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Carbon stock estimation in an unmanaged old-growth forest: a case study from a broad-leaf deciduous forest in the Northwest of Italy/Estimation de stockage de carbone dans une vieilles foret: etude de cas sur une foret temperee decidue au nord-ouest de l'Italie/Estimacion de almacenamiento de carbono de un bosque de edad madura no manejados: un estudio de caso de un bosque caducifolio en el noreste de Italia.

INTRODUCTION

Forest ecosystems are important components of the global carbon cycle. The Kyoto Protocol (UNFCCC 1997) recognized the role of forests in carbon sequestration to mitigate climate change and encouraged forestation projects and strategies for adapted forest management activities (Brown et al. 2002). The Inter-governmental Panel on Climate Change highlights that the forestry sector has one of the greatest potential to reduce atmospheric C[O.sub.2] at a reasonable cost in the next decades, compared to all other mitigation activities (IPCC 2007). In fact, forests contribute to climate change mitigation by removing atmospheric carbon dioxide and storing it in different carbon pools (i.e., biomass, soil, dead organic matter, litter) accounting for 77-82% of the total carbon stocked by the terrestrial vegetation (Garcia-Gonzalo et al. 2007). Carbon is accumulated in forests through biomass, dead organic matter, litter and soil while it is released throughout respiration and decomposition (Del Rio et al. 2008). Forests switch between being a source or a sink of carbon, depending on the succession stage, forest type, disturbance and management activities (Masera et al. 2003). The capacity of forests to act as a carbon sink generally decreases with age as respiration begins equal or exceeds net photosynthesis (Odum 1969). However, little evidence exists that this hypothesis holds true for unmanaged forests covering a wide range of age classes due to natural regeneration and canopy structure (Knohl et al. 2003). Forest management has an important impact on carbon balance (McGrath et al. 2015) and human activities have several direct and indirect influences on forest ecosystems and thus, on carbon sequestration potential (Nabuurs and Schelhaas 2002). In Europe, the total area covered by forests has increased by 25% since 1950 (Fuchs et al. 2013) resulting in a 44% forested area of ecological, political and economic importance (Gallaun et al. 2010). In particular, the European forests absorb about 10% of the European C[O.sub.2] emission (Cameron et al. 2013). There has been a long history of forest exploitation and management in Europe. Thus, the conservation of mature forests is important for the long-term permanence of forest C sinks (Carey et al. 2001). In such context, a forested area of 30 million of ha in Europe has been protected with the main objective to conserve the biodiversity and landscape as triggered by the EU's biodiversity policy (Forest Europe et al. 2011). In particular, old-growth forests provide a large number of ecosystems services such as biodiversity conservation, carbon reservoir and the opportunity for studying ecological process in undisturbed conditions (Wirth et al. 2009). Thus, due to the importance of the forest role in carbon stored and biodiversity conservation, the interest in forested areas has increased in recent years (Parviainen 2005, Kallio et al. 2008, Hein 2011). Moreover, carbon stock estimation and knowledges about its distribution in the different compartments (i.e. aboveground, belowground, deadwood, litter and soil) is essential to evaluate the quantity of carbon that is potentially emitted to the atmosphere when natural or human-induced disturbance occurs (Fonseca et al. 2012). In this context, the main objective of our research was to evaluate the amount of the total carbon stocked and its distribution in its compartments in a unmanaged old-growth broadleaf deciduous forest developed inside the Riserva Integrate Bosco Siro Negri (Northwest of Italy). We analyzed the effect of this type of management on the forest carbon stock also considering the plant species regeneration inside the forest and in the forest boundary.

