1 2 3 4 5 Title: Pinus halepensis regeneration after a wildfire in a semiarid environment: assessment using multitemporal Landsat images 6 Sergio M. Vicente-Serrano1*, Fernando Pérez-Cabello2, and Teodoro Lasanta1 Running title: Pinus halepensis regeneration using Landsat images 7 8 9 10 11 12 1 13 Additional keywords : NDVI, vegetation recovery, resilience, mediterranean, semiarid, Ebro 14 Valley, Spain. Instituto Pirenaico de Ecología, CSIC (Spanish Research Council), Campus de Aula Dei, P.O. Box 202, Zaragoza 50080, Spain 2 Departamento de Geografía. Universidad de Zaragoza. C/ Pedro Cerbuna 12. 50009. Zaragoza. Spain. * svicen@ipe.csic.es 15 16 17 1 18 Abstract. Aleppo pine (Pinus halepensis Miller) is an important vegetation component in 19 Mediterranean ecosystems, and is a fire-prone species. We studied the spatial and temporal patterns 20 of forest regeneration using a 24-year time series of Landsat images and the normalized difference 21 vegetation index (NDVI) in a homogeneous P. halepensis forest, 3000 ha of which were extensively 22 burned in 1995. We demonstrated a progressive slow and linear recovery in NDVI values, based on 23 Landsat images between 1997 and 2007. The forest tended to recover to pre-disturbance conditions, 24 both with respect to the magnitude of the NDVI and in terms of the spatial pattern. In the burnt area, 25 the fire severity was slightly higher in areas with high pre-fire NDVI values, reflecting the high 26 density of trees and biomass amount. However, we found that the spatial differences in the rates of 27 NDVI recovery were not affected by the burn severity. Moreover, burn severity did not affect the 28 rates of NDVI recovery after the fire. Although highly homogeneous P. halepensis regeneration 29 was the dominant pattern in the study area (more than the 70% of the burn area showed positive and 30 significant trends), some spatial differences in the magnitude of change were observed. The forest 31 tended to recover the spatial pattern corresponding to the pre-fire condition, although it was difficult 32 to establish whether terrain elevation or the previous tree size and density were the main governing 33 factors, given the strong relationship between them. Other topographic factors, such as slope and 34 the incoming solar radiation, did not clearly influence regeneration. 35 Brief summary. We studied the spatial and temporal patterns of forest regeneration using a 24-year 36 time series of Landsat images and the normalized difference vegetation index (NDVI) in a 37 homogeneous P. halepensis forest, 3000 ha of which were extensively burned in 1995. The forest 38 tended to recover to pre-disturbance conditions, both with respect to the magnitude of the NDVI 39 and in terms of the spatial pattern. 40 2 41 Introduction 42 Fire has been an important ecological factor and management tool in Mediterranean ecosystems for 43 thousands of years (Naveh, 1975; Trabaud, 1994). However, wildfire frequency has increased 44 markedly in recent decades due to factors including increased fuel load as a consequence of 45 vegetation regrowth following rural abandonment (Moreno et al., 1998; Vicente-Serrano et al., 46 2000; Viedma et al., 2006), unfavorable climatic conditions (Pausas, 2004), and deliberate fires 47 (Martínez et al., 2008). 48 Wildfires have economic and environmental impacts. Amongst the most important effects of 49 wildfires on vegetation are disorganization of vegetation structure and alterations to successional 50 patterns (Rodrigo et al., 2004). In Mediterranean ecosystems, however, the plant species are 51 adapted to fires. Adaptive responses minimizing fire effects include active and passive mechanisms 52 such as thick insulating bark, sprouting from underground storage organs, and seedling re- 53 establishment. Thus, in spite of the negative short- and long-term effects of fire, these mechanisms 54 enable the rapid recovery of most Mediterranean plant species, and the re-establishment of 55 communities with similar characteristics to those prior to the fire. This is termed an auto- 56 successional process (Hanes, 1971), and several studies have concluded that regeneration following 57 fire is similar to an auto-successional process (Naveh, 1990; Trabaud, 2002). Therefore, fire 58 temporarily alters the structure and composition of the burnt plant communities. 59 Aleppo pine (Pinus halepensis Miller) is an important vegetation component in Mediterranean 60 ecosystems, and is a fire-prone species. P. halepensis seedlings are highly tolerant to hydric stress 61 (Zavala et al., 2000), which allows them to resist the harsh environmental conditions that occur in 62 burnt areas, with high temperatures and bare soil favoring water loss. This tree species has an 63 effective mechanism for fire-induced seed germination (Trabaud et al., 1987; Barbéro et al., 1998; 64 Nathan & Ne’eman, 2000), and is one of the most important serotinous tree species in 65 Mediterranean ecosystems (Barbéro et al., 1998). Serotinous species are characterized by long-term 3 66 retention of seeds within mature closed cones which, when heated by fire, open to release seeds 67 onto the soil. This behavior favors rapid tree regeneration, and a few years after a fire the P. 68 halepensis coverage may be completely recovered (Daskalakou and Thanos, 1996; Pausas et al., 69 2004). However, the process may be spatially inhomogeneous as a consequence of topographic 70 factors including exposure, but the occurrence of new fires may also affect the rate of P. halepensis 71 regeneration, and may produce spatial differences in forest recovery (Tsitsoni, 1997; Broncano et 72 al., 2005; Màrcia et al., 2006). 73 Forest regeneration processes after fire have been widely monitored using remote sensing (e.g. 74 Steyaert et al., 1997; Pérez-Cabello, 2002; Pérez-Cabello et al., 2006; Thompson et al., 2007). 75 Satellite images facilitate assessment of large areas and the temporal recurrence of events, enabling 76 analysis of regeneration processes with very high temporal resolution. The analysis of remote 77 sensing data has allowed assessment of the frequency and surface extent of forest fires over long 78 time periods (Díaz-Delgado and Pons, 2001; Díaz-Delgado et al., 2004), and has enabled analysis 79 of forest regeneration rates (White et al., 1996; Viedma et al., 1997; Epting and Verbyla, 2005), the 80 effect of topographic and geographic factors on the patterns of forest fires and vegetation recovery 81 (Viedma et al., 2006; Wittenberg et al., 2007), and processes related to resilience and forest decline 82 related to burn severity and fire recurrence (Díaz-Delgado et al., 2002; Thompson et al., 2007). 