Ecology, 88(9), 2007, pp. 2270–2279
Ó 2007 by the Ecological Society of America

September 2007                     DROUGHT RESISTANCE AND PLANT RICHNESS                                               227...
2272                                             F. LLORET ET AL.                                 Ecology, Vol. 88, No. 9
September 2007                      DROUGHT RESISTANCE AND PLANT RICHNESS                                                 ...
2274                                                 F. LLORET ET AL.                                  Ecology, Vol. 88, N...
September 2007                     DROUGHT RESISTANCE AND PLANT RICHNESS                                                  ...
2276                                             F. LLORET ET AL.                                Ecology, Vol. 88, No. 9

September 2007                   DROUGHT RESISTANCE AND PLANT RICHNESS                                               2277
2278                                                  F. LLORET ET AL.                                    Ecology, Vol. 88...
September 2007                      DROUGHT RESISTANCE AND PLANT RICHNESS                                                 ...
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  1. 1. Ecology, 88(9), 2007, pp. 2270–2279 Ó 2007 by the Ecological Society of America WOODY PLANT RICHNESS AND NDVI RESPONSE TO DROUGHT EVENTS IN CATALONIAN (NORTHEASTERN SPAIN) FORESTS F. LLORET,1,5 A. LOBO,2 H. ESTEVAN,3 P. MAISONGRANDE,4 J. VAYREDA,3 AND J. TERRADAS1 1 CREAF (Center for Ecological Research and Forestry Applications) - Departament de Biologia Animal, Biologia Vegetal i Ecologia, Universitat Auto `noma de Barcelona, 08193 Bellaterra, Barcelona, Spain 2 Institut de Cie`ncies de la Terra ‘‘Jaume Almera’’ (CSIC), Lluis Sole´ Sabarı´s s/n, 08028 Barcelona, Spain 3 CREAF (Center for Ecological Research and Forestry Applications), Universitat Auto `noma de Barcelona, 08193 Bellaterra, Barcelona, Spain 4 ´ Centre d’Etudes Spatiales de la Biosphe`re (CESBIO), bpi 2801, 18, avenue Edouard Belin, 31401 Toulouse Cedex 9, France Abstract. The role of species diversity on ecosystem resistance in the face of strong environmental fluctuations has been addressed from both theoretical and experimental viewpoints to reveal a variety of positive and negative relationships. Here we explore empirically the relationship between the richness of forest woody species and canopy resistance to extreme drought episodes. We compare richness data from an extensive forest inventory to a temporal series of satellite imagery that estimated drought impact on forest canopy as NDVI (normalized difference vegetation index) anomalies of the dry summer in 2003 in relation to records of previous years. We considered five different types of forests that are representative of the main climatic and altitudinal gradients of the region, ranging from lowland Mediterranean to mountain boreal-temperate climates. The observed relationship differed among forest types and interacted with the climate, summarised by the Thorntwaite index. In Mediterranean Pinus halepensis forests, NDVI decreased during the drought. This decrease was stronger in forests with lower richness. In Mediterranean evergreen forests of Quercus ilex, drought did not result in an overall NDVI loss, but lower NDVI values were observed in drier localities with lower richness, and in more moist localities with higher number of species. In mountain Pinus sylvestris forests NDVI decreased, mostly due to the drought impact on drier localities, while no relation to species richness was observed. In moist Fagus sylvatica forests, NDVI only decreased in plots with high richness. No effect of drought was observed in the high mountain Pinus uncinata forests. Our results show that a shift on the diversity–stability relationship appears across the regional, climatic gradient. A positive relationship appears in drier localities, supporting a null model where the probability of finding a species able to cope with drier conditions increases with the number of species. However, in more moist localities we hypothesize that the proportion of drought-sensitive species would increase in richer localities, due to a higher likelihood of co-occurrence of species that share moist climatic requirements. The study points to the convenience of considering the causes of disturbance in relation to current environmental gradients and historical environmental constraints on the community. Key words: climate change; ecosystem resistance; forest dieback; Mediterranean forests; NDVI; species diversity. INTRODUCTION between diversity and the resistance of the ecosystem The role of species diversity in the functioning of (Tilman and Downing 1994, McGrady-Steed et al. 1997, ecosystems has become one of the most challenging Naem and Li 1997). However, Loreau (2000) used a topics in recent ecological research. Evidence of great model approach to conclude that resistance may decrease human-induced transformations ranging from the local or increase with increasing diversity. A selection mech- to the global scale has highlighted the importance of this anism (Huston 1997) (equivalent to the sampling effect question. One particular issue concerns the role of species described by Tilman et al. 1997), by which ‘‘diversity diversity on ecosystems’ ability to face strong environ- increases the range of trait variation and a selective mental fluctuations, such as extreme climate events, process promotes dominance by species with extreme which in some cases can be considered as disturbances. trait values’’ (Loreau 2000), would explain these different Experimental results point to a positive relationship relationships. A positive relationship would be found if the disturbance has a negative effect on most species and diversity enhances the probability of finding the species Manuscript received 13 July 2006; revised 7 February 2007; best adapted to afford the new conditions (Loreau 2000). accepted 12 February 2007. Corresponding Editor: T. J. Stohlgren. This response would be enhanced by historically- 5 E-mail: fluctuating selective pressures that remain promoting 2270
