Forest Ecology and Management 389 (2017) 158–166
Contents lists available at ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
On the use of stable carbon isotopes to detect the physiological impact of
forest management: The case of Mediterranean coppice woodland
Giovanni Di Matteo a,⇑, Pierfrancesco Nardi a, Gianfranco Fabbio b
a
b
Council for Agricultural Research and Economics, Research Unit for Climatology and Meteorology applied to Agriculture (CREA-CMA), I-00186 Rome, Italy
Council for Agricultural Research and Economics, Forestry Research Centre (CREA-SEL), I-52100 Arezzo, Italy
a r t i c l e
i n f o
Article history:
Received 13 September 2016
Received in revised form 23 December 2016
Accepted 26 December 2016
Keywords:
Stable carbon isotopes
Forest stand density reduction
Meta-analysis
Coppiced stands
Released trees
Retrospective literature-analysis
Water-use efficiency
Mediterranean forest ecosystems
a b s t r a c t
This paper reviews the use of stable carbon isotope analysis to monitor the results of forest ecosystems management. Special focus is given to Mediterranean coppice woodland. We used this due to the high sensitivity
and spatial-temporal resolution of isotope analysis coupled with the complex attributes arising from the
composite management options now used in the coppice system. A meta-analysis based on 1428 publications from 1996 to 2015 revealed three distinct clusters of related terms in research carried out to answer
questions linked to the management of forests and terrestrial ecosystems namely, forest soil and forest carbon sequestration, the anthropogenic impact on plant and animal communities, and the physiological
response to silvicultural practices. Much physiological research on the study of the impact of silvicultural
practices on released trees has been carried out. A retrospective literature-analysis gave rise to three different functional hypotheses. The first hypothesis is that carbon isotope composition decreases after thinning,
mainly due to the rapid increase in soil moisture availability and decreased competition for water and
nutrients, i.e. decreasing intrinsic water-use efficiency (measured as the ratio of CO2 assimilation to stomatal
conductance, A/gs). Conversely, the second hypothesis is that d13C values increase due to the higher increase
in A over gs, especially observed in sites where water is not a limiting factor. The third hypothesis was that
there was no variation in d13C due to an equal and parallel increase in both A and gs. We found that the physiology of Mediterranean coppice stands is consistent with the first hypothesis, in accordance with other
analyses already performed on permanent research monitoring plots. The main finding however is that
stable isotope analysis does not overlap with any of the other investigation tools in use, but actually fills a
gap by providing further, effective insights into the ongoing functioning processes. Of course monitoring
these processes will take on increasing importance, especially in view of the climate shift in progress.
Ó 2016 Elsevier B.V. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Mapping using a science mapping approach: most commonly occurring and co-cited research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Data gathering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Bibliometric mapping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
How do the topic is structured?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4.
Most relevant research and its potential impact on forest management issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Reviewing literature on the response of released trees via stable carbon isotopes technique: a retrospective analysis. . . . . . . . . . . . . . . . . . . .
Coppice forests: customary and carbon isotopes analyses, common findings, roles and target . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Appendix A.
Supplementary material . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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⇑ Corresponding author at: Council for Agricultural Research and Economics, Research Unit for Climatology and Meteorology applied to Agriculture (CREA-CMA), Forest
Acclimation lab, Via della Navicella 2-4, I-00186 Rome, Italy.
E-mail address: [email protected] (G. Di Matteo).
http://dx.doi.org/10.1016/j.foreco.2016.12.030
0378-1127/Ó 2016 Elsevier B.V. All rights reserved.
G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
1. Introduction
A portion of broadleaved forests managed under the coppice
system was exploited for millennia as renewable resource, providing firewood and charcoal for the daily use of domestic heating and
cooking food all over Europe (Piussi, 2015). Following the first
industrial revolution, coppiced forests were again the most widespread and common energy source, especially in places where coal
was less available like the Mediterranean countries (Agnoletti,
2003). As a result, the forest landscape in five EU countries is still
characterized by coppice system features, in an area covering
about 8.5 million hectares (Morandini, 1994; Scarascia-Mugnozza
et al., 2000; UN/ECE-FAO, 2000). The coppice system, based on
the natural ability of broadleaved tree species to regenerate from
the stool after clear-cutting (i.e., coppicing), was usually managed
with short rotation cycles (10–15 to 20–25 years), in accordance
with the site index, the experienced growth pattern, and the ecological traits of tree species concerned (Serrada et al., 1998a;
Ciancio and Nocentini, 2002; Montes et al., 2004; Piussi, 2006;
Fabbio, 2015).
There was a significant reduction in the use of the coppice system in the mid-20th century (Terradas, 1999; Agnoletti, 2002;
Fonti et al., 2006; Burgi, 2015), when the use of new energy sources
based on oil and gas progressively replaced wood and charcoal for
both domestic and industrial uses. The concurrent migration of a
large part of the rural population towards industrial urban areas
and the end of traditional farming activities led to the abrupt abandonment of a portion of the coppice forests that had been regularly
and intensively managed over centuries; this resulted in the creation of excessively dense forest stands over large areas (Amorini
and Fabbio, 1990, 1992, 1994; Gracia et al., 1999; Terradas,
1999). The coppice woodlands were therefore exposed to high fire
risk, poor aesthetics, low biodiversity and arrested regeneration
(Palmberg-Lerche, 2001; Teissier Du Cros, 2001; Mairota et al.,
2014; Kirby, 2015; Mullerova et al., 2015a).
The proactive option was to convert the outgrown, overstocked
coppices back to high forest. As a rule, the high-forest type is considered more valuable because it provides higher-quality wood,
improved protection against natural hazards such as snow avalanches or landslides, the capability of enhancing societal and
ecosystem services-benefits, more attractive space for recreation
and more lasting types of biodiversity (Chatziphilippidis and
Grigoriadis, 1998; Cutini, 2000; Cutini and Hajny , 2006; Kopecky
et al., 2013; Bruckman et al., 2016). This technique is fully based
on thinning.
Reducing forest stand density by silvicultural practices is globally recognized as an approach to restore ecosystem resilience and
lower wildfire risks (McDowell et al., 2006; Allen et al., 2010). Silvicultural practices may also be used for the ecological restoration
of old-growth forests to trigger the regeneration phase (Covington
and Moore, 1994; Mast et al., 1999), or a more proactive approach
may be applied to younger forests (Skov et al., 2004). This topic is
of special concern to coppice forests in the Mediterranean area
where thinning is considered to be a management tool that (i)
avoids heavy intra-specific competition and increases tree resistance to drought stress (Ducrey and Toth, 1992; Gracia et al.,
1999); (ii) contributes to the improvement of tree water status
and productivity in water-limited systems (Canellas et al., 2004;
Moreno et al., 2007); (iii) addresses climate change mitigation
strategy in Mediterranean forest types (Serrada et al., 1998b;
Moreno and Cubera, 2008; Cotillas et al., 2009). The detrimental
effect of overstocking on tree vitality, growth and survival is also
highlighted (Amorini and Fabbio, 1994; Bréda et al., 1995;
Terradas, 1999; Barton and Montagu, 2006). This research gap
should be investigated for two reasons: firstly, in view of changing
climate scenarios, it could contribute further elements of concern
159
as drought will be a relevant issue in forestry (IPCC, 2014). It
seems, therefore, reasonable to carry out thinning in coppices to
increase soil moisture (Cotillas et al., 2009). In this context, the
Mediterranean area hosts the most vulnerable biomes to the
drought-heat shift in progress because it is in the transition zone
between arid and humid regions (Sabaté et al., 2002; Ogaya
et al., 2003; Peñuelas et al., 2004; Bréda et al., 2006; HernandezSantana et al., 2009; IPCC, 2014; Gratani et al., 2016). Secondly,
in relation to the environmentally induced changes faced by
released trees in the coppice turn-over or the transition from coppices to high-forest types. Here, particular attention was given to
the relationship between the carbon gain and water loss in order
to highlight the role of the functional ‘‘intrinsic water-use efficiency” (iWUE) trait. The iWUE may be indirectly estimated via
the stable carbon isotope analyses in phytomass for this purpose.
