Resin tapping influence on maritime pine growth depends on tree age and stand characteristics

Abstract

Resin is a renewable forest resource that can increase the economic value of some forests in rural areas. Resin production is associated with climatic conditions. However, its impact on trees’ growth remains unclear. Here, we studied radial growth in six Portuguese Pinus pinaster forests that had been resin tapped for 5–7 years along a latitudinal and climatic gradient to understand whether resin tapping affects tree growth, and how it is affected by climate, stand and tree traits. Tree-ring width (TRW) on tapped and untapped trunk sides was compared before and during the tapping period. Tree-ring width decreased in the three youngest populations (< 30 years), with no changes in older populations (> 40 years), while TRW increased after resin harvesting began in the oldest stand (> 55 years). Annual resin-tapping impact (RTI), calculated as the ratio between TRW during tapping years and the 5-year average TRW before tapping, was below and above 1 in the younger and older stands, respectively. Among stand characteristics and across sites, RTI was negatively correlated with tree competition and positively correlated with TRW, cambial age, and tree height. Climatic conditions had a minor role on tree growth response to resin tapping. Our main conclusion is that the effect of resin extraction on growth is age-dependent. Our results encourage the co-production of resin and wood on maritime pine stands over 40 years old where resin extraction impact on growth is negligible.

Full text

Vol.:(0123456789)
1 3
European Journal of Forest Research (2023) 142:965–980
https://doi.org/10.1007/s10342-023-01568-7
ORIGINAL PAPER
Resin tapping influence onmaritime pine growth depends ontree age
andstand characteristics
MikaelMoura1 · FilipeCampelo1· CristinaNabais1· NúriaGarcia‑Forner1
Received: 22 April 2022 / Revised: 9 February 2023 / Accepted: 3 April 2023 / Published online: 22 April 2023
© The Author(s) 2023
Abstract
Resin is a renewable forest resource that can increase the economic value of some forests in rural areas. Resin production is
associated with climatic conditions. However, its impact on trees’ growth remains unclear. Here, we studied radial growth
in six Portuguese Pinus pinaster forests that had been resin tapped for 5–7years along a latitudinal and climatic gradient to
understand whether resin tapping affects tree growth, and how it is affected by climate, stand and tree traits. Tree-ring width
(TRW ) on tapped and untapped trunk sides was compared before and during the tapping period. Tree-ring width decreased
in the three youngest populations (< 30years), with no changes in older populations (> 40years), while TRW increased after
resin harvesting began in the oldest stand (> 55years). Annual resin-tapping impact (RTI), calculated as the ratio between
TRW during tapping years and the 5-year average TRW before tapping, was below and above 1 in the younger and older
stands, respectively. Among stand characteristics and across sites, RTI was negatively correlated with tree competition and
positively correlated with TRW , cambial age, and tree height. Climatic conditions had a minor role on tree growth response
to resin tapping. Our main conclusion is that the effect of resin extraction on growth is age-dependent. Our results encourage
the co-production of resin and wood on maritime pine stands over 40years old where resin extraction impact on growth is
negligible.
Keywords Maritime pine· Resin tapping· Tree-ring width· Radial growth· Cambial age
Introduction
Resin tapping and harvesting is a traditional forestry activ-
ity that provides economical profit to rural populations and
other services like fire surveillance and sustainable forest
management (Pereira 2015; Soliño etal. 2018). Currently,
there is a new demand for natural resin (Génova etal. 2014)
leading to a price increase and to the resurgence of the activ-
ity in places where it was almost abandoned, such as in the
Iberian Peninsula (Girón, 2021).
Pine resin extraction has been usually done alongside
timber production in the Mediterranean basin (Soliño
etal. 2018), especially in Portugal and Spain, where Pinus
pinaster Aiton is the main species used for resin harvest-
ing. Despite this, it has been hypothesized that secondary
metabolism and growth may be competing for the available
photosynthates (Züst & Agrawal 2017) and thus, repeated
mechanical resin tapping could be stimulating resin bio-
synthesis at the expense of other carbon-dependent pro-
cesses such as wood production (Du etal. 2021). Support-
ing this idea, lower growth rates and narrower tree-rings,
as an estimate of biomass production, have been found in
resin tapped pine stands (Papadopoulos 2013; Génova etal.
2014; Chen etal. 2015; Zeng etal. 2021). Papadopoulos
(2013) showed a reduction of 14% in tree-ring width (6% of
latewood) in tapped Pinus halepensis Milltrees, compared
with non-tapped ones. Zeng etal. (2021) also found negative
effects of resin harvesting on tree-ring width of Pinus tabu-
liformisCarr, although it only persisted for two years after
the extraction ended. But, positive (Tomusiak & Magnusze-
wski., 2013; van der Maaten etal. 2017) or no resin tapping
effects (Rodríguez-García etal. 2015; Du etal. 2021) on
tree-ring formation have also been reported, suggesting low
Communicated by Thomas Seifert.
* Mikael Moura
mikael.moura@student.uc.pt
1 Centre forFunctional Ecology – Science forPeople &
thePlanet, Department ofLife Sciences, University
ofCoimbra, Calçada Martim de Freitas, 3000–456Coimbra,
Portugal
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