  2. 2. September 2007 DROUGHT RESISTANCE AND PLANT RICHNESS 2271 the occurrence of traits fitting the new conditions. In addition, extensive forest inventories provide Alternatively, a greater number of species may imply reliable information about the forest composition of greater changes in ecosystem properties under the new woody species across large territories, and both types of disturbance conditions when competitive pressures information may be integrated into geographical infor- under non-disturbance conditions tended to eliminate mation systems (GIS). disturbance-tolerant species from the community. During the summer of 2003 an intense drought Climate models and current empirical trends point to an episode occurred in southwestern Europe, which was increase of climatic variability in some regions, resulting in well documented by remote sensing imagery (Gobron et a greater number and intensity of extreme events (Voss et al. 2005, Lobo and Maisongrande 2005). In the present al. 2002). In the particular case of the Mediterranean study, we analyze the relationship between woody Basin, where water availability is the major environmental species richness obtained from extensive forest invento- constraint to plant growth, and where episodes of drought ries in Catalonia (northeastern Spain) and drought resulting in forest dieback have been recorded in the last impact on the canopy of forests, estimated as NDVI decades (Penuelas et al. 2001, Lloret et al. 2004), current ˜ anomalies of the year 2003 in relation to median NDVI models predict warmer and drier conditions (Houghon et records of previous years. We assume that the canopy al. 2001, Gibelin and Deque 2003), with increased NDVI values in the dense forests under study were seasonal and inter-annual variability resulting in more mostly determined by woody species. We consider five common and intense drought events (Houghton et al. different types of forests, defined by their dominant tree 2001, Sanchez et al. 2004). species, which are representative of the main climatic As experimental manipulation of climate and richness and altitudinal gradients of the region. Our main in forest ecosystems is unlikely to be performed, direct hypothesis is that species richness correlates positively with canopy resistance to drought, this pattern being observations of the effect of extreme climate events are more evident in those communities where drought currently the most reliable approach for investigating intensity was higher, and where drought-driven selection the relationship between forest species richness and the has been historically prevalent. effects of extreme drought on forest properties. In addition, extensive sampling is recommended to inves- METHODS tigate regional patterns, on a similar scale to that at Study area which drought occurs. The scaling-up of the level of observation requires integrative variables related to Catalonia (0815 E, 40830 0 N to 3815 0 E, 42840 0 N, 0 ecosystem functioning, although accurate details of ;31 900 km2) is located in the northeast of the Iberian functioning at stand level may be missed. Remote Peninsula, including the Pyrenean range to the north sensing imagery has been revealed as a useful tool to and bounded to the east by the Mediterranean Sea. describe structural patterns of vegetation determining Most of the area falls under different degrees of primary productivity in relation to between-year climat- Mediterranean climate, with a main climatic-topograph- ic variability at local and regional scales (Tucker and ic gradient from a temperate-boreal climate (mean Sellers 1986, Paruelo et al. 2001). NDVI (normalized annual precipitation of up to 1500 mm) in the Pyrenees, difference vegetation index) is a normalized contrast to a Mediterranean climate of mild winters and dry between near infrared and red reflectance, thus empha- summers (mean annual precipitation from 530 mm) in sizing the presence of green vegetation in the area the southern extreme. There is also a continental, corresponding to the pixel. Since NDVI integrates both semiarid gradient inland towards the west, with colder the abundance of green vegetation and its greenness, it winters, very hot summers, and low rainfall (mean has a certain consubstantial ambiguity. Also, as NDVI annual precipitation around 400 mm). Vegetation types is a two-dimensional approximation to a three-dimen- across the climatic-topographic gradients include scle- rophyllous, evergreen shrublands and forests, deciduous sional reality in which leaves tend to be arranged in forests, and coniferous forests (Folch 1981), all with a different layers, the relationship between NDVI and long history of human management. PAR tends to saturate in the case of highly multilayered canopies. Notwithstanding, if time series are available Climatic data and remote sensing estimation for post-processing and certain observations (i.e., of forest drought extreme angles) are disregarded, NDVI is a linear ` From the Atlas Climatic Digital de Catalunya, we estimate of the fraction of photosynthetically active obtained for each plot locality the Thorntwaite index as radiation (PAR) that is intercepted by the photosynthe- a standard index that effectively describes the aridity– sizing tissue of vegetation present in the pixel. Because moisture climatic gradient, from the Mediterranean of the aforementioned multilayering, NDVI correlations coast to the mountains inland (Lloret et al. 2005; atlas between NDVI and LAI (leaf area index; i.e., Chen and available online). 6 The Thorntwaite index was Cihlar 1996, Cohen et al. 2003) are more variable, with a calculated as follows: less close fit and quicker saturation than in the case of APAR. NDVI has also been found to correlate to ecosystem CO2 flux (Wylie et al. 2003, Li et al. 2005). 6 h
