Introduction 

In the recent past an increase of surfaces covered by maquis was observed in Europe due to a reduction in cultivated areas ([42]). However, in southern Europe, most of the Mediterranean maquis surfaces are secondary successions of forested areas as consequence of human activities (e.g., utilization for timber, fires, grazing) and climatic stress factors (elevated summer temperatures and drought), which cause the conversion from forests to maquis and slow down the transition of maquis to forest.

The assessment of carbon stock of these surfaces plays a key role in evaluating the ecosystem resources, both for traditional goods production (such as timber or food, biodiversity assessment - [15], or related services such as soil protection, water and nutrients cycling, biodiversity, and pollution control) as well as in function of climate regulation. After the Kyoto protocol (KP), the role of shrub species was highlighted in 2005 during the Marrakech summit ([32]); recently, the international challenges related to the carbon issue were renewed following the Doha agreements in 2012, when the KP objectives to pursue the reduction and constraint of greenhouse gases emission at global level were extended to 2020. New environmental policies and carbon market mechanisms are being developed in southern Europe ([8]), including the improvement of forest ability to sequester carbon with proper silvicultural practices ([14]) and fire management ([9], [18]). In most of these cases, the biomass stock assessment plays a key role ([5]).

The “Good Practice Guidance for Land Use, Land Use Change and Forestry” (GPG-LULUCF - [38]) is the official guide developed by the IPCC National Greenhouse Gas Inventories Programme to estimate the carbon stock and its changes in relation to the KP ([35], [45]). It defines five terrestrial carbon pools: above- and below-ground biomass, dead wood, litter, and soil organic matter. In forestry systems, the above-ground biomass (AGB) stock and changes are mostly assessed through a combination of inventory data and the use of allometric equations that relate plant dendrometric measurements (trunk diameter at breast height, tree height, etc.) to the AGB weight. However, the application of the GPG-LULUCF protocols is difficult when Mediterranean maquis is involved. In such ecosystems, the quantification of the AGB stock is challenging due to the high variability in species composition and because of the shrub architecture ([19]), which limits the application of traditional techniques developed for forestry tree species. As a consequence, there is still little information on the carbon stock capacity and changes in such ecosystems ([36]). This fact is particularly vexing in Italy, where the maquis ecosystem is one of the most represented forest categories (3.34% of the national surface and 8.05% of forested area, with more than 1 million ha), denoting a critical issue in the context of the carbon credits market ([1]). In addition, the available AGB data are also characterized by a wide range of variability and uncertainty; this has been demonstrated by recent efforts to harmonize, at international level, the allometric equations available for supporting volume and biomass assessment in tree/forestry systems ([46], [30]).

Currently, different methods are used to estimate the AGB in the maquis species. The destructive sampling method is accurate but time consuming and not always applicable (e.g., in protected areas - [29]). Most used methods are based on allometric equations relating AGB to its proxies, such as the shrub height ([29], [47], [6], [13], [44], [16]) or the crown diameter ([29], [31], [41], [47], [13], [37], [21], [43], [15]). Gratani et al. ([29]) estimated the apparent volume (AV) from the crown diameter and height measurements, while Catarino et al. ([10]) used plant height and stem diameter measurements. The shrub AV can be also used as a proxy of the AGB stock. Montès et al. ([34]) proposed a computerized methodology to estimate the AV based on orthogonal-view digital images of the shrub. Other authors ([49], [11], [2], [48], [47], [22]) developed a methodology where the AV is estimated assuming the shrub shape to be similar to a 3D regular solid (i.e., cylinder, sphere, rotation paraboloid, etc.). In all cited cases, reliable data on the specific apparent density of the shrub (i.e., weight/AV, kg m^-3) are needed.

Chirici et al. ([12]) and Bacciu ([4]) applied an expeditious method to estimate a “volume index” as the product between the vegetation coverage degree and shrub height, while in recent years a growing interest was addressed to the application of the Light Detection And Ranging (LiDAR) systems which estimates the AGB stock from the relationship between plant weight and canopy height or volume ([28], [33], [17]).