MATERIALS AND METHODS

Study area

The study was carried out in an old-growth deciduous forest developing inside the Riserva Integrale Bosco Siro Negri (45[degrees]12'39"N; 09[degrees]03'26"E, 74 m a. s. l) in Italy, in the period May-July 2015. The studied forest is one of the few relicts of the original forest which in the past covered the alluvional valley along the Ticino river and where no logging has been carried out since the establishment of the Reserve in 1970 (Sartori 1984, Motta et al. 2009, Castagneri et. al. 2013). The Reserve is a SIC (IT 2080014 'Bosco Siro Negri e Moriano'). The structure of the forest is that of a typical old-growth closed forest. It is characterized by a mosaic of different sized canopy gaps, decaying logs on the forest floor and dead standing trees. The tree layer has a mean height of 20 m and it is dominated by Quercus robur L., Acer campestre L., Robinia pseudoacacia L., Ulmus minor Mill., Populus nigra L. and Populus alba L. Many trees are more than 100-years old (Castagneri et al. 2013). The dominated tree layer is characterized by younger individuals of the dominant species and also by Corylus avellana L., Prunus padus L. and herbaceous species. The forest tree density is 237 [+ or -] 100 stems [ha.sup.-1], the total basal area 74.5 [+ or -] 24.6 [m.sup.2] [ha.sup.-1] and the Leaf Area Index (LAI) 4.5 [+ or -] 0.3 (Catoni et al. 2015a). The soil nitrogen content (N) is 0.16 [+ or -] 0.01%, the carbon/ nitrogen content ratio (C/N) 17 [+ or -] 1 and the organic matter (SOM) of 4.4 [+ or -] 0.1% (Catoni et al. 2015b).

The climate of the area is characterized by a total annual rainfall of 654 mm most of it falling in autumn and winter. The mean minimum air temperature ([T.sub.min]) of the coldest month (January) is -0.2 [+ or -] 1.8[degrees]C, the mean maximum air temperature ([T.sub.max]) of the hottest month (July) 30.1 [+ or -] 1.3[degrees]C and the mean annual temperature ([T.sub.m]) 13.7 [+ or -] 8.2[degrees]C. Floods occurred sporadically every 5-10 years during the last 40 years, with water levels up to 1.50 m height in the forest during exceptional events (Motta et al. 2009, Castagneri et al. 2013). On average, groundwater level is around -4.50 m in winter reaching -3.50 m in summer due to irrigation in the surrounding area. During the study period, total rainfall was 257 mm, [T.sub.m] 21.0 [+ or -] 4.9[degrees]C and [T.sub.max] (July) 32.8 [+ or -] 2.5[degrees]C (Lombardia Regional Agency for Environmental Protection, Meteorological Station of Pavia, Ponte Ticino SS35, data for the period 2002-2014 and May-July 2015).

Forest measurements

The forest extension was measured by the QGIS (Geographic Information System) which is a tool for the digital landscape exploration proving the necessary functions for spatial data collection, management, analysis and representation.

Forest measurements were carried out on 10 randomly sample areas (500 [m.sup.2] each, according to Gallaun et al. 2010). The following species were considered: A. campetre, C. avellana, Crateagus monogyna L., P. alba, P. nigra, P. padus, Q. robur, R. pseudoacacia and U. minor. Trees with a diameter greater than 5 cm (Tabacchi et al. 2011) and in a good condition (i.e. percentage of branch dieback in crown between 1% and 10%, according to Nowak et al. (2002) were considered. In particular, tree height (H) was measured by clinometers and diameter at the breast height (dbh) by callipers. The density of the considered species (plants [ha.sup.-1]) was determined in the whole area of the Reserve.

Plant regeneration

Plant regeneration was measured in 50 randomly selected plots (25 [m.sup.2] each) distributed inside the forest and in the forest boundary (parallel at the forest, at a distance of 5 m from the forest border). Saplings were defined as woody plants between 0.5 and 3 m tall, according to Hall and Swaine (1976).

Microclimate

Microclimate was measured in June, in the selected plots inside the forest (n = 10), in the forest boundary (n = 10 plots) and in the open (n = 10 plots in clearing outside the forest), from 12:00 p.m. to 04:00 p.m. in 4 days with comparable weather conditions and without clouds (the same plots used for plant regeneration were used). The photon flux density (PFD) was measured by a quantum radiometer (LI-189 LI-COR, USA) with a quantum sensor LI-190SA. The photon flux density was measured at soil level below the vegetation both inside the forest ([PFD%.sub.I]) and at the forest boundary ([PFD%.sub.B]) with the following formula:

[PFD.sub.%] = [PFD.sub.b]/[PFD.sub.o]

where [PFD.sub.b] was the photon flux density below the vegetation and [PFD.sub.o] was photon flux density measured outside the forest. Measurements of irradiance in red light (R, 660 nm), far-red light (FR, 730 nm) and blue spectral bands were carried out with a photometer IL 150 (International Light, U.S.A.) in each of the considered plots. Moreover, the ratio R/FR was calculated in order to quantify the quality of solar radiation (Mitchell and Woodward 1988).