  3. 3. 2272 F. LLORET ET AL. Ecology, Vol. 88, No. 9 Thorntwaite index ¼ ðP À ETP Þ 3 100=ETP average annual series of monthly mean NDVI images for the period 1999–2002, which we used as the where P is annual precipitation (mm), and ETP is annual ‘‘normal’’ reference, and an annual series of monthly potential evapotranspiration (mm), which is the sum of mean NDVI images for 2003. We calculated the monthly evapotranspiration values calculated following difference between the respective 2003 and 1999–2002 the Thorntwaite formula (Thorntwaite 1948). This mean NDVI values, and we finally estimated NDVI calculation considers for each plot locality the mean anomalies as the difference between the respective 2003 monthly average values of temperature, that were and 1999–2002 mean NDVI values (Fig. 1). Considering ` obtained from the Atlas Climatic Digital de Catalunya, that the period of drought concluded by the end of and a coefficient estimated by the numbers of days in a August in southwestern Europe, we use in this study the month and the daily hours of sun as a function of anomaly of NDVI in August 2003 as an estimate of the latitude. impact of the drought in the canopy. Also, this month is The difference between precipitation and evapotrans- at the peak of the dry season, when a large part of the piration can be considered as an estimation of the herbaceous vegetation has probably burned off, causing balance between atmospheric water supply and demand the minimal interference to the NDVI scores. (Lobo and Maisongrande 2005). During the drought episode of the summer of 2003, in most of our region of Species richness data study, the difference between total precipitation and evapotranspiration showed a negative anomaly of more Richness data are based on circular field plots than 100 mm (Lobo and Maisongrande 2005). This established in the Third National Forest Inventory of information was obtained by comparing climate and ´ Spain (IFN3; Direccion General de Conservacion de la´ meteorological data of June, July, and August 2003 to Naturaleza 2006). Sampling was conducted from 2000 to data of the same months for the period 1961–2000, 2001 at a density of 1 plot/km2, following a regular provided as grids of 5 3 5 km resolution by the Spanish design within the forested surface of the whole territory Instituto Nacional de Metereologia (INM) (Lobo and (Fig. 1). Each plot was located in the field by a global Maisongrande 2005). positioning system (GPS), allowing for cross-references The vegetation response to water deficit was assessed with climatic databases (see footnote 6). from the normalized difference vegetation index (NDVI; The IFN3 survey includes exhaustive information on Tarpley et al. 1984) included in the S10 products that are the composition of canopy and understory woody derived from images acquired by the VEGETATION species, as well as on production and structure. We instrument onboard satellite SPOT. VEGETATION is restricted our analysis to this group as no consistent an optical multi-spectral instrument that acquires a daily information is available for non-woody species. Shrub and almost complete cover of the Earth’s surface at 1- and regenerative trees (defined as those with a normal km2 resolution in four spectral bands (Hagolle et al. diameter, measured 50 cm above the ground surface, 2004). S10 products are calibrated, atmospherically and below 75 mm) were sampled within circular plots with a geometrically corrected images. radius of 10 and 5 m, respectively). Extensive stands of The VEGETATION S10 collection is produced from regenerative trees after clearing are not common in the temporal compositing of calibrated, atmospherically region and are not included in the study. Plot size for and geometrically corrected images, by the combination sampling the rest of the trees varied in order to sample of daily images in periods of 10 days. The aim is to enough individuals belonging to the largest size classes create a synthetic reconstruction from cloud-free images present in the plot. In order to minimize species richness that is assumed to be representative of each 10-day bias due to plot size, we compared the richness shown by period. The maximum value composite (MVC; Holben plots of different size in each forest type. In the cases 1986) procedure is used for compositing in VEGETA- where differences arose (Fagus sylvatica and Pinus TION S10 products. MVC selects, for each pixel, the sylvestris forests), we only selected the most common maximum NDVI value among 10 daily images. Al- size (15 m radius), which was considered to be the most though alternative compositing methods have been representative for that type of forest. When there were developed (Hagolle et al. 2005), MVC is the only no significant differences in species richness between method currently implemented in the processing chain plots of different size (Quercus ilex, Pinus halepensis, and of the S10 collection. Time series of NDVI composites Pinus uncinata forests), we pooled these plots in the produced by this method have been used successfully to analysis. This process reduced the original 9126 IFN3 monitor surface dynamics at global and regional scales plots for Catalonia to 7567, most of them with a radius (Zhou et al. 2001, Lucht et al. 2002, Nemani et al. 2003). of 15 m. Finally, since large variation in richness among We used a data set of S10 products of the region of plots may produce no significant differences between study from 1999 to 2003, with a resolution of 3200 plot size classes, we minimized the effect of plot size on (seconds). NDVI values in S10 products are linearly the relationship between NDVI anomaly and species scaled from the observed jÀ0.1, 0.9j range to the integer richness by including it as an explicative variable in the range j0, 250j, and we kept this scale. We computed an statistical analysis, as detailed below.