83 Nevertheless, few studies have analyzed fire impacts and vegetation recovery in coniferous forests 84 in semiarid areas near the limit of their ecological distribution, and very few studies focused on P. 85 halepensis forests have been conducted using remote sensing data (e.g., Reyes et al., 2004; 86 Clemente et al., 2009). Although there have been several reports concerning post-fire regeneration 87 of P. halepensis forests using field-collected data (e.g. Kazanis and Arianoutsou, 2004; Broncano et 88 al., 2005), there are few studies focused on this species over large areas representing a range of 89 environmental conditions. The broad spatial coverage and the high temporal and spatial resolution 90 of remote sensing facilitate this approach. 4 91 In this study we investigated the spatial and temporal patterns of forest regeneration using a 24-year 92 time series of Landsat images of a homogeneous P. halepensis forest in which 3000 ha were 93 severely burnt in 1995. The forest is in a semiarid region of northeast Spain characterized by low 94 and variable rainfall, and subject to frequent droughts. The main hypothesis of the research was that 95 the rates of tree colonization after the fire are sufficiently high to guarantee the forest recovery after 96 few years of a severe fire without the need of a human intervention in a well developed semiarid 97 forest and that recovery follows a coherent spatial pattern controlled by environmental or fire 98 factors. For the purpose of testing this hypothesis, multi-temporal Landsat TM and Landsat ETM+ 99 data have been used 100 101 Study area 102 The studied P. halepensis forest is about 35 km from Zaragoza, in the middle of the Ebro River 103 Depression (northeast Spain) in the Montes de Castejón region. The forest is on a structural 104 platform developed on Miocene carbonate and marl sediments, arranged on horizontal strata. Marls 105 are the predominant lithology, with the limestone and gypsum content producing greybrown limy 106 soils with some rendsines and xerorendsines in marly sectors (CSIC, 1970). The climate is 107 Mediterranean with semiarid features. The mean annual rainfall is approximately 400 mm. The 108 nearest weather stations (at Zaragoza and Zuera) are at a lower altitude and have an average annual 109 precipitation of 314 mm and 363 mm, respectively (Cuadrat et al., 2007). Severe droughts are 110 frequent in the region (Vicente-Serrano and Cuadrat, 2007) and periods of more than 50 days with 111 no precipitation are common (Vicente-Serrano and Beguería, 2003). A combination of the low 112 rainfall, the drying effect of the prevailing NW wind (which blows for almost one-third of the year; 113 109 days on average in Zaragoza), and the high temperatures during summer (mean maximum 114 temperature of 31ºC in Zaragoza; Cuadrat et al., 2007) poses extreme challenges to the 115 development of vegetation in the area. 5 116 The landscape is dominated by winter cereal crops (wheat and barley) with small patches of steppe 117 vegetation and forest with thermophilic species such as P. halepensis and Quercus coccifera 118 (Braun-Blanquet and Bolós, 1987). The studied pine forest (Pinares de Zuera) is a relict covering 119 about 17,273 ha, and is comprised mostly of P. halepensis with underlying vegetation dominated by 120 Buxus sempervirens, Juniperus communis and Q. coccifera. In the most degraded areas, mainly on 121 steep slopes, thermophilic shrubs occur, dominated by Rosmarinus officinalis, Thymus sp. and 122 Genista scorpius. Communities dominated by Ononis tridentata, Gypsophila hispanica and 123 Helianthemum squamatum occur on some gypsum outcrops. The area is included in the Natura 124 2000 as a place of special interest to the European Community, because it is the only semiarid forest 125 within a landscape dominated by steppe vegetation. Commercial exploitation of the forest is 126 marginal as the traditional extraction of wood for construction, firewood and resin has been 127 abandoned several decades ago. There is some recreational use of the forest because of its proximity 128 to the city of Zaragoza (population 700,000), a factor that significantly increases the risk of forest 129 fires. 130 131 Methods 132 Field evaluation of forest recovery after fire 133 As a consequence of the climatic conditions and the characteristics of the vegetation, the Zuera hills 134 are subject to recurrent forest fires. The most serious of these affected about 3000 ha of P. 135 halepensis forest in 24th June 1995, mainly in the eastern areas of the Zuera hills and covering a 136 diversity of elevation, aspect and slope conditions. The trees were logged following the fire, and the 137 forest was then abandoned to natural regeneration. In 2008, 13 years after the fire, the majority of 138 the burnt area exhibited complete coverage of P. halepensis with a dense underbrush, in which the 139 dominant species are Q. coccifera, R. officinalis and G. scorpius. As a consequence of the sprouting 140 characteristics of Q. coccifera, in the winter following the fire and in the spring of 1996 there was a 6 141 dense coverage (to 2050 cm) of this and other species (Pérez and Pérez, 2001). . In 2008 the 142 pattern within the fire perimeter was a very dense coverage of P. halepensis (up to 235,000 trees/ha 143 in some areas) 1113 years of age, 1.53 m high, and with basal diameters 39 cm. In some trees 144 early cones were apparent. Although the present coverage of P. halepensis is generally within the 145 fire perimeter, there are some differences in coverage, height and thickness of the trees, which 146 indicates different post-fire recovery rates. 