IntroductionTop

Episodes of drought-induced tree mortality have been recently observed worldwide (Allen et al., 2010). Under a climate change scenario, those effects may boost potential vegetation changes over large geographical areas, with major impacts on forests diversity and ecosystem function (Carnicer et al., 2011). Declination has also been reported in oak forests (Haavik et al., 2015), including the Persian oak forests (Quercus brantii Lindl. var. persica (Jaub & Spach) Zohary) in Zagros Mountains (Fatahi, 1995). Persian oak covers more than half of the Zagros forest area (west Iran), representing the most important tree species of this region (Bordbar et al., 2010; Hassanzad-Navroodi et al., 2015). These forests support valuable ecological and economic resources, as for instance the use of seeds in traditional medicine, fuel wood, charcoal, and timber hardwood (Fatahi, 1995). As a consequence, conservation of Persian oak forests is an impending management concern, currently challenged by drought-induced tree mortality and insect outbreaks.

Oak decline is a disease complex that involves the interaction of several biotic and abiotic factors (see Manion, 1991). The effects of decline on oak forests represent one of the most serious forest disease issues, with impacts that range from partial crown dieback to tree death (Starkey & Oak, 1989; Brasier, 1996; Rizzo & Garbelotto, 2003; Lloret et al., 2004; Heitzman et al., 2007; Fan et al., 2008). Due to the increasing risks (beetles attacks, root fungi, drought events, etc.,), forest owners and stakeholders require new adaptation guidelines to increase the resilience of those oak forests subjected to potential decline (Cescatti & Piutti, 1998; McEwan et al., 2011; Haavik et al., 2015).

Tree mortality drives the functional and structural dynamics of forest ecosystems, both as a sink/source of carbon and nutrients, and as a mechanism of forest structure and diversity change (Franklin et al., 1987; Allen & Breshears, 1998). Understanding tree mortality patterns is crucial to understand current forest community composition and to predict changes in stand structure and species composition (Chapman et al., 2006; Heitzman et al., 2007; Galiano et al., 2010; Carnicer et al., 2011; Lechuga et al., 2017). At a regional scale, tree mortality may be mainly influenced by climate, for instance extreme events, such as drought and high temperatures (Anderegg et al., 2012). Tree mortality can occur across a wide range of spatial and temporal scales, from the gradual death of individual trees (Ogaya & Peñuelas, 2007; Camarero et al., 2016) to the abrupt mortality of thousands of trees over large areas due to severe disturbance events (Allen et al., 2010).

As regards the need to improve our understanding of forest response to the current climate change, it might be of great importance to investigate site and stand structure effects, buffering or enhancing decline process of forests decline (Heitzman et al., 2007; Camarero et al., 2016; Colangelo et al., 2017a). As regards the specific case of oak trees, water deficit is the most common stressing factor related to physiological weakness (Jenkins & Pallardy, 1995; Lloret et al., 2004; Ogaya & Peñuelas, 2007; Fan et al., 2008; Haavik et al., 2015), triggering episodic tree declines and mortality (Fan et al., 2012; Keyser & Brown, 2016; Sánchez-Salguero et al., 2017). Furthermore, following drought, other events, such as beetle outbreaks, affect mortality of oak trees or increase its severity (Kabrick et al., 2008; Fan et al., 2008; Hosseini, 2012). As a result, mortality events are usually associated with complex interactions among endogenous factors, such as human use-related stand characteristics and genetics, and exogenous factors that include site conditions, insects and pathogens (Heitzman et al., 2007; Urbieta et al., 2008; McEwan et al., 2011; Haavik et al., 2015).

The effects of drought are more common visualized at the regional-scale (Keyser & Brown, 2016; Sánchez-Salguero et al., 2017), but its influence on crown dieback and tree death will be modulated at the local-scale, where factors such as topography, soil and stand structure might be as important as regional climate to understand oak forests dynamics (Jenkins & Pallardy, 1995; Chapman et al., 2006; Gea-Izquierdo et al., 2009; Galiano et al., 2010). Topographic characteristics such as slope and aspect also strongly influence soil moisture, and therefore drought-induced tree mortality may vary accordingly (Das et al., 2008). Consequently, spatial and temporal variation in site moisture conditions may influence the spatial pattern and severity of drought-induced forest decline, while tree mortality patterns at local scale are very difficult to forecast (Das et al., 2008; Anderegg et al., 2012).