  4. 4. September 2007 DROUGHT RESISTANCE AND PLANT RICHNESS 2273 FIG. 1. Map of the studied region (Catalonia, Spain) showing the pattern of the woody species richness obtained from field plots (left) and the 2003 summer NDVI (normalized difference vegetation index) anomaly (right). The darker the gray, the greater is the species richness and drought impact, respectively. Negative values of the NDVI anomaly correspond to lower values of NDVI in August 2003 than in the reference August. Values of NDVI are linearly scaled to the range j0, 250j. Data analysis from plots should show some degree of autocorrelation In order to ensure a reliable correspondence between in short distances (1 km). Alternatively, a random IFN3 information and pixel information, we applied an spatial distribution of richness values from sites 1 km additional filter to avoid plots located in heterogeneous apart would indicate that the richness estimated in small areas, so that reflectance from the forest canopy does sampling units is not representative of spatial patterns not dominate the corresponding pixel values. Thus, we on a larger scale. This assumption was supported by a defined a 1-km2 grid coincident with the pixels of the spatial autocorrelation analysis of the selected plots, imagery and selected those cells including inventory which indicated that the pattern of species richness does plots and satisfying two criteria: (1) land cover category not change across the neighbouring areas (Mantel test in having dense forest in more than 50% of the cell, and (2) which the main factors were the absolute differences tree canopy cover being more than 50% in the respective between species richness for each pair of inventory plots inventory plots. This second filter reduced the number of and the geographical Euclidean distance between them, r plots (and pixels) to 3504. After applying the filters, we ¼ 0.125, P , 0.001; for distances up to 15 km, r ¼ 0.075, crossed the selected inventory data and the NDVI values P , 0.001; for distances up to 60 km, r ¼ 0.036, P , obtained in the respective 1-km2 pixel surrounding the 0.001). plot location, following the nearest neighbor procedure We also tested this assumption by comparing plot of the Miramon GIS (Pons 2000). Since 1-km2 NDVI richness values to records of species richness on larger anomalies are obtained from averaged continuous forest spatial scales obtained from the BIOCAT data bank canopies, we assumed that they can be applied to smaller (available online).7 BIOCAT provides the list of plant pieces of forest, such as those sampled at the plot scale. species recorded by botanists at 10 3 10 km UTM grids We also assumed that the number of woody species at covering the whole Catalonia territory. We selected 33 10 plot level is a reliable estimate of woody species richness 3 10 km grids where forest cover was largely dominant in the surrounding forest areas. More specifically, we (more than 75% of the territory) and included at least 10 assumed that the spatial pattern of richness in small plots, from which we calculated the mean species sampling units 1 km apart follows the same pattern as adjacent 1-km2 units. If this assumption is true, richness 7
  5. 5. 2274 F. LLORET ET AL. Ecology, Vol. 88, No. 9 TABLE 1. GLM results for the different forest types considering NDVI anomaly (August 2003) as the dependent variable and woody species richness, Thorntwaite index, UTM x and y coordinates, and plot size as explicative variables. Pinus halepensis Quercus ilex Parameter Parameter Parameter F1, 457 P estimate F1, 556 P estimate Richness (R) 7.02 0.008 0.238 (0.009) 10.33 ,0.001 0.402 (0.105) Thorntwaite index (T ) 1.82 0.178 À0.118 (0.009) 14.61 ,0.001 0.115 (0.036) R3T 3.16 0.076 0.076 (0.011) 6.74 0.010 À0.007 (0.003) Coordinate x 0.08 0.776 0.79 0.374 Coordinate y 58.97 ,0.001 1.76 0.185 Plot size 0.01 0.909 0.27 0.603 Notes: Values in parentheses are SE. richness. We obtained a significant positive correlation (r may determine richness values and consequently may ¼ 0.765, F1,32 ¼ 43.74, P , 0.0001, slope ¼ 4.39) between indirectly influence the relationship between NDVI woody species richness at the plot scale and at the 10 3 10 anomaly and species richness we also included plot size km scale, supporting our assumption that richness values in the model as an additional explicative variable. obtained at plot level may be correlated to NDVI 1-km2 We also built similar GLMs for each type of forest, estimates at intermediate scales. including woody species richness, Thorntwaite index, We selected five types of forests that were represen- UTM x and y coordinates and plot size as explicative tative of the climatic conditions of the area of study. variables. Since all the plots in F. sylvatica and P. These forest types