147 148 Spectral signatures of vegetation components 149 A critical factor in monitoring forest regeneration is the feasibility of using remote sensing to 150 identify P. halepensis growth in a complex mosaic of bare soil and charcoal remains, Q. coccifera 151 and other shrubs, and herbaceous species. To assess the potential use of remote sensing to monitor 152 this process, in June and August 2008 we made spectrophotometric measurements in the burnt area 153 using an instrument consisting of two spectrometers (AvaSpec-2048 and AvaSpec-NIR256-1,7) in a 154 AvaSpec Multichannel platform. The spectrometers made measurements in the 4001750 nm 155 spectral range with an optical resolution of 2.46 nm. To improve the signal to noise ratio, spectral 156 data were calculated as the mean of 20 individual spectra on days with a clear sky and no haze. To 157 avoid problems related to variations in incident radiation, measurements were restricted to the 158 period about 2 h before solar noon, where the angle of incidence is close to the vertical. Spectral 159 measurements were performed with a hand-held radiometer pointed vertically downward (nadir) 160 from approximately 0.5 m above the plant canopy. Spectral measurements of a high albedo 161 “spectralon” reflectance panel (30 30 cm PTFE calibration panel) were made immediately before 162 each surface measurement. We obtained a sample of 60 continuous spectral signatures from each of 163 the following species: P. halepensis, Q. coccifera, R. officinales, G. scorpius, Brachipodium sp., 164 bare soil and dry matter within the fire perimeter, and also for ashes in a neighboring forest area 165 affected by fire in August 2008. Figure 1 shows the average spectral signatures obtained for 7 166 different components of the vegetation in August 2008. The spectral signature in the visible region 167 obtained for P. halepensis was similar to that for Q. coccifera and the other shrubs. However, there 168 were marked differences in the infrared region of the spectrum, where the magnitude of reflectance 169 for P. halepensis was approximately double that of the shrubs, indicating much higher vegetation 170 activity in the conifers than in the other cover classes. Thus, the field observations seem to borne 171 out the use of Landsat images for analysis of the regeneration of P. halepensis in relation to the 172 other components of the vegetation. Landsat TM spectral bands were simulated using the 173 continuous spectral signatures obtained in the field, taking into account the spectral responsivity of 174 each Landsat TM band (Teillet et al., 2001), and the normalized difference vegetation index 175 (NDVI; Rousse, 1973) was calculated from the simulated bands. The average NDVI for Q. 176 coccifera was 0.73, for P. halepensis was 0.82, for the other shrubs was 0.67, and for ashes and 177 charcoal was 0.13. 178 Therefore, based on the recovery process observed over 13 years, the spectral information collected 179 in the field, and the large differences in the vegetation activity between P. halepensis and other 180 components of the vegetation, it can be assumed that the baseline vegetation photosynthetic activity 181 after the fire would be lower than that of the original P. halepensis forest. 182 183 Landsat database 184 We used a database of Landsat TM and Landsat ETM+ images for the period 19842007. The 185 database comprised 28 images, 16 of which were from a summer time series and 12 from a spring 186 time series. The two time series were used to identify possible differences in forest recovery as a 187 function of seasonal differences in vegetation activity, and to assess with more robustness any 188 spatial and temporal patterns in the recovery process. Table 1 shows the dates of the images used in 189 each time series. The database was processed using a procedure that included calibration and cross- 190 calibration of the TM and ETM+ images, atmospheric correction using a radiative transfer model 8 191 (6S) that included external atmospheric information, a non-Lambertian topographic correction to 192 avoid errors caused by the differences in illumination conditions, and a relative normalization 193 between dates. The procedure allowed accurate measurements of physical surface reflectance units 194 to be obtained. The correction applied to the images guaranteed the temporal homogeneity of the 195 dataset, the absence of artificial noise caused by sensor degradation and atmospheric conditions, 196 and spatial comparability between different areas, given the accurate topographic normalization 197 applied. Details of the correction procedure applied to the images, and a complete description of the 198 data set and its validation can be found in Vicente-Serrano et al. (2008). 199 200 Estimation of burn severity from Landsat images 201 Burn severity can be obtained from remote sensing data using the spectral information in the images 202 (Brewer et al., 2005; Cocke et al., 2005). Much scientific effort has been devoted to this analysis, 203 and methods of varying complexity can be applied to derive an estimate of the level of damage 204 caused by fire (De Santis and Chuvieco, 2007). A band combination approach can provide a good 205 estimate of the burn severity (Epting et al., 2005), and among the possible band combinations the 206 normalized burnt ratio (NBR) index has provided good estimates of burn severity in several areas 207 (e.g. Epting et al., 2005; Loboda et al., 2007). The index integrates (albeit in opposite ways) the two 208 bands most responsive to burning: near infrared (NIR; 0.760.90 µm) and mid-infrared (SWIR; 209 2.082.35 µm) (Key and Benson, 2002) according to: 210 NBR 211 To provide a quantitative measure of change, the ∆NBR is obtained by subtracting the NBR dataset 212 derived after burning from the NBR dataset derived before burning. It is widely accepted that the 213 ∆NBR image is correlated to the environmental changes caused by fire (Key and Benson, 2004). 214 Numerous studies have found correlations between changes in NBR and field-based severity NIR SWIR NIR SWIR 9 215 metrics in different forest types (Van Wagtendonk et al., 2004). We calculated the ∆NBR using the 216 images for August 1993 and 1995, the latter image recorded two months after the forest fire. 217 218 Analysis of forest recovery from Landsat images 219 The Normalized Difference Vegetation Index (NDVI) has been the most frequently used tool for 220 monitoring, analyzing and mapping temporal and spatial post-fire forest recovery (e.g. Viedma et 221 al., 1997; Díaz-Delgado et al., 2002 and 2003) as it integrates two of the most important bands for 222 vegetation discrimination; the NIR (particularly responsible for the amount of vegetal biomass) and 223 the visible red reflectance (R; 0.630.69 µm). There are some shortcomings in the use of NDVI for 224 monitoring vegetation status. The relationships among vegetation parameters (leaf area index, 225 vegetation cover, green biomass, and NDVI) are often nonlinear (Choudhury et al., 1994; Gillies et 226 al., 1997) as the NDVI signal saturates before the maximum biomass is reached (Carlson et al., 227 1990). Moreover, the NDVI is affected by background soil properties (e.g. surface soil color) that 228 introduce errors (Huete 1988), and the NDVI does not distinguish among vegetation types. Despite 229 these shortcomings, numerous studies have reported a close relationship between the NDVI and 230 several ecological parameters. The NDVI measures the fractional absorbed photosynthetically 231 active radiation (FPAR) (Myneni et al., 1995), and exhibits a strong relationship with vegetation 232 parameters such as green leaf area index (Baret and Guyot, 1991; Carlson and Ripley, 1997), green 233 biomass (Tucker et al., 1983; Gutman 1991), and fractional vegetation cover (Gillies et al., 1997). 