966 European Journal of Forest Research (2023) 142:965–980
1 3
carbon competition between growth and resin, which accord-
ing to Hilty etal. (2021) can be considered as growth sensu
latu—the combination of reversible and irreversible biomass
or volume changes. Growth stimulation in tapped trees could
also reflect reaction tissues if annual growth was measured
too close to the tapping wound.
The contradictory results found in the literature concern-
ing resin extraction effects on wood production might be also
related to the studied species, the sampling design, and the
resin tapping method and intensity. For example, Zeng etal.
(2021) sampled both tapped and untapped sides to represent
the overall tree-ring growth and observed that resin tapping
in P. tabuliformis promotes asymmetrical radial growth,
with narrower rings near the tapped face, while Garcia-
Forner etal. (2021a, b) showed the opposite pattern in P.
pinaster. It was also observed that wood reaction to tapping
decreases when getting away from the wound upward as
shown in Pinus sylvestris L(Tomusiak & Magnuszewski.,
2013). Thus, resin extraction impact on growth will depend
on the sampling design performed (Williams 2017) hinder-
ing comparisons between studies. But even when the same
sampling procedure and species are used, other variables,
e.g., environmental conditions, can affect growth sensitivity
to resin harvesting (Garcia-Forner etal. (2021a, b).
Tree growth and resin production are both driven by envi-
ronmental conditions and depend on carbon availability to
produce new cells, which include the resin duct complex
formed by the resin canal and the adjacent resin-producing
epithelial cells that synthesize the defensive terpenoid mix-
ture. In P. pinaster, some studies connect favorable tempera-
tures, solar radiation and potential evapotranspiration with
increasing tree growth and resin duct traits or resin yield
(Rodríguez-García etal. 2014, 2015), variables that are phe-
notypically and genetically correlated (Vázquez-González
etal. 2019). However, literature is still scarce when it comes
to understand the resin tapping impact on wood production
under a climatic gradient, the key factor to identify the envi-
ronmental conditions that maximize both resin and wood
production. Another variable that should be considered is
the species provenance, as growth, as well as resin yield are
subjected to strong genetic control varying among families
and provenance regions (Vázquez-González etal. 2021). If
resin harvesting depletes carbon stocks, wood production in
fast-growing populations could be more susceptible to resin
extraction than in slow-growing ones (Zeng etal. 2021).
Stand and tree characteristics and forest management are
also important factors that should be considered since they
may determine resources availability at individual level, and
thus affect their growth rate and production of defenses. For
instance, at tree level, resin yield increases at lower stand
densities (McDowell etal. 2007; Rodríguez-García etal.
2014, 2015; Zas etal. 2020). In high density stands, trees
grow less, and smaller trees can be more affected (e.g., P.
tabulaeformis in He & Wang 2021) or end-up being less
resilient to drought (Fernández-de-Uña etal. 2015; Bottero
etal. 2017). The age of the trees affects their vitality, growth,
and their resin yield too. In this regard, Zas etal. (2020)
found that even if the mechanisms remain elusive, resin pro-
duction in P. pinaster increases as trees get older. Consider-
ing that in woody plants photosynthesis tends to decrease
with age (Yoder etal. 1994; Bond 2000), it is necessary to
understand whether resin yield increases as age increases
due to carbon allocation shifts from growth to defenses, or
because of higher carbon reserves in older trees.
Our aim is to understand whether resin tapping affects
tree-growth rates, and how tree, stand characteristics and
edaphoclimatic conditions modulate it. We have studied
six populations of P. pinaster along a latitudinal gradient
in Portugal and assessed tree-ring width before and dur-
ing resin tapping. Our hypotheses are that: i) resin tapping
reduces tree-ring width due to shifts in carbon allocation
to sustain resin production, but the impact will depend on
ii) local conditions, and iii) the characteristics of the trees,
i.e., trunk girth and height, tree density and competition
between neighbors, with younger trees being more affected
due to a lower capacity to acquire carbon and/or lower car-
bon reserves.
Materials andmethods
Study sites andresin harvesting
Maritime pine (Pinus pinaster Aiton) is a fast-growing
heliophytic tree species with a great ecological plasticity
and varied climatic spectrum (Farjon 2010). In Portugal,
this evergreen conifer represents 22% of the total forest area
(ICNF 2015) and is the main species used for resin tapping.
According to Portuguese law (see Art. 4th DL n.º 181/2015)
resin tapping is performed in trees with more than 63cm of
trunk girth at 1.30m from the ground, which is in line with
previous studies that recommended resin tapping only in
stands older than 30years (Zas etal. 2020). Tapping starts
on the trunk base at 20cm above the ground by removing
the bark and phloem every 15–20days and continues upward
for four years and up to 2m high. Afterward, when tree size
allows it, another vertical row is started 10cm apart from the
first wound and following the same procedure. Usually, the
tapping season goes from March until November, coinciding
with the radial growth of maritime pine.
For this study, we selected six stands of P. pinaster for
resin production in the Northern and Central regions of Por-
tugal, areas where this activity is traditionally done. Selec-
tion criteria of the stands was based on three main aspects:
(1) to have a minimum of five years of tapping exploita-
tion; (2) to have been exploited with only one resin wound
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

967European Journal of Forest Research (2023) 142:965–980
1 3
at a time and thus harmonizing the resin tapping intensity
between stands; (3) to have used the same resin extraction
methodology. We selected paired stands relatively close cli-
matically, but different in the average age to assess its role on
the impact of resin tapping on growth. The selected popula-
tions were located at Paredes de Coura (PCO), Vila Pouca de
Aguiar (VPA), Olho (OLH), Soure (SOU), Marinha Grande
(MGR) and Pataias (PAT) (Fig. 1). Across study sites,
resin tapping occurred between 2013 and 2019 (Table1).
The number of tapped years was 5 in OLH and SOU; 6 in
PCO, PAT and VPA and 7 in MGR (list of abbreviations in
TableS1).
Climatic data collection
Climatic data for each location was downloaded from the
Climate Explorer of the Royal Netherlands Meteorological
Institute (https:// clime xp. knmi. nl) using grid points 0.5 or
0.25. Due to their close proximity, MGR and PAT were
located at the same grid point, and thus shared climatic
data. Monthly time series of mean air temperatures (aver-
age, maximum and minimum; °C) and total precipitation
(mm month−1) were obtained from E-OBS 21.0e 0.25.
Self-calibrating Palmer Drought Severity Index (PDSI)
calculated from Climatic Research Unit Time Series (CRU
TS) data was obtained for 1901–2017 0.5° Global 3.26
early data set, and vapor pressure (hPa) from CRU TS
4.04 0.5° data set. Vapor pressure deficit (VPD, hPa) was
calculated from average temperature and vapor pressure
using the following formula:
where T and VP are the means of the monthly average air
temperature and vapor pressure, respectively. Maximum and
minimum VPD were also calculated for each location using
the respective temperatures and vapor pressure.
(1)
VPD =6.11∗exp ((17.27∗T)∕(T+273.3)) −VP
Fig. 1 Location and climatic diagrams of the study sites. The color
in the map represents the mean annual precipitation minus potential
evapotranspiration (P-PET, in mm) for the period 1990–2019. Nega-
tive P-PET values indicate drier sites. For each site, an ombrothermic
diagram is shown representing the average monthly air temperature
(T, in red) and precipitation (P, in blue) for the period 1990–2019,
and the gray area indicates the drought period (2T > P). The annual
average of air temperature and precipitation for a period of 30years is
displayed at the top of each climatic diagram
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

