1. Introduction
Forest ecosystems exert a fundamental role in the carbon (C) cycle at both global and local scales [
1]. Remote sensing and biogeochemical models are complementary tools for studying and monitoring the main processes of these ecosystems, with particular reference to gross and net C fluxes. Remote sensing techniques, in fact, provide synoptic and repetitive views of vegetation features and conditions at various spatio-temporal resolutions. Biogeochemical models, on the other hand, can simulate all main vegetation processes, and specifically forest photosynthesis and respiration. The two techniques are therefore intrinsically suited to be combined for estimating forest C fluxes, and in particular gross primary and net ecosystem production (GPP and NEP, respectively) [
2,
3,
4].
An example of this approach is given by the strategy developed and experimented by our research group in several European forest areas [
5,
6]. This strategy consists in combining the outputs of a radiation use efficiency (RUE) model, Modified C-Fix, with those of a model of ecosystem processes, BIOME-BGC. The former model estimates forest GPP based on standard meteorological observations and remotely sensed NDVI images, while the latter simulates all main ecosystem processes driven only by ancillary data descriptive of forest conditions. The outcomes of the two models are finally integrated using the ecosystem disequilibrium theory to take into account the effects of forest disturbances [
5]. Owing to this configuration, the modelling strategy is capable of analyzing the response of forest ecosystems to climatic changes [
7] but is also applicable to investigate on the impact of human activities (forest thinning, clearcuts, etc.).
The current communication aims at illustrating a first example of this possibility. In particular, the study shows how the modelling strategy can be applied to account for the partly contrasting influences of climatic and anthropogenic drivers on forest ecosystems and simulate the respective evolutions of gross and net C fluxes. The investigation concerns a Mediterranean coastal area, the San Rossore Regional Park (Central Italy), where two pine wood ecosystems are in different development phases due to the application of diversified management practices. Specifically, the impacts exerted by these conditions on the evolutions of forest GPP and NEP are preliminarily analyzed and discussed.
2. Materials and Methods
2.1. Study Area
The San Rossore Regional Park is located in a flat coastal area close to Pisa, Central Italy (43.68-43.78° N. Lat., 10.27-10.35° E. Long.;
Figure 1). This area has been the subject of several investigations concerning all main forest processes, and particularly water and C fluxes. The Park, in fact, includes a coastal stripe dominated by
Pinus pinaster Ait. (maritime pine), where an eddy covariance flux tower was set at the end of 90es. This forest was then struck by a parasitic attack of an insect (
Matsucoccus feytaudi), which damaged most pine trees and was faced by extensive clearcuts carried out in 2009-2012 [
8]. Since then, the forest is in a regrowing phase, i.e. is regenerating as a secondary ecological succession; most pine wood is now dense, with a mean height of 3-5 m. An inner, adjacent area of the Park is dominated by a
Pinus pinea L. (umbrella pine) forest, which, being not vulnerable to the insect attack, is presently in an old-growth phase. Most
P. pinea stands are, in fact, over 80-90 years old, relatively dense and with a mean height of 20-22 m.
The Park therefore includes two pine wood ecosystems subjected to the same climate but in completely different development phases. This offers a unique opportunity to investigate the impact which is contemporaneously exerted on forest C stocks and fluxes by climatic and anthropogenic factors.
2.2. Study Data
Spatially interpolated daily estimates of minimum and maximum air temperature, rainfall and solar radiation for ten years (2013-2022) were derived from the ground observations of the LaMMA Consortium (
http://www.lamma.toscana.it/) [
9,
10]. A soil organic carbon (SOC) map of Tuscany was obtained from the same database [
11]. All these datasets have a spatial resolution of about 250 m.
Normalized Difference Vegetation Index (NDVI) images taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) were derived from the NASA archive (
https://modis.gsfc.nasa.gov). This product is provided as maximum value composite (MVC) images referred to 16-day periods and with a spatial resolution of 250 m. All MVC images of the study area over the same years as above (2013-2022) were further pre-processed in order to reduce residual atmospheric contaminations (see [
12], for details).