234 Moreover, the common problem of NDVI saturation corresponding to the same vegetation coverage 235 or LAI levels does not affect our study, as it concerned the first stages of vegetation recovery, 236 which is clearly recognized in the NDVI (Salvador et al., 2000). To analyze the spatial and 237 temporal patterns of forest regeneration after the fire we calculated the NDVI for each available 238 image in the March and August series. 239 10 240 Statistical analysis 241 Spatial and temporal patterns in the NDVI 242 To determine the post-fire rates of vegetation recovery and its spatial pattern we used the two NDVI 243 time series (August and March) for each of the 32,243 pixels of 900 m2 burnt in 1995. To analyze 244 the statistical significance of the NDVI trends after the fire, we used a non-parametric coefficient 245 (Rho-Spearman), as it is less affected by the presence of outliers and the non-normality of the series 246 than are parametric coefficients (Lanzante, 1996). The analysis was conducted between 1995 (the 247 first image following the forest fire) and 2006 (the last image in the dataset) for the August time 248 series, and between 1997 and 2007 for the March series. The Spearman coefficient identifies 249 statistically significant trends but it does not identify the magnitude of change; for this purpose we 250 calculated for both time series the regression slope between each of the 32,243 series and the series 251 of years. This parameter indicated the rate of increase or decrease of the NDVI per year. 252 To determine the spatial pattern of the NDVI before and after the fire we applied two principal 253 component analyses (for the March and August series) using the NDVI of the 32,243 pixels for the 254 March and August series as variables. The PCA identifies common features, and also allows 255 particular local characteristics to be determined (Richman, 1986; Eastman and Fulk, 1993). A T- 256 mode PCA was applied to identify the general spatial patterns. Periods in which each component is 257 represented can be identified by temporal evolution of the factorial loadings. The number of 258 components was selected according the criteria of an eigenvalue > 1, and the components were 259 rotated (Varimax) to redistribute the final explained variance, and to obtain more stable and robust 260 patterns (Richman, 1986; Hair et al., 1998). 261 262 The role of environmental factors 263 We analyzed the role of a variety of environmental factors in explaining the spatial differences in 264 post-fire forest regeneration. For this purpose we used a 1-m digital elevation model (DEM) 11 265 obtained from pairs of stereo aerial photographs, and re-sampled at 30 m to match the spatial 266 resolution of the NDVI data. From the DEM we derived the terrain slope (degrees) using MiraMon 267 software (Pons, 2008), as some studies have shown that this factor plays a major role in explaining 268 rates of vegetation recovering after fire (Díaz-Delgado et al., 2002; Wittenberg et al., 2007). Instead 269 of using a categorical variable to define the terrain aspect we used a continuous model of incoming 270 solar radiation (Ra), as it provides more spatial details (northern and southern slopes have low and 271 high Ra values, respectively). Ra values were modeled from a DEM with a cell size of 30 m. For 272 this purpose we used an algorithm that includes the effects of terrain complexity (shadowing and 273 reflection) and the daily solar position (Pons and Ninyerola, 2008); this is also implemented in the 274 MiraMon GIS. Ra was measured in MJ m−2 day−1. We also analysed the role of climate parameters 275 in the post-fire forest regeneration. For this purpose, we used the digital layers of annual 276 precipitation and potential evapotranspiration (PET) obtained from the Digital Climatic Atlas of 277 Aragón (http://www.opengis.uab.es/wms/aragon/). Layers were obtained by means of regression- 278 based interpolation considering the 1970-2000 average climatologies, and PET using the 279 Hargreaves equation (Cuadrat et al., 2007). 280 To assess the significance of the relationships between the the environmental variables and the 281 spatial patterns of post-fire forest regeneration taking into account the large dataset (32,243 points), 282 we used a bootstrap approach considering the analysis of 1074 independent samples of 30 random 283 points for each one until complete the totality of the points. We used two different statistical 284 analyses to assess the influence of the variables. On the one hand, we used standard Ordinary Least 285 Square (OLS) regression. Nevertheless, given that the values of each variable are not commonly 286 spatially independent and, therefore, the presence of spatial autocorrelation can severely affect the 287 results, we have also applied a Generalized Least Square model (GLS), in which spatial 288 autocorrelation is accounted for. The method improves other statistical procedures to consider 289 spatial autocorrelation in the data (Beguería and Pueyo, 2009). GLS was performed using the nlme 12 290 package implemented in R software. In the GLS models we specified the correlation structure 291 defining an exponential semivariogram model with a single (range) parameter, which was 292 determined automatically. Analysis of variance (ANOVA) was applied for each one of the 1074 293 OLS and GLS models corresponding to each variable. The purpose was to determine if spatial 294 autocorrelation in the datasets is affecting noticeably the results and if significant differences are 295 obtained using OLS or GLS in the influence of each environmental variable on the vegetation 296 recovery after the fire. Given the large number of analysis performed using independent 30 point 297 samples, we considered a significant influence of each variable on post-fire forest regeneration 298 when more than 80% of the samples showed a significant relationship (for the OLS and GLS 299 methods) at the 95% significance level. 