968 European Journal of Forest Research (2023) 142:965–980
1 3
Stand andtree characteristics
Twenty P. pinaster trees per location were selected to inves-
tigate growth responses and the structure of the stand. We
first evaluated the trees’ canopy and then selected healthy
trees with average trunk girth for each stand. Trunk girth at
breast height (TG), total height and tree height until the first
branches with green needles were measured. The difference
between the two last variables was used as an estimate of the
tree canopy size (trunk foliated length).
To quantify the degree of competition between trees and
its potential effect on radial growth of selected trees, we
calculated two competition indices based on trees’ height
and trunk girth (CIH and CITG, respectively). This informa-
tion is not available for PCO because trees were felled before
collecting all data. We first identified all living trees in a
circumference of 5-m radius from the trunk of each target
tree, and then measured their trunk girth at breast height and
the two described heights. The number of present neighbors
was used to calculate tree density of the location (trees ha−1).
CIH and CITG were calculated as the sum of the ratio between
each competitor tree in the circumference and the target tree
as follows:
(2)
CI
TG =
∑
tgi∕
tg
where tgi is the trunk girth at breast height of ith competitor
and tg is the trunk girth at breast height of the target tree;
and
where hi is the trees’ height of ith competitor and h is the
height of the target tree.
Two soil samples per target tree were also collected at
50cm (0–10cm depth) from the north and south side of the
trunk. Pooled samples were dried at 60 ºC for four days and
sifted with a 2-mm sieve. Soil pH was measured with a pH
meter (JENWAY Model 3505) in a 1:2.5 (mass/volume, soil/
water) suspension. The percentage of organic matter (OM)
was assessed by loss on ignition at 450°C for 4h in a muffle
furnace (Nelson & Sommers, 2018; Roberston 2011).
Dendrochronological sampling andprocessing
Wood increment cores were collected on the 20 target trees
per site in 2019 at PCO and VPA and in 2020 on the remain-
ing sites. Two cores were taken from each tree at breast
height (ca. 1.3m), with an increment borer of 12-mm diame-
ter. Core extraction was done between resin-tapping wounds,
as all studied trees had been tapped for more than four con-
secutive years. The core between tapping wounds represents
the resin tapping face and the one from the opposite side
(3)
CI
H=
∑
hi∕
h
Table 1 Stand, tree, and resin tapping characteristics for each site (PCO—Paredes de Coura; VPA—Vila Pouca de Aguiar; OLH—Olho; SOU—
Soure; MGR—Marinha Grande; PAT—Pataias)
CITG and CIH are the two competition indexes using the trunk girths and heights of the neighbor trees divided by the trunk girths and heights of
the sampled trees, respectively. Means and standard errors (± SE) are shown for variables measured at tree level. Different letters represent the
statistical differences between sites for each parameter (p < 0.05)
Location Sites PCO VPA OLH SOU MGR PAT
Stand characteristics Latitude 41.87 41.47 40.33 40.05 39.73 39.63
Longitude − 8.60 − 7.52 − 8.65 − 8.59 −8.96 − 8.96
Altitude (m a.s.l.) 479 791 71 49 100 98
Soil organic matter (%) 21.87 ± 0.86 f 16.03 ± 1.14 e 4.72 ± 0.41 b 11.98 ± 1.19 d 5.78 ± 0.88 c 3.17 ± 0.19 a
Soil pH 4.07 ± 0.03 a 4.25 ± 0.05 b 5.01 ± 0.06 d 4.61 ± 0.06 c 5.43 ± 0.08 e 6.52 ± 0.05 f
Tree density (trees/ha) – 517 ± 42 d 554 ± 54 d 363 ± 33 a 357 ± 32 b 427 ± 23 c
Tree characteristics Cambial age (years) 34 ± 0.36 c 44 ± 0.53 d 29 ± 1.29 b 49 ± 1.71 e 58 ± 0.27 f 25 ± 0.23 a
Trunk girth (cm) 98.0 ± 3.5 b 88.1 ± 3.0 a 102.9 ± 2.1 c 96.0 ± 4.0 c 108.8 ± .1.6 d 108.4 ± .1.5 d
Total height (m) – 18.1 ± 0.3 a 21.5 ± 0.6 d 19.8 ± 0.4 c 22.4 ± 0.2 e 19 ± 0.3 b
Trunk foliated length (m) – 5.8 ± 0.4 b 6.1 ± 0.4 c 5.7 ± 0.3 b 5.2 ± 0.3 a 5.3 ± 0.3 a
Neighbor trees (no.) – 3.06 ± 0.34 3.40 ± 0.44 1.85 ± 0.26 1.8 ± 0.26 2.35 ± 0.18
Neighbors’ trunk girth (cm) – 84.0 ± 2.1 b 63.3 ± 3.7 a 88.5 ± 4.5 c 95.0 ± 2.3 d 102.5 ± 4.0 e
Height of neighbor trees (m) – 18.2 ± 0.3 b 15.1 ± 0.7 a 17.7 ± 0.5 c 22.1 ± 0.2 d 17.8 ± 0.5 e
CITG –2.96 ± 0.34 d 2.30 ± 0.28 b 2.76 ± 1.21 c 1.60 ± 0.24 a 2.23 ± 0.17 b
CIH–3.09 ± 0.34 d 2.34 ± 0.25 c 1.68 ± 0.22 a 0.25 b 2.23 ± 0.20 c
Resin Harvest Tapping period (years) 2013–2018 2013–2018 2015–2019 2015–2019 2013–2019 2014–2019
Number of tapped years 6 6 5 6 7 6
Tapped side (º) – 184 ± 36 ab 236 ± 15 b 195 ± 14 ab 154 ± 18 ab 119 ± 19 a
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

969European Journal of Forest Research (2023) 142:965–980
1 3
represents the untapped face (Fig.2). The orientation of each
core was recorded to verify if the exposition of the tapping
wound influenced growth response to tapping within and
between sites.
After harvesting, each core was immersed in 99% acetone
for 24h at 4 ºC to clean the samples from resin, dirt, and
debris. Then, they were air dried, glued on wooden mounts
and progressively polished (150, 400, 800 and 1200G) with
a belt sander (Bosch GBS 100 AE). Polished samples were
scanned at 2400 dpi and 48 bits in RGB using a photo-scan-
ner (EPSON Perfection 4990 Photo) and the EPSON Scan
software (2020 Seiko Epson Corporation). Increment core
images were analyzed using the xRing package for R to auto-
matically detect tree-ring borders and to measure tree-ring
width (TRW ) (Campelo etal. 2019; R Core Team 2020).
After visually cross-dating by comparing TRW within tree
(tapped and untapped sides) and site, the number of annual
rings from the pith was used to determine the cambial age.
The pith was not present in 1 tree at VPA, PCO, MGR and
SOU and in 3 trees at OLH. Trees with correlations below
0.4 were discarded for further analysis. Final chronologies
were computed with 15 trees for OLH, 18 for PCO and SOU,
20 for MGR, PAT and VPA. To remove size and age-related
trends, a cubic smoothing spline was applied to each indi-
vidual ring-width time-series. Due to the large variation in
the average length of ring-width time series between sites,
the recommendations of Klesse (2021) were followed to
define the length of the spline. Thus, the grand mean of the
mean of the time-series length for each site was used. In
doing so, each ring-width time-series was detrended using a
spline with a frequency response cut-off of 0.5 and a length
of 26years to enhance the climatic signal and to allow inter-
site comparisons. Autoregressive modeling was performed
on each standardized series to remove temporal autocorrela-
tion and to maximize the climatic signal. For each site, the
obtained residual ring-width indices (RWI) were averaged
using a bi-weighted mean to produce a site chronology. For
the common interval to all sites, the statistical quality of
each chronology was evaluated using the following vari-
ables: the expressed population signal (EPS) that indicates
the degree to which a given chronology approaches an infi-
nitely replicated chronology (Wigley etal. 1984a, b), the
r.tot which is the mean of all correlation between differ-
ent cores, r.wt which is the mean of correlations between
series from the same tree over all trees and r.bt which is the
mean inter-series correlation between all series from differ-
ent trees. The chronologies and detrending were developed
using dplR (Bunn 2010; R Core Team 2020) and detrendeR
(Campelo etal. 2012) packages for R version 3.6.2 (R Core
Team 2020).
Statistics
We characterized the climatic differences between sites by
conducting a principal component analysis (PCA) of the
main climatic variables between 1999 and 2019, the com-
mon period for all the chronologies. Variables with low
contribution percentage among principal components were
removed from the PCA. The variables included in the final
PCA were: mat (mean temperature), pp (mean annual pre-
cipitation), ts (temperature seasonality), maxvpd (maximum
vapor pressure deficit) and mpdsi (mean Palmer Drought
Severity Index). All variables were previously scaled, and
the analysis was computed using the function PCA from the
FactoMineR package (Lê etal. 2008) for R version 3.6.2 (R
Core Team 2020).
The parameters of the studied trees (TG, tree height, trunk
foliate length) and the structure of the stand (tree density,
core exposition, soil pH and OM, CITG and CIH) between
sites were compared using linear models. All response vari-
ables were normally distributed, except soil pH and OM that
were square root transformed to meet the assumptions of
parametric analyses. The respective tree/stand parameters
were the dependent variable, site the fixed factor and tree the
random factor. Bonferroni method was used for the pairwise
post hoc tests and alpha < 0.05 as a significant level. These
analyses were performed using the function from the nlme
package v.3.1–14 (Pinheiro etal. 2020)⁠ and the cld function
Fig. 2 Representation of an increment core sampled on the trunk of a
tree with two adjacent tapping wounds. Concentric circles represent
annual tree-rings. The green area represents the wound area where
resin tapping—bark and phloem removal—was performed, and the
red arrow shows the direction of the increment core, which starts
between resin tapping wounds (tapped side) and ends on the opposite
side (untapped side) of the trunk. The distance between tapped faces
is around 10cm according to the Portuguese law regulating the har-
vesting and marketing of pine resins (see Art. 4th DL n. º 181/2015)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