Indeed, the ratio of fixed carbon to lost water is controlled by both
stomatal conductance and photosynthetic capacity. Likewise, carbon isotope composition (d13C, the deviation from the unit of the
ratio of carbon isotope ratios of a sample and of the standard), of
photoassimilates is controlled by stomatal conductance and photosynthetic capacity (Farquhar et al., 1982; Ehleringer, 1993). Indeed,
iWUE is defined as:
iWUE ¼ A=gs ¼ ca ½1 ðci =ca Þð0:625Þ
ð1Þ
where A is the rate of CO2 assimilation, gs is stomatal conductance
of water vapor and ci and ca are the intercellular and atmospheric
CO2 concentrations respectively. A detailed experimental comparison of three different methods to investigate WUE is in Ripullone
et al. (2004).
The study aims are twofold. We firstly performed a bibliometric
analysis to answer the following questions: (i) how the topic
addressing the use of stable carbon isotopes in forest management
research is structured in terms of the most commonly occurring
research terms and how they are intra-related? (ii) did d13C analysis have an impact on forest management issues? (iii) if yes, which
were the most relevant research in terms of co-cited publications?
Furthermore, based on the bibliometric analysis outcomes, we conducted a retrospective literature-analysis to find out which functional research hypotheses could explain the carbon isotope
responses after forest stand density reduction, also in relation to
the complementary outcomes from the mensurational surveys in
coppice forests.
2. Mapping using a science mapping approach: most commonly
occurring and co-cited research
2.1. Data gathering
A bibliometric approach was used here to investigate global
research trends of stable carbon isotope technique applied to silvicultural research between 1996 and 2015. All bibliographic records
in English were retrieved from the Elsevier’s Scopus database using
the following keywords in the title, abstract and keywords fields:
carbon PRE/1 isotop⁄ AND silvicultur⁄ OR carbon PRE/1 isotop⁄
AND forest management OR carbon PRE/1 isotop⁄ AND thinning
OR carbon PRE/1 isotop⁄ AND wood harvest⁄ OR carbon PRE/1 isotop⁄ AND coppicing OR carbon PRE/1 isotop⁄ AND coppice cut OR
carbon PRE/1 isotop⁄ AND high forest OR carbon PRE/1 isotop⁄
AND mediterranean coppices OR carbon PRE/1 isotop⁄ AND coppice stand⁄ OR carbon PRE/1 isotop⁄ AND coppice woodland OR
carbon PRE/1 isotop⁄ AND canopy OR carbon PRE/1 isotop⁄ AND
forest cover OR carbon PRE/1 isotop⁄ AND competition OR carbon
PRE/1 isotop⁄ AND heavy thinning OR carbon PRE/1 isotop⁄ AND
adaptive management AND NOT marine sea AND NOT ocean sea.
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2.2. Bibliometric mapping
Based on the publications retrieved, we constructed a term map
using the VOSviewer software freely available at: www.vosviewer.com (van Eck and Waltman, 2010). The rationale underlying
a term map is to provide a visual representation of the domain subject to investigation, by showing the most important terms occurring in the titles and abstracts of publications. Thanks to the VOS
(Visualization of Similarities) mapping technique, terms that often
co-occur in the same publications are located close to each other in
a term map, while terms that have no or almost no co-occurrences
are located further away from each other. Each term is represented
by a circle, where its diameter and the size of its label indicate the
number of publications that have the corresponding term in their
title or abstract. Additionally, using the VOS clustering technique,
the software identifies clusters of related terms. Therefore, the
grouping of terms in a term map provides an overview of the main
topics in a field. We should note that in term maps colors are used
to identify clusters of related terms, while in the citation maps the
colors indicate the average citation impact of publications in which
the term occurs. More detailed methodological indications are
reported in Nardi et al. (2016).
2.3. How do the topic is structured?
A total of 1428 publications over the surveyed period was
found. Articles (1350) were the most-frequently used document
type, amounting to 94% of the total, followed by conference papers
(34; 2.4%), reviews (19; 1.3%), plus other less significant issued
papers such as book chapters, notes and letters.
Fig. 1 shows the term map over the period investigated. The
term map was set up based on 490 terms grouped into three clusters (red, blue and green) (see also S1). The green cluster (left side
of the map) grouped terms that were closely-related to the management of forest soil and forest carbon sequestration research
topics (i.e., soil organic carbon, organic matter, forest soil, microbial community, soil respiration, pool, carbon dioxide, flux, respiration and fungi). The blue cluster (left side of the map) grouped
terms mainly related to the management of terrestrial ecosystems,
especially in addressing research questions related to the impact of
human activities on plant and animal communities. Interestingly,
this cluster showed a sub-topic, which accommodates terms
related to fauna research topics (i.e., bird, fish, trophic level, animal, diet, food resource, predator, and prey). The red cluster (right
side of the map) grouped terms mainly related to the management
of forest ecosystems, with particular regard to the ecophysiological response of forest stands after silvicultural practices.
Overall, all these terms showed high intra-relationships with the
term ‘‘carbon isotope discrimination”, and ‘‘discrimination”, thus
indicating the exclusive use of the carbon isotope approach to
answer the research questions raised by forest management issues.
Yet, a further interpretation of this finding could be found in
searching for the physiological responses leading to the d13C variations after forest stand density has been reduced.
Fig. 1. Term map depicting the global research trends of carbon isotope technique applied to silvicultural research over the period of 1996–2015. The higher the occurrence of
terms, the larger are their labels and circles. Colors correspond to clusters and lines (300) indicate co-occurrence links between terms. (For interpretation of the references to
colour in this figure legend, the reader is referred to the web version of this article.)
G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
161
Fig. 2. Term citation impact map depicting the global research trends of carbon isotope technique applied to silvicultural research over the period of 1996–2015. Blue, green
and red colors indicate, low, normal and high citation impact, respectively based on the fixed threshold ranging from 0 (minimum) to 2 (maximum). Lines (300) indicate cooccurrence links between terms. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
2.4. Most relevant research and its potential impact on forest
management issues
Based on the citation map (Fig. 2) we assumed that highly cited
terms (highlighted as red), i.e. based on the average citation impact
scores (see also S1) correspond to the most relevant research in
addressing forest management issues using the isotope approach.
