Eduardo Gonza ´lez

Etienne Muller

Belinda Gallardo

Francisco Antonio Comı

Marı ´a Gonza ´lez-Sanchis

Factors controlling litter production in a large Mediterranean river floodplain forest

Although litter production is an essential floodplain forest function, the drivers and their relative importance remain largely unknown, especially in semi-arid rivers. The influence of forest structure, flooding regime, soil conditions, and litterfall chemistry (a total of 17 variables) on spatial variability of litter production within the Middle Ebro River floodplain forests (northeastern Spain) was examined by monitoring litterfall in 12 forest plots in 2007. Linear mixed effects (LME) models, using stem density (SD), river distance (RD) (or soil total organic C (TOC)), and soil total P (TP) as independent predictors, explained 51% of the variance in litter production, while an alternative LME model using SD and P use efficiency (P-NUE) explained 40%. In particular, litter increased with SD and TP and decreased with RD, P-NUE, and TOC. Based on these results, P limitation appears to be controlling litter production in a rather dry hydrological regime. We hypothesized that a deficient sediment input at the plot scale (especially in the outer floodplain), with flood quality (overbank flooding, ground-water seepage, ponding) being a greater determinant than quantity (flood duration, water table levels), might ultimately be responsible for the spatial variability observed in litter production.

Re ´sume ´: Bien que la production de litie `re soit une fonction essentielle des fore ˆts inondables, les facteurs qui la de ´terminent restent largement inconnus, spe ´cialement dans les rivie `res semi-arides. L'influence de la structure forestie `re, du re

´gime des inondations, de la nature du sol et de la chimie des litie `res (en tout 17 variables) sur la variabilite ´spatiale de la production de litie `re a e ´te ´e ´tudie ´e dans la plaine d'inondation du cours moyen de l'Ebre (nord-est de l'Espagne) par le suivi de la chute des litie `res dans 12 sites en 2007. Des mode `les line ´aires a `effets mixtes (LME) ont permis d'expliquer 51 % de la variance de la production de litie `re en utilisant la densite ´des arbres (SD), la distance a `la rivie `re (RD) (ou le C organique total (TOC)) et le P total (TP) comme pre ´dicteurs inde ´pendants. Les mode `les LME utilisant uniquement SD et l'efficience d'utilisation du P (P-NUE) expliquaient 40 % de cette variance. En particulier, les litie `res augmentaient avec SD et TP et diminuaient avec RD, P-NUE et TOC. Ces re ´sultats montrent que le manque de P semble contro ˆler la production des litie `res sous un re ´gime hydrologique pluto ˆt sec. Nous avons alors formule ´comme hypothe `se qu'un apport insuffisant de se ´diments a `l'e ´chelle des sites (en particulier dans les zones pe ´riphe ´riques de la plaine d'inondation) et la qualite des inondations (de ´bordement de rive, recharge de la nappe, zones d'accumulation d'eau) pluto ˆt que leur quantite ´(dure ´e des inondations, niveaux de la nappe) sont finalement responsables de la variabilite ´spatiale observe ´e dans la production de litie `res.

*By default, litterfall is expressed as g dry matterÁm -2 Áyear -1 . { Expressed as g ash free dry matterÁm -2 Áyear -1 . { Leaf litter only.

Introduction

Floodplain forests perform essential ecological functions such as flood buffering, water quality improvement, wildlife refuge, channel stabilization, and nutrient recycling. They are also great primary producers [START_REF] Brinson | Riverine forests. In: Forested wetlands. Ecosystems of the world 15[END_REF][START_REF] Naiman | Riparia. Ecology, conservation, and management of streamside communities[END_REF]. Overall, within the framework of regional geochemistry, with higher productivity in eutrophic than in oligotrophic floodplains [START_REF] Lockaby | N:P balance in wetland forests: Productivity across a biogeochemical continuum[END_REF][START_REF] Schilling | Relationships between productivity and nutrient circulation within two contrasting southeastern U.S. floodplain forests[END_REF], the productivity of riparian forests is determined by the flooding regime and soil fertility. Floods may increase productivity by improving soil fertility through the deposition of nutrient-laden sediments [START_REF] Noe | Carbon, nitrogen, and phosphorus accumulation in floodplains of Atlantic Coastal Plain Rivers[END_REF], the enhancement of decomposition [START_REF] Baker | Leaf litter decomposition and nutrient dynamics in four Southern forested floodplain communities[END_REF], and P availability [START_REF] Wright | Phosphorus availability in an artificially flooded southeastern floodplain forest soil[END_REF]. Simultaneously, floods can decrease productivity because of prolonged anoxic conditions that damage roots [START_REF] Odum | Perturbation theory and the subsidy-stress gradient[END_REF][START_REF] Megonigal | Aboveground production in Southeastern floodplain forests: A test of the subsidy-stress hypothesis[END_REF]. Within an entire growing season, the negative effects (stresses) of cumulative flood events can offset the positive (subsidies), depending on their timing, duration, hydrologic energy, and the biomass compartment analyzed (i.e., roots, wood, and litterfall) [START_REF] Megonigal | Aboveground production in Southeastern floodplain forests: A test of the subsidy-stress hypothesis[END_REF]).

Among the biomass compartments, litterfall represents a critical pathway for nutrient transfer in riparian ecosystems [START_REF] Wallace | Multiple trophic levels of a forest stream linked to terrestrial litter inputs[END_REF]). Notable differences in litter production within riparian forests can be found among geoclimatic regions. In floodplain forests, the highest litter productions C/nutrient ratios in litterfall. Thus, the nutrient use efficiency (NUE) of a given nutrient (total litterfall divided by total nutrient content in litterfall) [START_REF] Vitousek | Nutrient cycling and nutrient use efficiency[END_REF]) at the community level would provide information on possible nutrient deficiencies in the system and subsequent constraints to litter production. Nutrient resorption proficiency, the terminal concentration of nutrients in senesced leaves (sensu [START_REF] Killingbeck | Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency[END_REF], is another parameter that can respond to changing nutrient availabilities. Finally, nutrient ratio imbalances in plant tissues are indicative of differences in vegetation productivity [START_REF] Bedford | Patterns in nutrient availability and plant diversity of temperate North American wetlands[END_REF][START_REF] Lockaby | N:P balance in wetland forests: Productivity across a biogeochemical continuum[END_REF], and their examination complements the interpretation of NUEs and resorption proficiencies. For example, N/P balances in senesced leaves have been proposed as a tool to examine differences in vegetation productivity in forested wetlands [START_REF] Lockaby | N:P balance in wetland forests: Productivity across a biogeochemical continuum[END_REF]. Indeed, N and P are the most commonly studied nutrients in floodplain forests, as previous studies have shown their limitations in the environment [START_REF] Vitousek | Nitrogen limitation on land and in the sea: How can it occur?[END_REF][START_REF] Bedford | Patterns in nutrient availability and plant diversity of temperate North American wetlands[END_REF][START_REF] Lockaby | N:P balance in wetland forests: Productivity across a biogeochemical continuum[END_REF].

The main purpose of this study was to assess the factors driving local spatial variability in litter production of a Mediterranean floodplain forest. More specifically, we aimed (i) to test the hypothesis that, within a floodplain section characterized by an intermediate to dry flooding gradient, litter production is less in drier local flooding regimes than in wetter regimes, and (ii) to examine the capacity of litterfall chemistry parameters as alternative litter production predictors, compared with forest structure, soil fertility, and flooding parameters.

Materials and methods

Study area

The study was conducted in the Alfranca Reserve (41836'N, 0846'W), an 8 km segment of forest along the Middle Ebro River (NE Spain), the second largest river in the semi-arid Mediterranean region. At the Zaragoza gauging station (41839'N, 0852'W), which is 12 km upstream from the study area, the Ebro is a 9th order river (A. Ollero, personal communication (2009)) with an average monthly discharge of 230 m 3 Ás -1 . The flow regime is characterized by a severe summer drought and high flow periods during winter and spring, coinciding with higher precipitation and snow-melt in the bordering mountain ranges. Nutrient loads in the Middle Ebro River are rather high as a consequence of widespread agricultural, urban, and industrial activities in the floodplain [START_REF] Torrecilla | Nutrient sources and dynamics in a Mediterranean fluvial regime (Ebro River, NE Spain) and their implications for water management[END_REF]. Total annual precipitation recorded at the Alfranca weather station is 374 mm (Regional Weather Agency). Flow regulation and flood protection, including the construction of dams, dikes, and diversions, have been especially intense since the 1950s and have severely disrupted the natural hydrologic and geomorphologic dynamics of the studied stretch during the last few decades [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: Assessment and management[END_REF]. Land reclamation for agriculture and human settlements has reduced the surface occupied by natural forest to ~4.5% of the Middle Ebro floodplain [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: Assessment and management[END_REF]. Today, the surviving riverine tree community is dominated by several phreatophyte species, namely European white poplar (Populus alba L.), European black poplar (Populus nigra L.), white willow (Salix alba L.), and saltce-are generally found in the equatorial zone (1072 gÁm -2 Áyear -1 ) and progressively decrease to the poles (98 gÁm -2 Áyear -1 ) [START_REF] Naiman | Riparia. Ecology, conservation, and management of streamside communities[END_REF]). Within a particular major world biome, various studies collectively support that flooding regime and soil fertility also control litter production [START_REF] Naiman | Riparia. Ecology, conservation, and management of streamside communities[END_REF], although their interaction is not well understood. In fact, the majority of litterfall productivity comparisons under different flooding regimes have been developed in wetland forests on the ''wet side'' of the subsidy-stress curve, especially of the Southeastern US region (see review by [START_REF] Clawson | Changes in production and nutrient cycling across a wetness gradient within a floodplain forest[END_REF], whereas the ''dry side'' of the curve has received much less attention (e.g., [START_REF] Megonigal | Aboveground production in Southeastern floodplain forests: A test of the subsidy-stress hypothesis[END_REF][START_REF] Burke | Aboveground production and nutrient circulation along a flooding gradient in a South Carolina Coastal Plain forest[END_REF]. In this sense, the Mediterranean region offers an excellent framework to study floodplain forest response under rather dry hydrologic regimes, where the anoxic conditions typical of wetter areas are less likely to constrain litter production compared with nutrient and moisture limitations that are subsidized by flooding. Despite this potential, the factors affecting litterfall have never been assessed in the Mediterranean region. Indeed, the few existing studies of litterfall in Mediterranean riparian settings estimated litter production with the purpose of quantifying the total input of allochthonous material to streams, instead of seeking the mechanisms controlling litter production itself (e.g., [START_REF] King | Particulate organic matter in a mountain stream in the south-western Cape, South Africa[END_REF][START_REF] Maamri | Allochthonous input of coarse particulate organic matter to a Moroccan mountain stream[END_REF].