were defined by its respective sylvestris were of the same size (15 m radius), this dominant species (accounting for .50% of the plot variable was not included in the analysis of these two basal area): Pinus halepensis (Mediterranean, coniferous types of forests. forests), Quercus ilex (broadleaf, evergreen, Mediterra- nean), Pinus sylvestris (mesic and mountain coniferous RESULTS forests), Fagus sylvatica (moist, broadleaf, deciduous The relationships between NDVI anomaly and woody forests), and Pinus uncinata (high-mountain, coniferous species richness and between NDVI anomaly and forests) (Folch 1981, Gracia et al. 2004). As we Thorntwaite index were not the same in the different disregarded those plots located in other types of forests, types of forests, as shown by the significant interactions the total number of plots (and pixels) was 2087: 464 P. forest type 3 richness and forest type 3 Thorntwaite halepensis plots, 565 Q. ilex plots, 749 P. sylvestris plots, (F4,2063 ¼ 3.37, P , 0.005 and F4,2063 ¼ 2.56, P ¼ 0.037, 91 F. sylvatica plots, and 218 P. uncinata plots. respectively). NDVI anomaly was also significantly We built a general linear model (GLM), including the influenced by the UTM y coordinate (F4,2063 ¼ 74.42, NDVI anomaly (difference between August 2003 and P , 0.001). Therefore, we analyzed these relationships mean values for the same month of the period 1999– for each forest type separately. The effect of plot size 2002) as the dependent variable, and forest type, woody was not significant in the analysis of the model species richness, and Thorntwaite index as independent considering the five types of forests (F2,2065 ¼ 0.63, P ¼ factors. We included the interactions between these independent variables in the model. Since some sam- 0.533), nor was it in the analysis of each forest separately pling points may experience some degree of spatial (Table 1). autocorrelation, we included in the model two spatial NDVI values in P. halepensis forests significantly terms corresponding to UTM x and y coordinates. decreased in the 2003 summer (anomaly mean: À2.14, Including the x and y coordinates may not compensate SD ¼ 7.98, Student’s t test of significant differences from for small scale spatial biases. Given the large number of zero, t ¼ 5.77, P , 0.001). NDVI loss was lower in P. sampling points, small scale heterogeneity is unlikely to halepensis plots with higher woody species richness bias strongly our main results, but we tested the (Table 1, Fig. 2). Although NDVI loss was not autocorrelation pattern of NDVI anomalies by correlo- significantly influenced by the Thorntwaite index, a gram based on Mantel tests and we found that when marginally significant interaction between woody species considering larger distances, NDVI anomaly tends to richness and Thorntwaite index points to more vulner- diverge gradually without relevant leveling that could ability to the 2003 drought episode in moist localities indicate small scale heterogeneity at range lower than (within the distribution range of these forests) with less about 40 km. We also checked GLM analysis including species (Table 1, Fig. 1). NDVI anomaly was signifi- higher order spatial coordinate parameters, but they did cantly influenced by the UTM y coordinate, with less not improve the model, instead in several cases they drought impact in northern localities occupied by this resulted in collinearity problems. Finally, since plot size type of forest.
  6. 6. September 2007 DROUGHT RESISTANCE AND PLANT RICHNESS 2275 TABLE 1. Extended. Pinus sylvestris Fagus sylvatica Pinus uncinata Parameter Parameter Parameter F1, 743 P estimate F1,85 P estimate F1, 210 P estimate 0.17 0.680 À0.015 (0.073) 5.96 0.017 À0.187 (0.114) 0.28 0.595 0.502 (0.943) 11.15 ,0.001 0.119 (0.031) 2.71 0.104 À2.194 (0.899) 0.84 0.361 0.038 (0.042) 0.17 0.678 À0.0004 (0.0003) 1.38 0.243 0.014 (0.012) 0.06 0.813 À0.002 (0.007) 9.48 0.002 6.54 0.012 46.80 ,0.001 22.15 ,0.001 14.08 ,0.001 1.68 0.197 0.35 0.704 FIG. 2. Contour graphs of the 2003 summer NDVI (normalized difference vegetation index) anomaly (linearly standardized) in relation to woody species richness and Thorntwaite index (lower values are found under drier conditions) for the five types of forests. Darker surfaces indicate more negative anomalies, i.e., lower NDVI than in previous years, as shown by anomaly values drawn over the contour lines. Arrows show the direction of the drought impact, estimated by NDVI decrease in relation to the species richness and the climatic gradient. Dots indicate the situation of field-sampled plots in the richness–Thorntwaite index space. The graphs were obtained after fitting a second-order polynomical surface, following the GLM module of the Statistica 5.1. package (StatSoft, Tulsa, Oklahoma, USA).