Therefore, within the forest soil and forest carbon sequestration
research topics (green cluster), highly cited terms such as ‘‘fungi”,
‘‘bacterium”, ‘‘soil microorganism”, ‘‘microbe”, ‘‘carbon allocation”,
‘‘phloem”, ‘‘photosynthate”, ‘‘recent photosynthate”, ‘‘phospholipids fatty acid analysis” and ‘‘arbuscural mycorrhizal fungi” represented the most cited terms. Terrestrial ecosystem
management and the related human impact research (blue cluster)
showed only four highly cited terms such as ‘‘biomarker” (score:
1.61), ‘‘canopy cover” (score: 1.36), ‘‘evolution” (score: 1.22), and
‘‘particulate organic matter” (score: 1.21). Conversely, the forest
ecosystem management (including silviculture and ecophysiology) topic (red cluster) showed several highly cited terms,
particularly associated to forest productivity and physiological
traits (mainly related to water-use efficiency and leaf gas
exchanges). Some terms here exceeded the fixed maximum threshold score (i.e., >2), namely ‘‘severe drought” (score: 2.29), ‘‘FACE”
(score: 2.11) and ‘‘elevated CO2” (score: 2.07), indicating the very
high impact of this research in the management of forest ecosys-
tems. We also found highly cited terms linked to forest research
practices here such as ‘‘fertilization”, ‘‘irrigation”, ‘‘survival”, ‘‘mortality”, and ‘‘genotype”.
3. Reviewing literature on the response of released trees via
stable carbon isotopes technique: a retrospective analysis
Based on the higher occurrence of research terms and the
higher average citation impact scores of the red cluster (i.e., ecophysiological responses after forest stand density reduction) as
compared to the rest of clusters (S1), we performed a retrospective
literature-analysis across the globe to understand which functional
processes affected forest stand density reduction.
Carbon isotope composition (d13C) and carbon isotope discrimination (D13C) responses to forest stand density reduction have
mainly been studied in leaves and wood (mainly tree rings), conifers (Leavitt and Long, 1986; Walcroft et al., 1996; Warren et al.,
2001; McDowell et al., 2003, 2006; Martín-Benito et al., 2010;
Moreno-Gutierrez et al., 2011; Fernandes et al., 2016; Giuggiola
et al., 2015), and European beech (Duquesnay et al., 1998;
Gessler et al., 2001; Fotelli et al., 2003; Keitel et al., 2003), with
varying site conditions (from boreal to semi-arid). Stable carbon
isotopes in tree-rings (cellulose or whole wood) were mainly used
in studying retrospective physiological responses to forest
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G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
management over decades, especially when a nearby stand that
had not been subject to forest management practices could act as
a control for separate climate effects (Brooks and Mitchell, 2011).
Little is known about the Mediterranean coppice forests as ecophysiological studies testing the effect of silvicultural practices on
standing trees have been limited to the analysis of stomatal conductance and transpiration (Cutini and Mascia, 1998; Granier
et al., 2000; Holisova et al., 2015; Pietras et al., 2016), soil water
content (Cutini and Benvenuti, 1998; Moreno and Cubera, 2008),
water potential (Aussenac and Granier, 1988; Bréda et al., 1995;
Moreno and Cubera, 2008; Hernandez-Santana et al., 2009), leaf
area index (Cutini, 1994a,b, 1997, 2006; Cutini and Hajny , 2006;
Cotillas et al., 2009) and C and N pools (Di Matteo et al., 2014a;
Bruckman et al., 2016). No study of d13C spatio-temporal variability
has been performed so far.
We found a pioneering study in Mediterranean coppice forests
aimed at investigating the response of carbon isotope composition
in tree rings following coppice management (Di Matteo et al.,
2010). This study pointed out decreased carbon isotope composition values both after coppice harvesting (clear-cutting) and following its conversion into high forest (heavy thinning),
suggesting a decrease in water-use efficiency (WUE) caused by
the parallel increases in gs and A. Other authors hypothesized that
the decrease in carbon isotope composition in standing trees probably indicates improved water availability, possibly induced by a
decrease in competition or a decrease in the precipitation intercepted by the canopy (i.e., a heavier increase in gs than in A,
whereas a decrease in A was highly unlikely), i.e. the first
hypothesis.
However, the lagged tree-rings d13C response to thinning was
noteworthy, as it showed a significant response only from the second year. Previous studies explained this delay by the presence of
carbohydrates assimilated the year before in the tree ring of a
given year (Kozlowski, 1992; Gessler et al., 2001; Fotelli et al.,
2003; Keitel et al., 2003; Skomarkova et al., 2006), thus not fully
reflecting the environmental condition at the time of sampling.
Moreover, even if the theory underlying stable isotope fractionation at the leaf scale and its transference to the tree-ring archive
has been well-developed, several studies issued in recent years
highlighted missing processes in the theory, especially with regard
to the path from leaf photosynthate production to wood formation
(Gessler et al., 2014). This would produce partial decoupling
between the leaf signals recording physiological processes (stomatal conductance, transpiration and photosynthesis) and the wood
or cellulose signals that are assumed to store the physiological
record. This also suggests that the physiological acclimation to silvicultural practices is a gradual process as the lagged response in
d13C is consistent with the delayed growth rates noticed in conifers
after forest stand density reductions (McDowell et al., 2003, 2006;
Bebber et al., 2004; Bevilacqua et al., 2005). This pattern could be
associated with the physiological acclimation to the establishment
of canopy gaps, a slow process mainly driven by changes in leaf
morphology as well as by the time needed to main canopy layer
closure.
Based on the hypothesis that gs increases after the silvicultural
practices (i.e., the first hypothesis), Cutini and Mascia (1998) stated
that trees released by the conversion of a Mediterranean coppice to
high forest (about 60% of basal area removed) showed higher gs
values compared to the trees in a unthinned plot. Furthermore,
the maximum gs values were recorded generally at midday when
VPD (Vapor Pressure Deficit) and temperatures were below
1.5 kPa and 25 °C. The authors concluded that the higher daily pattern of stomatal conductance in the thinned plot could be
explained by lower competition for nutrients, especially water,
rather than increased light availability. These findings were in
agreement with stable carbon isotope analyses conducted in man-
aged forest ecosystems that had Mediterranean and xeric site conditions (McDowell et al., 2003, 2006; D’Alessandro et al., 2006; Di
Matteo et al., 2010; Moreno-Gutierrez et al., 2011; Giuggiola et al.,
2015).
Conversely, there is a research hypothesis that attributes
increased d13C values after forest stand density reduction as the
result of greater changes in A compared to gs (Warren et al.,
2001; Powers et al., 2010; Brooks and Mitchell, 2011), i.e. the second hypothesis. This occurrence was observed however in mesic
sites and wet areas where water is not a limiting factor. These findings were also confirmed by a recent work from Navarro-Cerrillo
et al. (2016) as they found higher iWUE values (i.e., increased
d13C values) following thinning practices in mountain Pinus pinaster stands, essentially due to higher overall photosynthetic assimilation ability rather than better stomatal control of water losses or
to a combination of both factors.
These differing research hypotheses to forest stand density
reduction would lead to two contradictory functional hypotheses,
i.e. canopy light exposure and soil water supply. Increased canopy
light would increase A, while increased soil moisture would
increase gs. However, we should also consider that an increase in
canopy light would also have positive effects on stomatal opening.
Martín-Benito et al. (2010) did not find any significant differences in tree-ring carbon isotopes between unthinned and thinned
plots, thus indicating that stomatal conductance and photosynthetic capacity did not change or changed in the same direction,
i.e. the third hypothesis.
