growth. Only variations in cumulative growth with site class
and TIMEF for different AGEF classes for P⫹ treatments
are shown in Figure 1. Dry moorland sites (dune sites were
not available for this variable) did not respond to P⫹
treatments, whereas mesic and humid moorland sites
(merged for the purpose of illustration) responded positively
to P⫹ treatments up to a TIMEF of approximately 20 years,
with the greatest response in the lowest AGEF classes. The
effects of different site classes and P⫹ treatments versus
P⫺ treatments on cumulative percent growth response are
presented in Table 4. This table shows that for AGEF ⬍ 20
years and TIMEF ⬍ 20 years, P⫹ had a strong positive
effect on cumulative percent growth response on mesic
(⫹78%; P ⫽ 0.012) and humid moorlands (⫹71%; P ⫽
0.006), but not on dry moorlands (P ⫽ 0.34). Overall, P⫹
treatments showed a strong positive effect (P ⫽ 0.0001) on
cumulative growth relative to control treatments, whereas
P⫺ treatments did not differ significantly (P ⫽ 0.42) from
control treatments (Table 4). Additions of N or K together
with P had no further stimulating effect on cumulative
volume growth (Table 3). Surprisingly, the P rate had no
Table 3. Summary statistics for a generalized linear model on cumulative growth, AGEshift, and incremental growth compared
with control treatments
P
Source
Cumulative growth
(n ⫽ 141) (% gain)
AGEshift (n ⫽ 122)
(years gained)
Incremental growth
(n ⫽ 131) (% gain)
TIMEF
AGEF
Site class
P rate
P form
AGEF ⫻ TIMEF
P rate ⫻ N rate
P rate ⫻ K rate
P rate ⫻ site class
0.054
0.058
0.001
0.229
0.508
0.361
0.539
0.751
0.065
0.000
0.514
0.007
0.885
0.021
0.493
0.521
0.559
0.074
0.000
0.011
0.795
0.900
0.110
0.247
0.866
0.818
0.585
For the cumulative and incremental growth variables, a log transformation was applied before the generalized linear model was run. For AGEshift, a log
on (AGEshift ⫹ 2) was applied before the model was run. For each of the three variables P values are presented.
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Forest Science 55(5) 2009
but differences between the three forms were not significant
(P ⫽ 0.39).
Incremental Percent Growth Response
Figure 1. Cumulative gain in growth compared with controls
for all treatments containing P (Pⴙ) as a function of TIMEF.
significant effect on cumulative percent growth response,
suggesting that even the lowest range of P fertilizer rates
reached a cumulative growth that was equivalent (i.e., not
significantly different) to the higher P rates applied (data not
shown separately).
AGEshift Effects
The main AGEshift effects are presented in Table 3 and
reveal a significant effect of TIMEF (P ⬍ 0.0001), site class
(P ⫽ 0.0007), and P form (P ⫽ 0.021) and some further
effect of the P rate ⫻ site class interaction (P ⫽ 0.074) on
the AGEshift value. In general, the P⫺ treatments (N and
NK) generally did not have a positive effect on the AGEshift
value (Figure 2, open symbols). Treatments containing N or
K in addition to P followed the same pattern as those
containing P alone. On average, the final AGEshift values
ranged from 3 to 5 years, and these were reached 10 –17
years after fertilization, after which no further increases
appeared (Figure 2). The AGEshift values as a function of
TIMEF for P⫹ treatments alone are shown in Figure 3 and
separate the three moorland classes available in the data set.
This figure shows that the dry sites differed from the mesic
and humid moorlands in that there was no, or only a limited,
effect of treatments on the AGEshift value at dry moorland
sites in contrast to the effects on the other two site classes.