Tree decline has been related to stand structure, otherwise supporting that tree response to water stress also relies on tree-to-tree competition (Das et al., 2011; Lechuga et al., 2017). Episodic tree mortality is usually related to dry site conditions and high stand density (Chapman et al., 2006; Gea-Izquierdo et al., 2009). Specifically, trees subjected to higher competition show lower radial growth and they are more prone to die following extreme drought events (Das et al., 2008; Galiano et al., 2010; Linares et al., 2010; Colangelo et al., 2017b). As a result, contrasting stand structure may act modulating the individual tree responses to drought (Lechuga et al., 2017). Persian oak forests display a wide range of stand structural heterogeneity (Erfanifard et al., 2009), which might be, at least in part, due to contrasting land use practices (Fatahi, 1995; Urbieta et al., 2008). Hence, understanding the effects of drought and tree mortality must take into account stand structure in a spatially explicit context (Das et al., 2008).

Extensive oak mortality is a significant threat to Zagros forests health and economic value of their inhabitant. In this study, we attempt to investigate recent climate trends and the effect of topography, soil, stand structure and tree-to-tree competition on widespread tree mortality in Zagros forests in west of Iran. Specifically we aim to (1) quantify the extent to that recent drought events support a long-term increasing aridity at regional scale; (2) identify stands that are at high risk for oak decline, as regards site conditions (elevation, aspect, slope, soil); and (3) identify the mortality pattern for individual trees within declining stands, according to individual characteristics (size, coppice, standard, etc.) and tree-to-tree competition.

Material and methodsTop

Study area

The study area is located in the Zagros Range, southwestern Iran; 36°.31' N, 51°.45' E (Fig. 1). The region is mainly affected by westerly disturbances and the Azores High during the cold (November–March) and warm (May–September) season, respectively, resulting in a clear distinction between a wet winter and a dry summer (Asakereh, 2007; Azizi et al., 2013). Precipitation occurs during an eight month period from previous October to current May with a maximum during December to March. During June to September, almost no effective precipitation occurs. The mean annual temperature of the region is 16 °C, and the mean annual precipitation is 509 mm (Azizi et al., 2013). Meteorological data for our study were available from the climate station of Ilam (33°38'N, 46°26'E; 1337 m a.s.l., about 10 km apart from the study area), covering the time span 1986–2010. Total annual precipitation and dust events (number of days with dust) were investigated. In addition of this local climate dataset, to obtain a long-term regional climate dataset, we analyzed mean annual temperature, total annual precipitation and Palmer Drought Severity Index (PDSI), obtained from the KNMI Climate Explorer web site for the period 1901-2015. We used CRU TS3.24 dataset (http://climexp.knmi.nl/select.cgi?id=someone@somewhere). Annual trends were statistically tested by regression analysis.

Figure 1. Location of the study area in the central Zagros range, SW Iran (a). Spatial distribution of the topographic units (b) obtained by overlapping digital layers of aspect, slope, and elevation (see also Table S1 [suppl.]).

Field sampling methods

The study area is mainly comprised by forests dominated by Quercus brantii var. persica Lindl., Pistacia atlantica Desf., Acer monspessulanum subsp. cinerascens (Boiss.) Yalt., Crataegus pontica C. Koch, Amygdalus orientalis L., and Cerasus microcarpa C.A. Mey. Boiss. These mixed oak forests grow on contrasting aspects, slopes, and elevations, ranging from 1500 to 2000 m a.s.l. (Fatahi, 1995). The limits of the study area were determined on a topographic map with a scale 1:50000, to account for a wide range of environmental variables, and contrasting forest stand structures and mortality. Geographic information system analyses were performed by using ArcGIS 9 ArcMap version 9.2 (ESRI, 2006) to investigate digital layers of slope, aspect and elevation. Aspect data were grouped within four categorical factors: N, north; S, south; W, west; and E, east aspect, respectively. Slope data were grouped within three categorical factors: 0-30%, 30-60%, > 60%. Elevation data were grouped within two categorical factors: 1500-1700 and 1700-2000 m a.s.l. The obtained categorical factors were overlapped, accounting for 24 combinations of topographic units (TUs; 3 slopes Х 4 aspects Х 2 elevation categories, respectively), however only 20 combinations of TUs were suitable for further field sampling (Fig. 1; Table S1 [suppl.]).