Our interpretation of these different results of the different
thinning intensities of the stands is as follows: both coppice
clear-cutting and conversion thinnings cause a heavy and sudden
reduction in LAI (Leaf Area Index) and alter the aerodynamic characteristics of the canopy, with increased ‘‘coupling” with the free
atmosphere. Therefore, in a dense forest, the carbon isotope composition of atmospheric CO2 may be relatively more negative,
due to increased recycling of light-respired CO2, as compared to
thinned and coppiced stands.
The studies formulating the first hypothesis showed that A/gs is
negatively correlated with water availability because gs increases
more in response to increasing water availability than the concomitant increase in A (see also Meinzer et al., 1993; Livingston
and Spittlehouse, 1996). Warren et al. (2001) pointed out that
the increase in light availability due to thinning may be associated
with a parallel increase in the nitrogen content on a leaf area basis
(which should increase A/gs) and soil moisture (which should
decrease A/gs), thus balancing the two effects, i.e. no A/gs response
to thinning according to the third hypothesis.
In general, increased d13C values after forest stand density
reduction could be driven by a higher increase in leaf nitrogen
and chlorophyll content (i.e., A increase) compared to the increase
of gs (the second hypothesis), possibly due to the higher amount of
nitrogen assimilated in the stand during rain episodes, especially
when forest stands are located in wet areas where water is not a
limiting factor. This was because forest stand density reduction
affects the canopy, increasing the percentage of gap fraction and
thereby improving soil moisture due to the reduced amount of
rainfall intercepted by the canopy. This was also observed in other
stands a few years after thinning (Cantore and Iovino, 1989;
Ducrey and Toth, 1992; Stogsdill et al., 1996; Aussenac and
Granier, 1988; Gracia et al., 1999; Canellas et al., 2004; Moreno
et al., 2007; Moreno and Cubera, 2008; Cotillas et al., 2009). By
increasing the coppice canopy gaps via thinning, the radiation
regime also changes (Cutini, 2006; Cutini and Hajny , 2006) and
these modifications can be detected by stable carbon isotopes
(Gessler et al., 2001). D’Alessandro et al. (2006) observed decreasing leaf and tree-ring d13C values after heavy thinning as a consequence of the higher stomatal conductance due to higher
G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
irradiance levels. Moreover, decreased competition for light, water
and nutrients, such as the presence of logging due to silvicultural
practices, may increase the amount of nutrients available for a
notable growth increase and change of leaf area index (LAI) (De
las Heras et al., 2012). Conversely, under conditions of relatively
low irradiance (dense forest stands), spots of high irradiance (sunflecks) may occur frequently, but with limited duration, thus
increasing A (Chazdon, 1988) and decreasing gs. Indeed, stomata
may not react as quickly as the photosynthetic apparatus to sudden changes of irradiance, thus implying lower stomatal conductance to water vapor and increased WUE (Nobel, 1991).
However, in Mediterranean site conditions, other factors may
be related to the physiological response to forest stand density
reduction, such as nutrient limitation, microclimate acclimation,
and reallocation of carbohydrates to other tissues with higher priority as C sinks (Peñuelas et al., 2011).
4. Coppice forests: customary and carbon isotopes analyses,
common findings, roles and target
Classic mensurational and eco-physiological praxis do not get
the accurate resolution as the technique with stable isotopes does.
That is why coppice forests analysis incorporates well any supplement of knowledge provided by this specific tool. As a general rule,
the main purpose of the applied research in forest management
issues is devoted to answering research questions linked to the
ecological, technical and economic viability of the options tested
by permanent research plots; this is because the organisms are
long-lived (the trees) and forest stands are permanent structures.
The analysis allows the direction of change to be checked, along
with the relative distance from expected goals. Inventories of the
main mensurational variables (individual to stand descriptors)
are therefore routinely performed every few years, i.e. a five-year
interval was the ICP-Forests choice (http://icp-forests.net/) to verify growth pattern tree mortality rates, the distribution across the
tree size distribution (i.e., stand dynamics).
A shorter time span (i.e., one growing season or intra-annual
growth) can be used for tree-ring analysis (radial stem growth)
and stem analysis, with this technique detailing the threedimensional growth pattern of a tree. The same resolution can be
achieved by repeated readings throughout the growing season by
precision growth girth bands. The intra-annual timing is commonly used to find out relationships between radial growth,
species-specific ecological requirements and seasonal climate
course. These tools are especially used when new mensurational
knowledge is needed because further growth conditions are being
established as in the case of coppice forest management options
mentioned above.
Stem analyses and modelling undertaken so far as part of longterm monitoring trials (Amorini and Fabbio, 1986, 1989; Amorini
et al., 1995) were aimed at reconstructing individual/stand growth
in the main crop layer following customary rotation time (the ageing period) and after the thinning (the first step of conversion
phase). Common responses were: (i) the positive growth pattern
while ageing; (ii) the prompt growth rate increase in the year following the thinning.
Functional responses detected by stable carbon isotope analysis
explain this last finding well as the rapid acclimation response to
the drastically changed ecological condition after thinning. The
transient effect also detected by the isotopic analysis due to the
re-establishment of canopy closure 5–7 years later (oak stands),
matches the results of stem analysis well (Amorini and Fabbio,
1986, 1989), in addition to eco-physiological investigations
(Cutini and Benvenuti, 1998; Cutini and Mascia, 1998; Espelta
et al., 2003; Cutini, 2006; Cotillas et al., 2009). These results are
163
in full accordance with the first hypothesis. Thinning is the driver
promoting the heavy reduction of inter-individual competition
among shoots on the same stool and among neighbouring stools.
Positive feedback is the increased water availability, which triggers
the growth rate increase, while a possible limiting factor is the soil
drying due to higher incoming radiation, especially in heat and
drought-sensitive environments. In this sense, a working hypothesis based on two MEDCOP experiments on Turkey oak (Cutini and
Benvenuti, 1998) and holm oak (Huc and Ducrey, 1998) found that
soil water balance was not affected by even heavy thinnings, at
least in the upper soil layers. This might be due to the compensation between the increased water losses by evapotranspiration due
to higher irradiance at ground level, the increased water input due
to the lower rainfall interception by canopy, and the reduced stand
transpiration, i.e. the lower incidence of the main component of
evaporative water flux (Huxman et al., 2005).
The basic role of isotope analysis therefore would appear to
support the analysis tools already in use where these cannot reach
the same sensitivity and resolution.
Mensurational analysis has reached mature status, with development of a series of tools working with different purposes at complementary spatial-temporal scales. Eco-physiological analysis has
developed and verified the underlying theories. It covers the full
range of issues and its current advancement is linked more to
the instrumental progress. The analyses provided usually refer to
when they were carried out.
Isotope analysis widens the capability of eco-physiology investigations both in terms of sensitivity and retrospective analysis.
This helps in the further understanding of the interplay between
the different eco-physiological factors, which can lead to new
working hypotheses and support the relative scientific evidence,
as in the case-studies reported in the paper.
All of the above tools therefore have a role in principle and in
practice, since each of them provides different scales of evidence
from the suitability of a management option to the forest manager,
up to the fine bio-ecological response in terms of time, extent and
length of the acclimation response of trees to a disturbance (a silvicultural practice, in the case).
A common goal of the proposed multi-type and multi-scaled
analysis is to make the best-fitting tools available to handle current
uncertainties and future unpredictability and related management
risks linked to climate shifting (Millar et al., 2007; Lindner et al.,
2010; Di Matteo et al., 2014b; Allen et al., 2015).