  7. 7. 2276 F. LLORET ET AL. Ecology, Vol. 88, No. 9 In Q. ilex forests, NDVI in August 2003 was among coniferous forests, NDVI decreased in Mediter- significantly higher than in previous years (anomaly ranean (P. halepensis) and mesic (P. sylvestris) forests, mean ¼ 0.98, SD ¼ 6.61, t ¼ 3.53, P , 0.001). Although while it did not change significantly in mountain (P. both richness and the Thorntwaite index were positively uncinata) pine forests. The lack of drought effect on P. correlated to this increase (Table 1), a significant uncinata forests also concurs with the patches of positive interaction between them indicates that lower NDVI NDVI anomaly found by Lobo and Maisongrande values were observed in drier localities with lower (2005) in high-mountain areas, where water availability species richness and they also appear to be in moister was sufficient to compensate for the 2003 drought event. localities with a higher number of species, although This general concordance with studies based on land relatively few plots shared this profile (Table 1, Fig. 2). cover maps supports our approach based on scaling- Pinus sylvestris forests showed a significant decrease down parameters obtained for large spatial units, in in NDVI values (mean ¼ À3.80, SD ¼ 7.02, t ¼ 14.81, P which remote-sensing information is available, to stand , 0.001). This decrease was not related to woody species level information taken from field surveys. In fact, richness, but was lower in moister localities (Table 1, special care was taken to select representative forest Fig. 2). The NDVI anomaly was significantly influenced stands that were located in the middle of forested by the UTM x and y coordinates, indicating less drought patches of land. This is relevant because an important impact in southern and western inland localities. source of variability in NDVI signal comes from NDVI values of Fagus sylvatica forests were not herbaceous vegetation, which experiences important significantly lower in August 2003 (mean ¼ À0.44, SD ¼ phenological changes over the course of a summer 8.03, t ¼ À0.52, P ¼ 0.606), and consequently there was (Lobo and Maisongrande 2005). Furthermore, upscal- no significant correlation with the Thorntwaite index ing approaches have been used when field measures of a (Table 1). However, NDVI values decreased significant- given variable are unlikely to be obtained for the whole ly in plots with higher woody species richness (Table 1, territory (Williams and Rastetter 1999, Hernandez- Fig. 2). NDVI anomaly was significantly determined by Stefanoni and Ponce-Hernandez 2004). In our case, the the UTM x and y coordinates, with less drought impact assumption that species richness recorded at plot level is in northern and eastern localities. a reliable estimate of woody plant diversity on a larger Pinus uncinata forests did not show significantly scale is supported by correlation to records for larger different values of NDVI in August 2003 when pieces of land (10 3 10 km) obtained from plant compared to previous years (mean ¼ À0.22, SD ¼ 7.10, distribution data banks. Also, the observed autocorre- t ¼ À0.46, P ¼ 0.643) (Table 1), and this pattern lation in Mantel tests ensures that local heterogeneity remained present in the plots with higher species does not result in random patterns on a scale of 1 km. richness (Fig. 2). NDVI anomaly was significantly Finally, extensive forestry inventories are the most influenced by the UTM x coordinate, with less drought reliable source of information at a regional level on impact in eastern localities. species coexisting in the field. This empirical information avoids the problems of other estimates of regional DISCUSSION patterns of species richness based on merging individual The regional decrease in vegetation green cover species distribution maps, which do not take into (NDVI) in southern Europe (Gobron et al. 2005, Lobo account species interactions or local habitat variability and Maisongrande 2005) during the 2003 drought (Terradas et al. 2004). However, our study does not episode exhibited important differences between forest consider habitat heterogeneity within 1-km2 pixels. This types, although water deficit occurred across the whole may result in a source of error when estimates of species territory under study. Lobo and Maisongrande (2005), richness are scaled-up. after crossing the 2003 remote-sensing anomaly with The relationship between species richness and drought CORINE Land Cover 2000 cartography, reported resistance showed an important variability between the higher anomalies in herbaceous than in woody vegeta- different types of forests. Forest type is a complex tion, and in deciduous than in evergreen broadleaf category involving species composition and forest forests, but no analysis of coniferous forests was structure resulting from community assembly under undertaken. Our study excludes herbaceous communi- different climatic constrictions and human management. ties but also found more NDVI loss in F. sylvatica In fact, the five selected forests correspond to categories forests than in Q. ilex ones. Evergreen canopies are distributed in a complex gradient from drier, warmer expected to be more resistant to NDVI changes than conditions for open P. halepensis and close Q. ilex deciduous canopies, which should be able to respond forests to moister conditions for P. sylvestris and F. faster to changes in water availability by shedding leaves sylvatica ones, and to cold, mountain conditions for P. or losing other photosynthetic tissues. Unexpectedly, Q. uncinata ones. However the climatic gradient, synthe- ilex forest even showed higher NDVI values in the 2003 sized by the Thorntwaite index, failed in itself to explain summer than in previous years, perhaps due to the loss the pattern of NDVI anomaly variation, as reflected by of old leaves that are more likely to fall under drought the significant interaction between forest type and the conditions (Ogaya and Penuelas 2003). As expected, ˜ climatic index. The Thorntwaite index is a complex