Each TU was sampled in the field by mean of three circular plots, 1000 m2 surface, randomly established (Fig. 2). Within each plot, site characteristics (slope, aspect, elevation) were measured. We performed a soil profile per TU to measure soil properties. Soil depth was measured in the field, while physical and chemical soil properties were measured in the laboratory using a soil sample per TU (Sparks et al., 1996). We determined texture and soil moisture, total nitrogen percentage (N), organic carbon percentage (OC), organic matter percentage (OM), and total neutralizable material percentage (TNV, CaCO3).

Figure 2. Field sampling design at each topographic unit. The competition intensity (CI) experienced by the focal i tree was calculated as the sum of the quotients between the ratio of the diameter at 1.3 m from the ground (DBHj/ DBHi) for all j neighbouring trees surrounding the focal i tree, and the distance between the i and the corresponding j trees (distij).

In each plot, we recorded all tree and shrub species and measured its diameter at 1.3 m from the ground (DBH) for all trees above 5 cm DBH, maximum and minimum crown diameter, crown dieback percentage, and mortality density. Tree habit (coppice or standard) was also noted (coppice trees are considered those originated by new growth from the stump or roots after cutting), using for coppices equivalent diameter estimation (Grier et al., 1992):

where RCDi is the root collar diameter of each of the individual i stems.

Tree-to-tree competition and crown dieback were assessed in each TU by sampling six transects 100 m length (Fig. 2). We sampled five points at 25 m intervals on each transect. In each point, the closest live and dead trees (focal trees), as well as their neighborhoods trees, were characterized as indicated in Fig. 2. We estimated the tree-to-tree competition intensity (CI, Fig. 2) that each focal tree was subjected to by calculating a distance-dependent competition index, which takes into account the number, size and distance to the neighbouring competitors (Hegyi, 1974). The degree of competition experienced by the focal i tree was calculated as the sum of the quotients, for all j neighbouring trees surrounding it within a radius R of 8 m, between the ratio DBHj/DBHi and the distance between the i and the corresponding j trees (distij) (see also Fig. 2):

The condition of tree crowns is also an important indicator of tree and forest health (Kabrick et al., 2008). Thus, crown conditions were evaluated using a crown dieback classification for each tree, conducted as follows (Fig. 2): (i) healthy, if the canopy defoliation and browning were less than 5% of the crown length; (ii) weak, if the canopy damage were between 5 to 33% of the crown length; (iii) moderate, if canopy damage symptoms were between 34-66% crown length; and (iv) severe, if canopy damage symptoms were more than 66% crown length (Kabrick et al., 2008; see also Fig. 2).

Data analysis

The Kolmogorov-Smirnov and Levene tests were used to assess normality and homoscedasticity, respectively. Univariate relationships were modelled by linear, polynomial and exponential regressions. We used one-way ANOVA, Duncan and paired t-tests to perform multiple and paired means comparisons. Finally, a backward multiple regression models were performed to investigate the relationships between mortality and site (topography and soil variables) and stands structure characteristics. Total variance explained (R2 adjusted) and coefficients were computed separately for topographical, soil-related, and stand structure variables. Statistical analyses were carried out with the package Minitab Stat. Softw. v. 15 (Minitab, PA, USA).