The study also considered a high spatial resolution LiDAR acquisition taken over the San Rossore Park by a low altitude aircraft flight in May 2015. The products available were 1-m spatial resolution Digital Surface and Digital Terrain Models, which were processed to obtain the Canopy Height Model (CHM) of the area.
2.3. GPP and NEP Modelling Strategy
The following paragraphs describe the main characteristics of the two models utilized (Modified C-Fix and BIOME-BGC) and the combination of their outputs. Further details on the modelling strategy applied with relevant assumptions and approximations can be found in [
5] and [
13,
14].
C-Fix is a RUE model driven by daily meteorological and NDVI data, which was modfied by [
15] for improving the prediction of GPP in Mediterranean water-limited environments. Modified C-Fix, in fact, incorporates a water stress meteorological scalar (Cws), that simulates the impact of short-term water stress on forest GPP.
Hence, the model predicts the GPP of day i (GPP
i) as:
where ε is the maximum RUE of forests (1.2 g C MJ
-1 APAR); Tcor
i is the respective temperature correction scalar; Cws
i is the water stress scalar; fAPAR
i is the fraction of absorbed Photosynthetic Active Radiation (PAR) derived from NDVI and PAR
i is the incident PAR derived as a constant fraction of solar radiation, all referred to day i. The water stress scalar of this day (Cws
i) is computed as:
where AW
i is the ratio between rainfall and potential evapotranspiration (PET) bounded to 1 and cumulated over the preceding two months. PET is usually obtained from daily air temperature and solar radiation as described in [
15].
BIOME-BGC is a bio-geochemical model that predicts the storage and fluxes of water, C and nitrogen in terrestrial ecosystems [
16]. This model simulates all pools and processes of ecosystems in quasi-equilibrium condition using daily meteorological data and site information on soil, vegetation and eco-physiological parameters [
17]. BIOME-BGC then proceeds with a normal simulation of photosynthesis, respiration and allocation processes referred to the examined study period. The quasi-equilibrium simulation implies that the annual sum of all respirations roughly equals GPP, while mean annual NEP tends to zero. The parameter settings originally provided with the used model version (4.2) for seven biome types were modified by [
18] to adapt to Mediterranean water-stress conditions.
The RUE model offers the advantage of a direct remote sensing estimation of total forest GPP, while BIOME-BGC permits a complete simulation of all main ecosystem processes. The estimates of the latter model can therefore be improved by multiplication for the ratio between C-Fix and BIOME-BGC GPP [
5]. The outputs obtained must be also corrected to account for the effects of natural and/or human-induced disturbances on the actual forest conditions [
19]. Based on the ecosystem equilibrium theory, the long-term net C exchange of undisturbed forest ecosystems is assumed to approach zero, while positive NEP of not fully stocked stands is mainly attributed to increasing woody biomass. Following this formulation, the ratio of actual over potential growing stock volume (GSV), the so-called normalized volume, is assumed to represent the distance from ecosystem equilibrium and used to correct the estimated C fluxes. The actual forest NEP of day i (NEP
i) is consequently estimated as:
where GPP
i, Rgr
i, Rmn
i and Rh
i are the BIOME-BGC estimates of photosynthesis, growth, maintenance and heterotrophic respirations improved by the combination with C-Fix GPP, while the three scalars FC (forest cover), NV (normalized volume) and NS (normalized SOC) are descriptive of the ecosystem distance from the equilibrium condition [
5,
20]. Distinctively, FC is the fractional tree canopy cover, NV is the normalized GSV, and NS is the normalized SOC.