970 European Journal of Forest Research (2023) 142:965–980
1 3
from the multcomp during pairwise post hoc tests (Hothorn
etal. 2008) function for R (R Core Team 2020).
To comprehend if resin tapping affects tree-ring width at
site level, we compared the TRW during the tapping years
and the same number of years before the start of resin har-
vesting, e.g., 2006–2012 before tapping vs. 2013–2019
during tapping in MGR. Then, linear mixed models were
performed using TRW as dependent variables, square root
transformed to meet a normal distribution. Site,tapping
(before vs. during),and trunk side (tapped vs. untapped)
were considered as fixed factors, while tree within site was
considered a random factor. Pairwise post hoc tests with
Bonferroni corrections were carried out to compare differ-
ences between trunk side, and period of tapping for each site.
The same procedure was applied to RWI to assess the results
after removing age influence on growth trends.
To compare resin harvesting impact between years and
stands with different growth rates, we standardized data
calculating the resin tapping impact (RTI), i.e., the ratio
between TRW of each tapping year and the mean TRW for
the 5years before tapping started. The RTI corresponds to
the resistance index proposed by Lloret etal. (2011), which
estimates the performance during and before a disturbance,
i.e., resin tapping in this study. We have used 5years aver-
ages for the pre-disturbance period to reduce the weight of
any natural trend, and to account for inter-annual climatic
variability. Values > 1 and < 1 indicate that wider and nar-
rower rings were produced during tapping relative to the
previous period, respectively. To compare the RTI between
tapping years and sites, we used linear mixed models where
RTI was the dependent variable, site, and the tapping year
the fixed factors and tree the random factor. More com-
plex models with autocorrelation were considered but did
not improve model performance according to Akaike and
Bayesian information criteria. When significant effects
were detected, a pairwise post hoc test with Bonferroni cor-
rections was applied to account for multiple comparisons
between years and sites. For these analyses, it was used the
lme function from the nlme package v.3.1–14 (Pinheiro etal.
2020)⁠ and the cld function from the multcomp during pair-
wise post hoc tests (Hothorn etal. 2008).
To assess the effect of tree traits, stand characteristics,
and climate on RTI, the Spearman’s rank correlation coef-
ficient was calculated within and across sites. The param-
eters used for the tree and stand characteristics were TRW
, TG, tree height, tree foliated height, tree density, the
competition indices (CITG and CIH), soil pH, soil OM and
cambial age. For the PCO site, where trees were felled
before we could collect data for radial growth. Only TRW
, TG, and the soil pH and OM variables were used. The
climatic parameters used were based on the scores of the
first, second, third, and fourth principal components of
the PCA (mat, ts, pp, maxvpd and mpdsi). These analyses
were conducted using rcorr.adjust function of the Hmisc
package for R version 3.6.2 (R Core Team 2020).
Results
Climate andstand characteristics
The sampling sites showed a latitudinal climatic gradient
with the coldest location, VPA, with an average tempera-
ture of 12.1 ºC, also located at the highest altitude, 791m
(Table1, Abbreviations in TableS1). The warmest loca-
tion was SOU, whereas MGR and PAT were the driest
ones, with negative P–PET values (Fig.1). PCO showed
the highest precipitation levels (1471mm on average) and
highest average VPD (6.88hPa) (Fig.1, TableS2). The
average Palmer Drought Severity Index (PDSI) was close
to 0 and similar between sites, but slightly more negative
in the lower latitudes (TableS2).
The PCA retained 5 climatic variables: mat, pp, ts,
maxvpd and mpdsi. The two firstprincipal components
(henceforth described as PC1 and PC2) explained 38.9%
and 23.2% of the overall variance, respectively (Fig.3).
The variables ts and maxvpd were positively related to
PC1, while mat, pp and mpdsi were negatively correlated.
Precipitation (pp)was negatively correlated with PC2,
while the other variables were positively related. The PC1
and PC2 aggregated the sites in three main groups: i) PCO,
ii) VPA and iii) OLH, SOU, MGR and PAT (Fig.3). PCO
was positively related to pp and mpdsi, and negatively to
mat, while VPA had a positive correlation with ts. The rest
of the locations correlated positively with PC2, with mat,
maxvpd and mpdsi (Fig.3).
Soil OM and pH were different among sites (Table1)
with PCO and VPA (Table1) showing higher OM and
lower pH values. Across sites, average cambial age var-
ied from 58 to 29years-old TG and height between 88
and 108cm and 18 and 22m, respectively (Table1). The
biggest and tallest trees were found in MGR, the old-
est stand; however, TG in PAT, the stand located at the
same climatic grid point, was similar, even if the latter
was the youngest sampled population (Table1). Marinha
Grande(MGR) and SOU showed, on average, less than
two neighbors, in contrast with the 3.4 per target tree iden-
tified in OLH; however, competitor trees were smaller in
the latter (Table1). Olho(OLH) was the densest stand
with the highest inter-tree competition (554 trees/ha and
CITG 2.30), and MGR the one with the lowest density and
competition indices (357 trees/ha and CITG 1.60). Across
locations, the tapped side of the trunk (tapped increment
core) tended to be exposed to south, varying between
southeast and southwest (Table1).
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

971European Journal of Forest Research (2023) 142:965–980
1 3
Tree‑ring width beforeandduringtapping
In general, the tree-ring width index series considering
the common interval within (TableS3) and between sites
(TableS4; 1999–2019) showed EPS values above 0.85,
except in OLH and SOU that showed slightly lower values
from 1999 to 2019 and including the tapped and untapped
side of the trunk. PAT, the youngest stand, was the site
with the highest average TRW values (5.53mm), followed
by OLH (4.22mm), PCO (3.73mm), VPA (2.54mm),
MGR (2.27mm) and SOU (1.91 mm). In general, all
chronologies showed the age growth trend producing nar-
rower tree-rings with increasing tree age (Fig.4). TRW
of the untapped side was smaller in PCO and OLH; how-
ever, this trend was present before the resin tapped period
(Fig.4). To understand if TRW was affected by resin har-
vesting, we compared the mean TRW between the resin
tapped years and the same number of years before tapping
Fig. 3 Principal component
analysis of the climate data
[annual mean temperature
(mat), annual mean precipita-
tion (pp), temperature seasonal-
ity (ts), maximum vapor pres-
sure deficit (maxvpd) and mean
Palmer Drought Severity Index
(mpdsi)] for the six study sites
[Paredes de Coura (PCO), Vila
Pouca de Aguiar (VPA), Olho
(OLH), Soure (SOU), Marinha
Grande (MGR) e Pataias (PAT)]
with the two principal compo-
nents explaining 62.1% variance
overall. Different sites are
depicted by different symbols
and colors. Due to its proximity,
MGR and PAT share the same
climatic data
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