The statistical effect of different site classes and P⫹ versus
P⫺ treatments on the AN-AGEshift value is presented in
Table 4. This table shows that for AGEF ⬍ 20 years and
TIMEF ⬍ 20 years, P⫹ significantly affected the ANAGEshift value on mesic (P ⫽ 0.017) and humid moorlands
(P ⫽ 0.0001) but not on dry moorlands (P ⫽ 0.64). P⫹
treatments had a significant effect on the AN–AGEshift
values (P ⬍ 0.0001), whereas the effects of P⫺ treatments
did not differ significantly from those of the control treatments (P ⫽ 0.20). The significance of the form of P in the
general model (Table 3) appeared to be related to the fact
that proportionally superphosphates were applied more often to dry moorlands, which were shown to be less responsive. Therefore, we restricted the data set to humid moorlands to investigate the effects of the form of P on the
AN–AGEshift value. This investigation showed that all three
forms of P had a significant effect (P ⬍ 0.0001) (Table 5),
Incremental percent growth responses were significantly
scaled to time effects, i.e., TIMEF (P ⬍ 0.0001) and AGEF
(P ⫽ 0.011), whereas site class, P rate, P form, and interactions were not significant (Table 3). However, a separate
analysis of P⫺ versus P⫹ treatments helped the interpretation of the time effects. The P⫺ treatments were never
significant and the change in incremental percent growth
response was ⫺7 to ⫹5% for humid, mesic, and dry moorland sites, and ⫹42 ⫾ 28% change for dune sites (n ⫽ 2
observations), indicating some potential for N-based fertilizers at these sites (data not shown separately). For a more
specific investigation of TIMEF effects, the data set was
restricted to P⫹ treatments and showed weakly significant
to significant positive effects on incremental percent growth
response up to a TIMEF of 16 years (P ⫽ 0.0046 to P ⫽
0.080) (Table 6). Beyond 16 years, incremental growth was
not significantly affected (P ⫽ 0.32; TIMEF ⫽ 17–25 years)
or even negatively affected (P ⫽ 0.049; TIMEF ⫽ 26 – 45
years). To evaluate the effects of AGEF, the data set was
restricted to TIMEF ⱕ16 years and P⫹ treatments with the
exclusion of dune sites (Table 6). This evaluation showed
that incremental percent growth response was affected in all
of the three AGEF classes (P ⫽ 0.0102 to P ⫽ 0.073) but
was significantly higher in young stands (AGEF 0 –5 years)
than in older stands (AGEF 21–55 years) (P ⫽ 0.0412).
Discussion
General Considerations
Gurevitch and Hedges (1999) put forward two potential
biases for meta-analyses: a publication bias and a research
bias. The former originates from the tendency that results
which are statistically significant are more likely to be
published than those which are not significant. In our case,
most of the data were found in unpublished reports or in
local to national publications. We therefore assumed that the
publication bias was unlikely to exert a marked influence on
the composition of the present data set. The latter bias is the
result of the tendency to perform experiments on topics that
have a reasonable expectation of detecting statistically significant effects. This is probably the case for our fertilization trials. The initial results from the Landes de Gascogne
forest showed a significant positive effect of P on pine
growth (Guinaudeau et al. 1963), no significant effect of K
or N (Guinaudeau et al. 1963), and a negative effect of lime
(Duchaufour and Guinaudeau 1957). Consequently, most of
the indexed trials we found concern P fertilization. However, the research bias may be of particular importance
when results of the meta-analysis are extrapolated outside
their original context (Gurevitch and Hedges 1999). It is
thus important to be aware that the results of the present
meta-analysis are context-dependent. Hence, they should
not be directly extrapolated to other regions even though we
use them as a basis for comparison with other P-deficient
and intensively managed pine ecosystems.
The data set represented the forest area of the Landes
Forest Science 55(5) 2009
395
Table 4. Specific effects of fertilization on cumulative growth and annual shift in age (AN–AGEshift) compared with controls for
site class and P rate
Cumulative growth
Site class
Dry
Mesic
Humid
P⫹ versus P⫺
P⫹
P⫺
Controls
AN-AGEshift
n
Mean (SE)
(% gain)
Dunnett
Bonferroni
n
Mean (SE)
(yr yr⫺1)
Dunnett
Bonferroni
14
12
59
15 (11)
78 (13)
71 (13)
n.s.