5. Conclusions
The results of the review showed how useful stable carbon isotopic analyses are to study the impact of forest management on the
physiology of released trees. By studying the specific literature on
this topic, we found that forest ecosystems react to forest stand
density reduction by changing photosynthetic assimilation and
stomatal conductance in accordance with three research hypotheses, thus adjusting the iWUE of the trees to ensure their homeostatic maintenance and, where site conditions are favorable, in
stimulating growth rates. In particular, Mediterranean coppice forests react to silvicultural practices by decreasing iWUE, owing to a
higher increase in gs than A. Our interpretation of these findings is
that water, and more in general, nutrients, radiation and associated
meteorological variables like temperature, humidity and vapor
pressure deficit, significantly change after forest stand density
reduction, and continue up until when they are partly recovered
by canopy restoration. This may become a key-point in how to
interpret tree acclimation status via carbon isotope analyses, since
each specific forest ecosystem reacts to silvicultural practices differently, depending on the auto-ecology and site conditions.
164
G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
The classic forest mensuration interpretative ability, the wellknown techniques developed under eco-physiology and new tools
such as stable isotope identification would appear to provide additional support in a unique strategy to tackle current challenges.
Acknowledgments
GDM received funds from the ERANET FORESTERRA project
‘‘Enhancing Forest RESearch in the MediTERRAnean through an
improved coordination and integration” (Grant 291832). GDM conceived the research, wrote and performed the analysis of stable
carbon isotopes literature. PN performed the bibliometric analyses.
GF wrote and performed the analysis of coppice literature. We are
grateful to Patricia Crotty for editing and revising the usage of
English language. We would like to extend our gratitude to two
anonymous reviewers who helped us to improve an earlier version
of the paper.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.foreco.2016.12.
030.
References
Agnoletti, M., 2002. Bosco ceduo e paesaggio: processi generali e fattori locali
[Coppice woods and landscape: analysis and evaluation of a cultural factor]. In:
Ciancio, O., Nocentini, S. (Eds.), Il bosco ceduo in Italia. Accademia Italiana di
Scienze Forestali, Firenze, pp. 21–62.
Agnoletti, M., 2003. Note sui principali mutamenti avvenuti negli ecosistemi
forestali italiani dall’Unità ad oggi [Notes on main changes occurred in Italian
forest ecosystems from the Unity up to the present time]. In: De Angelis, et al.
(Eds), Atti III Congresso nazionale SISEF Alberi e Foreste per il nuovo millennio.
Viterbo, October 15–18, 2001, pp. 127–132.
Allen, C.D., Macalady, A.K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier,
M., Kitzberger, T., Rigling, A., Breshears, D.D., Hogg, E.H., Gonzalez, P., Fensham,
R., Zhang, Z., Castro, J., Demidova, N., Lim, J.H., Allard, G., Running, S.W., Semerci,
A., Cobb, N., 2010. A global overview of drought and heat-induced tree mortality
reveals emerging climate change risks for forests. Forest Ecol. Manage. 259,
660–684.
Allen, C.D., Breshears, D.D., McDowell, N., 2015. On underestimation of global
vulnerability to tree mortality and forest die-off from hotter drought in the
Anthropocene. Ecosphere 6 (8), 129.
Amorini, E., Fabbio, G., 1986. Studio auxometrico in un ceduo invecchiato e in una
fustaia da polloni di faggio, sull’Appennino toscano - Primo contributo [Growth
assessment at an outgrown beech coppice and at a transitory crop in the
Tuscany Apennines - First contribution]. Annali Istituto Sperimentale
Selvicoltura, Arezzo 14, 283–328.
Amorini, E., Fabbio, G., 1989. L’avviamento all’altofusto nei cedui a prevalenza di
cerro. Risultati di una prova sperimentale a 15 anni dalla sua impostazione.
Studio auxometrico. Secondo contributo [Conversion into high forest of Turkey
oak coppices. Results of an experimental trial fifteen years later. Growth
analysis. Second contribution]. Annali Istituto Sperimentale Selvicoltura, Arezzo
18, 19–70.
Amorini, E., Fabbio, G., 1990. Le ‘vieillissement’ des taillis en Italie: étude
auxométrique et traitement de la futaie sur souches [The ‘outgrowing’ of
coppice forests in Italy: growth analysis and silviculture of the conversion into
high forest]. In: Proceedings IUFRO, XIX World Congress, Montreal, vol. 1,
August 5–11, 1990, pp. 363–374.
Amorini, E., Fabbio, G., 1992. A rapidly changing cultivation system: the coppice.
Proceedings 1st European Symposium on Terrestrial Ecosystems. Forests and
Woodlands, Florence. Elsevier, London, pp. 902–903. May 20–24, 1991.
Amorini, E., Fabbio, G., 1994. The coppice area in Italy. General aspects, cultivation
trends and state of knowledge. Proceedings Workshop ‘Improvement of Coppice
Forests in the Med Region’. Arezzo, September 24–25, 1992, vol. 23. Annali
Istituto Sperimentale Selvicoltura, Arezzo, pp. 292–298.
Amorini, E., Fabbio, G., Tabacchi, G., 1995. Le faggete di origine agamica: evoluzione
naturale e modello colturale per l’avviamento ad alto fusto [Ageing beech
coppices: natural evolutive pattern and cultivation model for its conversion into
high forest]. In: Atti Seminario ‘Funzionalità del sistema faggeta’. AISF, Firenze
November 16–17, pp. 331–345.
Aussenac, G., Granier, A., 1988. Effects of thinning on water stress and growth in
Douglas-fir. Can. J. Forest Res. 60, 100–105.
Barton, C.V.M., Montagu, K.D., 2006. Effect of spacing and water availability on root
to shoot ratio in Eucalyptus camaldulensis. Forest Ecol. Manage. 221, 52–62.
Bebber, D.P., Thomas, S.C., Cole, W.G., Balsillie, D., 2004. Diameter increment in
mature eastern white pine Pinus strobus L. following partial harvest of oldgrowth stands in Ontario, Canada. Trees 18 (1), 29–34.
Bevilacqua, E., Puttock, D., Blake, T.J., Burgess, D., 2005. Long-term differential stem
growth responses in mature eastern white pine following release from
competition. Can. J. Forest Res. 35 (3), 511–520.
Bréda, N., Granier, A., Aussenac, G., 1995. Effects of thinning on soil water relations,
transpiration and growth in an oak forest (Quercus petraea Matt. Liebl.). Tree
Physiol. 15, 295–306.
Bréda, N., Huc, R., Granier, A., Dreyer, E., 2006. Temperate forest trees and stands
under severe drought: a review of eco-physiological responses, adaptation
processes and long-term consequences. Ann. Forest Sci. 63, 625–644.
Brooks, J.R., Mitchell, A.K., 2011. Interpreting tree responses to thinning and
fertilization using tree-ring stable isotopes. New Phytol. 190 (3), 770–782.
Bruckman, V.J., Terada, T., Fukuda, K., Yamamoto, H., Hochbichler, E., 2016.
Overmature periurban Quercus-Carpinus coppice forests in Austria and Japan:
a comparison of carbon stocks, stand characteristics and conversion to high
forest. Eur. J. Forest Res., 1–13
Burgi, M., 2015. Coppicing in the past - examples of practice, context and
consequences. In: ‘Coppice forests: past, present and future’ International
conference. Brno, Czech Republic, 9–11 April 2015. <http://coppice.
eu/conference_en.html>.