972 European Journal of Forest Research (2023) 142:965–980
1 3
calculated separately for the tapped and untapped trunk
sides (Fig.5). Pine trees in two of the youngest popu-
lations, PCO and OLH, showed a significant decrease
of the TRW during the tapping period on both sides of
the trees, while PAT—the youngest and fastest growing
population—showed a TRW decrease only in the untapped
side (Fig.5). All the other sites (VPA, SOU and MGR)
showed no significant growth decrease during tapping,
regardless of the side of the tree (Fig.5). In MGR, the
stand with the oldest tree population, TRW increased
Fig. 4 Average tree-ring widths
(TRW , mm) between 1999 and
2019 for the study sites: Paredes
de Coura, (PCO), Vila Pouca
de Aguiar (VPA), Olho (OLH),
Soure (SOU), Marinha Grande
(MGR) and Pataias (PAT). Red
and blue lines represent the
untapped and tapped side of the
trunk, respectively. The gray
shadow represents the resin
tapping period. The equivalent
number of years before the
beginning of tapping for each
site is shown in dark yellow.
Resin extraction started in 2013
in PCO, VPA and MGR, in
2014 in PAT, and in 2015 in
OLH and SOU. Note that TRW
scale varies between plots
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

973European Journal of Forest Research (2023) 142:965–980
1 3
during the tapping period on the tapped side of the trunk
(Fig.5). The same analysis was performed using the tree-
ring-width index (RWI), where the TRW age trend was
removed (Fig. S1). In this case, RWI increased during the
tapping period in VPA and MGR, regardless of the side
of the tree (Fig. S1). OLH showed the opposite trend, that
is, RWI was higher before than after the tapping started,
while PCO, PAT and SOU showed no significant differ-
ences (Fig. S1).
Fig. 5 Boxplots of the tree-ring
widths (TRW , mm) for each
side of the tree (tapped in blue
and untapped in red) before
and during resin tapping. Dif-
ferent letters indicate statisti-
cally significant differences
between groups at each location
(p < 0.05)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

974 European Journal of Forest Research (2023) 142:965–980
1 3
Resin tapping impact
On average, the RTI was < 1 in the youngest popula-
tions (PCO = 0.72, OLH = 0.84 and PAT = 0.85) and > 1
in the oldest populations (VPA = 1.17, SOU = 1.18 and
MGR = 1.41) (Fig.6). Despite RTI fluctuations between
different tapping years, no clear pattern associated with
cumulative stress due to repeated resin harvesting was
detected (Fig.6).
The Spearman’s rank correlation coefficients between
RTI, tree, and stand characteristics across sites were signifi-
cant and positive for TRW (+ 0.38), cambial age (+ 0.53),
total height (+ 0.24), and soil OM (+ 0.11), and negative
with CITG (− 0.22) and soil pH (− 0.14) (TableS5, Fig.7).
Fig. 6 Resin tapping impact
(RTI) per site during the
years of resin tapping. Values
of RTI < 1 and > 1 indicate
narrower and larger tree-
rings during resin extraction,
respectively, in comparison with
pre-disturbance. Letters denote
statistical differences between
resin tapping years within site
at p < 0.05. Sites are organized
from the youngest to the oldest
stands (from left to right). Resin
extraction started in 2013 in
PCO, VPA and MGR, in 2014
in PAT and in 2015 in OLH and
SOU
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

975European Journal of Forest Research (2023) 142:965–980
1 3
Within sites, RTI was positively correlated with TRW in all
cases (TableS5). In general, TG was strongly and positively
associated with RTI in VPA and PAT, to total height in PAT
and OLH, but to soil OM only in PCO. Negative RTI were
shown for cambial age in MGR and PAT (TableS5).
Spearman correlations were carried out between the
RTI and the scores of the first, second, third and fourth
components of the PCA (Fig.8). The scores of the prin-
cipal components were not significantly associated with
RTI, except for the PC4 that preserved only the 10.6% of
the climatic variance and was mainly explained by mat
(32.8%). In the latter, with the increasing mat, the RTI
decreases to values below 1 (Fig.8d).
Fig. 7 Spearman’s rank cor-
relations coefficients between
RTI with cambial age a, total
height b, trunk girth c and
CITG d across sites. Each gray
dot represents individual trees
(average RTI during the tapping
period and the characterization
variable measured during the
sampling campaign) and the
blue dots represent the average
value per site with its respec-
tive standard error bar (SE)
and regression line (in red).
Relationships between variables
are represented by dashed lines
when non-significant and by
solid lines when significant. The
Spearman’s correlation coef-
ficient (R) and the p-values are
shown (for p < 0.05)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

976 European Journal of Forest Research (2023) 142:965–980
1 3
Discussion
The aim of this study was to understand if resin tapping
affects wood growth of P. pinaster, and whether tree, stand
characteristics and edaphoclimatic conditions can modu-
late it or not. Our results show that radial growth is not
systematically reduced on maritime pine trees exploited
for resin production and hint that negative impacts are
more frequent in younger (< 30years-old) than older pop-
ulations as hypothesized. This result indicates that, as well
as being a profitable forest activity, resin and timber co-
production in maritime pine may be sustainable, especially
when performed in populations older than 40-year-old.
Fig. 8 Spearman’s rank correla-
tion coefficients between the
resin tapping impact (RTI) and
the scores of the first a, second
b, third c and fourth d climatic
principal components (PC1,
PC2, PC3 and PC4; see Fig.3)
for all studied locations. Each
dot represents each tapping
year for each site. Relation-
ships between variables are
represented by dashed lines
when non-significant and by
solid lines when significant
(p < 0.05). The PC1 is more
weighted by the variable ts and
the PC2 by pp. PC3 has mpdsi
has the highest contributed
variable and PC4 is with mat.
The Spearman correlation coef-
ficient (R) and the p-values are
shown
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