*
**
a
b
b
12
10
56
0.02 (0.03)
0.26 (0.06)
0.20 (0.02)
n.s.
*
***
a
b
b
96
7
38
57 (8)
4 (12)
0
***
n.s.
a
b
78
5
29
0.18 (0.02)
0.10 (0.07)
0
***
n.s.
a
a
Site class effects were evaluated with the restriction to AGEF ⬍ 20, TIMEF ⬍ 20, and P⫹ treatments. This concerned n ⫽ 85 observations for cumulative
growth (60% of all observations) and n ⫽ 78 observations for AN–AGEshift (64% of all observations). P⫹ versus P⫺ effects were evaluated using n ⫽
141 observations (no restriction, 100% of observations) for cumulative growth and using n ⫽ 112 observations (restriction to TIMEF ⬍ 20; 92% of
observations) for AN–AGEshift. Symbols for the Dunnett test: ***P ⬍ 0.001; **P ⬍ 0.01; *P ⬍ 0.05; n.s., not significant (i.e., P ⬎ 0.10). Different letters
in the Bonferroni test column denote significant differences between classes at P ⬍ 0.05 or less.
Table 5. Specific effects of fertilization related to form of
phosphorus on the annual shift in age
Phosphorus
form
n
Mean (SE)
Dunnett
Bonferroni
P_Slag
P_Rphos
P_Sphos
24
18
20
0.20 (0.02)
0.22 (0.02)
0.17 (0.03)
***
***
***
a
a
a
Presented are mean values (SE) for AN-AGEshift (gain in yr yr⫺1 relative
to control treatments). P_Slag, P slags; P_Rphos, rock phosphates;
P_Sphos, superphosphates. The data set was restricted to P⫹ and site
class ⫽ humid moorland (n ⫽ 62; 74% of observations). Symbols for the
Dunnett test: ***P ⬍ 0.001. Different letters in the Bonferroni test
column denote significant differences between phosphorus forms at P ⬍
0.05 or less.
Table 6. Specific effects of fertilization on incremental
growth for different periods of TIMEF and AGEF
Figure 2. AGEshift in years as a function of TIMEF for each
fertilizer combination for three site classes.
TIMEF
0–4 yr
5–8 yr
9–16 yr
17–25 yr
26–45 yr
AGEF
0–5 yr
6–20 yr
21–55 yr
n
Mean (SE)
Dunnett
Bonferroni
26
24
25
5
4
67 (24)
80 (28)
64 (12)
14 (10)
⫺33 (5)
关*兴
关*兴
***
n.s.
*
a
a
a
a
a
21
33
17
125 (31)
62 (18)
40 (12)
*
关*兴
*
b
ab
a
Mean values (SE) refer to % gains relative to control values. For TIMEF
the data set is restricted to P⫹ treatments (n ⫽ 84; 64% of observations).
For AGEF the data set is restricted to TIMEF ⬍ 16 yr, P⫹, and all site
classes except Dunes (n ⫽ 54; 41% of observations). Symbols for
Dunnett’s test: ***P ⬍ 0.001; *P ⬍ 0.05; 关*兴P ⬍ 0.10; n.s., not
significant (i.e., P ⬎ 0.10). Different letters in the Bonferroni test column
denote significant differences between classes at P ⬍ 0.05 or less.
Figure 3. AGEshift in years as a function of TIMEF for humid, mesic, and dry moorland sites (no observations for dunes
in the data set) for Pⴙ treatments only.