Forest biomass and carbon storage

The aboveground biomass ([AB.sub.S]) of each species was obtained by allometric equations (Zianis et al. 2005, Tabacchi et al. 2011) using dbh and H for each species. The forest aboveground biomass ([AB.sub.F]) was obtained by summing the product of [AB.sub.S] and the related plant density for each of the considered species. The forest belowground biomass ([BB.sub.F]) was obtained by multiplying [AB.sub.F] and the root/shoot ratio, according to Vitullo et al. (2007) and Federici et al. (2008). The forest dead wood biomass ([DB.sub.F]) was calculated by multiplying [AB.sub.F] by the Dead Factor Conversion (DFC = 0.14, IPCC 2003), according to Vitullo et al. (2007) and Federici et al. (2008).

The carbon storage in the aboveground ([C.sub.A]), belowground ([C.sub.B]) and deadwood ([C.sub.D]) biomasses was calculated by multiplying [AB.sub.F], [BB.sub.F] and [DB.sub.F] by 0.5, respectively (IPCC 2003). Carbon storage in the litter ([C.sub.L]) and in the soil ([C.sub.S]) was estimated using a linear correlation where [C.sub.L] and [C.sub.S] were the dependent variables and [AB.sub.F] the independent variable, according to Federici et al. (2008).

In particular, the relation between litter and aboveground C [ha.sup.-1] was expressed by the following equation:

y = -0.0299 [AB.sub.F] + 9.3665

and the relation between the soil and the aboveground C [ha.sup.-1] was expressed by the following equation:

y = 0.9843 [AB.sub.F] + 5.0746

The total forest carbon storage ([C.sub.Tot], Mg C [ha.sup.-1]) was obtained by summing [C.sub.A], [C.sub.B], [C.sub.D], [C.sub.L] and [C.sub.S].

Statistical analysis

All statistical tests were performed using a statistical software package (PAST, Version 3.10). Differences in the considered traits were determined by the analysis of variance (ANOVA) and the Tukey test for multiple comparisons. Kolmogorov-Smirnov and Levene tests were used to verify the assumption of normality and homogeneity of variances, respectively. Values are reported as mean [+ or -] standard error (S.E.).

RESULTS

Forest structure and microclimate

Among the considered species, U. minor had the highest density (45 plants [ha.sup.-1]), followed by Q. robur (40 plants [ha.sup.-1]), R. pseudoacacia and C. monogyna (38 plants [ha.sup.-1]), A. campestre (19 plants [ha.sup.-1]), P nigra (17 plants [ha.sup.-1]), C. avellana (15 plants [ha.sup.-1]), P.padus and P alba (9 plants [ha.sup.-1]).

Plant traits are shown in table 1. P nigra had the highest height and diameter at the breast height (38 [+ or -] 8 m and 106 [+ or -] 24 cm, respectively) and C. avellana the lowest (5 [+ or -] 1 m and 10 [+ or -] 4 cm, respectively). The diameter distribution of each of the considered species is shown in figure 1.

The ratio of red to far-red spectral bands (R/FR) were

0.5 [+ or -] 0.1, 0.78 [+ or -] 0.2 and 1.2 [+ or -] 0.2, inside the forest, in the forest boundary and in the open, respectively. Moreover, the photon flux density at soil level inside the forest ([PFD%.sub.I]) and in the forest boundary (PFD%B) were 0.77 [+ or -] 0.12% and 1.54 [+ or -] 0.12%, respectively.

Plant regeneration

Plant regeneration inside the forest and in the forest boundary is shown in table 2. In particular, inside the forest P. padus showed the highest density (3 000 [+ or -] 1 000 saplings [ha.sup.-1]) and C. monogyna (744 [+ or -] 179 saplings [ha.sup.-1]) the lowest. In the forest boundary, R. pseudocacia had the largest density (1 504 [+ or -] 262 saplings [ha.sup.-1]) and P. padus (18 [+ or -] 8 saplings [ha.sup.-1]) the lowest.