The aim of this paper is to contribute in evaluating methodologies able to estimate the AGB stock in Mediterranean maquis systems. In particular, this work explores the potential application of two expeditious and non-disruptive methodologies to be applied for three of the most representative maquis species of the Mediterranean basin: Pistacia lentiscus L., Cystus monspeliensis L. and Euphorbia dendroides L. Additional measurements of AGB were carried out in order to characterize the study area and to evaluate the two applied methodologies, thus increasing the availability of such data within the scientific community.

  Materials and methods 

Study site

The work was carried out in Sardinia (Italy), the second largest island (24 090 km²) of the Mediterranean Sea, where approximately half of the land surface is covered by forests and Mediterranean maquis. The site is located in the National Park of Asinara (40° 59′ - 41° 07′ N; 8° 12′ - 8° 21′ E; 51.2 km²), an island used as a State prison until 1997 ([27]). The climate is typically Mediterranean, with relatively mild winters, and warm and dry summers. The mean annual temperature is 16.1 °C (coldest month: February with 10 °C; warmest month: August with 23 °C). The climatic annual rainfall is 476 mm, among the lowest in Sardinia. More than 80% of the soil substrate consists of metamorphic rocks with sedimentary and volcanic origins, mainly represented by schist and sporadic granitic lithologies.

The vegetation is characterized by a mosaic of secondary Mediterranean maquis communities as a consequence of frequent fires in the past (frequently used during the penal colony period for agricultural purposes) and over-grazing (by goats, horses, and wild boars). The establishment of the National Park and the subsequent abandonment of agricultural activities favored the recolonization of these areas by Mediterranean maquis species, mainly Pistacia lentiscus L., Cystus monspeliensis L. and Euphorbia dendroides L. A detailed description of Asinara Island vegetation can be found in Pisanu et al. ([40]).

Application of two methodologies for above-ground biomass estimation

AGB estimation is based on the relationships between AV and the plant dry weight. Preliminary height and crown diameter measurements were carried out in different areas to characterize the structural variability of the plant community. Shrubs with different sizes of the three most diffuse species in the area (18 for C. monspeliensis, 12 for E. dendroides, and 8 for P. lentiscus) were randomly sampled to estimate the AV using the two methodologies described below.

1. Methodology 1. The AV was estimated assuming the shrub shape to be similar to a regular 3D solid. Measurements of plant height (H), maximum crown diameter (MD) and diameter orthogonal to MD (OMD) were used to calculate regular solid volumes (circular and elliptical cylinder, sphere, paraboloid, ellipsoid, and half ellipsoid).
2. Methodology 2. The AV was estimated using a methodology adapted from Montès et al. ([34]). The methodology includes the following steps (Fig. 1): (i) a digital camera was used to take two orthogonal view pictures in correspondence of plant MD and OMD sides; (ii) the software Microsoft Power Point^® ver. 2013 was used to manually digitize the plant contour displayed in the pictures; (iii) a worksheet (Microsoft Excel^® ver. 2013), with cells previously organized in a grid of 0.1 × 0.1 m, was used to place the plant digital contour on the grid and to calculate the apparent volume for each shrub layer. The AV of each shrub was obtained through the sum of each layer’s volume.

Fig. 1 - The apparent volume estimation with Methodology 2: digital photos and contouring (upper panels); a view of Excel worksheet for the volume calculation (lower panels). The apparent volume of the shrub is obtained summing the volume of each layer of 0.1 m height.



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The sampled shrubs were cut and oven-dried in a laboratory at 65 °C to obtain the dry weight.

The regressions between the AV estimated with the two methodologies and the dry weight were then calculated for each species. The AD values (dry weight/AV ratio) for each species were also obtained both with Methodology 1 and 2.

Field measurements: AGB stock estimation

The findings of the above analysis were applied to a case study. Three areas characterized by a different degree of soil cover and mean shrubs height (identified as low, medium, and high recolonization degree) were identified on the Asinara Island. In each area, three plots of 3.0 × 3.0 m were demarcated, where sub-plots of 0.5 × 0.5 m were further delimited. In each sub-plot and for each species, the basal area and the canopy height were measured (at 0.1 × 0.1 m points) to estimate the AV as the product of specific soil cover and plant height. This method was chosen since shrubs were highly intermingled. Given the small size of the sub-plots, it was assumed that the estimated AV for each plot was comparable to the AV of the single shrubs obtained with Methodology 2. Finally, the AGB was estimated by the product of the AV and the AD obtained from the Methodology 2.