well, although humid moorlands (27 trials, 56%) were
somewhat overrepresented and dunes (1 trial, 2%) were
underrepresented (Trichet et al. 1999: of the total area,
humid moorlands cover 44%, mesic moorlands 33%, dry
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Forest Science 55(5) 2009
moorlands 14%, and dunes 9%). Phosphorus fertilizers (P
only or P with N or K) resulted in a significant improvement
in cumulative growth on mesic and humid moorlands but
not on dry moorlands. This finding implies that for 77% of
the forested area of this P. pinaster forest (on mesic and
humid moorlands), P fertilization appears to be a valid
option for increasing overall forest productivity. This finding is in agreement with increases in productivity observed
by foresters since the introduction of P fertilizers to forestry
practice (Thivolle-Cazat and Najar 2001). The highest values for cumulated growth generally ranged between 100 and
250% relative to controls for sites fertilized at stand establishment (at a stand age 0 –5 years) in the first 10 –12 years
after fertilization. Values at the end of the rotation cycle
(34 – 42 years after P fertilization on mesic and humid
moorlands) ranged from 23 to 42% increase in cumulative
percent growth (Figure 1). These results were consistent
with those of other studies carried out on P-deficient soils.
Wells et al. (1986) observed 50 –140% increases in tree
height 5 years after P application to the most P-deficient
Pinus taeda stands in the Lower Coastal plains, and Payn
and Clough (1988) reported 50 –190% increases in height
growth of three pine species (including P. pinaster), 5 years
after P application on the most P-reactive sites in South
Africa. In the first 20 years after fertilization, the cumulative
percent growth response to P was much stronger in the
mesic and humid moorland sites than in the dry site classes.
This observation is in agreement with several experiments
in the United States (Pritchett and Comerford 1982, Wells et
al. 1986, Borders et al. 2004, Fox et al. 2006) and Australia
(Lewis and Harding 1963) where the effects of P fertilization at the wetter sites were either longer-lasting or of a
greater magnitude than those at the better drained sites.
However, water availability in itself may not explain the
differences in response in our study region in southwestern
France as suggested by Saur (1989a). This author used soils
from dunes, humid moorland, and dry moorland sites in a
pot experiment to evaluate the growth of P. pinaster seedlings in response to calcium carbonate amendments, P fertilization, and the addition of trace elements. He showed
that even when water was not a limiting factor and fertilizers were supplied, seedlings on humid moorland soils
showed a growth gain which was 5 to 6 times higher than
that of those grown on soils from drier sites. This result
suggests that other factors, such as the organic fraction, soil
solid phase, microorganisms, or other nutrients not included
in the fertilizer, are responsible for the differences in growth
performances between the site classes. More recently, annual water and nutrient manipulation experiments showed
that the effect of fertilization on tree productivity overruled
that of irrigation in a humid moorland subject to summer
droughts in southwestern France (Trichet et al. 2008) and in
an experimental site in the United States featuring comparable climatic and soil conditions (Albaugh et al. 2004). In
our coastal forested dunes, tree growth could be more limited by N than by any other nutrient (Illy 1964). Indeed, the
mean Ntotal/Ptotal ratio in the upper 100 cm of the soil was
close to 1 in the coastal dune soils in our study area (L.
Augusto and M. Bakker, unpublished data, Sept. 6, 2005),
whereas the same ratio was between 6 and 8 in the inland
moorland soils (Augusto et al. 2006), indicating low N
fertility in the dunes. The limited representation of dunes in
our data set did not permit us to investigate this finding.
Forms and Rates of Fertilizers
As in the study of Pritchett and Comerford (1982) on
Pinus elliottii in Florida, the form of P fertilizer did not have
a significant impact on the outcome of P addition for any of
the tree productivity variables in our study. Conversely,
McLaughlin and Champion (1987) and Donald (1990) reported strong interactions between the form of P fertilizer
and plant response for ryegrass and pines. McLaughlin and
Champion (1987), using two sesquioxic P-deficient soils
from South Africa in a pot experiment lasting 209 days,
found that sewage sludge acted as a slow-release P fertilizer
for ryegrass and that it was as effective as inorganic P
fertilizers. Although inorganic P fertilizers resulted in
higher plant uptake rates at the beginning of the experiment,
sludge-amended soils were able to maintain higher P uptake
rates over time. These authors assumed that either the organic P fraction in the sludge enabled a more gradual
release of P or that the organic fraction interfered with the
P adsorption sites (cf. Attiwil and Adams 1993, Hunt et al.