In addition to flooding regime and soil fertility, litter production depends on the structural characteristics of riparian forests. On one hand, forest composition must be considered, with more diverse forests usually exhibiting higher productivity [START_REF] Pozo | Inputs of particulate organic matter to streams with different riparian vegetation[END_REF]) and some species being more effective litter producers than others [START_REF] Meier | Litterfall in the hardwood forest of a minor alluvial-floodplain[END_REF]. On the other hand, part of the variability in litter production can be attributed to the successional stage of the forest [START_REF] Brinson | Riverine forests. In: Forested wetlands. Ecosystems of the world 15[END_REF][START_REF] O'keefe | The influence of forest structure on riparian litterfall in a Pacific Coastal rain forest[END_REF]. Therefore, traditional forest structural parameters such as basal area (BA), canopy and stem volume have been proven to be significant predictors of litter production as well (O'Keefe and [START_REF] O'keefe | The influence of forest structure on riparian litterfall in a Pacific Coastal rain forest[END_REF]. Although the importance of forest structural characteristics in determining litter production has been widely recognized, the extensive series of field measurements necessary to obtain accurate estimations of litter production is a serious drawback, and most studies addressing the influence of flooding regime and soil conditions on litterfall have deliberately minimized structural diversity in their sampling design. Likewise, studies examining the role of forest structural parameters as litter predictors do not usually focus on flooding gradients. Thus, the relative importance of flooding, soil conditions, and forest structural factors on litter production still remains largely unstudied.

Nutrient availability as reflected in litterfall chemistry is another possible factor influencing litter production in floodplain forests. Although litter nutrient content and nutrient circulation in floodplain forests are generally included in litterfall studies (see review [START_REF] Troxler Gann | Ecosystem structure, nutrient dynamics, and hydrologic relationships in tree islands of the southern Everglades, Florida, USA[END_REF], their potential as litter production predictors has received less attention, especially in tree communities. Forest stands may be classified as efficient or inefficient in their use of nutrients, the former suffering from higher nutrient limitations than the latter [START_REF] Vitousek | Nutrient cycling and nutrient use efficiency[END_REF][START_REF] Vitousek | Litterfall, nutrient cycling, and nutrient limitation in tropical forests[END_REF]. According to [START_REF] Vitousek | Nutrient cycling and nutrient use efficiency[END_REF][START_REF] Vitousek | Litterfall, nutrient cycling, and nutrient limitation in tropical forests[END_REF], an efficient community could fix a higher amount of C per unit of nutrient uptake, eventually leading to higher dar (Tamarix gallica L., Tamarix africana Poir., and Tamarix canariensis Willd.). Late-seral hardwood species such as field elm (Ulmus minor auct. non P. Mill.) and narrow leaf ash (Fraxinus angustifolia Vahl) are commonly found and, occasionally, attain tree size [START_REF] Gonza ´lez | Recent changes in the riparian forest of a large regulated Mediterranean river: implications for management[END_REF]. All tree species present in the floodplain forest are deciduous.

Plot selection

A total of 12 plots covering a variety of forest patches differing in tree species composition, structure, and flooding regime were established within the Alfranca Reserve (Fig. 1). The plots were placed within the floodplain according to the following criteria: (i) plots distributed according to the local proportion of existing geomorphic landforms (1 plot on a gravel bar, 5 plots on the natural levee of a permanent or intermittent channel, 6 plots on floodplain terrace), (ii) no more than one plot in each forest patch to avoid pseudoreplication bias, (iii) variable plot dimensions to geometrically adapt to each distinctive riparian forest patch but always with a size of 500 m 2 and rectangular-shaped to fit within the usually elongated forest patches, (iv) buffer dis-tance of at least 5 m from the plot to the forest edge, and (v) all plots in mature forests. The last condition was set to deliberately avoid sampling young successional forests, since litter traps are not designed to capture materials growing close to the ground, common in early-seral stages [START_REF] Naiman | Riparia. Ecology, conservation, and management of streamside communities[END_REF]. The plot Universal Transverse Mercator coordinates were recorded using a differential global positioning system (DGPS) Topcon1 with 3 cm of vertical accuracy.

Litterfall collection and processing

Litterfall was collected monthly from January 2007 to December 2007 after randomly setting up 10 litterfall traps in each plot. Each trap consisted of a 0.25 m 2 square metallic frame elevated 1 m above the forest floor, hanging from nearby trees by ropes. A synthetic 75 cm deep bag with a 1 mm mesh was attached to the frame, allowing rapid drainage of rainwater to reduce weight loss by leaching. Two small stones were placed in each bag to weight down the trapped material and keep the bag extended. Traps were emptied monthly, and the samples were brought to the laboratory to be sorted into five categories: woody (bark and samples of the remaining material through a 63 mm screen. Total organic C (TOC) (percent) was measured with a LECO SC 144 DR elemental analyzer after combusting a subsample of soil and soil ashes (previously burned at 450 8C for 3 h). Total N (TN) (percent) was measured by combustion using a varioMAX N/CN elemental analyzer. Total P (TP) (percent) was analyzed using an inductively coupled plasma emission spectrometer (ICP) after exposing soil subsamples to a HNO 3 -HCl solution and digesting them in a microwave digester MWS-3 Berghof.

Litterfall chemistry

Litter C and N concentrations (percent) were measured by combusting subsamples of each litter fraction collected in litterfall traps with a varioMAX N/CN elemental analyzer. Litter P concentration (percent) was determined by ashing the subsamples at 450 8C for 3 h, followed by digestion in a 3.5 molÁL -1 double-acid solution (HNO 3 -HCl, 1:3) and analyzed spectrophotometrically by the standard vanadate-molybdate method [START_REF] Allen | Chemical analysis[END_REF]. Total C, N, and P in litterfall were computed by multiplying the C, N, and P concentrations of each litter fraction by their respective weights and adding the subtotals, and then used to calculate C/N, C/ P, and N/P atomic ratios (molÁmol -1 ). Nitrogen use efficiency (N-NUE, gÁg -1 ) and P use efficiency (P-NUE, gÁg -1 ) were calculated as total litterfall divided by TN and TP in litterfall, respectively [START_REF] Vitousek | Nutrient cycling and nutrient use efficiency[END_REF]. Nitrogen and P resorption proficiency (%) were calculated by averaging the respective nutrient terminal concentration in fallen leaves of the different species composing each plot [START_REF] Killingbeck | Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency[END_REF].

Statistical analyses

The independent capacity of each variable (forest structure, flooding regime, soil condition, and litterfall chemistry) as a litterfall predictor was preliminarily evaluated by means of Spearman's rank correlation coefficient. To explore the relative importance of the variables on litter production, a series of linear mixed effects models (LME) [START_REF] Pinheiro | Mixed-effects models in S and S-Plus[END_REF] with litterfall as the response variable and different combinations of litterfall predictors were performed. LME models were selected because they allow introducing fixed and random effects, thus accounting for pseudoreplication. The models were run using (1) forest structure, (2) flooding regime, (3) soil conditions, and (4) litterfall chemistry variables alone and all their possible combinations (i.e., 1 + 2,1 + 3,1 + 4,2 + 3,2 + 4,3 + 4,1 + 2 + 3,1 + 2 + 4,2 + 3 + 4,1 + 2 + 3 + 4 = full model) as fixed effects. To correct the regression models for spatial pseudoreplication, the variable ''study plot'' was introduced as a random effect. As a high level of multi-collinearity was expected among the litterfall predictors, Spearman's rank correlation coefficients were used as preselection of predictors, selecting those having r s < 0.7. In this sense, when a pair of predictors had r s 0.7, the one registering a lower correlation with the response variable (litterfall) was removed from the analysis. After that, a stepwise backward selection of predictors was performed to retain only the most significant ones (p < 0.05) in explaining the response of litterfall, testing each step with a likelihood ratio-test [START_REF] Crawley | Statistical computing. An introduction to data analysis using S-Plus[END_REF]). Pearson's product-moment correlation between the observed and pre-twigs 1 cm diameter), buds and scales, reproductive (flowers, fruits, and seeds), leaves (by species), and unidentifiable debris. Large woody material (bark and twigs >1 cm diameter) and animal remains (excrement, dead bodies, molts, feathers) were removed from the samples. Samples were oven dried at 60 8C for at least 72 h until a constant mass was attained, and then weighed. Subsamples of each fraction were ground to a homogeneous powder using an IKA A10 mill and then stored in a dark desiccator until chemical analyses were performed. Vandalism, tree falls, and flooding caused the loss of 11% of the samples. Damaged bags were replaced during weekly patrols to maintain 10 traps per plot each month. Missing data were estimated using averaged daily litterfall rates per month and plot, calculated with the available data.

Forest structure

Diameter and species of every stem in a plot was recorded of individuals whose height was 1.3 m and diameter at breast height (dbh, 1.30 m) was 2.5 cm. Exceptions had to be made with saltcedars because of their shrubby architecture (diameter was measured at 0.30 m, d30 2.5 cm). BA (m 2 Áha -1 ) and stem density (SD) (stemsÁha -1 ) of live stems within each plot were then calculated. The contribution to litter production of the smaller stems was considered negligible and, therefore, they were not computed for BA and SD calculations. Tree species richness (RICH) was the number of species found in the plot. As determination of saltcedar species is difficult because of morphological similarities and frequent hybridization, the three existing species in the study area were considered as a group for all calculations.

Flooding regime

In 2006, a 6 m depth piezometer was installed in each study plot using a rotary drill rig. The water table level in each piezometer was measured manually on a weekly basis during 1 year in 2007 and was averaged to calculate the annual depth to ground water (DGW) at each plot. During floods, some of the piezometers were inaccessible. Then, the height of the water column was estimated as the difference between the top of the piezometer and the river water at an accessible position close to the plot, using the DGPS. For each plot, the flood duration (FD) was calculated as the number of weeks with the water table above substrate level. River distance (RD) was computed as the shortest distance from each plot to the unprotected main channel (i.e., river segment with no dikes) at low flow using ArcGis 9.2 (Fig. 1).