  8. 8. September 2007 DROUGHT RESISTANCE AND PLANT RICHNESS 2277 environmental variable correlated with altitude, temper- mountain P. uncinata forests where the drought effect ature, and precipitation that did not account for the was not significant, species richness was not related to complete set of factors contributing to forest canopy NDVI variability. response to drought. Structural differences among Therefore, the proportion of drought-tolerant species forests types also emerge (Gracia et al. 2004), associated within the community would play an important role in with different management including selection logging in explaining NDVI anomaly. In drier P. halepensis forests, Q. ilex and F. sylvatica forests, shelterwood systems in higher diversity would involve the recruitment of species P. sylvestris forests and seed tree systems in P. uncinata that are drought tolerant. In contrast, in F. sylvatica forest, while logging is relatively rare in unproductive P. forests, occurring in moister zones, higher diversity halepensis forests. Overall, these types of forest can be would be caused by the recruitment of drought- considered as distinct systems where the relationship intolerant species, and the more diverse canopy would between species diversity and ecosystem function may lead to higher evapotranspiration rates. Quercus ilex perform differently. forests, intermediate between dry and somewhat moister Within each type of forest, patterns of drought impact zones, seem to display a more complex response, in relation to species richness may result from the somewhere between that of the P. halepensis and F. interaction with other variables, such as those related to syvatica forests. climate. As previously reported in herbaceous commu- The recovery of forest canopy after the drought nities (Tilman and Downing 1994), the hypothesis of episode is not considered in this study, but canopy species richness enhancing drought resistance was greenness is expected to have achieved average values supported in forests growing under Mediterranean after rainfall, as reported by field observations in conditions, such as P. halepensis forests. According to previous drought episodes (Penuelas et al. 2001, Lloret ˜ the selection mechanism, the greater the number of et al. 2004). Since an increase of extreme climate species, the greater the probability of finding species able episodes is expected in some regions, further exploration to cope with drying conditions. In this case, the negative of the role of diversity in forest resistance in the face of effect of the drought episode on species performance frequent droughts may be achieved by increasing the coincides with the historical selective pressures that have effort put into long-term monitoring and the surveying promoted the acquisition of drought tolerance or ´ of climate forest diebacks (Suarez et al. 2004). avoidance traits in Mediterranean species (Mooney Our exploration of the relationship between species 1989, Martı´ nez-Ferri et al. 2000). This hypothesis is richness and ecosystem resistance may have also been also supported by the trend of drier localities of P. influenced by the parameter used to estimate ecosystem halepensis forests with more species to exhibit lower drought-resistance. NDVI is a rough estimate of some NDVI anomalies than moister ones. In the more mesic global ecosystem properties, such as productivity, that is Q. ilex forest, a more complex pattern of interaction affected by multiple factors, including canopy structure between species richness and climate appears. As in P. and moisture state. To minimize these limitations, we halepensis forests, NDVI values were higher in richer used forest homogeneous pixels, and the NDVI value forests growing in drier conditions, but the opposite obtained in the drought period was compared to average trend was observed in moister localities, where more values of normal years. Therefore, NDVI loss also NDVI was observed in forests with low richness. Sala illustrates the relevant ecological consequences of and Tenhunen (1994) also found that water deficits drought on the physiological (i.e., loss of photosynthetic during dry summers were more severe in valley bottom activity), structural (i.e., crown partial dieback), func- localities of Q. ilex forests than in ridge top ones, where tional (i.e., complete or partial foliage drop and trees may have developed more conservative strategies reduction leaf longevity with consequences on nutrient of water use. cycling), and demographic (i.e., tree mortality) proper- Significant relationships between species richness and ties of the forest ecosystem, although it reflects poorly drought resistance tended to disappear in more humid the details of these responses in the understory P. sylvestris forests, where NDVI decrease became vegetation. significant in drier localities. In these types of forests, Species homogeneity may be partly responsible for the historical selective pressures may have not favoured unexplained effect of richness on drought impact: plots those species able to face drought, making the whole with a high number of species may be dominated by just community more sensitive to drier conditions. Within a few of them, while a few species on poor plots may be the moister F. sylvatica forests, the climatic gradient evenly represented in the canopy, greatly influencing would not be sufficiently contrasted to produce such a NDVI. Unfortunately, our forestry inventories did not pattern. The distribution of these forests is restricted in provide enough reliable information to calculate this the moister temperate localities of the region and they parameter because the estimates of the abundance of are a refuge for many Euro-Siberian species (Folch rare species within plots were not accurate enough. 