2007) or that the sludge was involved in some other chemical interaction resulting in increased P availability to plants
over time (McLaughlin and Champion 1987). In contrast
with our study, Donald (1990) reported that the more soluble forms of P fertilizers had the quickest effect, whereas the
less soluble forms had the advantage in the long-term.
Overall, superphosphates had more effect than the other
forms in South Africa (Donald 1990). Possibly, the restriction to using only the latest available record of each site and
treatment in the current study (cf. considerations on metaanalysis for independence of data) obscured potential differences between forms of P in the short term, i.e., within
the first year or a few years after fertilization. This may be
the case particularly when the variable we evaluated was
cumulative growth, as the sum of rapid short-term plus slow
medium-term effects of a fast-release P fertilizer on tree
growth might be the same as slow short-term plus sustained
medium-term effects of a slow-release P fertilizer. Perhaps
the size and reactivity of the adsorption sites (Holford 1997)
are more important under our conditions (soils and time
span considered, i.e., 1– 41 years since fertilization) than the
release rate of different forms of fertilizer.
The rate of P fertilization was not very important in our
study, suggesting that even the lowest range of P fertilizers
applied, i.e., 17–35 kg of P ha⫺1, was sufficient to obtain a
significant improvement in cumulative growth. Higher rates
did not yield a significantly higher growth response. Our
results, showing the absence of an effect of P rate, are
similar to those reported by Donald (1990) in fertilization
trials in South Africa, where the P response was not linear
relative to the P rate. Comerford et al. (2002) compared the
long-term P fertilizer effects on soil P levels and tree productivity in P. taeda in Georgia (United States) and in Pinus
radiata in New Zealand. They found the effect of P to be
larger in Georgia, where a lower rate of P application was
sufficient to stimulate stand productivity and to enhance the
bioavailability of P in the soil. This result is comparable to
the absence of any clear rate effect in the Landes of Gascogne in the present study. At the New Zealand site, however, a clear rate effect appeared, which was due to the high
P adsorption capacity of the soils, and 125 kg of P were
needed to increase soil P levels significantly. Fox et al.
(2006) also showed an effect of P rate (comparing 0, 28, and
56 kg of P ha⫺1) on pines in southeastern United States for
rates of 0 to 111 kg of N ha⫺1, whereas the P rate effect was
Forest Science 55(5) 2009
397
less apparent at higher N rates (i.e., 28 and 56 kg of P ha⫺1
produced nearly the same result). The latter results are
comparable to our situation with higher N availability on the
humid moorland sites where no clear effect of P rate was
observed.
In addition to P, levels of other major and trace nutrients
are also very low in the soils of the Gascogne area (Saur
1989b), and one would thus have expected that growth
response to N and/or K in addition to P would have been
greater than that of treatments with P alone. The growth
response to P alone (compared with controls) was the highest, whereas an additional growth response from adding N,
K, or both to P was not shown to be significant. In South
Africa, N and K alone had no effect but resulted in a limited
further growth effect when P requirements were met first
(Donald et al. 1987, Donald 1990), suggesting that P was
the main growth-limiting nutrient there. Conversely, Fox et
al. (2006) demonstrated a clear effect of N rate and advocated the benefits of N ⫹ P fertilizers for mid-rotation P.
taeda (i.e., 8 –20 years old) in the southeast United States, as
long as any gross P deficiencies had been corrected at or
soon after planting. Our data set did not enable us to come
to a conclusion about any N ⫹ P effects in older stands with
a good P supply, as indicated by Fox et al. (2006), either
naturally or because of P application at stand establishment,
as all our trials in which different nutrients could be compared were based on applications made at the same time.