977European Journal of Forest Research (2023) 142:965–980
1 3
In general, when the TRW before and during resin tap-
ping is compared, the youngest populations (PCO, OLH
and PAT) showed a decreasing growth trend during resin
extraction, while the oldest populations showed no signifi-
cant differences (VPA, SOU) or even wider rings during
this period (MGR). Tomusiak & Magnuszewski (2013) and
van der Maaten etal. (2017) also showed positive influ-
ence of tapping on radial growth on Scots pine and no sys-
temic reductions in growth as we found in the older stands.
On the contrary, Chen etal. (2015) showed that younger
tapped Masson pine trees were able to enlarge and repair
their trunks faster than older trees, as their tree-ring index
only declined by 4.8%. However, theyonlyinvestigated
two sites, and no details about stand structure were given.
Discrepancies can also be partially explained by the use of
non-detrended series. Studying resin tapping impact through
tree-ring width may be confusing because the biologi-
cal trend associated with tree age is still present. Yet, our
results consistently showed that growth resistance increases
in older stands when RWI instead of the TRW was consid-
ered. In this case, two of the oldest stands (VPA and MGR)
showed higher growth indices during tapping than the pre-
disturbance period. Although resin production was not meas-
ured here, Zas etal. (2020) showed that resin production
increases considerably with tree age in maritime pine stands
growing under similar climatic conditions in northern Por-
tugal. Determining a minimum age to start resin harvesting
in this species becomes, therefore, a key factor to design
sustainable timber and resin forest exploitations, and future
studies should shed light on this.
Besides the stand age, other parameters must be taken
into account when trying to understand growth sensitivity
to resin harvesting, for instance the design of the increment
cores’ sampling. Wood formation in the trunk of tapped
pines is not uniform as growth is suppressed in the region
due to the mechanical injury of the bark and phloem tissues,
and asymmetrical rings can be produced in the remaining
surface depending on their distance to the wound (Grissino-
Meyer etal. 2001). Although our study did not measure the
effect of tapping on wood properties, other studies have
shown that resin tapping results in higher wood deforma-
tion and elasticity (Silva etal. 2018), but also increases wood
density (especially on the tapped side), which modifies its
mechanical properties (García-Iruela etal. 2016; Silva etal.
2018; Wu etal., 2022). Furthermore, if the wood core is
extracted too close to the wound, the increase in TRW can
just be related to the wood reaction to the injury. To take this
into account, Zeng etal. (2021) extracted six increment cores
per tree, and Papadopoulos (2013) measured TRW and late-
wood in three radial directions in Aleppo pines. Nonetheless,
impact assessment, as well as comparisons between studies,
is usually difficult as most of the sampling designs usually
include the extraction of a single increment core per tree and
height taken from the tapped or untapped face (Tomusiak &
Magnuszewski., 2013; Hood & Sala 2015; Zas etal. 2020;
Du etal. 2021). In this study, we harvested stands subjected
to the same tapping intensity (number of wounds at a time
and tapping frequency), and collected wood cores using the
same methodology, so that the comparison between sites can
disclose the effect of stand age and edaphoclimatic charac-
teristics among the studied sites.
Across sites, the locations characterized by taller trees
producing wider tree-rings, low inter-tree competition at
TG level, and greater content in soil organic matter tended
to show higher growth rates during tapping than the pre-
vious period (RTIs above 1). On the one hand, larger and
taller trees may have better access to light and can poten-
tially photosynthesize more, acquiring more carbon that can
be used for either resin or wood production. Furthermore,
taller trees usually have deeper roots and are less sensitive
to variations in precipitation because they can tap deeper
water sources and thus, keep high transpiration and pho-
tosynthesis rates for longer under drought (Brando 2018;
Giardina etal. 2018). On the other hand, the negative CITG
correlation with RTI suggests that competition for resources
could affect the capacity to respond to harvesting, as well as
shown in response to other disturbances (Rozendaal etal.
2020; Marqués etal. 2021). In addition, it has been shown
that at least in young Pinus oocarpaSchiede ex Schltdl, high
competition levels lead to decreasing resin yield, although
the opposite canoccur in adult trees (Egloff 2020). There-
fore, and specially in young stands, it is necessary to carry
out forest management practices such as thinning to reduce
inter-tree competition, as well as the associated growth and
resin production constraints.
Within sites, only PCO—the tree population growing in
more acidic soils—showed significant correlations between
soil organic matter, pH and RTI, positive and negative,
respectively. Organic matter is an important source of nitro-
gen, a macronutrient for plants and central for photosynthe-
sis, with leaves with higher amounts of nitrogen showing a
higher photosynthetic capacity and increasing the growth
potential of the trees. The negative association between soil
pH and RTI could simply reflect the effect of this variable on
the mineralization of the organic matter, and/or to a higher
nutrient availability under more acidic soils (Curtin etal.
1998).
Selected pine stands in this study could represent dif-
ferent P. pinaster provenances (ICNF 2012) and thus, their
annual growth could be strongly influenced by climatic
conditions and, to a lesser extent, by genetic plasticity
(Rozas etal. 2020). Despite this, the climatic sensitiv-
ity of tapped and untapped trees appears to be similar,
as shown by van der Maaten etal. (2017). In their study,
tapped and non-tapped P. sylvestris trees presented com-
parable sensitivities even in the occurrence of an extreme
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

978 European Journal of Forest Research (2023) 142:965–980
1 3
climatic event. In line with this, our results showed that
the climatic conditions had a marginal effect on RTI across
stands. Only 10% of RTI variance was explained by PC4
indicating that growth sensitivity across sites increases
with increasing average temperatures. Without taking
into account the potential effect of temperature on resin
production and considering the studied region—where
resin is traditionally harvested—warmer places seem to
be less profitable for timber production when the activity
is combined with resin harvesting, a trend that could be
exacerbated by rising temperatures.
In conclusion, this study showed that the age of maritime
pine stands had a strong effect on the impact of resin extrac-
tion on wood growth, with younger stands (< 30years-old)
showing a tendency to form narrower rings—reduced wood
production, and a lower capacity to buffer the resin extrac-
tion disturbance compared with older stands. Nonetheless,
we did not have access to the resin yield of the different
stands, an important information to deepen our knowledge
on the impact of resin extraction on the carbon economy of
maritime pine. Based on our results, to maximize resin and
wood co-production, resin extraction should be performed in
populations with more than 40years of age, and on managed
stands with controlled tree density to reduce competition and
thus provide greater growth resistance to resin extraction.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s10342- 023- 01568-7.
Acknowledgements We are very grateful for the help provided by:
RESIPINUS for providing the contacts of the resin tapping operators
and landowners; Gestão Integrada e Fomento Florestal Lda. as well
as J. Lousada e E. Silva for they collaboration during the samplings
in PCO and VPA; Pedrosa e Irmãos, Lda. and Mr. Carlos Simões for
helping us in SOU; Mr. Manuel Santos, resin worker at OLH for his
advice and permission to sample; and Mr. Luís Carpalhoso and Costa
e Irmãos Lda for allowing us to conduct this study at PAT and MGR.
The first author wishes to thank Ana Carvalho for her help and support
on the field and laboratory.
Author contributions All authors contributed to the study conception
and design. Field samplings, data collection and analysis were per-
formed by MM, NG-F and FC. All authors contributed to interpret the
data. MM wrote the manuscript with the help of the other authors, and
all read and approved the final version of the manuscript.
Funding Open access funding provided by FCT|FCCN (b-on). This
study was co-financed by the Portuguese Foundation for Science and
Technology (FCT) and the European Regional Development Fund
through the project PTDC/ASP-SIL/31231/2017. The corresponding
author is funded by a PhD Student Grant (SFRH/BD/145914/2019)
from the FCT. The investigation was carried out at the R&D Unit des-
ignated Center for Functional Ecology—Science for People and the
Planet (project UIDB/04005/2020) supported by Portuguese national
funds.
Data availability Data will be made available upon request.
Code availability Code will be made available upon request.
Declarations
Conflict of interest The authors declare that they have no known com-
peting financial interests or personal relationships that could have ap-
peared to influence the work reported in this paper.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
References
Bond BJ (2000) Age-related changes in photosynthesis of woody
plants. Trends Plant Sci 5(8):349–353. https:// doi. org/ 10. 1016/
S1360- 1385(00) 01691-5
Bottero A, D’Amato AW, Palik BJ, Bradford JB, Fraver S, Battaglia
MA, Asherin LA (2017) Density-dependent vulnerability of forest
ecosystems to drought. J Appl Ecol 54(6):1605–1614. https:// doi.
org/ 10. 1111/ 1365- 2664. 12847
Brando P (2018) Tree height matters. Nat Geosci 11(6):390–391.
https:// doi. org/ 10. 1038/ s41561- 018- 0147-z
Bunn AG (2010) Statistical and visual crossdating in R using the dplR
library. Dendrochronologia 28(4):251–258. https:// doi. org/ 10.
1016/j. dendro. 2009. 12. 001
Campelo F, García-González I, Nabais C (2012) detrendeR: a Graphi-
cal User Interface to process and visualize tree-ring data using R.
Dendrochronologia 30(1):57–60. https:// doi. org/ 10. 1016/j. dendro.
2011. 01. 010
Campelo F, Mayer K, Grabner M (2019) xRing—An R package to
identify and measure tree-ring features using X-ray microdensity
profiles. Dendrochronologia 53:17–21. https:// doi. org/ 10. 1016/j.
dendro. 2018. 11. 002
Chen F, Yuan YJ, Yu SL, Zhang TW (2015) Influence of climate
warming and resin collection on the growth of Masson pine
(Pinus massoniana) in a subtropical forest, southern China.
Trees – Struct Funct 29(5):1423–1430. https:// doi. org/ 10. 1007/
s00468- 015- 1222-3
Curtin D, Campbell CA, Jalil A (1998) Effects of acidity on mineraliza-
tion: pH-dependence of organic matter mineralization in weakly
acidic soils. Soil Biol Biochem 30(1):57–64. https:// doi. org/ 10.
1016/ S0038- 0717(97) 00094-1
Du B, Luan Q, Ni Z, Sun H, Jiang J (2021) Radial growth and non-
structural carbohydrate partitioning response to resin tap-
ping of slash pine (Pinus elliottii Engelm. var. elliottii). J
Forestry Research 33(2):423–433. https:// doi. org/ 10. 1007/
s11676- 021- 01357-1
Egloff, P. (2020). Tapping Pinus oocarpa Assessing drivers of resin
yield in natural stands of Pinus oocarpa Master thesis Philipp
Egloff AV2019–25. March.
Farjon A (2010) A handbook of the world’s conifers. BRILL, Leiden,
Boston, pp 533–1111
Fernández-de-Uña L, Cañellas I, Gea-Izquierdo G (2015) Stand com-
petition determines how different tree species will cope with a
warming climate. PLoS ONE 10(3):1–19. https:// doi. org/ 10. 1371/
journ al. pone. 01222 55
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