300 301 Results 302 Spatial patterns of fire severity 303 Figure 2 shows the spatial distribution of the NBR, which indicates the fire severity in the burnt 304 area 41 days (approximately two months) following the fire. At this time there was a predominance 305 of areas with moderately high and high fire severity (65.3% of the study area). The maximum 306 severity was recorded on southern and northern slopes of the main ravines, which are orientated 307 eastwest. There was no clear topographic or climatic relationship with the fire severity since no 308 significant relationship (> 80% of the samples at 95% significance level) has been found between 309 the spatial distribution of the NBR and the topographic and climatic variables. 310 311 Spatial and temporal patterns of vegetation recovery after fire 312 Figure 3 shows the evolution of average and standard deviation values for the NDVI in the burnt 313 area for the August and March time series. In both series there was a clear difference between the 314 pre-fire period, in which the NDVI generally showed low temporal variability, and the post-fire 13 315 period, in which the time series showed a general post-fire trend of a progressive increase in the 316 NDVI values. In the August series the NDVI between 1984 and 1993 showed similar average 317 values and very low temporal variability, indicating stability in the coniferous canopy. The 318 consistency of values could be associated with problems of signal saturation, although this is 319 unlikely, as in March the NDVI values were slightly higher than in August. A more likely 320 explanation is that the forest was well adapted to the limiting environmental conditions, which 321 included droughts that affected the region in some years; a drought in 1992 was associated with a 322 slight decrease in the average NDVI. Immediately after the fire there was an abrupt decrease in the 323 NDVI, from an average of approximately 0.6 to 0.4 in 1995 and 1997. The high NDVI baseline 324 after the 1995 fire, relative to the expected NDVI, was mainly a consequence of the reduction in 325 temporal variance through use of the relative radiometric correction method. This phenomenon is 326 common with the application of relative correction techniques, which reduce the variability related 327 to the most extreme values but provide a higher temporal consistency and homogeneity to the 328 resulting trends (Vicente-Serrano et al., 2008). In the following years there was a progressive 329 increase in the NDVI to an average of approximately 0.54 between 2004 and 2006, which was 330 similar to the pre-fire NDVI values. The standard deviation decreased markedly after the fire, 331 indicating a general spatial homogenization of the NDVI within the burnt area. After the fire the 332 standard deviation increased to approximately 0.1 between 1999 and 2002, and continued to 333 increase thereafter, with maximum standard deviations (0.13 in 2004, 0.12 in 2005 and 0.14 in 334 2006) much higher than during the pre-fire period (0.080.11). This indicates that natural forest 335 regeneration was accompanied by an increase in spatial variability in the NDVI, which suggests 336 spatial differences in forest regeneration. 337 The March series showed an abrupt decrease in the NDVI after the 1995 fire, even more marked 338 than for the August time series, although no images were available for the year immediately 339 following the fire (1996). The rate of recovery in the NDVI in the March time series was much 14 340 more rapid than for the August series. For the last two images the average NDVI was similar (0.66 341 and 0.65 for 2005 and 2007, respectively) to the pre-fire average NDVI value. Spatial variability in 342 NDVI values, indicated by the standard deviation, also showed a similar pattern to that observed in 343 the August series, indicating a decrease in variability immediately after the fire, and a progressive 344 increase after 2000. 345 Figure 4 shows the spatial distribution of NDVI values corresponding to years before and after the 346 fire. In 1993 the vegetation activity was higher in March than August over the whole study area, 347 although the spatial patterns of vegetation activity were highly related (R = 0.71 between the spatial 348 distribution of the NDVI in March and August 1993). The smaller magnitude of the index and the 349 greater variability of the values in August could be related to a contribution of herbaceous species, 350 which are much more sensitive to the drought conditions in summer. The same pattern was 351 observed for the years before the fire (R = 0.56 in 1997, R = 0.72 in 2005). This indicates there was 352 no seasonal effect on the pattern and rate of vegetation recovery, and suggests the results are robust. 353 The effect of the forest fire was evident in 1997, with a sharp decrease in the NDVI values over the 354 whole study area in both the March and August series. Five years after the fire, in 2000, there was 355 partial recovery in the NDVI value, but there were some spatial differences; in both the March and 356 August series the highest NDVI values were recorded in the northeast, whereas NDVI values in the 357 east and southeast were more similar to those in the immediate post-fire period. The last available 358 images, in 2006 and 2007, show that the NDVI was similar to that in the pre-fire period over the 359 majority of the burnt area, with a similar pattern for the August and March series. The exception 360 was a small area in the southwest, which was burnt in winter 2007 and had a NDVI value below 0.6 361 in March 2007. 362 Temporal analysis of the NDVI after the fire showed a general positive trend toward higher values 363 over most of the study area. The spatial pattern of recovery was very homogeneous for both the 364 August and March series. Of the area burnt in 1995, 71.6% showed a positive and significant trend 15 365 (p < 0.05) in the August NDVI values between 1995 and 2006, and 73% showed a similar trend for 366 the March series between 1997 and 2007. There were no areas with negative and significant trends 367 in the NDVI during the analyzed post-fire period, and 28.4% (August series) and 27% (March 368 series) of the area showed no significant changes during the analyzed period. 