Some of the previous studies in the region based on individual trials in which different nutrients were compared
showed that any additional effects of N or K occurred only
in the first few years after fertilization (Saur 1989a, Bonneau 1995). However, these effects were not significantly
detectable in our meta-analysis. One probable explanation
for this result is that our soils have a very low cation
exchange (Augusto et al. 2006) and cannot be expected to
adsorb a sufficient amount of cations (e.g., NH4⫹ and K⫹)
and subsequently supply them to the trees, whereas NO3⫺
can be leached easily. In addition, N can be fixed by
European gorse (Ulex europaeus L.) which is present in the
understory of the pine forest throughout the region. This
species is particularly abundant during the young stages of
stand development (Lee et al. 1986). It has been shown for
this region that on average 70% of the N immobilized in
Ulex comes from symbiotic fixation (Cavard et al. 2007),
and it forms more biomass with increasing P availability,
e.g., after P fertilization (Augusto et al. 2005). This finding
may explain why fertilizing with N and/or K at stand
establishment, despite likely soil deficiencies, does not
show tree growth responses because either these elements
are not retained in the soil or they continue to be supplied by
symbiotic fixation (in the case of N). However, in the case
of annual optimization of fertilizer inputs (P alone or a
NPKCaMg treatment; both applied at a much higher rate
than the studies evaluated in this work), the NPKCaMg
treatment resulted in significantly higher growth responses
than the P only treatment compared with controls, suggesting that additional elements can further increase tree productivity at least in the short term (Trichet et al. 2008),
provided that supplies are adequate. Thus, we cannot exclude the possibility that other nutrients besides P, i.e., N or
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Forest Science 55(5) 2009
K, may significantly stimulate growth even under our
growth conditions, when supplied at sufficient rates, as
repeated applications (Trichet et al. 2008) or at a later stage
of development (Fox et al. 2006).
Stand Age and Duration of Fertilizer Effects
The effect of P fertilization on the incremental growth of
P. pinaster was strong in the first 16 years after application
in all stand age classes, although it was the most pronounced
in the youngest stands. The AGEshift values also showed an
increase in the first 10 –12 years after fertilization, but
beyond 15 years no further increase occurred. This finding
suggests that stimulation of current growth by P fertilizers
lasts for approximately 15–20 years in the forest and fertilization contexts of our study. Previous studies evaluating
current tree ring increments at sites 3 and 26 showed that the
effects of P fertilization lasted for up to 22 years and neither
dry summers nor severe winters explained the decrease in
the effect of P fertilization on current growth over time
(Lemoine 1993, Vauchel 1996). The observation that stimulation of current growth by P fertilizers ceased after approximately 15–22 years is not new, and comparable observations exist elsewhere for pine species for which effects
were generally seen to cease after 20 –35 years (Mead and
Gadgil 1978, Pritchett and Comerford 1982, Lowell 1988;
de Ronde and Donald 1993, Comerford et al. 2002, Fox et
al. 2006).
The age and developmental stage of a tree stand at the
time of fertilizer application is often proposed as a key issue
when fertilizer effects are discussed and interpreted (Miller
1981, Fox et al. 2006). According to this concept, the
general productivity of trees declines with increasing stand
age as trees develop, grow taller, and possibly suffer from
hydraulic limitations to maintain productivity (Ryan et al.
1997, Binkley et al. 2002, Delzon and Loustau 2005, Delzon et al. 2005, Martinez-Vilalta et al. 2007), so that the
developmental stage rather than nutrient availability will
determine relative growth performances. Miller (1981) proposed that fertilized stands would initially be ahead in
development (a reduced rotation length, cf. our AGEshift),
but that they would eventually return to the same growth
curve as the control stands. Bonneau (1995) argued that this
proposal was probably more relevant to N fertilizers as N is
much more mobile than P, which can be bound to organic
compounds, aluminum, or iron oxides (Holford 1997, Vimpany et al. 1997). The rationale behind this core of literature
on fertilization and the developmental stage is that young,
open stands with root systems that are not fully established
and lower leaf area will profit more from an application of
fertilizer than older stands whose growth will gradually
slow down because of increased maintenance costs, respiration losses, hydraulic limitations, or interspecific competition or because they can benefit from internal retranslocation of nutrients to newly formed needle cohorts. A
considerable consensus exists that a large part of the variation in biomass and wood production results from variation
in light interception, i.e., a variation in the amount of leaf
area and/or leaf area efficiency (Fox et al. 2006). Thus, if P
fertilization results in a higher leaf area or leaf area efficiency in P. pinaster in this region, then it is likely that P
fertilizers increase biomass production, at least as long as
they remain ahead of control trees (Miller 1981). Local
evidence on such a relationship does exist. Three different
studies on P. pinaster in our region showed that leaf photosynthetic capacity benefited from P fertilization in a seedling experiment (Loustau et al. 1999), that photosynthetic
capacity was correlated to needle P in a chronosequence
approach (Delzon et al. 2005), and that P-induced increases
in leaf area index and growth efficiency were maintained up
to at least age 11 years (Trichet et al. 2008).