Soil conditions

Three topsoil (0-10 cm) samples were randomly collected from each plot in late summer 2006 using an undisturbed soil sampler (5 cm diameter steel tube, P.1.31 Eijkelkamp) after the litter layer had been manually removed. Samples were passed through a 2 mm sieve after air drying to remove rock and larger organic matter fragments. Samples were then treated with 10% hydrogen peroxide to eliminate the organic matter and a polyphosphate solution to disperse the soil particles. The fine (i.e., FINE silt plus clay, percent) fraction was calculated gravimetrically by sieving sub-dicted values was used to assess the goodness of fit of the final models. The LME models were carried out using the functions available in the package ''nlme'' [START_REF] Pinheiro | nlme: linear and nonlinear mixed effects models[END_REF]), R 2.8.1 software (www.R-project.org). Once the main predictors were identified, the sum of independent and shared variance in litterfall explained by each significant predictor (i.e., the relative contribution) in each model was assessed through hierarchical partitioning [START_REF] Chevan | Hierarchical partitioning[END_REF]. To that end, we used the functions available in the package ''hier.part'' [START_REF] Walsh | hier.part: Hierarchical Partitioning. R package version 1[END_REF], R 2.8.1 software.

Results

Litter production

Mean litter production recorded in 2007 over the 12 study plots was 563 ± 55 g of dry matterÁm -2 Áyear -1 (mean ± 1 SE). The range of variation was rather wide, with a factor of 4.6 between the minimum (199) and maximum (916 g of dry matterÁm -2 Áyear -1 ) (Table 1).

Forest structure

BA and SD notably differed along the studied plots (Fig. 2). The contribution of each species to BA and SD was also very variable, but 90% of the total BA and 80% of the total SD were generally provided by only three species (P. nigra, Tamarix spp., and P. alba). Tree species richness was even more uneven; ranging from monospecific stands to plots with up to six species, although the majority of plots were characterized by an overstory dominated by Populus spp. with a subcanopy of Tamarix spp. and (or) Ulmus minor.

Flooding regime

No plot was continuously flooded or permanently dry in 2007 (Fig. 1). All of them were inundated only during the episodic late-winter and spring flood events typical of the Middle Ebro flooding regime. However, differences in flood duration and mean depth to ground water were observed between plots. The plots with greater RD were usually the drier (fewer number of weeks flooded), but there were a few exceptions to this trend (e.g., plots 11 and 12). Although not specifically measured in this study, the same flood event could cause either overbank flood or ground-water seepage (and occasionally water ponding) depending on the position of the plot in the floodplain.

Soil conditions

Soils of the Ebro River floodplain were dominated by fine particles in 10 of the 12 plots (Table 2). Although all soils were mineral (TOC <5%), a TOC gradient was observed along the plots. Soil TOC, and also soil TN, corresponded well with the geomorphic landform, with the floodplain terrace soils being more organic and N-rich than the levees and point bar. Soil TP was about three times lower (by mass) than soil TN.

Litterfall chemistry

Litter C/N, C/P, and N/P atomic ratios averaged 53, 1382, and 26 molÁmol -1 , respectively, but varied widely between plots (Table 3), with CV C/N = 16%, CV C/P = 32%, and CV N/P = 20%. N-NUE and P-NUE averaged 99 and 1184 gÁg -1 and also substantially differed along the floodplain (CV N-NUE = 15% and CV P-NUE = 32%). Likewise, proficiency was less variable for N (CV N = 15%) than for P (CV P = 27%) with respective means of N = 0.9% and P = 0.07%.

Predicting litter production

In a first stage, the 17 parameters were tested individually as litterfall predictors using Spearman correlation tests (Fig. 3). A total of 13 were significantly correlated with litter production. However, the models were generally weak, as they could only predict less than one third of the variance in litter production. In particular, two of the three structural parameters of the tree community (BA and SD) were significantly correlated with litter production. Litter increased with higher BAs and SDs, whereas species richness did not have a significant influence on litter production. Likewise, two of the three flooding regime surrogates exhibited a significant relationship with litter production. In particular, litter was inversely related to RD and positively related to depth to ground water. Concerning soil conditions, the response of litter production was significant for two of the four parameters. It increased with higher TP concentrations, but decreased with more organic soils. Lastly, litter production responded significantly to the seven litterfall chemistry parameters. It decreased in tree communities that were more efficient (with higher NUEs) in using nutrients and proficient (with lower %N and %P in senesced leaves) in their resorption, but increased with decreasing litter C/N and C/P. Litter also decreased at low litter P concentrations relative to N, as shown by the inverse relationship between litter N/P and litter production.

In a second stage, correlations between litterfall predictors were tested (Table 4). A rather high level of multi-collinearity was found. Soil TOC and soil TN varied in concordance with the flooding regime, whereas soil TP and soil fine fraction (FINE) tended to be significantly correlated with the litterfall chemistry variables and not with any of the flooding regime parameters. The forest structural parameters were neither correlated between them nor with the flooding, soil, or litter chemistry variables. Lastly, high multi-collinearity was observed within the litterfall chemistry variables.

In a third stage, attempts were made to find the best LME models for predicting litter production. The three best LME models for predicting litter production using a combination of forest structure, flooding regime, soil conditions, and litterfall chemistry variables are summarized in Table 5. The remaining seven LME models were discarded, as the Pearson's correlation coefficient (R) was notably smaller (data not shown). The LME model performed with the four groups of variables (combining the 17 variables = full model) finally selected only 3 (RD, soil TP, and tree SD) and explained 51% of the variance in litter production. In particular, it predicted higher litter production with decreasing RD, which accounted for the highest contribution to the model, and with increasing TP and SD; whereas it excluded all the litterfall chemistry variables. A second alternative LME model, performed with only the forest structural and soil variables (7 variables) also explained 51% of the variance in litter production, predicting higher production with increasing TP (highest contributor), increasing SD, and decreasing TOC. A third alternative LME model, performed with forest structure and litterfall chemistry variables only (10 variables), explained 40% of the variability in litter production with only 2 variables, namely SD and P-NUE (highest contributor). As expected, the model predicted a positive litter production response to increasing SD and decreasing P-NUE. No parameter on litterfall N concentration was included in this last model.

Discussion

Drier hydroperiods may limit litter production by a deficient input of nutrients

Within the framework of an intermediate to dry flooding gradient, the examination of the interaction between flooding regime, soil conditions, and litterfall chemistry variables with litter production suggests the existence of nutrient con-straints to litter production in the study area. The more efficiently (i.e., higher NUE values) and proficiently (i.e., lower nutrient concentration values in litter leaves) N and P circulate, with increasing C/N and C/P ratios, the less litterfall is produced. According to the weak, but significant, positive correlation between depth to ground water (DGW) and litter production, it would seem that, in this case, the stresses of floods slightly exceed the subsidies. However, DGW and flood duration (FD) are not included in any of the LME models explaining the variability in litter production. To understand this contradiction, we hypothesize that the detected nutrient constraints to litter production are more influenced by a relatively deficient input of allochthonous nutrients to forest soils, rather than by the changing soil fertility and physiological responses following water table fluctuations. We base our suggestion on the high predictive capacity of the full LME model, with RD contributing up to 39% of the total explained variance in litterfall (following an inverse relationship), while FD and DGW were excluded. RD is a determinant for the input of allochthonous nutrients to forest stands through sediment deposition during overbank floods. The deposition of sediment-borne nutrients across the floodplain is enhanced by the physical interaction with plant communities and other elements of the floodplain, as the river water flows across the floodplain and de-creases the carrying capacity of sediments with slower flow velocities [START_REF] Vought | Nutrient retention in riparian ecotones[END_REF][START_REF] Reddy | Phosphorus retention in streams and wetlands: A review[END_REF][START_REF] Venterink | Importance of sediment deposition and denitrification for nutrient retention in floodplain wetlands[END_REF]). Thus, less deposition during overbank flood events is expected with increasing RD [START_REF] Kleiss | Sediment retention in a bottomland hardwood wetland in eastern Arkansas[END_REF][START_REF] Walling | Investigating spatial patterns of overbank sedimentation on river floodplains[END_REF]. Meanwhile, the fact that the type of inundation (overbank flooding, ground-water seepage, or ponding) is not considered in the FD and DGW parameters limits a clear relationship between these variables and the input of allochthonous nutrients, which hence, according to our hypothesis, would reduce their capacity of prediction. In other words, we interpret that the quality (overbank flooding, ground-water seepage, or ponding, in turn determining sediment-borne nutrient deposition) rather than the quantity (flood duration and water table levels, in turn determining the changing soil chemistry) of the flooding regime could be the main driver of litter production in the study area. Thus, drier flooding regimes would be actually more detrimental to litter production than wetter regimes in the ''dry side'' of the subsidy-stress curve, because of a deficient input of nutrients with RD. The future use of tools to accurately predict the type of inundation at the plot level, such as flow models [START_REF] Beffa | Two-Dimensional flood plain flow -Part I: Model description[END_REF], and the monitoring of sediment deposition rates and sediment quality [START_REF] Noe | Carbon, nitrogen, and phosphorus accumulation in floodplains of Atlantic Coastal Plain Rivers[END_REF][START_REF] Venterink | Importance of sediment deposition and denitrification for nutrient retention in floodplain wetlands[END_REF]) seem necessary to complement the simple hydrological surrogates (e.g., RD, FD, and DGW), and test our hypothesis. At the very least, the high contribution of soil TP in the two best LME models indicates the importance of the flooding regime on litter production, as soil TP integrates the historical hydrological conditions of the site [START_REF] Mitsch | Estimating primary productivity of forested wetland communities in different hydrologic landscapes[END_REF], which would have influenced the phenotypic response of trees in terms of litter production under different soil fertilities.

P more limiting than N Generally, productivity in terrestrial forests is primarily limited by N and secondarily by P [START_REF] Vitousek | Nitrogen limitation on land and in the sea: How can it occur?[END_REF]. However, in forested wetlands, P limitation or N and P co-limitation is more common than N limitation [START_REF] Bedford | Patterns in nutrient availability and plant diversity of temperate North American wetlands[END_REF]). In the Ebro River, the inverse relation between N/P ratio and litter production, the presence of TP in the first two LME models, and P-NUE in the third one might indicate higher P deficiencies in the ecosystem relative to N. Other authors also found a stronger limitation in P than in N when examining the nutrient cycling in forested wetlands. For instance, [START_REF] Schilling | Relationships between productivity and nutrient circulation within two contrasting southeastern U.S. floodplain forests[END_REF] reported higher NUE and resorption proficiency in P than in N in an oligotrophic river in Georgia (USA) but attributed them to the deficient P inputs because of the low sediment loads characterizing the river waters. In the case of the Ebro River, a stronger P than N limitation to litter production is consistent with our suggestion of deficient nutrient input to forest soils controlled by RD and subsequent quality of the flood events. In general, more than one half of the TP flowing in river waters is transported as particulate P, whereas less than 10%-20% of the TN travels bound to particles [START_REF] Vought | Nutrient retention in riparian ecotones[END_REF], with direct uptake from ground water and mineralization from soil organic matter [START_REF] Schade | Sources of nitrogen to the riparian zone of a desert stream: Implications for riparian vegetation and nitrogen retention[END_REF] and, to a lesser extent, atmospheric deposition and N 2 fixation (Olde [START_REF] Venterink | Importance of sediment deposition and denitrification for nutrient retention in floodplain wetlands[END_REF] as alternative sources of N for floodplains forests. Therefore, an eventual deficit of nutrient deposition by sedimentation would be more detrimental for P plant availability than for N, ultimately affecting litter production. Consistently with these ideas, the significant contribution of TOC to the second-best LME model, although low, might be due to the capacity of soil organic matter to sequester P [START_REF] Reddy | Phosphorus retention in streams and wetlands: A review[END_REF], thus making it less available to plants, leading, in turn, to lower productivity.