ResultsTop

Climate trends

Long-term regional climate dataset showed a significant rise trend in mean annual temperature (R2 = 0.49, p<0.0001; Fig. 3a), while total annual precipitation (Fig. 3a), and PDSI (Fig. 3b) showed no significant trends for the period 1901-2015. Meteorological data obtained from the climate station of Ilam (about 10 km apart from the study area; time span 1986–2010) showed a significant decline in total annual precipitation (R2 = 0.30, p<0.01; Fig. 3c), with extreme drought events in 1999, 2007 and 2008. Moreover, dust events showed a significant exponential trends (R2 = 0.62, p<0.0001; Fig. 3c), with increasing number of days with dust mainly from the year 2000 onward.

Forest structure and decline patterns

The study area ranges from 1510 to 1880 m elevation. Soil samples texture was mainly clay (Fig. S1 [suppl.]), with mean values of total organic carbon and nitrogen percentages of 1.66% and 0.17%, respectively, while neutralizable material percentage was on average 43.6%. Persian oak is the dominant species within the study area, accounting for 95.3% of the total tree density and 93.6% of the total basal area (Table S2 [suppl.]). Crataegus pontica and Pistacia atlantica were the second and third most abundant tree species; the relative contribution of P. atlantica to stand basal area was higher, than that of C. pontica. Acer cinerascens showed the lowest stand density and basal area among trees as well as the highest mortality rate (48%), while Amygdalus orientalis and Cerasus microcarpa were minor components among the shrub strata (Table S3 [suppl.]). The average stand canopy cover was 32.5%, the majority of which belongs to Q. persica (31.5%). Many trees in the study area (especially Q. persica) are sprouts of coppices. Mortality was significantly higher for coppices, expressed as tree density: 23.83 trees/ha vs. 11.5 trees/ha, for coppices and standard respectively (t-test, p=0.002; Table 1). Nonetheless, given that total density of coppices was also higher, expressed as percentage, mortality rate was higher among the standard growth form (Table 1), however, this difference on mortality percentage was not significant (t-test, p=0.106).

Table 1. Stand density, basal area and canopy cover of coppices and standard grow forms.

The most frequent tree diameters were those among 15-25 cm DBH classes (Fig. 4a), as well as the most frequents tree sizes of dead trees (Fig. 4b), nonetheless, basal area percentage of dead trees was higher among tree diameters belonging to 25 and 30 cm DBH classes (Fig. 4c). The mean DBH decreased, while stand mortality increased, as stand density becomes higher (Fig. 5a; Table S4 [suppl.]). The competition index (CI) of alive trees increased significantly according to stand density (Fig. 5b; p<0.02), while the CI of the dead trees was significantly higher than that of the alive trees (within plots) but was not related to stand density (among plots; Fig. 5b, see also Tables S5 and S6 [suppl.]).

Crown dieback was also significantly related to stand density, similar to mortality did; thus, moderate and severely defoliated trees increasing as stand density was higher. As regard environmental variables, total stand density was positively correlated to elevation (Fig. S2 [suppl.]). Nonetheless, expressed as percentage, higher elevation stands showed the lower fraction of healthy trees, as well as the higher fraction of trees with crown damages (Fig. 6). However, mortality rate (i.e., expressed as percentage) was only marginally significant regarding elevation, supporting that the main effect relies on stand density (Fig. 6; Fig. S2 [suppl.]). This result was also supported by multiple regression analyses (Table 2), where mortality percentage was significantly related to aspect (higher mortality percentage at southern and western aspects), but did not showed significant relationship with elevation or slope. According to soil variables, mortality percentage was higher on shallower soils, while regarding stand structural variables, total basal area showed a positive relationship (and negative for mean DBH), indicating that mature stands, with higher mean DBH and lower basal area, show lower mortality rates. On the other hand, canopy cover showed a negative relationships, i.e. higher canopy cover is related to lower mortality percentage, likely reflecting the covariance of defoliation and mortality (Table 2).

Table 2. Results of multiple regression analysis using the percentage of dead trees as response variable. Total variance explained (R²) and coefficients were computed separately for topographical, soil-related, and stand structure variables. SD indicates the standard deviation. The multiple regression T statistic and p values are also showed.