369 Although an increase in the NDVI was the general pattern over the burnt area, there were marked 370 spatial differences in the rates of vegetation recovery and, therefore, in the magnitude of the NDVI 371 changes throughout the post-fire period. Figure 5 shows the NDVI change per year based on the 372 spatial distribution of regression slopes between the series of years (independent variable) and the 373 NDVI series (dependent variable). The assumption of a linear recovery appears reasonable given 374 the evolution for the study area (Fig. 3). The range of vegetation recovery ranged from a minor 375 decrease in NDVI values per year (< 0.005 units per year) to a substantial increase (> 0.045 units). 376 The magnitude of the NDVI increase was higher for the March series than the August series, and 377 this was not affected by the period used to calculate the regression slopes: the magnitude of the 378 NDVI change and the spatial pattern was similar (data not shown) for the August series slopes 379 calculated over the 19972006 period. Although the rate of NDVI increase was higher in the March 380 time series, the spatial pattern was similar, with strong agreement between the patterns of NDVI 381 recovery in both time series. Thus, there was a significant correlation (R = 0.57) between the spatial 382 distribution of the NDVI rates per year in the March and August time series showing that patterns in 383 the rates of vegetation recovering after the fire are well identified using Landsat images 384 independently of the season used for monitoring. 385 Figure 6 shows the spatial pattern of the three components obtained from the T-mode PCA for the 386 NDVI time series for March and August. Figure 7 shows the similarity of each NDVI image to the 387 three patterns as a plot of the component loadings (correlation between the patterns and the NDVI 388 for each date) to identify which periods are representative of each pattern. The first three 389 components explained 77% of the variance for the August series, and 59% for the March series. 16 390 This indicates there was higher temporal variability in the NDVI spatial patterns in the August 391 series. The first component explained more than 30% of the variance for both the March and 392 August series. Both the August and March components showed similar spatial patterns with few 393 differences. The first component had a very homogeneous pattern of high values over the most 394 elevated areas. The lower NDVI values were at the margin of the forest, mainly in the lower areas 395 of the south and southeast, where the greatest aridity was recorded. Figure 6 also indicates the high 396 spatial homogeneity of the P. halepensis forest prior to the fire, as this pattern was representative of 397 the pre-fire period for both the March and August series; this pattern is characteristic of a mature 398 forest in which the differences in vegetation activity are determined by varying environmental 399 conditions. After the fire, the spatial organization of the NDVI changed markedly relative to the 400 pre-fire period. The spatial configuration of the NDVI in the years immediately following the fire is 401 represented in both time series by the second component. This shows a pattern of the highest NDVI 402 values occurring in the northwest of the study area, and the lowest values in the east and southeast. 403 The temporal evolution of the pattern showed some differences between the March and August 404 series: although the loading values were maximum after the fire in both series, the pattern was 405 evident for more years (19972001) for the August series than for the March series (only 1997 and 406 1998). These results indicate that vegetation recovery was favored by the higher moisture 407 conditions common in spring, making the pattern less consistent. In contrast, with the high water 408 stress in summer, the pattern would be more consistent. The third component showed the general 409 pattern for the last years in the August time series, whereas for the March series the pattern was 410 clearly dominant in 1999 and 2000; the following years showed some similarity to the second 411 component, but also with the pre-fire conditions represented by the first component, mainly for the 412 March time series. These results suggest that in the two years following the fire, the spatial 413 configuration of vegetation activity was different from the previous conditions, and that it was 414 determined by other factors, such as the previous vegetation cover or the spatial pattern of fire 17 415 severity. As the regeneration processes progressed, the spatial pattern would tend to be more similar 416 to the pre-fire conditions. 417 418 Factors affecting spatial patterns of vegetation recovery after fire 419 Figure 8 shows the relationship between the rates of vegetation recovery after the fire (NDVI 420 increase per year, derived from the regression slopes between each of the 32,243 NDVI series and 421 the time series) and some topographical and climatic variables (elevation, slope, Ra, precipitation 422 and PET), the pre-fire and immediately post-fire NDVI, and the NBR for the August series. The 423 results found for the March series are very similar and they are not shown. The percentage of the 424 1074 independent analysis in which the relationship between the rate of forest recovery after the fire 425 and each variable was significant using the OSL and GLS methods is shown in Table 2. The results 426 are quite similar considering OLS and GLS approaches, and the ANOVA analysis does not show 427 large percentage of cases in which OLS and GLS significantly provide different results regarding 428 the role of the environmental variables on the forest recovery after the fire. Both procedures show 429 that the rates of vegetation recovery were directly related to the elevation and the spatial distribution 430 of the pre-fire NDVI. 431 The slope and exposure (solar radiation) did not explain the spatial pattern of forest regeneration. 