Table 4.

Spearman's correlation coefficients between the parameters describing the tree community structure, flooding regime, soil conditions, and litterfall chemistry across the 12 study plots. { RD, river distance; TP, total P in soil; SD, stem density; TOC, total organic C in soil; P-NUE, P use efficiency.

{

The relative contributions (%) of each explanatory variable to the total explained variance in litter production were calculated by means of hierarchical partitioning. with one parameter (SD) included in the three best LME models, and significant relative contributions of *30%. It is not surprising that a greater number of trees (measured as SD or as BA) leads to higher litter production with an upper limit (e.g., plot 12 in our study area), as shown by [START_REF] Meier | Litterfall in the hardwood forest of a minor alluvial-floodplain[END_REF], and to decreasing litter production with higher densities (plots 11 and 3) and BAs (plot 7), probably because of competence for light, space, and other resources. However, although BA alone explained more litter variability than SD (Fig. 3), the presence of the latter variable over the former one in all the models might reflect that the flooding and soil predictors shared less explained variance in litter production with SD than with BA. While the local size of the trees (partially registered in BA but not in SD) may eventually depend on the ordinary provision of water and nutrients by floods, their number is more determined by extraordinary events driving historical recruitment and tree scouring. Thus, SD might be integrating relatively more unique information than BA for the prediction of litter production, in turn being a consistently strong predictor in the LME models. Nevertheless, it is likely that the use of additional structural forest parameters, such as stem and canopy volume and dieback, tree height, or complexity indexes, could help to clarify part of the unexplained percentage of variance in the proposed models.

Litterfall chemistry as a complementary litter production predictor

The results reported here also highlight the potential of litterfall chemistry parameters as complementary litter production predictors. On the one hand, alone, they correlated well with litter production. On the other hand, the LME model including forest structure and litterfall chemistry variables predicted amounts of variance similar to the two better adjusted LME models, with P-NUE integrating the predicting capacity of flooding regime and soil surrogates (i.e., RD, soil TP and TOC). This suggests the existence of an intimate relationship between nutrient use by plants and hydrologic and nutrient fluxes that deserves further study. In this perspective, LME models are proven to be an effective statistical tool for optimum selection of the best litter production predictors at a lower data collection cost and to better evaluate the relative role of each potential predicting factor.

Conclusions

Within the framework of a diverse tree community subjected to an intermediate to dry flooding regime, nutrient circulation (represented by flooding regime and soil variables, or alternatively, by litterfall chemistry surrogates) seems to drive the spatial variation of an overall medium to high litter production in a Mediterranean riverine forest, resulting in occasional nutrient (especially P) limitation to litter production in the outer floodplain. In the case of the Middle Ebro, river distance is the most influencing component of the flooding regime on litter production; whereas the effects of flood duration and depth to ground water are more unclear. Overall, it seems that the lack of subsidies characterizing drier hydroperiods is more detrimental to litter production than the possible stresses caused by prolonged inundations. It would be interesting to test in further

Forest structure determining litter production at both plot and floodplain scales

The observed nutrient constraints to litter production at plot level contrast with the medium to high total recorded litterfall at the floodplain level, if compared with other forested ecosystems in Mediterranean riparian settings (Table 6). In addition, the mean of 563 gÁm -2 Áyear -1 found in the Ebro floodplain is slightly higher than the global means reported by [START_REF] Bray | Litter production in forests of the world[END_REF] (550 gÁm -2 Áyear -1 ) and [START_REF] Naiman | Riparia. Ecology, conservation, and management of streamside communities[END_REF] (498 gÁm -2 Áyear -1 ) for riparian forests of the warm temperate zone. Although there is no clear relationship between nutrient concentration in water of wetlands and nutrient availability for plants [START_REF] Bedford | Patterns in nutrient availability and plant diversity of temperate North American wetlands[END_REF], the high nutrient loads of the surface and ground water of the Ebro River [START_REF] Torrecilla | Nutrient sources and dynamics in a Mediterranean fluvial regime (Ebro River, NE Spain) and their implications for water management[END_REF]) could be one of the factors underlying the rather high productivity at the floodplain level. This would be consistent with the rather low averaged NUEs registered in the Ebro, if compared with the mean values reported by Troxler [START_REF] Troxler Gann | Ecosystem structure, nutrient dynamics, and hydrologic relationships in tree islands of the southern Everglades, Florida, USA[END_REF] for seven studies in temperate floodplain forests (N-NUE = 111, P-NUE = 1464); with the overall intermediate resorption proficiencies (N 0.7% and 1.0% and P 0.05% and 0.08% sensu [START_REF] Killingbeck | Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency[END_REF]; and with the mean N/P ratio of 26.0, close to the optimum atomic ratio of 26.5 proposed by [START_REF] Lockaby | N:P balance in wetland forests: Productivity across a biogeochemical continuum[END_REF] for a balanced element supply for forested wetlands productivity. However, possible high nutrient availabilities for plants in the Ebro would contrast with the observed high litter C/N, C/P ratios (well above the respective C/N and C/P ratios of 16 and 200, necessary for complete litter decay according to [START_REF] Brinson | Decomposition and nutrient exchange of litter in an alluvial swamp forest[END_REF] and with the low soil TP and TN, if compared with the values reported by [START_REF] Bedford | Patterns in nutrient availability and plant diversity of temperate North American wetlands[END_REF] for mineral soils of temperate North American wetlands (P ranging from 0.01% to 0.70% and N from 0.09% to 1.50%).

An alternative explanation to the high forest productivity could rely on the structural characteristics of the tree community in the Ebro River, with notably higher BAs and stem densities than the average of 94 temperate riparian forests worldwide [START_REF] Brinson | Riverine forests. In: Forested wetlands. Ecosystems of the world 15[END_REF]), namely 21% and 194% higher, respectively. Nevertheless, the comparisons must be made with caution. Firstly, the woody fraction is not always computed in litterfall studies, and then global means can underestimate the actual litter production of a region. Secondly, the inter-annual variability was not registered in this study with only 1 year of litterfall monitoring, so the effects of some factors, such as annual rainfall, on litter production could not be assessed. For example, [START_REF] Greenway | Litter accession and accumulation in a Melaleuca quinquenervia (Cav.) S.T. Blake Wetland in South-eastern Queensland[END_REF] reported a decrease of about 10% of total litterfall in a drought year compared with the precedent wet year in a wetland of southeastern Queensland (Australia). In our study area, the cumulative precipitation in 2007 was 383 mmÁday -1 , only 2.4% higher than the mean value supplied by the Regional Weather Agency. Thirdly, the extremely high SD in the Ebro River forests relative to other studies might also be due to the frequent exclusion of saplings in SD calculations and the prevalence of shrubby saltcedars in the study area [START_REF] Shafroth | Riparian vegetation response to altered disturbance and stress regimes[END_REF].

In any case, the importance of forest structure parameters in the prediction of variability in litter production within the floodplain was notable with regard to the rest of the factors, studies whether the same tendency occurs within the root and wood compartments, as trees may allocate resources to different compartments depending on the flooding regime [START_REF] Megonigal | Aboveground production in Southeastern floodplain forests: A test of the subsidy-stress hypothesis[END_REF][START_REF] Clawson | Changes in production and nutrient cycling across a wetness gradient within a floodplain forest[END_REF]. The role of forest structure parameters on the prediction of litterfall is also notable with constant contributions of ~30% in all the proposed models. Overall, further comprehensive studies including (by decreasing order of importance) flooding regime, soil fertility, and forest structure are necessary to understand the complex process of litter production, while litterfall chemistry may be considered as a useful substitute of flooding and soil surrogates in litterfall predictions.

E.

  Gonza ´lez, 1 B. Gallardo, F.A. Comı ´n, and M. Gonza ´lez-Sanchis. Pyrenean Institute of Ecology, Spanish National Research Council (CSIC), Avda. Montan ˜ana 1005, Zaragoza, Aragon 50192, Spain. E. Muller. Universite ´ de Toulouse, Universite ´ Paul Sabatier (UPS), Institut national polytechnique de Toulouse (INP), EcoLab (Laboratoire d'e ´cologie fonctionnelle), 29 rue Jeanne Marvig, 31055 Toulouse, France; Centre national de la recherche scientifique (CNRS), EcoLab (Laboratoire d'e ´cologie fonctionnelle), 29 rue Jeanne Marvig, 31055 Toulouse, France.

Fig. 1 .

 1 Fig.1. Location of the 12 study plots within the Middle Ebro River floodplain with corresponding local flooding regimes. FD, flood duration (weeksÁyear -1 ); DGW, annual mean depth to ground water (cm); RD, river distance (m). The plots were numbered by FD in decreasing order. White lines represent the lateral dikes built for flood protection. Broken white lines denote the limits of the Alfranca Reserve. The variation in water level at the 12 study plots was registered by weekly measurements in a piezometer installed in each plot. The Middle Ebro River flow discharge data were collected at the Zaragoza gauging station. The 2007 curve was made using 15 min interval data, whereas the curve for the period 1981-2003 is the monthly average flow.

Fig. 3 .

 3 Fig. 3. Response of litterfall to the 17 explanatory variables and the squared Spearman's coefficients (R 2 ). When the relationship was significant (*, p < 0.05) a linear function was adjusted. Each point represents the total litter collected in a single trap in 2007 (n = 120). Each column of points corresponds with a plot (n = 12).

  Variable abbreviations are explained in the text.*, p < 0.05.

Table 1 .

 1 Total litter production in 2007 collected in the 12 study plots within the Middle Ebro River floodplain. Forest structure characteristics of the 12 study plots within the Middle Ebro River floodplain.

		Plot
		1	2	3	4	5	6	7	8	9	1 0	1 1	1 2
	Litter production	508	773	552	748	536	605	381	431	548	199	559	916
	Fig. 2.

Table 2 .