Canellas, I., del Rio, M., Roig, S., Montero, G., 2004. Growth response to thinning in
Quercus pyrenaica Willd. coppice stands in Spanish central mountain. Ann.
Forest Sci. 61, 243–250.
Cantore, V., Iovino, F., 1989. Effetti dei diradamenti sull’umidità del suolo in
popolamenti di douglasia della Catena Costiera (Calabria) [Effects of different
thinning regimes on stand stability and timber assortments in a Douglas-fir
forest]. Annali Istituto Sperimentale Selvicoltura 20, 13–39.
Chazdon, R.L., 1988. Sunflecks and their importance to forest understorey plants.
Adv. Ecol. Res. 18, 1–63.
Chatziphilippidis, G., Grigoriadis, N., 1998. Natural regeneration in Quercus frainetto
Kit. Annali Istituto Sperimentale Selvicoltura, Arezzo 27, 177–181.
Ciancio, O., Nocentini, S. (Eds.), 2002. Il bosco ceduo in Italia [The coppice forest in
Italy]. Accademia Italiana di Scienze Forestali, Firenze, p. 678.
Covington, W.W., Moore, M.M., 1994. Post-settlement changes in natural fires
regimes and forest structure: ecological restoration of old-growth ponderosa
pine forests. J. Sustain. Forestry 2, 153–181.
Cotillas, M., Sabaté, S., Gracia, C., Espelta, J.M., 2009. Growth response of mixed
Mediterranean oak coppices to rainfall reduction: could selective thinning have
any influence on it? Forest Ecol. Manage. 258 (7), 1677–1683.
Cutini, A., 1994a. Indice di area fogliare, produzione di lettiera ed efficienza di un
ceduo di cerro in conversione [Leaf Area Index, litterfall and efficiency of a
Turkey oak coppice in conversion into high forest]. Annali Istituto Sperimentale
Selvicoltura, Arezzo 23, 147–166.
Cutini, A., 1994b. La stima del LAI con il metodo delle misure di trasmittanza in
popolamenti diradati e non diradati di cerro [The estimate of LAI from canopy
transmittance in thinned and unthinned Turkey oak stands]. Annali Istituto
Sperimentale Selvicoltura, Arezzo 23, 167–181.
Cutini, A., 1997. Drought effects on canopy properties and productivity in thinned
and unthinned Turkey oak stands. Plant Biosyst. 131 (1), 59–65.
Cutini, A., 2000. Produttività e processi ecologici in popolamenti di origine agamica
[Stand productivity and ecological processes into coppice forests]. In: Bucci, G.,
et al. (Eds), Atti II Congresso nazionale SISEF Applicazioni e prospettive per la
ricerca forestale italiana. Bologna, October 20–22, 1999, pp. 131–134.
Cutini, A., 2006. Taglio di avviamento, ceduazione e matricinatura: effetti sulle
caratteristiche della copertura forestale in cedui a prevalenza di cerro [Coppice
conversion cuts, coppicing and standards density: effects on canopy properties
of Turkey oak coppice stands]. Annali Istituto Sperimentale Selvicoltura, Arezzo
33, 21–30.
Cutini, A., Benvenuti, C., 1998. Effects of Silvicultural Treatment on Canopy Cover
and Soil Water Content in a Quercus cerris L. Coppice. Annali Istituto
Sperimentale Selvicoltura, Arezzo 27, 65–70.
Cutini, A., Mascia, V., 1998. Silvicultural Treatment of Holm Oak (Quercus ilex L.)
Coppices in Southern Sardinia: Effects of Thinning on Water Potential,
Transpiration and Stomatal Conductance. Annali Istituto Sperimentale
Selvicoltura, Arezzo 27, 47–53.
Cutini, A., Hajny, M., 2006. Effetti del trattamento selvicolturale su produzione di
lettiera, caratteristiche della copertura ed efficienza in un ceduo di cerro in
conversione [Effects of the silvicultural treatment on litter production, canopy
characteristics and stand efficiency in a Turkey oak coppice in conversion to
high forest]. Annali Istituto Sperimentale Selvicoltura, Arezzo 33, 131–142.
D’Alessandro, C.M., Saracino, A., Borghetti, M., 2006. Thinning affects water use
efficiency of hardwood saplings naturally recruited in a Pinus radiata D. Don
plantation. Forest Ecol. Manage. 222, 116–122.
De las Heras, J., Moya, D., López-Serrano, F.R., Rubio, E., 2012. Carbon sequestration
of naturally regenerated Aleppo pine stands in response to early thinning. New
Forest. 44, 457–470.
Di Matteo, G., De Angelis, P., Brugnoli, E., Cherubini, P., Scarascia-Mugnozza, G.,
2010. Tree-ring D13C reveals the impact of past forest management on wateruse efficiency in a Mediterranean oak coppice in Tuscany (Italy). Ann. Forest Sci.
67 (5), 510.
Di Matteo, G., Tunno, I., Nardi, P., De Angelis, P., Bertini, G., Fabbio, G., 2014a. C and
N concentrations in different compartments of outgrown oak coppice forests
under different site conditions in Central Italy. Ann. Forest Sci. 71 (8), 885–895.
G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
Di Matteo, G., Perini, L., Atzori, P., De Angelis, P., Mei, T., Bertini, G., Fabbio, G.,
Scarascia, Mugnozza G., 2014b. Changes in foliar carbon isotope composition
and seasonal stomatal conductance reveal adaptive traits in Mediterranean
coppices affected by drought. J. Forest. Res. 25 (4), 839–845.
Ducrey, M., Toth, J., 1992. Effects of clearing and thinning on height growth and
girth increment in Holm oak coppices (Quercus ilex L.). Vegetatio 99 (100), 365–
376.
Duquesnay, A., Breda, N., Stievenard, M., Dupouey, J.L., 1998. Changes of tree-ring
d13C and water-use efficiency of beech (Fagus sylvatica L.) in north-eastern
France during the past century. Plant, Cell Environ. 21 (6), 565–572.
Ehleringer, J.R., 1993. Variation in leaf carbon isotope discrimination in Encefalia
farinosa: implications for growth, competition, and drought survival. Oecologia
95, 340–346.
Espelta, J.M., Retana, J., Habrouk, A., 2003. Resprouting patterns after fire and
responses to stool clearing of two coexisting Mediterranean oaks with
contrasting leaf habits on two different sites. Forest Ecol. Manage. 179, 401–
414.
Fabbio, G., 2015. Shaping future coppice forestry on the legacy of the past: lesson
learnt and perspectives. In: ‘Coppice forests: past, present and future’.
International Conference, Brno, April 9–11, 2015. <http://coppice.
eu/conference_en.html>.
Farquhar, G.D., O’Leary, M.H., Berry, J.A., 1982. On the relationship between carbon
isotope discrimination and the intercellular carbon dioxide concentration in
leaves. Aust. J. Plant Physiol. 9, 121–137.
Fernandes, T.J., Del Campo, A.D., Herrera, R., Molina, A.J., 2016. Simultaneous
assessment, through sap flow and stable isotopes, of water use efficiency (WUE)
in thinned pines shows improvement in growth, tree-climate sensitivity and
WUE, but not in WUEi. Forest Ecol. Manage. 361, 298–308.