Following Miller’s (1981) assumption that fertilization
results in an increase in development before returning to the
same growth curve as the control stands with time, it is not
unreasonable to expect this to happen at, or shortly after,
maximum stand growth (full canopy closure). Where the
control stand is subject to a time lag and will thus be located
on the increasing part of the growth curve, the fertilized
stand will already be beyond the point at which annual
growth starts to slow down. Decreases in growth efficiency
in P. pinaster were suggested to occur somewhere between
age 18 and 32 years (Delzon and Loustau 2005, Delzon et
al. 2005), in Pinus sylvestris after the age of 20 (Mencuccini
and Grace 1996), and in P. taeda after the age of 17
(Albaugh et al. 2004) but have been reported to have occurred before the age of 15 in P. taeda and P. elliottii
(Jokela and Martin 2000). We may thus expect different
effects of fertilizers applied to young trees (i.e., up to 20
years of age when fertilizers were received) compared with
those for older trees. In the southeastern United States, P
fertilizer application to pine trees was recommended essentially for young stands with a very low level of soil P (Fox
et al. 2006). In the present study, P fertilization had an effect
on incremental growth even when the fertilizers were applied to older stands, although the increase was lower when
applied to these stands (21–55 years old) than to younger
stands (0 –5 years old). In our study, the intensities of
thinning and weed control were similar between controls
and fertilizer treatments as far as we know and were not
likely to interfere with the fertilizer responses observed
within at least the first 10 –15 years since fertilization. On
the contrary, in the absence of weed control, the fertilizer
response can be expected to be lower, as a part of the
nutrients will be incorporated in the understory vegetation.
Martinez-Vilalta et al. (2007) suggested that even very old
P. sylvestris trees (⬎200 years old) were able to revert to a
growth efficiency level equivalent to that of young trees,
once released from competition. Miller (1981) also suggested that fertilizing older stands could be efficient if
nutrients immobilized in the soil organic matter had become
unavailable for tree growth. This corroborates our observation that even older stands can respond to P fertilizers.
Therefore, stand developmental stage may contribute to the
explanation of the decrease in overall productivity and of
fertilizer effects with age in our study region, but all of the
observed decreases in the effect of P fertilization probably
cannot be explained by the developmental stage of the stand
alone.
Although stand developmental stage is thus likely to
interact with the effects of fertilization observed over time
as it is linked to stand nutrient requirements, two further
hypotheses can be proposed to explain why the P fertilizers
ceased to yield higher tree productivity over time. The first
hypothesis suggests that both nutrient availability and nutrient requirements change throughout stand development
(Kimmins 1974, Miller 1981, Bonneau 1995, Albaugh et al.