 2 Soil characteristics of the 12 study plots within the Middle Ebro River floodplain.

		Plot
		1	2	3	4	5	6	7	8	9	1 0	1 1	1 2
	Geomorphic landform	G	L	L	L	L	L	T	T	T	T	T	T
	Fine-textured fraction (FINE) (%) 30	83	66	73	94	70	34	67	81	86	90	74
	Total organic C (TOC) (%)	0.3	1.6	1.6	1.4	1.9	1.5	1.7	4.2	2.1	3.6	2.6	2.5
	Total N (TN) (%)	0.05	0.14	0.15	0.15	0.16	0.11	0.10	0.35	0.20	0.29	0.24	0.24
	Total P (TP) (%)	0.041 0.063 0.061 0.064 0.065 0.061 0.026 0.057 0.064 0.055 0.064 0.070

Note: G, gravel bar; L, natural levee; T, floodplain terrace.

Table 3 .

 3 Litterfall chemistry of the 12 study plots within the Middle Ebro River floodplain.

		Plot
		1	2	3	4	5	6	7	8	9	1 0	1 1	1 2
	Litter C/N atomic ratio (CN)	64	50	50	49	39	50	65	50	49	65	45	53
	(mol CÁmol N -1 )
	Litter C/P atomic ratio (CP)	1248 1129 1329 1196 961	1187 2340 1633 1169 2148 992	1263
	(mol CÁmol P -1 )
	Litter N/P atomic ratio (NP)	19	22	27	25	24	24	36	32	24	33	22	24
	(mol NÁmol P -1 )
	Nitrogen use efficiency (N-	120	96	95	92	75	97	124	96	97	121	81	99
	NUE) (gÁg -1 )
	Phosphorus use efficiency (P-	1055	969 1142 1018 829	1034 2032 1407 1033 1808 811	1068
	NUE) (gÁg -1 )
	Nitrogen resorption proficiency	0.8	1.2	1.0	1.0	1.0	0.8	0.7	0.8	0.9	0.8	0.8	0.9
	(N) (%)
	Phosphorus resorption profi-	0.09	0.10	0.07	0.07 0.08	0.06	0.04	0.05	0.07	0.04 0.07	0.08
	ciency (P) (%)

Table 5 .

 5 Results of linear mixed effects models (LME) performed between total litter production (response variable) and forest structure, flooding regime, soil conditions, and litterfall chemistry surrogates (explanatory variables). AIC and BIC are the Akaike and Schwarz-Bayesian information criteria and complement R 2 to indicate the fitness of the models, with the small values the best models.

						Relative
			Pearson	Explanatory		contribution
	Approach	Model fit*	correlation	variable {	p	(%) {
	Forest structure + flood-	AIC = 1588.711	R 2 = 0.51	RD	0.003	39
	ing + soil + litter chem-
	istry (full model)
	Performed with 17 vari-	BIC = 1605.436	t = 11.0849 TP	<0.001	34
	ables
			df = 118	SD	<0.001	27
			p < 0.001
	Forest structure + soil	AIC = 1588.091	R 2 = 0.51	TP	<0.001	57
	Performed with 7 vari-	BIC = 1604.816	t = 11.1411 SD	<0.001	28
	ables
			df = 118
			p < 0.001	TOC	0.003	15
	Forest structure + litterfall	AIC = 1604.350	R 2 = 0.40	P-NUE	<0.001	70
	chemistry
	Performed with 10 vari-	BIC = 1618.287	t = 8.9258	SD	0.003	30
	ables
			df = 118
			p < 0.001			.

*

Table 6 .

 6 Summary of annual litterfall for forests in Mediterranean riparian settings.

	Study area	Litterfall*	Dominant species	Climate	Reference
	Margarac ¸a Forest, central Portugal 715 {	Castanea sativa, Quercus ro-	Atlantic/Mediter-	Abelho and Grac ¸a 1998
			bur, Prunus spp.	ranean
	Garonne River, SW France	539	Alnus glutinosa	Atlantic/Mediter-	Chauvet and Jean-Louis 1988
				ranean
		523	Salix alba
		471	Populus nigra
		470	Salix alba
	Middle Ebro River, NE Spain	563	Populus nigra, P. alba, Ta-	Mediterranean	This study
			marix spp., Ulmus minor
	Fuirosos Forest, NE Spain	861. {	Alnus glutinosa, Platanus	Mediterranean	Acun ˜a et al. 2007
			acerifolia
	Fuirosos Forest, NE Spain	563. {	Alnus glutinosa, Platanus	Mediterranean	Bernal et al. 2003
			acerifolia
	Fuirosos Forest, NE Spain	697. {	Alnus glutinosa, Platanus	Mediterranean	Sabater et al. 2001
			acerifolia
	Oued Zeghzel, N Morocco	474	Nerium oleander, Salix pedi-	Mediterranean	Maamri et al. 1994
			cellata, Populus spp.
	Window Stream, SW South	426	Ilex mitis, Cunonia capensis,	Mediterranean	Stewart and Davies 1990
	Africa		Secamone alpine
	Langrivier, SW South Africa	500	Brabejum stellatifolium, Me-	Mediterranean	King et al. 1987
			trosideros angustifolia
		486	Brabejum stellatifolium, Me-
			trosideros angustifolia
		434	Ilex mitis, Cunonia capensis		.

Corresponding author (e-mail: edusargas@ipe.csic.es).

Acknowledgements

We thank A. Frutos, L. Gonza ´lez, D. Jime ´nez, L. Mancebo, A. Villarroya, F. Reverberi, and C. Aniento for helping with field and lab work. The authors are also grateful to B. Sa ´nchez and P. Romeo, who collaborated in the design and manufacture of the litterfall traps. This research was funded by the Department of Environmental Science, Technology and University (Government of Aragon, research group E-61 on Ecological Restoration), and the Ministry of Science and Innovation of Spain (MICINN, CGL2008-05153-C02-01/BOS). The first author was supported by a grant from the Ministry of Education and Science of Spain (MEC).


Eduardo Gonza ´lez •

Marı ´a Gonza ´lez-Sanchis

´lvaro Cabezas

Francisco A Comı ´n •

Etienne Muller

E Gonza ´lez

Á M Gonza ´lez-Sanchis

A ´ Cabezas

F A Comı

Recent Changes in the Riparian Forest of a Large Regulated Mediterranean River: Implications for Management

Keywords: Floodplain forests, River regulation, Middle Ebro River, Salicaceae, Tamarix, Canopy dieback, Stand structure, Hydrogeomorphic

The structure of the floodplain forests of the Middle Ebro River (NE Spain) was examined at patch and landscape scales along a three-step chronosequence defined according to the extent of flow regulation-induced hydrogeomorphic changes, with the ultimate purpose of producing baseline information to guide through management and restoration plans. At patch scale, a total of 6,891 stems within 39 plots were registered for species, diameter and health status. The stem density, size class distribution, canopy dieback and mortality were further compared by means of non-parametric tests. At landscape scale, the temporal evolution of the area occupied by forest stands of different ages in the floodplain along the chronosequence was evaluated using four sets of aerial photographs dated in 1927, 1957, 1981 and 2003. The within-patch structure of pioneer forests (\25-30 years old) was characterized by dense and healthy populations of pioneer species (Populus nigra, Salix alba and Tamarix spp.), but the area occupied by these forest types has progressively decreased (up to 37%) since the intensification of river regulation (ca. 1957). In contrast, non-pioneer forests ([25-30 years old) were characterized by declining and sparse P. nigra-S. alba-Tamarix spp. stands, where late-seral species such as Ulmus minor and Fraxinus angustifolia were frequent, but only as small-size stems. At landscape scale, these type of senescent forests have doubled their surface after river regulation was intensified. Populus alba only appeared in the oldest plots recorded (colonized before 1957), suggesting sexual regeneration failure during the last five decades, but usually as healthy and dense stands. Based on these findings, measures principally aimed at recovering some hydrogeomorphic dynamism are recommended to guarantee the self-sustainability of the floodplain forest ecosystem.

Introduction

The variety of riparian plant communities found in natural floodplains is mainly controlled by the flow regime (Poff and others 1997), which generates physical disturbance and environmental stress on riparian vegetation, ultimately affecting its temporal and spatial dynamics (Shafroth and others 2002). The effect of flow regime on riparian vegetation is hydrologic and geomorphologic [START_REF] Bendix | Hydrological and geomorphological impacts on riparian plant communities[END_REF]. On the one hand, hydrology influences the regeneration and maintenance of floodplain vegetation by transporting propagules, wetting floodplain soils, recharging ground-water and providing nutrients to the existing vegetation. On the other hand, fluvio-geomorphologic events create new bare substrates necessary for the establishment of pioneer plants [START_REF] Mahoney | Streamflow requirements for cottonwood seedling recruitment-an integrative model[END_REF][START_REF] Stromberg | Dynamics of Fremont cottonwood (Populus fremontii) and saltcedar (Tamarix chinensis) populations along the San Pedro River, Arizona[END_REF]Cooper and others 1999), which are progressively and sequentially succeeded by late-seral stages until eventually a severe flood brings the system back to a starting point (Johnson and others 1976;[START_REF] Schnitzler | Successional status of trees in gallery forest along the river Rhine[END_REF][START_REF] Ward | Ecological connectivity in alluvial river ecosystems and its disruption by flow regulation[END_REF]Cordes and others 1997;Stromberg and others 1997;[START_REF] Stromberg | Dynamics of Fremont cottonwood (Populus fremontii) and saltcedar (Tamarix chinensis) populations along the San Pedro River, Arizona[END_REF]van Pelt and others 2006).

Flow regulation and flood protection infrastructures strongly modify the flow regime of rivers and, thereby, disrupt the hydrogeomorphic-dependent structure of plant communities [START_REF] Busch | Mechanisms associated with decline of woody species in riparian ecosystems of the Southwestern U[END_REF][START_REF] Ward | Ecological connectivity in alluvial river ecosystems and its disruption by flow regulation[END_REF]Friedman and others 1996;Stromberg and others 1996;Poff and others 1997;Rood and others 1999;Gergel and others 2002;Shafroth and others 2002;Dufour and others 2007). Accordingly, it might be expected that the effects of regulation on the structure of the riparian tree community (i.e., the pattern of tree species composition, abundance and size class distribution) are reflected on within-patch forest metrics, such as stem density (Shafroth and others 2002). Other measurements, such as canopy dieback or stem mortality, might also give valuable information about the species fitness to the changing hydrologic conditions. Indeed, it was proposed by Rood and others (2000) that branch dieback in some species of Populus is auto-induced in drought stress scenarios, so that trees would reduce their water use. Horton and others (2001) showed that other riparian tree species besides Populus, namely Salix gooddingii and Tamarix chinensis, also sacrifice some branches in order to improve water status in the surviving shoot. Sometimes branch sacrifice is not enough to cope with dry conditions and water table depletions, and mortality can not be prevented. In fact, significant proportions of dead stems in stands can be interpreted as an evidence of severe hydrologic alteration (Megonigal and others 1997;Scott and others 2000).