979European Journal of Forest Research (2023) 142:965–980
1 3
Garcia-Forner N, Campelo F, Carvalho A, Vieira J, Rodríguez-Perei-
ras A, Ribeiro M, Salgueiro A, Silva ME, Louzada JL (2021a)
Growth-defence trade-offs in tapped pines on anatomical and resin
production. Forest Ecol Manag 496:119406. https:// doi. org/ 10.
1016/j. foreco. 2021. 119406
Garcia-Forner N, Carvalho A, Campelo F (2021b) Water and stem
girdling affect the tracheids’ number more than their shape in
Pinus pinaster saplings. Trees 35:1921–1931. https:// doi. org/ 10.
1007/ s00468- 021- 02160-5
García-Iruela A, Esteban L, De Palacios P, García-Fernández F, De
Miguel A, Vázquez E, Simón C (2016) Resinous Wood of Pinus
pinaster Ait. Physio-Mech Prop Bioresour 11:5230–5241. https://
doi. org/ 10. 1007/ 978-3- 319- 95432-5_5
Génova M, Caminero L, Dochao J (2014) Resin tapping in Pinus
pinaster: Effects on growth and response function to climate.
Eur J Forest Res 133(2):323–333. https:// doi. org/ 10. 1007/
s10342- 013- 0764-4
Giardina F, Konings AG, Kennedy D, Alemohammad SH, Oliveira
RS, Uriarte M, Gentine P (2018) Tall Amazonian forests are less
sensitive to precipitation variability. Nat Geosci 11(6):405–409.
https:// doi. org/ 10. 1038/ s41561- 018- 0133-5
Susana Girón. (2021). Spain’s untapped “liquid gold.” https:// www. bbc.
com/ travel/ artic le/ 20211 014- spains- untap ped- liquid- gold
Grissino-Meyer HD, Blount HC, Miller AC (2001) Tree-ring dating
and the ethnohistory of the naval stores industry in southern Geor-
gia. Tree-Ring Res 57(1):3–13
Hao-ran Wu, Yan-ru F, Xiao-yun N, Qi-fu L, Yan-jie Li, Jing-min J,
Jian-er J (2022) Effects of resin-tapping year on wood properties
of living Pinus elliottii. Forest Res 35(1):31–39. https:// doi. org/
10. 13275/j. cnki. lykxyj. 2022. 01. 004
He R, Wang X (2021) Impact of Competition on the Growth of Pinus
Tabulaeformis in Response to Climate on the Loess Plateau of
China. Plant Ecol 223:353–368
Hilty J, Muller B, Pantin F, Leuzinger S (2021) Plant growth: The what,
the how, and the why. New Phytologist 232(1):25–41. https:// doi.
org/ 10. 1111/ nph. 17610
Hood S, Sala A (2015) Ponderosa pine resin defenses and growth:
metrics matter. Tree Physiol 35(11):1223–1235. https:// doi. org/
10. 1093/ treep hys/ tpv098
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in gen-
eral parametric models. Biom J 50(3):346–363. https:// doi. org/
10. 1002/ bimj. 20081 0425
ICNF. (2012). Regiões de proveniência de Portugal. Instituto Da Con-
servação Da Natureza e Das Florestas, Lisboa., 1–88. https://
www. icnf. pt/ api/ file/ doc/ 7eba7 3fd7d 9976f1
ICNF. (2015). 6.o Inventário Florestal Nacional (IFN6) - Relatório
Final. 284. http:// www2. icnf. pt/ portal/ flore stas/ ifn/ ifn6
Klesse S (2021) Critical note on the application of the “two-third”
spline. Dendrochronologia 65:125786. https:// doi. org/ 10. 1016/j.
dendro. 2020. 125786
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multi-
variate analysis. J Stat Softw 25:1–18
Lloret F, Keeling EG, Sala A (2011) Components of tree resilience:
Effects of successive low-growth episodes in old ponderosa pine
forests. Oikos 120(12):1909–1920. https:// doi. org/ 10. 1111/j. 1600-
0706. 2011. 19372.x
Marqués L, Camarero JJ, Zavala MA, Stoffel M, Ballesteros-Cánovas
JA, Sancho-García C, Madrigal-González J (2021) Evaluating
tree-to-tree competition during stand development in a relict Scots
pine forest: how much does climate matter? Trees – Struct Funct
35(4):1207–1219. https:// doi. org/ 10. 1007/ s00468- 021- 02109-8
McDowell NG, Adams HD, Bailey JD, Kolb TE (2007) The role of
stand density on growth efficiency, leaf area index, and resin flow
in southwestern ponderosa pine forests. Can J for Res 37(2):343–
355. https:// doi. org/ 10. 1139/ X06- 233
Nelson, D. W., & Sommers, L. E. (2018). Total carbon organic carbon
and organic matter. Methods of Soil Analysis: Part 3 Chemical
Methods, 5 7 961–1010 doi https:// doi. org/ 10. 2136/ sssab ookse
r5.3. c34
Papadopoulos AM (2013) Resin tapping history of an Aleppo Pine for-
est in central Greece. The Open Forest Science Journal 6(1):50–
53. https:// doi. org/ 10. 2174/ 18743 98601 30601 0050
Pereira, J. M. R. (2015). Estimativa do potencial produtivo de resina em
pinheiro-bravo no concelho de Castro Daire. Mestre em Engenha-
ria Florestal e dos Recursos Naturais.pp 62.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Team, R. C. (2020).
nlme: Linear and Nonlinear Mixed Effects Models [WWW Docu-
ment]. R Packag. Version 3.1–151.
R Core Team (2020) R: A language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna, Aus-
tria. URL http:// www.R- proje ct. org/.
Roberston, S. (2011). Direct estimation of organic matter by loss on
ignition: methods. SFU Soil Science Lab (2011).
Rodríguez-García A, López R, Martín JA, Pinillos F, Gil L (2014)
Resin yield in Pinus pinaster is related to tree dendrometry, stand
density and tapping-induced systemic changes in xylem anatomy.
For Ecol Manage 313:47–54. https:// doi. org/ 10. 1016/j. foreco.
2013. 10. 038
Rodríguez-García A, Martín JA, López R, Mutke S, Pinillos F, Gil L
(2015) Influence of climate variables on resin yield and secretory
structures in tapped Pinus pinaster Ait. in central Spain. Agric
for Meteorol 202:83–93. https:// doi. org/ 10. 1016/j. agrfo rmet. 2014.
11. 023
Rozas V, Sampedro L, Vázquez-González C, Solla A, Vivas M, Lom-
bardero MJ, Zas R (2020) Site conditions exert more control than
genetic differentiation on modulation of secondary growth and cli-
mate sensitivity of Pinus pinaster. Dendrochronologia 63:125732.
https:// doi. org/ 10. 1016/j. dendro. 2020. 125732
Rozendaal DMA, Phillips OL, Lewis SL, Affum-Baffoe K, Alvarez-
Davila E, Andrade A, Aragão LEOC, Araujo-Murakami A, Baker
TR, Bánki O, Brienen RJW, Camargo JLC, Comiskey JA, Djuik-
ouo Kamdem MN, Fauset S, Feldpausch TR, Killeen TJ, Laur-
ance WF, Laurance SGW, Vanderwel MC (2020) Competition
influences tree growth, but not mortality, across environmental
gradients in Amazonia and tropical Africa. Ecology 101(7):1–11.
https:// doi. org/ 10. 1002/ ecy. 3052
Silva ME, Loureiro C, Gaspar MJ, Pires J, Ribeiro M, Loureiro C,
Coutinho JP, Santos E, Carvalho A, Brito JL, Salgueiro A, Lou-
sada JL, 2018. RESIMPROVE - Desenvolvimento de processos
de produção e extração de resina de pinheiro para a melhoria
da eficiência, racionalização e expansão da atividade. ISBN
978–989–704–264–5
Soliño M, Yu T, Alía R, Auñón F, Bravo-Oviedo A, Chambel MR, de
Miguel J, del Río M, Justes A, Martínez-Jauregui M, Montero G,
Mutke S, Ruiz-Peinado R, García del Barrio JM (2018) Resin-
tapped pine forests in Spain: Ecological diversity and economic
valuation. Sci Total Environ 625:1146–1155. https:// doi. org/ 10.
1016/j. scito tenv. 2018. 01. 027
Tomusiak R, Magnuszewski M (2013) Effect of resin tapping on radial
increments of Scots pine (Pinus sylvestris L.). Lesne Prace Bad-
awcze 74(3):273–280
van der Maaten E, Mehl A, Wilmking M, van der Maaten-Theunissen M
(2017) Tapping the tree-ring archive for studying effects of resin
extraction on the growth and climate sensitivity of Scots pine.
Forest Ecosyst 4:1–7. https:// doi. org/ 10. 1186/ s40663- 017- 0096-9
Vázquez-González C, López-Goldar X, Zas R, Sampedro L (2019)
Neutral and climate-driven adaptive processes contribute to
explain population variation in resin duct traits in a mediterra-
nean pine species. Front Plant Sci 10:1–12. https:// doi. org/ 10.
3389/ fpls. 2019. 01613
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