1998, Ranger and Turpault 1999, Jokela and Martin 2000,
Albaugh et al. 2004, Fox et al. 2006). The observation of
higher foliar P levels together with very low foliar N levels
at a long-term monitoring site 38 years after P application
(Nys et al. 1995, 1996) corroborates this theory. Also,
where fertilizers were applied annually, the complete fertilizer treatment (with N and K) resulted in significantly
higher increases in growth compared with P only treatments
(Trichet et al. 2008) up to 11 years old, which further points
to the role of other nutrients in this context. In the southeastern United States, Fox et al. (2006) reported the highest
response of pine stands to N ⫹ P fertilizers at canopy
closure and maximum growth rate (mid-rotation, i.e., 8 –20
years old). However, in our data set, N and/or K applications were applied at the same stand age as P and were not
being applied regularly at the time when the stand could be
assumed to have had the highest requirements for these
nutrients (cf. Fox et al. 2006). This is one possible explanation as to why the effects of N and K did not explain the
observed increases in tree growth due to fertilization to a
greater extent, but it may be that they explain why the
fertilizer effect finally ceases as N and K become more
limiting than P (see also Trichet et al. 1999 for an overview
of nutrient limitations in our study area).
The second hypothesis is that P fertilization resulted in a
stock of available P that is exhausted over time. Soil P levels
based on classic soil extractions (e.g., P-Olsen or PDuchaufour) were close to or slightly above control levels
more than 35 years after P fertilization (Nys et al. 1995),
whereas the influence of P fertilization on tree growth
(yearly increment values) had already ended after 20 years
at this site (Lemoine 1993, Vauchel 1996). This finding may
imply that classic soil extraction methods were not adequate
to account for the fraction of P that is still available to the
plant. Uptake by vegetation, trees, and the understory is one
possible pathway for P released from the fertilizers and may
explain the disappearance of soil P over time. Based on
Lemoine et al. (1988), Trichet et al. (2000), and Augusto et
al. (2005), we estimated that between 28% (in the case of a
rate of 52 kg of P ha⫺1, which is the most common case in
regular forestry) and 85% (for 17 kg of P ha⫺1) of applied
P may be taken up by the trees or the understory in the 16
years after fertilization. Part of this P may have been returned as organic P to the soil (Attiwil and Adams 1993),
but the remainder of the P applied should still be in the soil,
providing that its P adsorption capacity is sufficient. Indeed,
for three P fertilization trials on humid moorland with low,
moderate, and strong P effects on tree height, P fixation in
soils, assessed using an isotope dilution method (Morel et
al. 2000), was well correlated with the P growth response of
the trees (data not shown separately). When P is supplied as
a fertilizer on a more reactive soil, this increases the P
uptake potential and improves tree growth. Conversely,
Forest Science 55(5) 2009
399
when the soil is less reactive because of very low amounts
of iron and aluminum hydrous oxides (Holford 1997, Vimpany et al. 1997), P cannot be retained adequately and may
leach freely within the soil profile and, as a consequence,
will be less beneficial to tree growth. The duration of the P
fertilization effect should thus be linked to the capacity of
the soils to retain P. Therefore, the P exhaustion hypothesis,
along with the exhaustion of other nutrients that become
co-limiting with increasing stand development (Bonneau
1995, Fox et al. 2006), appears to be very plausible.
Conclusion
Our analysis showed that there was an overall improvement in tree productivity by P fertilization on the humid and
mesic moorland sites (which together comprise 77% of the
forested area concerned), but this was less marked on the
dry sites (dunes and dry moorlands: i.e., 23% of the area).
Other nutrients did not significantly increase tree growth.
The form of P fertilizer did not affect the response. A rate
of between 17 and 35 kg of P ha⫺1 applied at stand establishment was sufficient to stimulate tree growth, and higher
rates did not increase productivity proportionally. In addition to a gain in volume productivity (because of increased
thinning volumes and a higher stand volume at the final cut,
approximately 20 – 40% by the end of the rotation; cf.
Figure 1), foresters may also gain 4 –5 years in rotation
length. The duration of the effect of P fertilization on annual
increments appears to be variable (up to 20 years after
application in the best cases). The use of a metadata analysis
made it possible to confirm the general P effect and to refine
our knowledge regarding the age and time effects of fertilization but did not highlight any clear effects of other
nutrients. Differences in responsiveness to P fertilizers according to site class or stand age may be related to differences in the P-fixing capacity of the soils, to differences in
stand developmental stage, or to other limitations such as
nitrogen.
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