Fonti, P., Cherubini, P., Rigling, A., Weber, P., Biging, G., 2006. Tree rings show
competition dynamics in abandoned Castanea sativa coppices after land-use
changes. J. Veg. Sci. 17, 103–112.
Fotelli, N.M., Rienks, M., Rennemberg, H., Geßler, A., 2003. Effect of climate and
silviculture on the carbon isotope composition of understorey species in a beech
(Fagus sylvatica L.) forest. New Phytol. 159, 229–244.
Gessler, A., Schrempp, S., Matzarakis, A., Mayer, H., Rennemberg, H., Adams, M.A.,
2001. Radiation modifies the effect of water availability on the carbon isotope
composition of beech (Fagus sylvatica L.). New Phytol. 150, 653–664.
Gessler, A., Ferrio, J.P., Hommel, R., Treydte, K., Werner, R.A., Monson, R.K., 2014.
Stable isotopes in tree rings: towards a mechanistic understanding of isotope
fractionation and mixing processes from the leaves to the wood. Tree Physiol.,
1–23 http://dx.doi.org/10.1093/treephys/tpu040.
Giuggiola, A., Ogée, J., Rigling, A., Gessler, A., Bugmann, H., Treydte, K., 2015.
Improvement of water and light availability after thinning at a xeric site: which
matters more? A dual isotope approach. New Phytol. 210, 108–121.
Gracia, C.A., Sabate, S., Martınez, J.M., Albeza, E., 1999. Functional responses to
thinning. In: Rodà, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecological Studies.
Ecology of Mediterranean Evergreen Oak Forests, vol. 137. Springer, Berlin, pp.
329–338.
Granier, A., Loustau, D., Breda, N., 2000. A generic model of forest canopy
conductance dependent on climate, soil water availability and leaf area index.
Ann. Forest. Sci. 57, 755–765.
Gratani, L., Catoni, R., Varone, L., 2016. Evergreen species response to Mediterranean
climate stress factors. iForest (early view). doi: <http://dx.doi.org/10.3832/
ifor1848-009> [online 2016-07-07].
Hernandez-Santana, V., Martınez-Vilalta, J., Martınez-Fernandez, J., William, M.,
2009. Evaluating the effect of drier and warmer conditions on water use by
Quercus pyrenaica. Forest Ecol. Manage. 258, 1719–1730.
Holisova, P., Pietra, J., Darenova, E., Novosadova, K., Pokorny, R., 2015. Comparison
of assimilation parameters of coppice and non-coppiced sessile oak. In: Coppice
Forests: Past, Present And Future. International Conference, Brno, April 9–11,
2015. <http://coppice.eu/conference_en.html>.
Huc, R., Ducrey, M., 1998. Ecophysiological Response to Thinning in a Quercus Ilex L.
Coppice Stand. Annali Istituto Sperimentale Selvicoltura, Arezzo 27, 39–45.
Huxman, T.E., Wilcox, B.P., Breshears, D.D., Scott, R.L., Snyder, K.A., Small, E.E.,
Hultine, K., Pockman, W.T., Jackson, R.B., 2005. Ecohydrological implications of
woody plant encroachment. Ecology 86, 308–319.
IPCC, 2014. Climate change, impacts, adaptation and vulnerability. Available at
<http://www.ipcc.ch/ report/ar5/wg2/> (accessed 12.01.16).
Keitel, C., Adams, M.A., Holst, T., Matzarakis, A., Mayer, H., Rennemberg, H., Geßler,
A., 2003. Carbon and oxygen isotope composition of organic compounds in the
phloem sap provides a short-term measure for stomatal conductance of
European beech (Fagus sylvatica L.). Plant Cell Environ. 26, 1157–1168.
Kirby, K., 2015. Coppice woods: temporal and spatial diversity creating rich wildlife
assemblages. In: ‘Coppice forests: past, present and future’ International
conference. Brno, Czech Republic, 9–11 April 2015. <http://coppice.
eu/conference_en.html>.
Kopecky, M., Hedl, R., Szabo, P., 2013. Non-random extinctions dominate plant
community changes in abandoned coppices. J. Appl. Ecol. 50, 79–87. http://dx.
doi.org/10.1111/1365-2664.12010.
Kozlowski, T.T., 1992. Carbohydrate Sources and Sinks in Woody Plants. Botan. Rev.
58, 109–130.
Leavitt, S.W., Long, A., 1986. Influence of site disturbance on d13C isotopic time
series from tree rings. In: Proceedings of the International Symposium of
Ecological Aspects of Tree-Ring Analysis, 17–21 August, 1986, Tarrytown, NY,
USA, pp. 119–129.
165
Lindner, M., Maroschek, M., Netherer, S., Kremer, A., Barbati, A., Gonzalo, J.G., Seidl,
R., Delzon, S., Corona, P., Kolstrom, M., Lexer, M.L., Marchetti, M., 2010. Climate
change impacts, adaptive capacity, and vulnerability of European forest
ecosystems. Forest Ecol. Manage. 259, 698–709.
Livingston, N.J., Spittlehouse, D.L., 1996. Carbon isotope fractionation in tree ring
early and late wood in relation to intra growing season water balance. Plant,
Cell Environ. 19, 768–774.
Mairota, P., Manetti, M.C., Amorini, E., Pelleri, F., Terradura, M., Frattegiani, M.,
Savini, P., Grohmann, F., Mori, P., Piussi, P., 2014. Socio-economic and
environmental challenges of responsible coppice management: Italian
examples. In: COST Action FP 1301 EuroCoppice. International event ‘People
and Coppice’, November 3–5, University of Greenwick, UK.
Mast, J.N., Fulé, P.Z., Moore, M.M., Covington, W.W., Waltz, A.E.M., 1999. Restoration
of presettlement age structure of an Arizona ponderosa pine forest. Ecol. Appl.
9, 228–239.
Martín-Benito, D., Del Río, M., Heinrich, I., Helle, G., Cañellas, I., 2010. Response of
climate-growth relationships and water use efficiency to thinning in a Pinus
nigra afforestation. Forest Ecol. Manage. 259 (5), 967–975.
Millar, C.I., Stephenson, N.L., Stephens, S., 2007. Climate change and forest of the
future: managing in the face of uncertainty. Ecol. Appl. 17 (8), 2145–2151.
Montes, F., Cañellas, I., del Río, M., Calama, R., Montero, G., 2004. The effects of
thinning on the structural diversity of coppice forests. Ann. Forest Sci. 61, 771–
779.
McDowell, N., Brooks, J.R., Fitzgerald, S.A., Bond, B.J., 2003. Carbon isotope
discrimination and growth response of old Pinus ponderosa trees to stand
density reductions. Plant Cell Environ. 26, 631–644.
McDowell, N., Henry, D., Adams, J., Bailey, D., Marcey, H., Kolb, T.E., 2006.
Homeostatic maintenance of ponderosa pine gas exchange in response to
stand density changes. Ecol. Appl. 16 (3), 1164–1182.
Meinzer, F., Goldstein, G., Grantz, C., 1993. Carbon isotope discrimination and gas
exchange in coffee during adjustment to different soil moisture regimes. In:
Ehleringer, J.R., Hall, A.E., Farquhar, G.D. (Eds.), Stable Isotopes and Plant
Carbon-Water Relations. Academic Press Inc, San Diego, CA, USA, pp. 327–348.