Shifts in the structure of the riparian tree community after human-induced hydrogeomorphic changes have been largely studied in North America (Johnson and others 1976;[START_REF] Johnson | Dams and riparian forests: case study from the upper Missouri River[END_REF]1998;Rood and others 1999;[START_REF] Bendix | Hydrological and geomorphological impacts on riparian plant communities[END_REF][START_REF] Merritt | Riparian vegetation and channel change in response to river regulation: a comparative study of regulated and unregulated streams in the Green River Basin, USA[END_REF]Gergel and others 2002;Shafroth and others 2002;Katz and others 2005) and Northwestern Europe (Marston and others 1995;Tre ´molie `res and others 1998;Dufour and others 2007). However, few such studies have been developed in the Mediterranean region (Crivelli and others 1995;Aguiar and others 2001;[START_REF] Salinas | Riparian vegetation of two semi-arid Mediterranean rivers: basin-scale responses of woody and herbaceous plants to environmental gradients[END_REF]. In Spain, although the hydrogeomorphic patterns of one of the largest rivers, namely the Ebro River (NE Iberian Peninsula), have dramatically changed during the last decades as a consequence of flow regulation and flood protection (Batalla and others 2004;[START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF]Cabezas and others 2009), there has been no attempt to date to quantify how the structure of the riparian tree community has been affected by the progressive disruption of river-floodplain interactions. To guide management plans, a better understanding of the relationships between the structure of riparian woodlands and their hydrogeomorphic drivers is required.

In this context, the main objective of this study is to describe the structure and health of the riparian tree community in the Middle Ebro River, within a framework of historic and recent hydrogeomorphic change. In particular, the composition, stem density, size class distribution, canopy dieback and mortality of the dominant tree species were expected to vary through an *80-year chronosequence characterised by changing fluvio-geomorphic patterns that have resulted from river regulation. It was also hypothesized that the change of hydrogeomorphic dynamics would have influenced the relative proportions of forest stands of different ages along the chronosequence. The ultimate objective of this work is to provide background data useful for management and restoration decisions.

Methods

Study Area

The studied area is the Natural Reserve of the Alfranca Galachos (41°36 0 N, 0°46 0 W), an 8-km river segment located 12 km downstream of the city of Zaragoza in the Middle Ebro River, which is a 346-km reach between Logron ˜o and La Zaida (NE Spain) (Fig. 1). The Ebro River is the second largest river in the Iberian Peninsula in terms of length (930 km), annual averaged discharge (*12,000 hm 3 year -1 ) and drainage area (85,534 km 2 ). The average monthly discharge registered at the gauging station of Zaragoza is 230 m 3 s -1 , and the elevation in the study reach ranges between 175 and 185 m above sea level (a.s.l.). The precipitation regime of the semiarid Ebro depression is characterized by rainfall scarcity (annual average *400 mm), high inter-and intra-annual variability, with maximum levels in spring and autumn and minimum levels in summer [START_REF] Pinilla | The development of irrigated agriculture in twentieth-century Spain: a case study of the Ebro basin[END_REF]. The overstory of the natural floodplain forest is composed of three softwood Salicaceae species: white poplar (Populus alba), European black poplar (P. nigra) and white willow (Salix alba), and five hardwood species: saltcedar (Tamarix gallica, T. africana and T. canariensis), narrow leaf ash (Fraxinus angustifolia) and field elm (Ulmus minor). Other species, such as the shrubs common hawthorn (Crataegus monogyna) and bay laurel (Laurus nobilis) rarely attain tree size on the floodplain. The exotics box elder (Acer negundo), black locust (Robinia pseudoacacia), babylon willow (Salix babylonica) and some fruit trees have been occasionally detected as tree-size stems. Steppic shrubby vegetation dominates the uplands adjacent to the floodplain.

Hydrogeomorphic Background

The hydrogeomorphology of the Middle Ebro River during the twentieth century has evolved during three major periods following human interventions [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF]Cabezas and others 2009):

(1) In a pre-regulation period (before the 1950s), the natural pluvionival hydrological regime of the Ebro River remained practically unaltered. In the absence of regulation, floods usually occurred in winter and spring, when precipitation was more frequent, and after the snowmelt. Low water levels normally lasted from July to October (Fig. 2a). The inter-annual variability of the flow regime and flood pulses was high (Fig. 2b). With an almost unmodified flow regime and absence of significant flood protection, the middle stretch of the river had a braided-meandering channel with unstable riverbanks. In this period, changes in the channel morphology (i.e., meander cut-offs produced during flood episodes and channel migration caused by progressive bank erosion) were continuous and, consequently, natural forests concentrated in the outer floodplain. However, agricultural practices started to convert extensive areas of the floodplain to anthropic landcover and to narrow the natural riparian corridor.

(2) Regulation period (1950-1980s). Although humans had been building some flood defences along the Ebro River for centuries, it was not until the highest flood of the century, which occurred in 1961 (instantaneous peak of 4,130 m 3 s -1 at the gauging station of Zaragoza, 74-year recurrence interval), that the number of dykes, levees, ripraps, breakwaters, concrete walls and dredging operations dramatically increased in the Middle Ebro (from *5 defence works year -1 before 1961 to *25 defence works year -1 in the period 1961-1980) [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF]. This fact severely limited channel migration. In parallel, the largest reservoirs currently operating upstream of the study area were built at the beginning of this period (Fig. 1; Table 1). Surprisingly, these new dams did not alter significantly the timing (Fig. 2a) and flood pulses (Fig. 2b;

Table 2) of the flow regime with regard to the previous period, although it is likely that the peak in precipitation registered in almost all the Ebro River Basin during the 1970s (Abaurrea and others 2002) dampened the effects of dams on the hydroperiod (Cabezas and others 2009). Likewise, the dams probably limited the provision of sediments as well and, together with river embankment, they may have increased river bed incision, and (1927-1957), regulation (1957-1981) and stabilization period progressively fixed the channel [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF]). In addition, land reclamation by agriculture continued with the expansion of irrigation, reducing the surface occupied by natural vegetation (Cabezas and others 2009).

(3) Stabilization period (1980s-present). The construction of flood protection structures in the Middle Ebro was intensified in the 1980s (up to 32 works year -1 ) [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF], covering the meander concave bars of the entire channel (e.g. study area, Fig. 1). The mean annual discharge in the Ebro since the 1980s has decreased by 30% with regard to the previous two periods due to, among other factors, a shift to high water-demand crops, such as rice, fruit and vegetable (Frutos and others 2004;Cabezas and others 2009). In addition, the magnitude, frequency, duration, and variability of flood events were also reduced (Fig. 2; Table 2), while the frequency and duration of lowwater events increased compared to the previous period [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF]. These low-water events were mainly recorded during the summer but they also appeared in spring and autumn (Frutos and others 2004). In fact, June's mean flow discharge has notably decreased in this period (Fig. 2a). Finally, agricultural land cover has been maintained until the present time, limiting the surface occupied by natural forests to only 4.5% of the 5-km mean width Middle Ebro floodplain [START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF].

Forest Patches Age-Classification and Plot Selection Among existing aerial missions, the photos of 1927, 1957, 1981 and 2003 were chosen as representative of the three above-mentioned periods, and used to classify forest patches according to their age. Each image was rectified and georeferenced and the open water, barren sites (potential recruitment sites), non-woody vegetation (herbaceous and macrophytes), natural floodplain forests, and anthropic landcovers (including poplar crops and agricultural fields) were digitized using ArcGis 9.2 Ò . Patches were identified through a fixed scale of 1:3,000 following patterns of texture, colour, vertical structure, position in the landscape and previous channel migration dynamics. A stereoscope was used to improve picture interpretation. The digitation was limited to the area flooded during the 10-year flood of February 2003 (2,230 ha) (map provided by the Ebro River Basin Administration; Losada and others 2004).

The four maps compiled from the aerial photos were used to distinguish the following three age-forest categories on the aerial photo of 2003: young forests (i.e., an absence of forest in 1981's image but a presence in 2003's) (\25 years old), mature forests (i.e., an absence of forest in 1957's image but a presence in 1981's) (25-50 years old) and old forests (i.e., the forest was present before 1957) ([50 years old). For a detailed field survey, a total of 13 patches of each category (i.e., 39 patches in total) were selected (Fig. 3). The following criteria were used to select a patch: (1) evidence of the establishment from an initial cohort of pioneer trees; (2) patch size C0.25 ha; (3) location within a distinctive geomorphic landform (gravel bar, natural levee of permanent/intermittent channel, floodplain terrace); (4) no evidence of current or former human disturbance, such as planting, grazing, cutting, irrigation, gravel pit extraction or cultivation and (5) all the successional pathways and the full range of elevations and distances from the main channel had to be represented.

The same procedure was applied to the aerial photographs of 1957 and 1981 to calculate the area occupied by pioneer forests (i.e., \25-30 years old, presence of forest in the image under examination but absence in the previous image), non-pioneer forests (i.e., [25-30 years old, presence of forest in the image under examination and in the previous image) and undated (presence of forest in the image under examination but absence of previous image) for each year.

Only one field plot was randomly placed in each patch to avoid pseudoreplication bias and to cover a broader area. Rectangular plots were used because they adapted geometrically to the usually elongated riparian forest patches. Table 2 Bankfull discharge, flood frequency and duration at the gauging station of Zaragoza (41°39 0 N, 0°52 0 W) (Middle Ebro River, NE Spain) for the pre-regulation (1927-1957), regulation (1957-1981) and stabilization periods; a flood event is defined as one exceeding 600 m 3 s -1

1927 -1957 1957-1981 1981-2003 Bankfull discharge (m 3 s -1 ) 1980 1957 1410

Flood frequency (events year -1 ) 7.6 6.6 4.2

Flood duration (days event -1 ) 5.1 5.9 4.4

Plot dimensions varied proportionally to tree height, to capture the maximum variability without over-sampling (van Pelt and others 2006). The long axis of each plot was made at least twice the dominant height (i.e., mean height of the two highest trees). The short axis was long enough to make the plot area = dominant height 2 . In all, plot areas ranged from 25 to 1,000 m 2 .