In the original formulation of the modelling strategy all scalars of Eq. 3 were derived from the ratio of actual over potential GSV [
5]. This method, however, is effective only in forests where all C pools are approximately in equilibrium, as assumed by BIOME-BGC. To address different cases, such as even-aged or regenerating stands, the three scalars should be estimated independently, allowing a more flexible and efficient simulation of the respective terms of the forest C cycle (i.e. photosynthesis, autotrophic and heterotrophic respirations) [
20].
2.4. Data Processing
The data processing consisted of applying the GPP/NEP modelling strategy to the two forest stands shown in
Figure 1, which were selected among the largest ones of the Park representative of different forest development phases. The first, in fact, is an old-growth stand of about 15 ha dominated by mature umbrella pines, while the second is a stand of nearly 20 ha covered by a secondary succession of maritime pine.
Daily meteorological data of the ten study years (2013-2022) were averaged from an area including both stands. Next, NDVI data were extracted from four MODIS pixels approximately coincident with each stand. These data were then averaged on a stand basis (NDVI 1 and NDVI 2), linearly interpolated to a daily time step and combined with the weather data to drive Modified C-Fix (equation 1). A BIOME-BGC version parameterized for Mediterranean pines was then applied using the same meteorological dataset and ancillary information [
20]. Three series of GPP estimates were thus obtained, the first from BIOME-BGC, referred to both stands (GPP BIOME), and the others from C-Fix driven by the NDVI series of the two stands (i.e., GPP C-Fix 1 for umbrella pine and GPP C-Fix 2 for maritime pine).
The application of BIOME-BGC also yielded NEP estimates descriptive of quasi-equilibrium condition (NEP BIOME). The actual status of the two stands was instead accounted for by modifying the model combination strategy on the basis of the previously exposed considerations. The scalars describing vegetation status required by equation 3 (FC and NV) were derived from the analysis of the LiDAR dataset of 2015 using the allometric relationships described in [
21]. These scalars were kept constant during the simulation period for the mature umbrella pine stand, where great green and woody biomass variations are not expected in a relatively short time period. On the contrary, the two scalars were initialized using the LiDAR data and updated annually through the consideration of net primary production (NPP) estimates for the regrowing maritime pine stand. As described in [
20], the annual updating was performed by converting the respective NPP estimate into FC and NV increments. For both stands, the scalar which regulates soil heterotrophic respiration (NS) was assumed to remain constant and was obtained from the SOC map of Tuscany corrected for the soil depth considered by BIOME-BGC [
11]. For each of the two stands, all terms of equation 3 were improved using the respective GPP predicted by C-Fix, thus obtaining corresponding series of NEP estimates (i.e., NEP C-Fix 1 and NEP C-Fix 2).
Both the inputs (i.e., the meteorological water stress factor and the NDVI values) and the outputs (i.e., the GPP and NEP estimates) of the strategy were aggregated on an annual basis and analyzed by standard regression and correlation analyses.
3. Results
The meteorology of the study area shows a clear trend towards drier condition during the examined 10-year period, which is reflected into a highly significant decrease of the AW scalar (
Figure 2). This trend is induced by a combination of meteorological factors: annual rainfall is, in fact, irregularly decreasing (from over 1000 to around 700 mm), while annual PET is slightly increasing (from about 1200 to 1300 mm), due to a quite regular temperature rise.
This trend has a marginal impact on the NDVI of the umbrella pine stand (NDVI 1), which is moderately correlated with AW (
Table 1) and only marginally decreasing. In contrast, increasing dryness is nearly uninfluential on the NDVI of the regrowing maritime pine stand (NDVI 2), which is negatively correlated with AW and shows a highly significant rise (
Table 1;
Figure 2). The influence of dryness on this stand is reflected only by the NDVI drops coincident with the main AW decreases (e.g. in 2017 and 2022).
These patterns have clear consequences on the GPP predicted by the two models considered, which, as previously noted, work using different principles and drivers. BIOME-BGC, in fact, being parameterized and driven in the same way for both pine species, provides the same estimates for the two stands. In contrast, C-Fix, which is mostly driven by the NDVI of the two stands, yields diversified predictions.