[FIGURE 1 OMITTED]

Forest carbon storage

The forest aboveground ([AB.sub.F]), belowground ([BB.sub.F]), and deadwood ([DB.sub.F]) biomasses were 348 Mg [ha.sup.-1], 80 Mg [ha.sup.-1] and 49 Mg [ha.sup.-1], respectively. The species aboveground bio mass contribution to the forest aboveground biomass for each of the considered species is shown in table 3.

The total forest carbon storage ([C.sub.Tot]) was 418 Mg C [ha.sup.-1] to which carbon storage in above-ground (CA) and in soil (CS) gave the same contribution (42% each), carbon storage in belowground contributed for 10%, in deadwood for 6% and in litter for 1% (Figure 2).

DISCUSSION

Carbon stock is associated with plant biomass which, in turn, depends on different factors such as forest management, climate and soil type (van Kooten et al. 2004). Moreover, the structure and the species composition contribute to the forest carbon stock. The current tree species composition and structure of the forest under study are the result of the conservative management carried out from the establishment of the Reserve resulting in a high tree density (237 [+ or -] 100 stems [ha.sup.-1]) and LAI (4.5 [+ or -] 0.3; Catoni et al. 2015a), in the range of broadleaf deciduous forests in Italy (Gratani and Crescente 2000). The high tree density determines a high light extinction at soil level (i.e. [PFD%.sub.I] = 0.77 [+ or -] 0.12% and R/FR = 0.5 [+ or -] 0.1), which is in the range of the typical close canopy forests (0.5-5%; Chazdon and Percy 1991). This result is related to the dominant tree layer largely constituted by Q. robur, P. nigra and P. alba (height = 34 [+ or -] 4 m, mean value). The light amount in the forest understory is considered a crucial factor driving many processes such as understory tree regeneration, seedling survival (Kozlowski et al. 1991, Lieffers et al. 1999), growth (Page et al. 2001) and biomass allocation (Messier and Nikinmaa 2000). Thus, the assessment of available light in forest understory is important for a better understanding of a wide range of different processes (Sonohat et al. 2004). In this case, the low light in the forest understory determines a low regeneration of the dominant species. In fact, Q. robur and Populus spp. require sufficient light penetration and large opening for regeneration (Humphrey et al. 2002, Motta et al. 2009). In particular, regeneration of Q. robur (one of the most important European oak species) has been considered a concern in temperate forests because of the extreme scarcity of established saplings and young trees (Kelly 2002). This is due to competition with other species (i.e. shading and root competition) (Shaw 1974), mechanical smothering (Humphrey and Swaine 1997) and the presence of inhibitory substances by field species (Jarvis 1964). In the forest understory there are also few sapling of R. pseudoacaia, a typical shade-intolerant specie (Motta et al. 2009, Catoni et al. 2015a). This result highlights that the conservative management carried out in the Reserve has contributed to maintain under control the spread of this highly invasive species. On the contrary, C. avellana, U. minor, A. campestre (shade-tolerant species) and other broadleaves (C. monogyna and P. padus) can successfully regenerate at the low light intensity inside the forest and in the gaps (Motta et al. 2009) as confirmed by the large saplings density (2 049 [+ or -] 368 saplings [ha.sup.-1], mean value).

[FIGURE 2 OMITTED]