Tree Survey

Forest structure and health were analyzed within each field plot. Every stem in the plot was registered for species, diameter and health status from late-spring to mid-summer of 2006 and 2007. Three size classes were defined for each species, according to their stem height and diameter: seedlings (0.3 m B height \ 1.3 m or diameter at breast height [d.b.h., 1.3 m] \ 2.5 cm), saplings (height C 1.3 m and 2.5 C d.b.h. \ 7.5 cm) and adults (height C 1.3 m and d.b.h. C 7.5 cm). An exception had to be made with saltcedars because of their shrubby architecture: seedlings (0.3 m B length \ 1.3 m or diameter at 0.30 m [d30] \ 2.5 cm), saplings (length C 1.3 m and 2.5 C d30 \ 7.5 cm) and adults (length C 1.3 m and d30 C 7.5 cm). In addition, saltcedars could not be described at species level in the absence of inflorescence during the sampling period. Adult stems were further arbitrarily divided into small (d.b.h.: \ 22.5 cm) and large (d.b.h.: C 22.5 cm). Stem density (stems ha -1 ) was calculated including all size classes. Within an age-forest category, the presence (%) of each species was calculated as the percentage of plots where at least one stem of the given species was present.

Regarding health status, every stem was registered as dead or alive. Additionally, the canopy dieback (i.e., a measure of the extent of leafless branches in the tree canopy) of each adult live stem was estimated visually by class defined according to the following criteria: none = foliage remaining rich and dark green; moderate = existing dead or precociously senescing branches (excluding selfpruning and infections by pathogens as causes of death); severe = senescing stem.

Statistical Analyses

As most of the data did not follow a normal distribution, non-parametric statistics were used. The non-parametric Kruskal-Wallis H test, analogous to the one-way analysis of variance (ANOVA), followed by Mann-Whitney U pairwise comparisons, were used to test for significant differences between species or size classes for the measured variables. A particular non-parametric test analogous to the one-way ANOVA (the Jonckheere-Terpstra test), which assumes that there is an a priori ordering (ascending or descending) in the chronosequence, was used to analyze whether the differences found in the measured variables followed age order. SPSS 13.0 was used for all statistical analyses.

Results

Changes at Landscape Scale

The total surface occupied by natural forests and barren sites (potential recruitment sites) in the 10-year floodplain decreased progressively from 1927 to 1981 (Fig. 4; Table 3). During the stabilization period , the loss of barren sites continued, but at a lower rate and the floodplain forest recovered to such an extent that the total floodplain forest area in 2003 was higher than in 1957. However, within the natural forest category, the area occupied by pioneer forests decreased in the period 1981-2003 (Table 3). As a result, the natural forests shifted from a dominance of pioneer units in 1957 and 1981 to a dominance of non-pioneer forest in 2003.

Stem Density

The live stem density (excluding dead stems) along the chronosequence (Fig. 5) was highly contrasted, averaging 24,804 stems ha -1 in the young, 2,444 stems ha -1 in the mature and 3,843 stems ha -1 in the old plots (P = 0.001, d.f. = 2, X 2 = 13.931, Kruskal-Wallis test). In the young forests, the high stem density was mainly due to the contribution of Tamarix spp., P. nigra and, to a lesser extent, S. alba. Tamarix spp. also exhibited the highest live stem densities within mature forests, but with a mean density almost twentyfold lower than in the young forests, followed by F. angustifolia and U. minor. In the old forests: U. minor, Tamarix spp. and P. alba, which surprisingly was significantly present only in this age category, contributed the most to live stem density.

Mortality

The proportion of dead stems (Fig. 5) was lower in young (12%) than in mature (23%) and old plots (27%) (P = 0.022, Z = -2.284, Mann-Whitney U = 40 and P = 0.007, Z = -2.643, Mann-Whitney U = 33, respectively). Indeed, the proportion of standing dead stems increased as plot aged (P = 0.004, Std. Jonckheere-Terpstra Statistic = 2.847). In young forests, mortality was equally distributed among the species. However, in mature and old forests, mortality was generally higher in P. alba, P. nigra, S. alba and Tamarix spp. than in F. angustifolia, U. minor and other species (P \ 0.05, Mann-Whitney tests) (Fig. 5). Mortality was regularly distributed among the size classes within each species. The only exception to that trend was P. alba, whose proportion of dead small stems (62%) was higher than that of dead adults (11%) (P = 0.031, Z = -2.155, Mann-Whitney U = 6.0).

Size Class Distribution

The distribution of live stems into size classes (Fig. 6) provided complementary information to stem density and a better understanding of the population structure and dynamics of each species in the chronosequence. As expected, small stems (i.e., seedlings and saplings) clearly predominated in the young forests, with a mean live stem density (excluding dead stems) of 23,329 stems ha -1 , compared to adults with 1,474 stems ha -1 (P = 0.013, Z = -2.491, Mann-Whitney U = 36.0). Tamarix spp., P. nigra and S. alba shared a similar population structure and were in a very active recruitment phase. In mature and old plots, the live small stems were dominant within F. angustifolia and U. minor species (P = 0.010, Z = -2.562, Mann-Whitney U = 37.5 and P = 0.014, Z = -2.451, Mann-Whitney U = 83.0, respectively). However, the density of live small stems of P. nigra and S. alba was extremely low, and significantly higher in the rest of species (P \ 0.05, Mann-Whitney tests), although the small stems densities of P. alba, Tamarix spp., U. minor and F. angustifolia never reached the ones found in young forests (P \ 0.05, Mann-Whitney statistics). Furthermore, the largest individuals found in the study area were Salicaceae spp., whereas species in the remaining families rarely attained sizes larger than 22.5 cm in d.b.h.

Canopy Dieback

The likelihood of finding an individual affected by canopy dieback (Fig. 7) was high in mature (74%) and old forests (52%) and significantly lower in young forests (21%)

Discussion

Forest Structure

P. nigra and S. alba are the most widespread Salicaceae species in the European floodplains, exhibiting clear pioneer establishment traits (van Splunder and others 1995; [START_REF] Barsoum | Regeneration response of black poplar to changing river levels[END_REF]Hughes and others 2001;Guilloy-Froget and others 2002). Their widespread presence and high dominance (especially as live small-size stems) in the young forests reflect a relatively recent colonization and indicate that the hydrogeomorphic requirements for their establishment were met during the stabilization period, but only in 5% of the 10-year floodplain. In contrast with young forests, P. nigra and S. alba exhibited low small-stem densities in mature and old forests, which is typical of a community with low recruitment levels and provides evidence of an unsuitable hydrogeomorphic regime at site scale to recruit individuals of the two species in the remaining 11% of the 10-year floodplain covered by natural forests. An unusual feature of the Ebro River, compared with the Northern-European environments, is not only the presence of Tamaricaceae spp. but also their high density and dominance. Like P. nigra and S. their high density of small stems suggests that their hydrogeomorphic requirements were met during the stabilization period. Tamarix spp. are also prolific seed producers which need recently disturbed areas for seedling establishment (di Tomaso 1998). However, it is likely that they adapted better than Salicaceae to the changing hydrogeomorphic conditions in the Middle Ebro, as they could maintain a higher stem density than P. nigra and S. alba along the chronosequence. Traditionally, Tamaricaceae spp. have been considered to respond to the impacts derived from river regulation better than Salicaceae, principally because of their greater tolerance to water stress and salinity [START_REF] Glenn | Comparative ecophysiology of Tamarix ramosissima and native trees in western U.S. riparian zones[END_REF] and their longer and later dispersal of seeds [START_REF] Gladwin | Survival of plains cottonwood (Populus deltoides subsp. monolifera) and saltcedar (Tamarix ramosissima) seedlings in response to flooding[END_REF][START_REF] Roelle | Establishment of woody riparian species from natural seedfall at a former gravel pit[END_REF]Roelle and others 2001). However, the high stem densities of saltcedar in mature and old forests may be due not to a more effective regeneration than P. nigra and S. alba, but to their shrubby architecture. Indeed, Cleverly and others (1997) reported lower stem growth rates (narrower annual tree rings) in Tamarix compared to co-existing Salix. This would partly explain why saltcedars rarely attained diameters larger than 22.5 cm (Fig. 6). P. alba seems the species most affected by regulation, since it only appeared in the stands colonized before the regulation period (i.e old stands). The few individuals detected in mature forests (plots 19, 20 and 22) could be root suckers from adjacent old P. alba stands. Although not specifically addressed in this study, the origin of most P. alba stems is probably vegetative, as homogeneous phenology and morphology has been observed in P. alba stands (i.e., stems grouped by sex, neighbour females coupling flowering and seed dispersal periods) (Gonza ´lez, personal observation). Legionnet and others (1997), [START_REF] Gom | Patterns of clonal occurrence in a mature cottonwood grove along the Oldman River, Alberta[END_REF] and Barsoum and others (2004) described significant vegetative propagation in some Populus species. However, to our knowledge, there is no study of P. alba vegetative regeneration in the existing literature. The apparent sexual regeneration failure of P. alba during the last few decades is especially surprising, as it has been recently shown that their sexual regeneration strategies are similar to those of other riparian Populus (Gonza ´lez and others 2010), and deserves further research.

The loss of riparian habitats, especially those in the outer floodplain, caused by the increase of the area occupied by crops, together with the spreading of the Dutch Elm Disease, have caused the disappearance of most U. minor Analyses were not performed when a given species was present in less than three plots stands in Spain (Garcı ´a [START_REF] Garcı ´a Nieto | Los olmos en el paisaje vegetal de la Penı ´nsula Ibe ´rica[END_REF]Lara and others 2004;[START_REF] Lo ´pez-Almansa | Review. Reproductive ecology of riparian elms[END_REF]. However, the high sprouting rate from surviving roots of unhealthy trees, as reported for Spanish elms (Lo ´pez-Almansa 2004), could explain the widespread presence and relative abundance observed in the Middle Ebro. Ulmus high regeneration, and high mortality in young trees caused by Dutch Elm Disease were also reported in the Upper Rhine nearby Strasbourg (France) by Tre ´molie `res and others (1998). F. angustifolia is frequently found in most river margins of the Northern Iberian Peninsula, including the Ebro River, but rarely dominating (Lara and others 2004), as happens in this study area. Oszla ´nyi (1997) also described a vigorous F. angustifolia regeneration (up to 240,000 small stems ha -1 ) under a declining tree layer of P. nigra, S. alba and P. alba in a disconnected forest in the Slovakian Danube River. Both U. minor and F. angustifolia establish and regenerate more effectively in mature and old forests, which suggests not only that they are less opportunistic than the other species, but also that their regeneration is not so dependent on recurrent fluvio-geomorphic events. Nevertheless, it is yet unknown whether succession under the current hydrogeomorphic regime would lead to a more widespread presence of larger size classes of these hardwood species in the future.

In short, P. nigra, S. alba and Tamarix spp. may be defined as pioneer tree species in the Ebro River, whereas P. alba, U. minor and F. angustifolia would rather be considered as non-pioneer species.