In order to better characterize the site, the litter and dead wood stock were also calculated. Ten aluminum frames of 0.1 × 0.1 m were randomly distributed in each plot to estimate the litter amount, and all the dead wood material inside each plot was collected. Both litter samples and dead wood were oven-dried (65 °C) and then weighed in the laboratory.

  Results and discussion 

Application of two methodologies for above-ground biomass estimation

The main attributes of the sampled shrubs are reported in Tab. 1. The lowest and highest mean height was found in C. monspeliensis and E. dendroides, respectively, while P. lentiscus showed the mean highest crown diameters. C. monspeliensis and P. lentiscus showed the lowest and highest mean dry weight and AV per shrub, estimated with both Methodology 1 and 2.

Differences in the AV depend not only on the methodology used for its estimation but also on the species. In this analysis, higher differences were found for C. monspeliensis (62%) and E. dendroides (60%) than for P. lentiscus (26%), mainly due to the more irregular crown contour of the first two species with respect to P. lentiscus.

Results also confirm that the method used for the AV estimation should be appropriately considered when AD values are used, since the two terms are strictly related. In Methodology 1 the shrub shape is assumed to be regular (i.e., the plant contour irregularities are not considered), while in Methodology 2 the canopy contour is more detailed. Consequently, AVs calculated with Methodology 1 show higher values than those obtained by Methodology 2 (Tab. 1). This result highlights the importance to have specific AV-AGB relationships for a reliable biomass stock assessment.

Results from the two methodologies were compared and a strong relationship between the AV estimated with Methodology 1 and 2 (R² = 0.95-0.98 - Fig. 2) was found. This confirms that reliable AGB assessments based on AV estimates can be obtained both with Methodology 1 and 2, when appropriate AD values are used.

Fig. 2 - Relationships between the apparent volume (AV) estimated with Methodology 1 (Met.1) and Methodology 2 (Met. 2).

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The corresponding AD values for Methodology 1 and 2 are reported in Tab. 1. The AV estimation methodology also affects the distribution of the apparent density values between species. Higher AD values for each species were found when AV was obtained with Methodology 2 (Cystus +85.3%, Euphorbia +106.0%, Pistacia +26.2%). With Methodology 1, the highest mean AD value was found for P. lentiscus, followed by C. monspeliensis, but the opposite was obtained using Methodology 2. The lowest mean AD value was obtained for E. dendroides with both methodologies.

Furthermore, simple relationships between the estimated AV and the dry weight of the sampled plants were calculated. The R² value ranged from 0.89 to 0.96 (Fig. 3) with Methodology 1 (AV estimated as 3D shape) and the best 3D shape (higher R² value) is different depending on the species (sphere for C. monspeliensis and E. dendroides, and ellipsoid for P.lentiscus). Comparable R² values between species were indeed obtained when AV was estimated with Methodology 2 (R² = 0.91-0.96 - Fig. 4).

Fig. 3 - Relationships between the apparent volume (AV) estimated with Methodology 1 and the above-ground biomass (AGB).

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Fig. 4 - Relationships between the apparent volume (AV) estimated with Methodology 2 and the above-ground biomass (AGB).

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Previous studies did apply similar methods to maquis species. Gratani et al. ([29]) obtained a R² value of 0.85 for P. lentiscus by estimating the AV as D² · H (D: diameter, H: height). Usó et al. ([48]) did not find statistical differences in using the circular cylinder, elliptical cylinder, and paraboloid of rotation as proxies of the AGB stock in Cistus albidus, Thymus vulgaris, and Rosmarinus officinalis. A similar approach was used in a study conducted in arid sites in Israel, where Sternberg & Shoshany ([47]) calculated the AV for more than 20 shrub species using the formula of several solids (as inverted cone, spheroid, cylinder, etc.). However, no indication about the solid shape showing the best fit with the AGB stock values was reported by the authors.

Our results confirmed that AV can be used as a proxy of the AGB weight with quick field measurements, but providing appropriate AV-AGB relationships is crucial. Although this analysis was based on a limited number of samples, results are promising also in view of the growing interest on proximal sensing techniques (e.g., LiDAR) for the AGB assessment.