Morandini, R., 1994. Proceedings of the Workshop ‘Improvement of Coppice Forests
in the Mediterranean Region’, September 24–25, 1992, Arezzo, Italy, vol. 23.
Annali Istituto Sperimentale Selvicoltura, Arezzo, pp. 257–333.
Moreno-Gutierrez, C., Barbera, G.G., Nicolas, E., De Luis, M., Castillo, V.M., MartinezFernandez, F., Querejeta, J.I., 2011. Leaf d18O of remaining trees is affected by
thinning intensity in a semiarid pine forest. Plant, Cell Environ. 34, 1009–1019.
Moreno, G., Cubera, E., 2008. Impact of stand density on water status and leaf gas
exchange in Quercus ilex. Forest Ecol. Manage. 254 (1), 74–84.
Moreno, G., Obrador, J.J., Garcıa, E., Cubera, E., Montero, M.J., Pulido, F.J., Dupraz, C.,
2007. Driving competitive and facilitative interactions in oak dehesas with
management practices. Agroforest. Syst. 70, 25–44.
Mullerova, J., Szabo, P., Hédl, R., Dorner, P., Veverkova, A., 2015. The rise and fall of
coppicing - historical processes and consequences for nature conservation. In:
Coppice forests: past, present and future. International Conference, Brno, April
9–11, 2015. <http://coppice.eu/conference_en.html>.
Nardi, P., Di Matteo, G., Palahi, M., Mugnozza, G.S., 2016. Structure and evolution of
mediterranean forest research: a science mapping approach. PLoS ONE 11 (5),
e0155016.
Navarro-Cerrillo, R.M., Sánchez-Salguero, R., Herrera, R., Ruiz, C.C., Moreno-Rojas, J.
M., Manzanedo, R.D., López-Quintanilla, J., 2016. Contrasting growth and water
use efficiency after thinning in mixed Abies pinsapo-Pinus pinaster-Pinus
sylvestris forests. J. Forest Sci. 62 (2), 53–64.
Nobel, P.S., 1991. Physicochemical and Environmental Plant Physiology. Academic
Press Inc, San Diego.
Ogaya, R., Penuelas, J., Martınez-Vilalta, Mangiron M., 2003. Effect of drought on
diameter increment of Quercus ilex, Phillyrea latifolia, and Arbutus unedo in a
holm oak forest of NE Spain. Forest Ecol. Manage. 180, 175–184.
Palmberg-Lerche, C., 2001. Conservation of forest biological diversity and forest
genetic resources. In: Forest Genetic Resources 28 Rome, FAO.
Peñuelas, J., Sabaté, S., Filella, I., Gracia, C., 2004. Fectos del cambio climatico sobre
los ecosistemas terrestres: observacion, experimentacion y simulacion. In:
Valladares, F. (Ed.), Ecologıa del bosque mediterraneo en un mundo cambiante.
Ministerio de Medio Ambiente, EGRAF, S.A., Madrid, pp. 425–460.
Peñuelas, J., Canadell, J.G., Ogaya, R., 2011. Increased water-use efficiency during the
20th century did not translate into enhanced tree growth. Global Ecol. Biogeogr.
20, 597–608.
Pietras, J., Stojanović, M., Knott, R., Pokorný, R., 2016. Oak sprouts grow better than
seedlings under drought stress. iForest 9, pp. 529–535. doi: <http://dx.doi.org/
10.3832/ifor1823-009>.
Piussi, P., 2006. Close to nature forestry criteria and coppice management. In: Diaci,
J. (Ed.), Nature-based forestry in Central Europe. University of Lubiana Biotechn.
Faculty, pp. 27–30.
Piussi, P., 2015. Coppice management and nutrition. In: Coppice forests: past,
present and future. International Conference, Brno, April 9–11, 2015.
<http://coppice.eu/conference_en.html>.
Powers, M.D., Pregitzer, K.S., Palik, B.J., Webster, C.R., 2010. Wood d13C, d18O and
radial growth responses of residual red pine to variable retention harvesting.
Tree Physiol. 30, 326–334.
Ripullone, F., Lauteri, M., Grassi, G., Amato, M., Borghetti, M., 2004. Variation in
nitrogen supply changes water-use efficiency of Pseudotsuga menziesii and
Populus x euroamericana; a comparison of three different approaches to
determine water-use efficiency. Tree Physiol. 24, 671–679.
166
G. Di Matteo et al. / Forest Ecology and Management 389 (2017) 158–166
Sabaté, S., Gracia, C.A., Sanchez, A., 2002. Likely effects of climate change on growth
of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica
forests in the Mediterranean region. Forest Ecol. Manage. 162, 23–37.
Scarascia-Mugnozza, G., Oswald, H., Piussi, P., Radoglou, K., 2000. Forests of the
Mediterranean region: gaps in knowledge and research needs. Forest Ecol.
Manage. 132, 97–109.
Serrada, R., Bravo, A., Sanchez, I., Allué, M., Elena, R., San, Miguel A., 1998a.
Conversion into high forest in coppices of Quercus ilex subs. ballota L. in Central
region of Iberian Peninsula. Annali Istituto Sperimentale Selvicoltura, Arezzo 27,
149–160.
Serrada, R., Allué, M., San, Miguel A., 1998b. The coppice system in Spain. Current
situation, state of art, and major areas to be investigated. Annali Istituto
Sperimentale Selvicoltura, Arezzo 27, 266–275.
Skomarkova, M.V., Vaganov, E.A., Mund, M., Knohl, A., Linke, P., Boerner, A., Schulze,
E.D., 2006. Inter-annual and seasonal variability of radial growth, wood density
and carbon isotope ratios in tree rings of beech (Fagus sylvatica) growing in
Germany and Italy. Trees 20, 571–586.
Skov, K.R., Kolb, T.E., Wallin, K.F., 2004. Tree size and drought affect ponderosa pine
physiological response to thinning and burning treatments. Forest Sci. 50, 81–
91.
Stogsdill, W.R., Wittwer, R.F., Hennessey, T.C., Dougherty, P.M., 1996. Water use in
thinned loblolly pine plantations. Forest Ecol. Manage. 50, 233–245.
Terradas, J., 1999. Holm oak and holm oak forests: an introduction. In: Roda, F.,
Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak
Forests. Springer-Verlag, Berlin, pp. 3–14.
Teissier du Cros, E., 2001. Conserving forest genetic resources: objectives, research,
networks. In: Forest Genetic Resources Management and Conservation, INRA
DIC, Paris, pp. 4–5.
UN/ECE-FAO, 2000. Forest resources of Europe, CIS, North America, Australia, Japan
and new Zealand. Main report. Geneva. Timber and Forest Study Papers 17,
Geneva, Switzerland.
van Eck, N.J., Waltman, L., 2010. Software survey: VOSviewer, a computer program
for bibliometric mapping. Scientometrics 84, 523–538.
Walcroft, S.A., Silvester, W.B., Grace, J.C., Carson, S.D., Waring, R.H., 1996. Effects of
branch length on carbon isotope discrimination in Pinus radiata. Tree Physiol.
16, 281–286.
Warren, C.R., Mcgrath, J.F., Adams, M.A., 2001. Water availability and carbon isotope
discrimination in conifers. Oecologia 127, 476–486.