This is visible in
Figure 3; the GPP simulated by BIOME-BGC is close to that predicted by C-Fix for the umbrella pine stand (around 1900-2000 g C m
-2 year
-1) and follows a similar decreasing trend. The GPP predicted by C-Fix for the maritime pine stand is instead lower but increases following the respective NDVI rise. The correlations of
Table 1 confirm these patterns, in particular concerning the low accordance between NDVI 2 and the GPP of BIOME-BGC and, above all, C-Fix 1.
Finally,
Figure 4 shows the NEP trends simulated as described above for the two stands. In accordance with the theoretical foundation of the model, the NEP simulated by BIOME-BGC is, on average, very close to 0 g C m
-2 year
-1, and shows a slightly decreasing trend.
The case is different when applying the model combination, which is also driven by the three scalars of equation 3. The vegetation scalars (NV and FC) obtained from the processing of the LiDAR data for the umbrella pine stand are descriptive of a mature forest (NV = 0.60 and FC = 0.72); the NS derived from the corrected SOC of the Tuscany map is typical of a similar ecosystem condition (0.59). The NEP simulated by the model combination using this setting follows a trend that is almost parallel to that of BIOME-BGC but is always positive around 200 g C m-2 year-1.
A different NEP evolution is predicted by the model combination for the regrowing maritime pine stand. In this case, in fact, FC rises from around 0.4 to 0.8 and NV increases from about 0.04 to 0.11. Following these trends and that of GPP C-Fix 2, the simulated NEP increases almost linearly from around 200 to over 600 g C m-2 year-1.
Again,
Table 1 provides insights on the correlations between NEP and the other variables. The NEP series simulated by BIOME-BGC and by the model combination for the umbrella pine stand is highly dependent on the AW meteorological scalar, as well as on the respective GPP estimates. The NEP simulated by the model combination for the maritime pine stand instead shows a negative correlation with most other variables and a highly significant positive correlation only with NDVI 2 and GPP C-Fix 2.
4. Discussion and Conclusions
The current study is based on the consolidated capacity of Modified C-Fix to predict forest GPP in Mediterranean areas, which has been demonstrated in previous investigations [
12,
14]. A similar capability has been proven for the calibrated BIOME-BGC versions to simulate all forest processes in the same region. Further investigations have supported the efficiency of the model combination for predicting the actual processes of forest ecosystems in different development phases [
22]. In particular, the independent estimation of the three C pools which regulate photosynthesis, autotrophic and heterotrophic respirations permits an efficient simulation of the processes of ecosystems far from equilibrium conditions [
20].
Owing to these properties, the strategy can be adapted to analyzing the impacts of both natural factors and human-induced disturbances. A first example of this possibility has been currently illustrated for a Mediterranean coastal area covered by two pine forest ecosystems in different development phases. The results obtained show that the first stand, representative of an old-growth forest, is mostly controlled by meteorology, i.e., by the increasing dryness of the area, which induces slightly decreasing GPP and NEP trends. In accordance with the forest equilibrium theory adopted by the model combination strategy, the GPP of this stand is quite high, while the NEP is moderate.
The second stand, representative of a secondary succession after clearcuts, partly counteracts the influence to increasing dryness by a rapid regrowing, which induces significant increases of NDVI and simulated GPP. This evolution is accompanied by an intense biomass accumulation which is typical of the initial phase of a secondary succession. Still in accordance with the mentioned equilibrium theory, the simulation of the stand NEP takes into consideration this evolution through the progressive increase of the two vegetation scalars (NV and FC). The modelling exercise finally results in clear rises of simulated NEP and C stock.