980 European Journal of Forest Research (2023) 142:965–980
1 3
Vázquez-González C, López-Goldar X, Alía R, Bustingorri G, Lario
FJ, Lema M, de la Mata R, Sampedro L, Touza R, Zas R (2021)
Genetic variation in resin yield and covariation with tree growth
in maritime pine. Forest Ecol Manag 482:118843. https:// doi. org/
10. 1016/j. foreco. 2020. 118843
Wang Z, Calderon MM, Carandang MG (2006) Effects of resin tapping
on optimal rotation age of pine plantation. J for Econ 11(4):245–
260. https:// doi. org/ 10. 1016/j. jfe. 2005. 10. 001
Wigley TML, Briffa KR, P. D. J. (1984a) On the average value of
correlated times series, with applications in dendroclimatology
and hydrometeorology. J Clim Appl Meteorol 23(1984):201–213
Wigley TML, Briffa KR, Jones PD (1984b) On the average value of
correlated time series, with applications in Dendroclimatology
and Hydrometeorology. J Climate Appl Meteorol 23:201–213
Williams R (2017) The effects of resin tapping on the radial growth
of masson pine trees in South China-A case study. Agricult Res
Technol 8(2):8–11. https:// doi. org/ 10. 19080/ artoaj. 2017. 08.
555732
Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994)
Evidence of reduced photosynthetic rates in old trees. Forest Sci
40(3):513–527. https:// doi. org/ 10. 1093/ fores tscie nce/ 40.3. 513
Zas R, Quiroga R, Touza R, Vázquez-González C, Sampedro L, Lema
M (2020) Resin tapping potential of Atlantic maritime pine forests
depends on tree age and timing of tapping. Industrial Crops and
Prod 157:112940. https:// doi. org/ 10. 1016/j. indcr op. 2020. 112940
Zeng X, Sun S, Wang Y, Chang Y, Tao X, Hou M, Wang W, Liu X,
Zhang L (2021) Does resin tapping affect the tree-ring growth and
climate sensitivity of the Chinese pine (Pinus tabuliformis) in the
Loess Plateau, China? Dendrochronologia 65:125800. https:// doi.
org/ 10. 1016/j. dendro. 2020. 125800
Züst T, Agrawal AA (2017) Trade-offs between plant growth and
defense against insect herbivory: an emerging mechanistic syn-
thesis. Annu Rev Plant Biol 68(1):513–534. https:// doi. org/ 10.
1146/ annur ev- arpla nt- 042916- 040856
Publisher's Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com