432 Precipitation and PET show a direct and inverse relationship with forest regeneration, respectively 433 although the percentage of analysis with a significant relationship was very low (35% and 0.13% 434 for precipitation in August and March, respectively, and 21% and 10% for PET considering the 435 GLS method). Generally, it is interesting to note that the influence of the climate variables on 436 vegetation recovery is stronger in summer, when water stress is higher. Although the fire severity 437 (NBR) had a positive relationship with the rates of forest regeneration, the influence was only 438 significant for the 38% and 27% of the models for August and March, respectively. The post-fire 439 NDVI pattern (NDVI-95) was not significantly related to the spatial pattern of forest regeneration 18 440 but the relationship was positive in both seasons (R = 0.35 and R= 0.33, for August and March, 441 respectively), which indicates that post-fire forest regeneration could be favored by the patterns of 442 post-fire tree survival. The variable that contributed most to explaining the spatial patterns of forest 443 regeneration rates was the pre-fire NDVI pattern (92% and 75% of the models showing a significant 444 influence for the August and March series, respectively), again indicating the tendency of the forest 445 to recover to pre-fire conditions. 446 447 Discussion and conclusions 448 This study analyzed the impact of forest fire on the spatial and temporal patterns of vegetation 449 activity in a homogeneous P. halepensis forest in a semiarid region subject to limiting 450 environmental conditions. The hypothesis formulated at the beginning of the study has been 451 confirmed. Thanks to the use of long time series of satellite imagery we have shown that in a semi- 452 arid region with no human intervention after the fire disturbance, the rates of tree colonization after 453 the fire are sufficiently high to guarantee the forest recovery 13 years after a severe fire. Moreover, 454 the results also indicate that the spatial pattern of the forest growth tended to recover to the pre- 455 disturbance conditions. 456 The use of two seasonal remote sensing series conferred a high degree of reliability on the results, 457 and also demonstrated that the use of remote sensing data to monitor the fire consequences and the 458 regeneration processes was not affected by the season selected for analysis. Although the rates of 459 vegetation recovery were slightly greater in spring than summer, the spatial patterns of forest 460 recovery were quite similar, as were the roles of the various topographic and environmental factors 461 analyzed. 462 The close relationship between the results obtained for the summer and spring series also indicated 463 the robustness of the use of the NDVI to monitor the growth of P. halepensis in relation to other 464 species in the canopy. The forest regeneration observed in the field indicates that the first available 19 465 satellite images after the fire (1997) reflected very diverse vegetation cover, mainly composed of 466 various shrub and herbaceous species and bare soil, but dominated by Q. coccifera because of its 467 capacity for rapid sprouting. At this stage the P. halepensis density was low, although the first trees 468 had appeared a few months after the fire. Using field radiometry we showed that P. halepensis has a 469 much higher vegetation activity and NDVI value than the other components of the canopy. This 470 would explain why two years after the fire, despite the vegetation cover being high over the 471 majority of the study area (average about 50%), the NDVI fell dramatically relative to the pre-fire 472 conditions characterized by a dense P. halepensis forest with high vegetation activity. 473 The vegetation recovery observed in the field was consistent with the progressive recovery of the 474 NDVI value, as determined from the Landsat images for 19972007. It is widely accepted that 475 Mediterranean ecosystems affected by fire show direct regeneration, which tends to be 476 characterized by restoration of the community that was present immediately prior to the disturbance 477 (Trabaud and Lepart, 1980; Trabaud, 1994). The high capacity of P. halepensis forests to recover 478 after fire is well known, due to the large seed bank stored in the canopy (Tapias et al., 2001). This 479 capacity was highlighted by Broncano et al. (2005), who showed that monospecific forests of P. 480 halepensis have a high probability of returning to their original composition after fire, whereas the 481 resilience of mixed forests is much lower. For the Zuera hills we showed that the forest tended to 482 recover to the pre-disturbance conditions, both with respect to the magnitude of the NDVI and the 483 spatial pattern. This pattern could be related to two factors acting individually or in combination. 484 On the one hand, in dense areas the canopy seed bank should favor the development of a denser 485 coverage of trees after fire. This hypothesis is consistent with the finding of Pausas et al. (2004) that 486 the recovery P. halepensis forests of southeast Spain was related to the height of the trees prior to 487 disturbance. 488 In the burnt area, the fire severity was slightly higher in areas with previously high NDVI values, 489 indicative of the high density of trees and the amount of biomass. This is a common pattern which 20 490 has been identified using remote sensing data under a variety of environmental conditions (e.g. 491 Epstein and Verbyla, 2005; Thompson et al., 2007). Generally speaking, high-severity burnt areas 492 register higher rates of soil loss and lower rates of vegetation recovery, due to the higher destruction 493 of the forest floor and shallow buried seeds, and destruction of the canopy (DeBano et al., 1998). 494 The corollary is that a rapid return to pre-fire conditions is expected in low-severity burnt areas. 495 Nevertheless, in the Zuera forest we found that the spatial differences in the rates of NDVI recovery 496 were not affected by the burn severity. In contrast to other studies showing that the largest decline 497 in the NDVI corresponded to the highest burn severity (Díaz-Delgado et al., 2003; Epstein and 498 Verbyla, 2005), in the Zuera forest the spatial distribution of NDVI values two years after the fire 499 (1997) was not correlated to the burn severity. Moreover, the burn severity did not affect the rates 500 of NDVI recovery after the Zuera forest fire. These patterns could be related to the homogeneity of 501 the fire severity that affected the Zuera forest, as evidenced by the NBR values. Good regeneration 502 of forests affected by high burn severity is not rare (Donato et al., 2006). Pausas et al. (2003) 503 showed better regeneration of P. halepensis forests in sites of high fire severity in southeast Spain. 