Field measurements: AGB stock estimation

Previous results were applied for estimating the AGB in the same area, with the aim of increasing the limited availability of AGB data in maquis systems within the scientific community. Tab. 2 shows the structural characteristics of the areas where the woody stocks were estimated. On average, the AV ranged from 0.18 m³ m^-2 to 1.34 m³ m^-2 from low to high recolonization degree sites. The AGB of C. monspeliensis inversely decreased with respect to the recolonization degree (Tab. 2), with values ranging from 1.91 to 4.21 Mg d.m. ha^-1. An opposite trend was observed both for P. lentiscus (2.83-17.51 Mg d.m. ha^-1) and E. dendroides (2.83-28.64 Mg d.m. ha^-1), whose AGB values increased from low to high recolonization degree. These results are in accordance with the patterns of vegetation dynamics related to secondary succession models (also conceptualized as vegetation series - [24]), already described for north-western Sardinia ([7]) and for the Asinara National Park ([25], [26], [3], [40]). Due to these succession dynamics, and to the consequent species distribution and structure, the AGB ranged from 7.04 (low recolonization degree) to 48.05 Mg d.m. ha^-1 (high recolonization degree - Tab. 3).

Results were also compared with findings from a literature survey, even if this comparison may be affected by a certain degree of uncertainty due to different reasons: the reduced size of the surveyed area, the low number of replicates in our analysis, and the high variability in species, structural characteristics, and methodologies used in different studies. Only a few papers reported results related to a single species. For P. lentiscus, Gratani et al. ([29]) found an AGB value ranging from 0.90 to 2.17 Mg d.m. ha^-1, while Peressotti et al. ([39]) reported a value of 1.30 Mg d.m. ha^-1, lower than our findings. More similar results were reported for P. lentiscus (19.67 Mg d.m. ha^-1 - [36]; 5.80 to 9 Mg d.m. ha^-1 - [16]). For E. dendroides, Corona et al. ([16]) reported a value ranging from 3.60 to 11.30 Mg d.m. ha^-1.

Less marked differences within the investigated areas were observed for the litter and dead woody material. In particular, the litter load ranged from 19.9 to 23.5 Mg d.m. ha^-1. In Greece, Dimitrakopoulos ([23]) found that the average litter load in an evergreen-sclerophyllous shrubland, with height up to 1.5 m, was 2.51 Mg d.m. ha^-1, and slightly higher (3.38 Mg d.m. ha^-1) in the same vegetation with height up to 3 m. In California, Countryman ([20]) collected dry weight of litter ranging from 6.77 to 49.60 Mg d.m. ha^-1. These extreme differences are not only related to different structural and vegetation characteristics, but also to sampling methodologies: according to Countryman ([20]) litter included all dead organic material above the mineral soil in the surface layer, whereas Dimitrakopoulos ([23]) supposedly considered only the freshly fallen leaves and spines. In our sampled areas, the dead woody material load was relatively low compared with AGB and litter, and it decreased from low to highly recolonized plots. This fact is partially due to the grazing pressure (mainly by horses and goats), causing mechanical damages to the Cystus vegetation in low recolonized areas. Overall, the sum of living and dead mass ranged from 31.68 to 69.17 Mg d.m. ha^-1 from low to high recolonization degree (Tab. 3).

  Conclusions 

Consistent and wider datasets of carbon stock in Mediterranean forests are essential for studies related to nutrient cycles, ecology, global change impact assessment, and for management purposes. This is a critical issue especially for Mediterranean maquis systems, where the quantification of the above-ground biomass is challenging. Our results showed that expeditious measurements of the apparent canopy volume can be used for assessing the above-ground biomass of these ecosystems. The two applied methodologies performed well in estimating AV. Results showed that the apparent canopy density values depend on the methodologies used for the apparent volume estimation. In addition, the combination of data related to shrubs volume and density can be of great help in other studies where plant volume assessment is made using different methods (e.g., LiDAR scanner).

This study confirms the high degree of heterogeneity of these systems, and highlights that species and applied methodologies are factors that should be taken into account in order to generalize the results from different studies. Moreover, it provides AGB data and equations for AGB estimation in three widespread shrub species, thus contributing to enhance the limited datasets and information for these ecosystems.

  Acknowledgements 

This work was partially funded by the research project MIUR PRIN: CARBOTREES - Climate change mitigation strategies in tree crops and forestry in Italy (2013-2016, Project Coordinator: Prof. Riccardo Valentini).

  References