1981). In these cases, species-rich communities made up Nevertheless, we managed to detect that the number of of many drought-sensitive species exhibited high nega- species significantly explained the variability of NDVI tive NDVI anomalies. Finally, as expected, in high anomalies, probably because plot richness acts as a
  9. 9. 2278 F. LLORET ET AL. Ecology, Vol. 88, No. 9 robust indicator of diversity patterns in this group of biophysical variables and Landsat ETMþdata. Remote plants on a larger scale, as supported by correlations Sensing of Environment 84:561–571. ´ ´ Direccion General de Conservacion de la Naturaleza. 2006. with the number of woody species recorded at a scale of Tercer Inventario Forestal Nacional 1997–2006, Barcelona. 10 3 10 km in the BIOCAT data bank (see footnote 6). Ministerio de Medio Ambiente, Madrid, Spain. In spite of the difficulties of scaling up the species ´ Folch, R. 1981. La vegetacio dels Paı¨ sos Catalans. Ketres, diversity patterns, our study provides a novel insight Barcelona, Spain. Gibelin, A. L., and M. Deque. 2003. Anthropogenic climate into large-scale empirical patterns in the relationship change over the Mediterranean region simulated by a global between the species richness and drought-resistance of variable resolution model. Climate Dynamics 20:327–339. temperate forests, in the face of increasing episodes of Gobron, N., B. Pinty, F. Melin, M. Taberner, M. M. rapid climate change. Thus, our study expands the Verstraete, A. Belward, T. Lavergne, and J. L. Widlowski. information provided by experiments in diversity 2005. The state of vegetation in Europe after following the 2003 drought. International Journal of Remote Sensing 26: manipulation on herbaceous communities across climat- 2013–2020. ic gradients that have shown a positive correlation ` ˜ Gracia, C., J. A. Burriel, J. J. Ibanez, T. Mata, and J. Vayreda. between species diversity and productivity (Hector et al. ` 2004. Inventari Ecologic i Forestal de Catalunya, Catalunya. 1999). ` Centre de Recerca Ecologica i Aplicacions Forestals, Bellaterra, Spain. Our study supports the idea that diversity–stability Hagolle, O., A. Lobo, P. Maisongrande, B. Duchemin, and A. relationships are not simple, as established by other De Pereira. 2005. Quality assessment and improvement of empirical and theoretical studies (Loreau 2000, Pfisterer SPOT/VEGETATION level temporally composited products and Schmid 2002). Overall, a shift in this relationship of remotely sensed imagery by combination of VEGETA- TION 1 and 2 images. Remote Sensing of Environment 94: seems to appear across the regional aridity gradient. 172–286. Forests from drier localities seem to have a pool of Hagolle, O., J. M. Nicolas, B. Fougnie, F. Cabot, and B. species that allow a selection mechanism to operate Henry. 2004. Absolute calibration of VEGETATION de- under extreme drought conditions. This results in an rived from an interband method based on the sun glint over improvement in resistance in accordance with species ocean. IEEE Transactions of Geoscience and Remote Sensing 42:1–20. richness. However, in moister localities, drought-resis- Hector, A., et al. 1999. 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J. van when the climatic episode is not intense enough, as in the der Linden, X. Dai, K. Maskell, and C. A. Johnson, editors. P. uncinata forests of the Pyrenean Mountains, no 2001. Climate change 2001: the scientific basis. Contribution relationship is found. Thus, the study points to the of Working Group I. Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge necessity of incorporating into the analysis of the University Press, Cambridge, UK. richness–resistance relationship an axis relating the Huston, M. A. 1997. Hidden treatments in ecological experi- causes of disturbance (i.e., in our case, water availabil- ments: re-evaluating the ecosystem function of biodiversity. ity) to current environmental gradients and to historical Oecologia 110:449–460. environmental constraints on the community. Li, S. G., J. Asanuma, A. Kotani, W. Eugster, G. Davaa, D. Oyunbaatar, and M. Sugita. 2005. Year-round measurements ACKNOWLEDGMENTS of net ecosystem CO2 flux over a montane larch forest in Mongolia. Journal of Geophysical Research: Atmospheres We thank J. Penuelas for the comments to an earlier version ˜ 110(D9): Article No. D09303. of the manuscript and J. J. Ibanez for his advice on the ˜ Lloret, F., H. Estevan, J. Vayreda, and J. Terradas. 2005. Fire inventory data. We also are grateful to P. Lambdon and an regenerative syndromes of forest woody species across fire anonymous reviewer for their suggestions. The study has been and climatic gradients. Oecologia 146:461–468. supported by SI02IR0010 project of the Institut d’Estudis Lloret, F., D. Siscart, and C. Dalmases. 2004. Canopy recovery Catalans (IEC), by REN 2003-07198 and CGL2006-01293/BOS after drought dieback in holm-oak Mediterranean forests of projects of the Spanish MCYT and by project HIDROLIM, of Catalonia (NE Spain). 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