Discussion Top

Climate trends and likely influence on Persian oak decline and mortality

Rising temperatures are amplifying drought-induced stress and mortality in forests globally (Allen et al., 2010). For the Zagros range, precipitation indices have fewer significant trends in the decrease of amount, frequency, and intensity of precipitation when compared with temperature (Fig. 3). Based on tree-rings width linear regression model, October–May precipitation has been reconstructed for the central Zagros region over the last 170 (1840–2010) years (Rahimzadeh et al., 2009). This study revealed that severe dry years occurred in 1847, 1853–55, 1870–71, 1904, 1910, 1918, 1929, 1932, 1944, 1948, 1951, 1960, 1964–65, 1984, 1999 and 2008–2009. Anyway, the number and the intensity of dry periods seem to have increased during the last 170 years (Azizi et al., 2013). Despite the limitation of instrumental records and the low number of meteorological stations in our study area, available information supports that precipitation has reduced significantly at regional scale during recent decades (Asakereh, 2007; Rahimzadeh et al., 2009).

At regional scale, the spatial and temporal patterns of climate extreme indices in the Zagros range support a warming trend over the period 1975–2010 (Soltani et al., 2015). Over the last 15 years (1995–2010), the annual frequency of warm days and nights has increased by 12 and 14 days/decade, respectively. The number of cold days and nights has decreased by 4 and 3 days/decade, respectively. The annual mean maximum and minimum temperatures averaged across Iran both increased by 0.031 and 0.059 °C/decade. The probability of cold nights has decreased from more than 20% in 1975–1986 to less than 15% in 1999–2010, whereas the mean frequency of warm days has increased between the first 12-year period (1975–1986) and the recent 12-year period (1999–2010) from 18 to 40%, respectively (Soltani et al., 2015).

Nonetheless, the same spatio-temporal study revealed that there are no systematic regional trends in total precipitation, nor in the frequency and duration of extreme precipitation events (Soltani et al., 2015, and references therein). Indeed, statistically significant trends in extreme precipitation events have been observed at less than 15% of the investigated weather stations, with no spatially coherent pattern of change, whereas statistically significant changes in extreme temperature events have occurred at more than 85% of the investigated weather stations. Notwithstanding, it has been noted an increasing trend of warm extremes with elevation, suggesting a higher impact of the warming trend in the mountains. Specifically, the trend in maximum temperature (see details in Soltani et al., 2015) shows positive correlation with elevation in the Zagros mountain range. This observation may be related to the increasing trend of crown dieback (Fig. 6) and mortality at higher elevation found in our study, although, the relationships between climate extremes and elevation are not quite clear. Furthermore, our understanding of the influence of drought on mortality remains limited as they are the result of multiple years of prolonged drought.

Long-term climate forecasts for the Zagros range indicate warming temperatures (Christensen et al., 2007). Coupled with this, the severe drought years recently occurred and their incidence on tree mortality may have profound implications for carbon storage and ecosystem services (Carnicer et al., 2011). Our results suggest that Persian oak is sensitive in terms of crown defoliation to warm and dry conditions, as well as they have been found for other mediterranean oaks, like Q. faginea, Q. Ilex and Q. suber (Sánchez-Salguero et al., 2017). Warm spring conditions and severe summer drought have been already recognised as triggers of crown defoliation, whereas growth of oaks in Mediterranean environments is linked to late spring-early summer water availability, at both annual and decadal timescales, suggesting oak growth decline was associated with a delayed response to climate (Di Filippo et al., 2010; Natalini et al., 2016).

The significant trend observed in dust events also suggests a regional forest decline, despite the limited time span of the available dataset (Fig. 3c). Rising levels of dust deflation may be related to tree mortality and subsequent reductions in vegetation density (Engelstaedter et al., 2003). Regional studies support that forest cover and soil moisture are important controls on dust emission, as atmospheric dust frequency is inversely correlated with leaf area index (i.e., vegetation density) and net primary productivity (Tegen et al., 2002). Forest stands supporting relatively high biomass and vegetation cover protect the surface from deflation, while the presence of healthy trees results in a high surface roughness that reduces surface wind energy and therefore also dust emissions. In contrast, extensive tree decline and mortality led to sparser vegetation and more bare soil (Allen & Breshears, 1998; Engelstaedter et al., 2003).