A direct validation of the GPP and NEP estimates obtained by the model combination is not presently feasible due to the lack of ground observations taken during the ten years examined. The mean values of both these variables, however, are comparable to those measured by an eddy covariance flux tower which was active in an adjacent maritime pine stand during the period 2001-2005. This stand was representative of a relatively mature (60-70 years old) but not fully stocked forest, where woody biomass was still accumulating. The average values of GPP and NEP observed by that tower were around 1600-1800 and 400-500 g C m
-2 year
-1, respectively [
14]. The lower NEP currently simulated for the first, mature stand can be reasonably attributed to its smallest distance from equilibrium (fully stocked) condition. The higher net C flux predicted for the second stand in the last years can instead be attributed to the respective intensive biomass accumulation phase.
These patterns are in accordance with the variations of woody biomass which have been observed on the ground during the study decade. No significant change in GSV has, in fact, been detected by the forest managers in the umbrella pine stand (personal communication of F. Logli, Regional Park Authority). In contrast, the storage of woody biomass which accompanies the NEP evolution simulated for the maritime pine stand is testified to by the increasing tree canopy density and height observable in situ. The mean canopy height of this stand, in fact, rises from nearly 0 m in 2013 to 3-4 m in 2023.
The results of the described experiment are affected by several sources of uncertainty. In addition to the limits of the modelling background, discussed in previous publications [
5,
20], the use of interpolated and remotely sensed input datasets induces inaccuracies that cannot be presently quantified. In particular, the utilization of a unique weather dataset to guide all modelling exercises introduces a spurious component into most of the statistical relationships found between the input and output data series. The simulation strategy applied, however, also takes into account major forest attributes which counteract the impact of meteorology (i.e., the NDVI and vegetation scalars), thus providing information which is partly independent of this.
The datasets utilized are differently capable of describing the main ecosystem features regulating gross and net C fluxes. The spatio-temporal variability of meteorology in the flat study area is presumably reproduced well by the interpolated weather dataset. The same, however, is not fully the case for the MODIS NDVI imagery, which has a spatial resolution insufficient to capture the fine spatial details of the examined stands. The uncertainty of the simulation process could therefore be reduced by the use of higher spatial resolution images such as those taken by Landsat TM/ETM+/OLI and Sentinel-2 MSI. The use of NDVI imagery taken by these sensors in the current case, however, is hampered by issues of temporal resolution and coverage, respectively [
23]. A similar problem affects the SOC map utilized, which, however, has the finest spatial resolution (250 m) allowed by the soil mapping technologies applicable at regional scale [
24]. The issues induced by the use of low spatial resolution datasets are anyway mitigated by the combination with aircraft LiDAR observations, which can properly predict the scalars related to static vegetation properties (FC and NV).
In summary, the current investigation has illustrated the potential of the proposed model combination strategy to quantify the different C accumulation capacities of forests subjected to the same meteorological constraints but in diverging development phases due to different human controls. Such assessment is relevant for providing the information required for sustainable forest management, concerning in particular ecosystem services linked to the C cycle.
The potential of the strategy, however, should be confirmed by future investigations carried out using more complete ground and remote sensing observations of C fluxes and stocks taken in the same and other forest areas. These investigations could also consider different methods to integrate remotely sensed GPP estimates with models of ecosystem processes taking into account the actual forest structure and development phase.
Funding
This research received no external funding.
Data Availability Statement
Acknowledgments
The authors want to thank Dr. L. Bottai (LaMMA Consortium) for providing a preprocessed version of the utilized LiDAR dataset and Dr. F. Logli (San Rossore Regional Park Authority) for providing forestry information on the study area. The authors wish to thank three anonymous RS reviewers for their helpful comments which improved the quality of the original manuscript. This work has been partially supported by MIUR Project (PRIN 2020) “Unraveling interactions between WATER and carbon cycles during drought and their impact on water resources and forest and grassland ecosySTEMs in the Mediterranean climate (WATERSTEM)” (Project number: 20202WF53Z).
Conflicts of Interest
The authors declare no conflict of interest.
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