The environmental conditions at forest boundaries are intermediate between those in clearings and those inside the forest resulting in a [PFD%.sub.B] of 1.54 [+ or -] 0.12% and a 56% higher ratio of red to far-red light than the forest interior. Accordingly, the species composition in the forest boundary is characterized mainly by shade-intolerant species, in accordance with the results of Chen et al. (1992) for temperate-forests. In fact, our results show the largest sapling density for R. pseudoacacia (1 504 [+ or -] 262 saplings [ha.sup.-1]) and a relatively high sapling number of Q. robur (109 [+ or -] 42 saplings [ha.sup.-1]) in the forest boundary rather than inside the forest. Otherwise, there are few saplings for the typical shade-tolerant species, i.e. 50 [+ or -] 10, 300 [+ or -] 58 and 116 [+ or -] 55 saplings [ha.sup.-1], for C. avellana, A. campestre and U. minor, respectively. The different plant regeneration patter in the forest boundary in respect to the interior forest could be seen as the potential forest dynamic if management activities are undertaken. Several type of management, particularly thinning, can modify light solar transmission, which in turn can modify tree growth and development along with other processes such as those involved in plant diversity. Thus, the trees species currently present in the Reserve by fixing C[O.sub.2] via photosynthesis and storing the carbon in excess as biomass (Nowak et al. 2002) determine a total forest above-ground of 348 Mg [ha.sup.-1], 64% higher than the mean value shown by Saugier et al. (2001) for the temperate forests. Among the considered species, Populus spp. and Q. robur show the higher contribute to the forest aboveground biomass (by 31% and 63%, respectively). The capacity of the species to sequester C[O.sub.2] and then to act as carbon sinks depends on their physiology, growth rate, plant structure and coverage (Nowak et al. 2002). In this case, these species are characterized by higher photosynthetic rates (Catoni et al. 2015a) and [AB.sub.S] values (3 707 and 5 547 Kg, respectively). In particular, the larger diameter at breast height (87 [+ or -] 20 cm and 73 [+ or -] 22 cm, respectively) highlights that the diameter is the main driver of the biomass accumulation and, in turn, of the species carbon stocked capacity. On the contrary, R. pseudoacia despite a relatively higher plant density (38 plants [ha.sup.-1]) and a higher photosynthetic rates (Catoni et al. 2015a) contributes by 3% to the forest aboveground biomass. This result can be justified by its high growth rate (Mohan et al. 2007), due to the negative correlation between relative growth rate and the increased partitioning into non-photosynthetic tissue, as suggested by Shipley and Peters (1990) and resulting in a lower [AB.sub.S] (319 Kg). The other species (A. campestre, C. avellana, C. monogyna, U. minor, P. padus, tree density = 25 [+ or -] 15 tree [ha.sup.-1], mean value) contribute less than 2% to [AB.sub.F] due to their lower [AB.sub.S] (45 [+ or -] 12 Kg, mean value) and diameter at breast height (14 [+ or -] 1 cm, mean value).

The carbon stocked in the above-ground biomass ([C.sub.A] = 174 Mg C [ha.sup.-1]) represents the 42% of the total carbon storage by the forest, which is in the range of temperate forests (147-377 Mt C [ha.sup.-1]) with comparable climatic conditions (Keith et al. 2009). Moreover, the carbon stocked by the studied forest is more than 100% higher than that of the Italian Parks (Marchetti et al. 2015) confirming that old unmanaged forests can sequester large C amounts.

In addition, our results highlight an equivalent contribution from the soil carbon pool (by 42%), in accordance with the results of Nabuurs et al. (2003) for European forests, indicating a significant sink strength of soils. The turnover of soil organic matter depends on soil composition and climate (Jandl et al. 2007) and the larger proportion in soils of temperate forests compared to soils in tropical forests is related to a slower decomposition rates (Gorte 2009). Another aspect which should be considered is the species composition (Jandl et al. 2007), tree density and root characteristic (i.e. shallow Vi deep roots). In particular, the rooting depth is relevant for C because root growth is a most effective way of introducing C into the soil (Vesterdal et al. 2002). Populas spp. and Q. robur largely contribute to the soil C pool for the studied forest due to their well-developed root systems (Wong et al. 1985, Rosengren et al. 2006). The others compartment belowground, deadwood and litter account for 10%, 6% and 1% to [C.sub.Tot], respectively. In particular, deadwood is a structural and functional element in a forest ecosystem and unmanaged forests typically have more deadwood compared to managed forest (Vandekerkhove et al. 2009) providing a resource for plant, animal and fungi. Moreover, the quantity and quality of deadwood provide information on mortality processes and disturbance regime (Castagneri et al. 2010) suggesting the degree of forest naturalness and indicating the nearness to the old-growth stage (Winter et al. 2010). In the considered forest, a natural disturbance results in the individual-tree death or in small-scale disturbances mainly caused by wind, insects and fungi. The absence of anthropogenic stumps (i.e. a proxy variable of human impact) confirms the high degree of naturalness. Despite litter shows the minor contribution to [C.sub.Tot], among the five compartments, it results an important component of the carbon biogeochemical cycle (Zhang et al. 2007) being the interface between vegetation and soil (Fonseca et al. 2012). The litter layer is, in fact, an important pool of nutrients and organic material and its quantity and quality determines the decomposition rate, which in turn defines the availability and mobility of essential elements influencing the functional processes in the forest ecosystems (Walle et al. 2001).