504 Pausas et al. (2003) suggested that high fire severity favored seeding species over sprouting species, 505 as a consequence of higher mortality among the latter due to the fire severity. This pattern is in 506 agreement with the observed recovery of vegetation after the fire in the Zuera forest; although Q. 507 coccifera was the dominant species in the canopy during the first years after the fire, its maximum 508 coverage was only 40% in the most favorable areas (Pérez and Pérez, 2001), and several years after 509 the fire P. halepensis was again the dominant species. 510 Although homogeneous P. halepensis regeneration has been the dominant pattern in the Zuera 511 forest (more than the 70% of the burnt area showed positive and significant trends), some spatial 512 differences in the magnitude of change were observed. However, as noted previously, the forest 513 tended to recover to the pre-fire spatial pattern, and it was difficult to establish whether differences 514 in the elevation (affecting climate conditions) or the previous tree size and density were the main 21 515 governing factors, given the strong relationship between these factors in the forest preceding the 516 fire. Other topographic factors, such as slope and exposure, did not clearly influence regeneration. 517 Although regeneration of vegetation since the Zuera forest fire has been successful with high 518 regeneration rates in few years without the need of human intervention, the present high tree density 519 poses risks to forest development due to high mortality and high dry biomass accumulation, but also 520 because of high water stress coupled with the low capacity of the trees to develop root systems. 521 Thus, if a new forest fire occurs in these immature stages of the forest, the consequences could be 522 serious, as the success of recovery is mainly dependent on the canopy seed bank to enable rapid and 523 dense post-fire natural revegetation. The production of seeds by immature trees is low, and 524 regeneration after a new fire may have a low probability of success. It is well known that recurrent 525 wildfires have caused a decline in growth and decreased the recovery capacity of Mediterranean 526 forests (Díaz-Delgado et al., 2002; Màrcia et al., 2006). Consequently, it is essential that forest 527 management strategies be put in place to diminish the fire risk and to favor the development of 528 mature forests similar to those of pre-fire conditions. 529 530 Acknowledgements 531 This work has been supported by the research projects CGL2008-01189/BTE, CGL2006- 532 11619/HID and CGL2008-1083/CLI financed by the Spanish Commission of Science and 533 Technology and FEDER, EUROGEOSS (FP7-ENV-2008-1-226487) and ACQWA (FP7-ENV- 534 2007-1- 212250) financed by the VII Framework Programme of the European Commission, “Las 535 sequías climáticas en la cuenca del Ebro y su respuesta hidrológica” and “La nieve en el Pirineo 536 aragonés: Distribución espacial y su respuesta a las condiciones climática” Financed by “Obra 537 Social La Caixa” and the Aragón Government and “Programa de grupos de investigación 538 consolidados” financed by the Aragón Government. 539 540 References 22 541 Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean 542 basin. 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Two last columns show the percentage of the 1074 models in which the analysis 740 of variance (ANOVA) indicates significant differences in the results between the OLS and GLS 741 methods. 742 Figure captions 743 Figure 1: Average spectral signatures of Pinus halepensis, Quercus coccifera, ashes and charcoal, 744 and various other shrub and herbaceous cover, determined in the field in the Zuera forest in August 745 2008. 746 Figure 2. Spatial distribution of the NBR in the burnt areas, and histogram of NBR values 747 within the fire perimeter. 50 m. contour lines are included in the figure. 748 Figure 3. Average and standard deviation values for the NDVI for the March and August time series 749 for areas within the 1995 fire perimeter. 750 Figure 4. Spatial distribution of NDVI values in August and March for different years. 751 Figure 5. Spatial distribution of the rates of NDVI recovery per year (regression slopes) after the 752 1995 fire (19952006 for the August time series, and 19972007 for the March time series). 753 Figure 6. Spatial distribution of the T-mode Rotated PC-scores corresponding to the August and 754 March NDVI series. 755 Figure 7. Temporal evolution of the T-mode Rotated PC loadings obtained from the August and 756 March NDVI series. The percentage of the explained variance by each component is shown. 757 Figure 8. Relationship between the spatial distribution of the rates of NDVI regeneration after the 758 fire for the August series, quantified using the regression slopes, the NDVI before and after fire, the 759 topographic and climatic variables and the NBR. 760 31 761 762 Table 1. March Date 03/11/1989 03/30/1990 03/06/1993 03/09/1994 03/28/1995 03/17/1997 03/20/1998 03/23/1999 03/17/2000 03/10/2003 03/07/2005 03/13/2007 Sensor TM TM TM TM TM TM TM TM ETM+ ETM+ TM TM August Date 08/20/1984 08/07/1985 08/13/1987 08/02/1989 08/24/1991 08/10/1992 08/29/1993 08/03/1995 08/24/1997 08/14/1999 08/08/2000 07/26/2001 08/30/2002 08/27/2004 08/14/2005 08/01/2006 Sensor TM TM TM TM TM TM TM TM TM TM ETM+ ETM+ ETM+ TM TM TM 763 764 32 765 766 Table 2. NDVI-95 NDVI-93 Elevation Slope Solar Radiation NBR Pecipitation PET OLS August 47 95 84 2 March 51 80 82 1 GLS August 39 92 78 8 March 42 75 75 6 ANOVA August 18 11 11 34 March 24 22 18 37 0 29 46 0 2 21 21 0 16 38 35 21 9 27 13 10 35 38 22 29 36 41 37 38 767 768 33 769 0 .3 5 0 .3 0 P in u s h a le p e n s is R eflectance 0 .2 5 Q u e rc u s c o c c ife ra 0 .2 0 0 .1 5 S h ru b s 0 .1 0 A s h e s a n d d ry m a tte r 0 .0 5 0 .0 0 400 770 771 772 773 500 600 700 800 900 1000 W a v e le n g h t ( m ) Figure 1. 34 774 775 776 777 778 779 780 Figure 2. 35 781 Fire 0.8 0.7 NDVI 0.6 0.5 0.4 0.3 August 0.2 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 0.8 0.7 NDVI 0.6 0.5 0.4 0.3 March 782 783 784 785 0.2 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 Figure 3. 36 786 787 788 Figure 4. 37 789 790 791 792 793 Figure 5. 38 794 795 796 797 798 799 800 Figure 6. 39 August March 0.8 1.0 PC 1 (35%) 0.6 0.4 0.2 R-Pearson R-Pearson 1.0 0.8 PC 2 (26%) 0.6 0.4 0.2 0.0 0.2 0.8 PC 2 (16%) 0.6 0.4 0.2 1.0 PC 3 (17%) 0.6 0.4 0.2 0.0 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 R-Pearson R-Pearson 801 802 803 804 805 0.4 0.0 1.0 0.8 PC 1 (32%) 0.6 0.0 1.0 R-Pearson R-Pearson 0.0 1.0 0.8 0.8 PC 3 (11%) 0.6 0.4 0.2 0.0 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 Figure 7. 40 806 807 808 809 810 811 Figure 8. 41