Forest Health

The higher canopy dieback of pioneer species observed in mature and old stands might be due not only to natural senescence but also to the hydrologic regime change, as most of the trees colonized those patches before 1981 and, therefore, under different hydrological conditions. Thus, human activity might be causing a decline of P. nigra and S. alba along the Ebro River, being both species extremely affected by dieback, as it has been reported for other Salicaceae species along dam-regulated rivers elsewhere [START_REF] Rood | Abrupt riparian forest decline following river damming in Southern Alberta[END_REF][START_REF] Rood | Collapse of riparian poplar forests downstream from dams in Western Prairies: probable causes and prospects for mitigation[END_REF][START_REF] Johnson | Dams and riparian forests: case study from the upper Missouri River[END_REF]Rood and others 1995;Stromberg and others 1996;Cordes and others 1997;[START_REF] Merritt | Riparian vegetation and channel change in response to river regulation: a comparative study of regulated and unregulated streams in the Green River Basin, USA[END_REF]Muller and others 2002;[START_REF] Williams | Mechanisms of riparian cottonwood decline along regulated rivers[END_REF]. The better health status of saltcedars in the Middle Ebro compared to the Salicaceae species is consistent with their abovementioned properties, although saltcedars could also be sacrificing branches in response to water stress. The rest of the species are much less affected by dieback, as found by Oszla ´nyi (1997), who also reported partial destruction of the canopy of almost all the P. nigra and S. alba individuals in the Slovakian Danube River, whereas the co-occurring F. angustifolia showed an excellent health status. Nevertheless, the great variability in dieback among plots within the same age category also suggests the need for more detailed studies aiming to identify the ultimate factors driving this morphological response to hydric stress.

Likewise, the change in hydrologic conditions could have increased mortality among pioneers in mature and old forests. However, the higher mortality among small P. alba stems could be due to natural thinning in the absence of light under the usually dense and healthy canopy of P. alba, as young individuals of Salicaceae do not tolerate shade [START_REF] Sacchi | The relative roles of abiotic and biotic factors in seedling demography of Arroyo Willow (Salix lasiolepis)[END_REF]Cooper and others 1999).

Management Implications

The area occupied by non-pioneer forests relative to pioneer forests today is much higher than it was in the absence of regulation (Table 3). If the current hydrogeomorphic patterns are maintained, it is likely that most of the existing forests will not disappear but will keep ageing (as it occurred during the stabilization period, Table 3), whereas new pioneer forests will be confined to smaller and more dynamic areas, where the effect of floods is recurrently destructive (usually close to the main channel or in-channel areas; Figs. 3,4). Consequently, stands with structural characteristics like the ones observed in young forests would be progressively less common, while stands structurally similar to mature and old forests would predominate. Under this scenario, P. nigra, S. alba and, to a lesser extent, Tamarix spp. populations could notably decline in the Middle Ebro floodplain forests during the twenty first century. Their progressive substitution by U. minor and F. angustifolia is uncertain. In the short and medium term, the maintenance of P. alba populations at patch scale seems guaranteed. However, at landscape scale, it is unlikely that P. alba will colonize new sites, so its future in the Middle Ebro is also compromised. Nevertheless, as the regulation infrastructures are relatively recent (less than 50 years), their effects on vegetation structure are probably not yet fully manifested [START_REF] Johnson | Adjustment of riparian vegetation to river regulation in the Great Plains, USA[END_REF]Katz and others 2005) and our predictions should be taken with caution. Another uncertainty may come from the exotic species (e.g., A. negundo, R. pseudoacacia) already detected, which are not yet invasive in the Middle Ebro, and from the effects of climate change. Fortunately, the potential for ecological restoration remains high. Even in pristine environments, regeneration of pioneers can systematically fail for years because the precise hydrologic conditions required for seedling establishment are only occasionally satisfied [START_REF] Mahoney | Streamflow requirements for cottonwood seedling recruitment-an integrative model[END_REF]. Thus, these populations have developed the faculty of keeping an enormous reproductive potential [START_REF] Gom | Patterns of clonal occurrence in a mature cottonwood grove along the Oldman River, Alberta[END_REF]Karrenberg and others 2002) and, when appropriate restoration measures are taken, successful regeneration occurs rapidly and effectively [START_REF] Rood | Revised instream regulation enables cottonwood recruitment along the St[END_REF]Stevens others 2001;[START_REF] Stromberg | Restoration of riparian vegetation in the south western United States: importance of flow regime and fluvial dynamism[END_REF]Rood andothers 2003, 2005).

In this sense, the most effective restoration approach in the Middle Ebro should focus on the recovery of some hydrogeomorphic dynamism (i.e., channel migration, periodic creation of new barren sites, reactivation of secondary channels, meander cut-offs, renaturalized hydroperiod, etc.) both at basin and reach scale, within the current socioeconomic context (Comı ´n and others 2005). Thus, the ideal hydrogeomorphic regime would not necessarily be the preregulation state but one 'renaturalized', which led to a selfsustainable forest structure at patch and landscape scale, guaranteed their ecological functions and provided services to society [START_REF] Dufour | From the myth of a lost paradise to targeted river restoration: forget natural references and focus on human benefits[END_REF]. However, more research is needed to define those ideal conditions locally. At this point, the most urgent actions to be implemented seem those aimed at maintaining a mosaic of forest patches of different age by creating opportunities for the periodic colonization of new pioneer forests. These actions should be implemented at basin and reach scale.

At basin scale, water demand by society is expected to increase in the future (Cabezas and others 2009), so the 'renaturalization' of the flow regime through dam operations (e.g., raise of low water levels, release of controlled floods and sediments) is not likely to occur.

At reach scale, returning part of the land back to the river (the 'mobility space' concept) seems more feasible. Such approach has been recognized as the most effective and cheapest strategy to promote the creation of new riparian forests, as it resizes rivers to their new hydrologic situation and allows them to do the work [START_REF] Middleton | The flood pulse concept in wetland restoration[END_REF]Rood and others 2005;[START_REF] Ollero | Channel adjustments, floodplain changes and riparian ecosystems of the Middle Ebro River: assessment and management[END_REF]Stromberg and others 2007). The implementation of this strategy might include some of the following measures: removal and set back of flood defence structures; recovery of agricultural lands which are no longer profitable; reconversion of poplar crops (*50 ha in the 10-year floodplain in 2003) to natural floodplain after harvest; lowering floodplain heights to improve the erosive capacity of floods and in-channel reallocation of extracted sediments to facilitate the creation of nursery sites; locally controlled flooding to promote regeneration of desirable tree species, especially P. nigra, S. alba, Tamarix spp. and P. alba, preceded by mechanical disturbance of the substrate and removal of ruderal vegetation in stabilized sites; and prohibition of grazing in potential nursery sites.

In case of economic shortage, these actions should be priorized over the maintenance of the existing senescent forests (those that increased during the stabilization period) although, meanwhile, drops in water table levels and the duration of low-water periods should be controlled to minimize the high canopy dieback and mortality observed in non-pioneer forests. A similar forest management strategy should be applied to other Mediterranean watersheds with hydrogeomorphic constraints similar to those of the Middle Ebro River.

Fig. 1

 1 Fig. 1 Localization of the study area. The grey zone represents the area flooded during the 10-year flood of February 2003. Dotted white lines are flood defence structures

Fig. 3

 3 Fig.3Localization of the study sites within the Natural Reserve of the Alfranca Galachos, Middle Ebro River (NE Spain). Rectangular sampled plots are shown in black. White, grey and black labels indicate young (colonized after 1981 and numbered from 1 to 13), mature (colonized after 1957 and numbered from 14 to 26) and old forest plots (colonized before 1957 and numbered from 27 to 39), respectively. The location of the five aerial images is represented in Fig.1and denoted by uppercase letters. The aerial photo was taken in 2003

Fig. 4

 4 Fig. 4 Historical evolution of the 10-year recurrence interval floodplain in 2003 (2,230 ha) during the twentieth century in the Natural Reserve of the Alfranca Galachos, Middle Ebro River (NE Spain)

Fig. 5

 5 Fig. 5 Stem density along the chronosequence with young (tree colonization after 1981), mature (tree colonization after 1957) and old (tree colonization before 1957) forest types. For each tree species: the bars represent stem density in each plot (denoted in the X axis), numbers indicate the mean live stem density (n = 13); percentage (in

Fig. 6

 6 Fig. 6 Size class distribution along the chronosequence with young, mature and old forest types. For each species, the bars represent the

Fig. 7

 7 Fig.7Canopy dieback along the chronosequence with young, mature and old forest types. For each species: bars represent the 100% of live adults in each plot (denoted in X axis); numbers represent the mean proportion of live adults exhibiting canopy dieback (grey) and severe canopy dieback (black). For each forest type and species:

Table 1

 1 Largest dams currently operating in the EbroRiver Basin upstream of the study area (Natural Reserve of the Alfranca Galachos, 41°36 0 N, 0°46 0 W)

		Capacity (hm 3 )	River	Distance from	Year of completion
				study area (km)
	Ebro Dam	540	Ebro	350	1952
	Yesa Dam	447	Arago ´n	115	1959
	Sotonera Dam	189	Soto ´n-Ga ´llego	65	1963
	Tranquera Dam	84	Piedra	165	1959
	Mansilla Dam	68	Najerilla	190	1960

Table 3

 3 Floodplain area (ha)

	occupied by the different		Floodplain area (ha)
	ecotopes within the 10-year		1927	1957	1981	2003
	recurrence interval floodplain
	in 2003	Open water	194	170	171	135
		Barren sites	254	167	77	43
		Non-woody vegetation	157	114	40	65
		Anthropic	1,125	1,441	1,654	1,627
		Natural forests	500 (100%)	338 (100%)	288 (100%)	360 (100%)
		Pioneer	0	174 (52%)	188 (65%)	110 (31%) a
		Non-pioneer	0	126 (37%)	100 (35%)	250 (69%) b
	a Young forests b Mature ? old forests	Undated Total	500 (100%) 2,230	38 (11%) 2,230	0 2,230	0 2,230

Acknowledgments The authors thank A Frutos, M Gargallo, L Gonza ´lez, D Jime ´nez and T Pascual for their field assistance. We also express our appreciation to Prof. CS Crawford and two anonymous reviewers who provided helpful comments on the manuscript drafts. This research was funded by the Department of the Environmental Science, Technology and University, Aragon Government (Research group E-61 on Ecological Restoration) and the Ministry of Science and Innovation of Spain, MICINN (CGL2008-05153-C02-01/BOS). The first author was granted by the Ministry of Education and Science of Spain, MEC (FPU program).