Site factors modulating Persian oak decline and mortality

The extent to which site factors such as topography and aspect influence the severity Persian oak decline is poorly understood. Several researches performed on different oak forests have reported that shallow soils and/or dry aspects account for the greatest amount of oak decline (Starkey & Oak, 1989; Rizzo & Garbelotto, 2003; Heitzman et al., 2007; Fan et al., 2008; Colangelo et al., 2017a). Trees growing in shallower and poorer soils appear to persist close to their limits of climatic tolerance, while populations in wetter and fertile soils sites may have larger physiological buffers (Johnson et al., 2016). Shallow soils are frequent at higher elevations, likely affecting the obtained spatial patterns of tree mortality. Drought effect is enhanced by lower water availability and limited rooting depth, as may occur in clay soils (Fig. S1 [suppl.]), enhancing drought sensitivity of trees (Johnson et al., 2016). Despite in our study area mortality was inversely related to soil deep (Table 2), there were not consistent patterns regarding soil texture or the amount of organic material and nitrogen. These results suggest that factors other than (or perhaps in addition to) soil properties, topography and aspect, such as species composition, tree age and size structure, and competition, are important determinants of oak decline, likely confounding climate- and site-related influences (Ogaya & Peñuelas, 2007; Bordbar et al., 2010; Lechuga et al., 2017).

Persian oak decline likely involves the interaction of multiple biotic and abiotic factors, with impacts that range from partial crown dieback to tree death. Such decline complex may be framed in terms of predisposing factors, inciting factors, and contributing factors (sensu Manion, 1991). Some suggested predisposing factors include high density of lower-size DBH classes, shallow and rocky soils (Table 2). As regards the inciting factors, it is likely that regional drought spells are related to oak decline (Jenkins & Pallardy, 1995; Fan et al., 2012; Keyser & Brown, 2016), while contributing factors may include different oak borers and diseases (Haavik et al., 2015).

An important indicator of the health of a tree is the condition of its crown (Rizzo & Garbelotto, 2003; Lloret et al., 2004; Ogaya & Peñuelas, 2007). Declining trees are initially point out by foliage wilt and browning followed by progressive branch dieback (Starkey & Oak, 1989). Trees with vigorous, healthy crowns tend to have higher growthrates. By contrast, trees with damaged crowns have a reduced capacity for photosynthesis (Brasier, 1996). Many stressors have been related with crown dieback including site factors and tree-to-tree competition (Heitzman et al., 2007; Camarero et al., 2016; Colangelo et al., 2017a). In our study, elevation showed a significant relationship with crown dieback (Fig. 6), nonetheless, expressed as percentage, mortality rate was not related to elevation, supporting that the main effect relies on stand density.

Competition increases Persian oak decline and mortality

Forest dynamics encompass changes in stand structure, species composition, and species interactions with disturbance and environment over a range of spatial and temporal scales (Kabrick et al., 2008; McEwan et al., 2011). Forest structure modifies the effect of regional climate on drought-induced forest mortality, as individual trees respond to climate and resource limitation differently depending on their competitive environment (Heitzman et al., 2007; Clark et al., 2016; Lechuga et al., 2017). Higher levels of competition within a forest stand can increase mortality probability, interacting with the effects of drought on mortality, particularly where water is a limiting resource (Voelker et al., 2008; Ruiz-Benito et al., 2013).