On the whole, the considered forest at an 'advanced' stage of development stores a large C amount ([C.sub.Tot] = 418 Mg C [ha.sup.-1]) with the greater pool in the aboveground biomass and in the soil. Management providing the conservation of carbon stocks in a forest meets with the major climate change mitigation strategies under UNFCCC (United Nations Framework Convention on Climate Change) and assuming a monetary value for stored C[O.sub.2] of 0.00334 $/lb (i.e. 0.00736 $/kg) (Peper et al. 2007) the total economic benefits of carbon storage in this forest amounts to 11 209 $ [ha.sup.-1].

In conclusion, this study highlights that the conservative management carried out in this forest can ensure the maintenance of the actual carbon stocked. Thus, our results are an incentive to persist with the conservative management, carried out since the establishment of the Reserve. In fact, considering the plant regeneration potential in the forest boundary compared to the forest interior, it is important to maintain this type of management in the future since creating gaps could allow a greater regeneration of R. pseudoacacia over Q. robur and Populas spp. (i.e. the major carbon sink). Therefore, preserving this type of forest structure and tree species composition can ensure in the future the same forest contribution to the local carbon stock.

ACKNOWLEDGMENTS

This work was supported by the 'Natural Reserve Bosco Siro Negri' funded by The Ministry of the Environment and Protection of Land and Sea of Italy.

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M.U. GRANATA (a), L. GRATANI (b), F. BRACCO (a), F. SARTORI (a) and R. CATONI (b)

(a) Department of Earth and Environmental Sciences, University of Pavia, Via S. Epifanio 14, 27100 Pavia, Italy

(b) Department of Environmental Biology, Sapienza University of Rome, P. le A. Moro 5, 00185 Rome-Italy

Email: mirkoumberto.granata@unipv.it; loretta.gratani@uniroma1.it; francesco.bracco@unipv.it; francesco.sartori@unipv.it
TABLE 1 Structural traits of the considered species; H--plant
height, dbh--diameter at breast height. Mean values [+ or -]
S.E. are shown (n = 100)

                             H               dbh
                             m               cm

Acer campestre         10 [+ or -] 5    14 [+ or -] 5
Corylus avellana        5 [+ or -] 2    10 [+ or -] 4
Crataegus monogyna      6 [+ or -] 2    11 [+ or -] 4
Popolus alba           32 [+ or -] 4    67 [+ or -] 19
Popolus nigra          38 [+ or -] 8   106 [+ or -] 24
Prunus padus           11 [+ or -] 8    16 [+ or -] 7
Quercus robur          31 [+ or -] 8    73 [+ or -] 22
Robinia pseudoacacia   18 [+ or -] 6    25 [+ or -] 8
Ulmus minor            12 [+ or -] 4    17 [+ or -] 7

TABLE 2 Plant regeneration (saplings [ha.sup.-1]) in the forest
interior and in the forest boundary. Mean [+ or -] S.E. are shown
(n = 50)

                           Saplings [ha.sup.-1]

                  Forest interior       Forest boundary

A. campestre      1 976 [+ or -] 619      300 [+ or -] 58
C. avellana       2 200 [+ or -] 653       50 [+ or -] 10
C. monogyna         744 [+ or -] 179      600 [+ or -] 173
P padus           3 000 [+ or -] 1000      18 [+ or -] 8
Q. robur                                  109 [+ or -] 42
R. pseudoacacia                         1 504 [+ or -] 262
U. minor          2 322 [+ or -] 985      116 [+ or -] 55

TABLE 3 Proportion in percentage of the species above-ground
to the forest above-ground biomass (ABS/ABF%) for
each of the considered species

                       [AB.sub.S]/[AB.sub.F (%)]

Acer campestre                    0.31
Corylus avellana                  0.08
Crataegus monogyna                0.23
Popolus alba                      4.77
Popolus nigra                    26.8
Prunus padus                      0.17
Quercus robur                    63.0
Robinia pseudoacacia              3.45
Ulmus minor                       1.10
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Author:Granata, M.U.; Gratani, L.; Bracco, F.; Sartori, F.; Catoni, R.
Publication:International Forestry Review
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Date:Dec 1, 2016
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