Forest structure mediates the effect of drought on oak forest dynamics at several scales (Clark et al., 2016; Colangelo et al., 2017b). Indeed, recruitment patterns and mortality in several oak species seem to be related to canopy closure (Gómez-Aparicio et al., 2008). Oak seedling survival and growth in Mediterranean forests rely significantly on stand structure, providing crucial implications for regeneration in current and future environmental scenarios (Espelta et al., 1995; Pausas et al., 2009; Sheffer et al., 2013; Pérez-Ramos et al., 2013). Furthermore, as regards the effects of pathogens, infestation may be related to structural variables (Sangüesa-Barreda et al., 2015), usually providing support to the hypothesis of increasing mortality in denser stands. Trees subjected to high competition, usually within high density stands, respond to similar climatic factors than those subjected to low competition, but their response is generally weaker (Gea-Izquierdo et al., 2009). Some oak species have shown an increasing sensitivity to climate in recent decades, which might be related to temperature rise (Di Filippo et al., 2010; Carnicer et al., 2011; Natalini et al., 2016). At this regional scale, the influence of average climate, competition, and their interaction on tree mortality during drought was supported by our study, where tree mortality occurred mainly in denser stand and affected significantly to those trees subjected to higher competition (Fig. 5).

Drought events often impact forests across large geographic areas that have substantial spatial variation in average climate and competitive environments (Jenkins & Pallardy, 1995; Chapman et al., 2006; Lechuga et al., 2017). Persian oak forests display a wide range of stand structural heterogeneity (Erfanifard et al., 2009), likely reflecting contrasting land use practices (Urbieta et al., 2008). Dead Persian oak trees occurred over a wide range of tree DBH (Fig. 4b), but they was most conspicuous among trees 15–25 cm. A similar pattern in oak forest decline was observed in North America (Kabrick et al., 2008; Heitzman et al., 2007; Haavik et al., 2015). Although no age data were collected in our study, it is likely that many small Persian oak trees located at higher elevations were about the same age. These high-elevation stands show the higher density, supporting the hypothesis that episodic tree mortality is related to dry site conditions, here likely relate to warming and drought events (Ogaya & Peñuelas, 2007; Soltani et al., 2015), and high stand density (Chapman et al., 2006; Gea-Izquierdo et al., 2009; Linares et al., 2010; Lechuga et al., 2017).

Many Persian oak forests in the Zagros range originated after timber harvests and pruning (Fatahi, 1995), as support the density of coppices. In the resulting even-aged stands, Persian oak can persist for extended periods as small trees in lower canopy positions (Shakeri et al., 2009). Notwithstanding, such suppressed and presumably older stems, growing as coppices, might be particularly vulnerable to decline (Hamzehpour et al., 2011). Specifically, these trees subjected to higher competition show lower radial growth and they are more prone to die following extreme drought events (Franklin et al., 1987; Das et al., 2008, 2011; Colangelo et al., 2017b). Greater mortality in coppice oaks could be related with the abandonment of stems harvest at earlier age, or with the undone reduction of the number of stems of each coppice, both management practices that could reduce stand-level decline and mortality (Di Filippo et al., 2010). Furthermore, stressed, low vigor oaks are especially susceptible to attack by a variety of organisms (Kabrick et al., 2008; Fan et al., 2008; Sangüesa-Barreda et al., 2015).

Concluding remarks

The magnitude and spatial distribution of mortality indicate that Persian oak decline is a landscape phenomenon. Based on previous oak decline events investigated worldwide, it is likely that Persian oak will remain an important forest component of the Zagros range at the regional scale despite extensive mortality. Over time, however, it is unclear how various levels of oak decline will affect forest structure, species composition, and regeneration dynamics at the local scale, particularly in areas exhibiting high levels of mortality. The consequences of climatic change for Persian oak dynamics and distribution need to be closely monitored, particularly in water-limited sites and degraded soils like those found in many locations along the Zagros range.

This study also highlights the importance of monitoring shifts in rainfall patterns and increasing temperatures, associated with climate change. Such changes might likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. Understanding forest responses to this extreme event is useful to adapt forest management, expecting for the impacts of climate change. The identification of stands prone to be affected by high tree mortality allows management efforts to be focused on higher vulnerability areas. Forest decline episodes as reported here may lead to the reordering of dominance between species within communities, which may persist if extreme events become more frequent. Management should adapt to this climatic variability, through stand competition management and promoting the establishment of more adapted species to the expected climatic scenarios, while ahead research is still required to properly address these important issues.

AcknowledgmentsTop

We thank the Handling Editor and two anonymous reviewers whose throughout revision and comments greatly helped to improve a previous version of the manuscript.