Physiological responses of cork oak and holm oak to infection by fungal pathogens involved in oak decline

The aim of this research was to study the changes in net photosynthesis and stomatal conductance values in 3‐year‐old cork oak and holm oak seedlings growing in natural conditions and inoculated with Apiognomonia quercina, Biscogniauxia mediterranea, Botryosphaeria corticola and Pleurophoma cava. Throughout the 4‐month experimental period, the evolution of visual external symptoms and the values of physiological variables were periodically recorded. All pathogens caused stem lesions around the infection point; however, the lesions caused by B. corticola were longer in both oak species. On cork oak seedlings, all pathogens induced a significant and gradual reduction in net photosynthesis and stomatal conductance values, whereas other physiological disturbances were induced only by B. corticola infections on holm oak seedlings.     

Pathways for resilience in Mediterranean cork oak land use systems

Context

Loss of woodlands and degradation of vegetation and soil have been described for all Mediterranean-type ecosystems worldwide. In the Western Iberian Peninsula, overexploitation of evergreen cork oak land use systems has led to soil erosion, failures in oak recruitment, and loss of forests. Degraded and dry sites are quickly colonised by pioneer heathland rockrose (Cistus spp.) shrubs forming highly persistent patches.

Aims

Although traditionally shrublands have been considered as a transient successional state, we present evidence that they can represent persistent alternative states to former cork oak forests.

Review trends and conclusions

We first describe how Mediterranean vegetation evolved in the Iberian Peninsula and the role of fire and long-term human management as main disturbances. We then discuss alternative pathways through state-and-transition models indicating the ecological and land use variables that halt cork oak regeneration and recruitment and drive vegetation transitions towards persistent shrublands. Unless concerted management actions and restoration programmes are undertaken, the cork oak land use systems will not be sustainable.     

Chronic cork oak decline and water status: new insights

Chronic decline and Sudden death are two syndromes of cork oak (Quercus suber) dieback. Mortality is associated with water stress, but underlying physiological mechanisms are poorly understood. Here, we investigated the physiological performance of declining trees during the summer drought. Leaf water potential, gas-exchange, fluorescence of photosystem II and leaf and root starch concentration were compared in healthy (asymptomatic) and declining trees. Low annual cork increment in declining trees indicated tree decline for several years. All trees showed similar water status in spring. In summer, declining trees showed lower predawn leaf water potential (?2.0 vs. ?0.8 MPa), but unexpectedly higher midday leaf water potential than healthy trees (?2.8 vs. ?3.3 MPa). The higher midday water potential was linked to by means of strongly reduced stomatal conductance and, consequently, transpiration. This study is pioneer showing that declining trees had high midday water potential. A tendency for lower sap flow driving force (the difference between predawn and midday water potential) in declining trees was also associated with reduced photosynthesis, suggesting that chronic dieback may be associated with low carbon uptake. However, starch in roots and leaves was very low and not correlated to the health status of trees. Declining trees showed lower water-use efficiency and non-photochemical quenching in summer, indicating less resistance to drought. Contrarily to chronic decline, one tree that underwent sudden death presented predawn leaf water potential below the cavitation threshold.     

Long-term understory recovery after mechanical fuel reduction in Mediterranean cork oak forests

In the Euro-Mediterranean region, mechanical fuel reduction is increasingly used in response to the mounting occurrence of catastrophic wildfires, yet their long-term ecological effects are poorly understood. Although Mediterranean vegetation is resilient to a range of disturbances, it is possible that widespread fuel management at short intervals may threaten forest structural complexity and the persistence of some plant species and functional types, with overall negative consequences for biodiversity. We used a chronosequence approach to infer woody vegetation changes in the first 70 years after understory clearing in upland cork oak (Quercus suber) forests, and to assess how these are affected by treatment frequency. Across the chronosequence there was a shift between plant communities with contrasting composition, structure and functional organization. Understory cover increased quickly after disturbance and a community dominated by pioneer seeder and dry-fruited shrubs (Cistus ladanifer, C. populifolius, Genista triacanthos, and Lavandula stoechas) developed during about 15 years, but this was slowly replaced by a community dominated by resprouters and fleshy-fruited species (Arbutus unedo, Erica arborea) >40 years after disturbance. During the first 15 years there were rapid increases in woody species richness, vertical structural diversity, cover by Q. suber juveniles and saplings, and shrub cover at <1.5 m strata, which levelled off or slightly declined thereafter. In contrast, tree species richness, tree density and density of arboreal A. unedo and E. arborea, vertical structural evenness, and cover at >1.5 m strata increased slowly for >50 years. Treatment frequency showed strongly negative relationships with species richness, structural diversity and evenness, and horizontal and vertical understory cover, particularly that of slowly recovering species. These findings suggest that fuel reduction programs involving widespread and recurrent understory clearing may lead to the elimination at the landscape scale of stands with complex multi-layered understory occupied by large resprouters and fleshy-fruited species, which take a long time to recover after disturbance. Fuel management programs thus need to balance the dual goals of fire hazard reduction and biodiversity conservation, recognizing the value of stands untreated for >50 years to retain ecological heterogeneity in Mediterranean forest landscapes.     

Conservation of Mediterranean oak woodlands: understorey dynamics under different shrub management

The effect of experimental disturbances on the dynamics of a shrub community was studied on a ‘Montado’ ecosystem, in southern Portugal. The evolution of the community physiognomy, composition and diversity were monitored after shrub clearing followed by biomass removal, deposition on soil surface and incorporation with the soil, over a 9-year period. Maximum shrub density was recorded in the first year after the disturbances, excepting in mulched plots which showed the greatest number of individuals 1 year later. The increment of shrub leaf biomass was very fast in the first 3 years, whereas wood production was slower but occurred along the whole study period. At the end of the study, leaf and wood biomass was still significantly lower than in the pre-disturbance situation. The variation pattern of leaf area index was similar to that of leaf biomass. The evolution of total plant cover and diversity was similar across treatments. The highest species richness and diversity were recorded 2 years after cutting, decreasing afterwards with the increasing dominance of shrubs. Thus it seems likely that, although a 9 year period is too short for these communities to reach steady equilibrium, they are very resistant and resilient to disturbances, as regeneration was fast and vegetation dynamics was not influenced by differences among treatments. We can conclude that shrub clearing promotes biodiversity and the time of permanence of shrub patches depends on the particular goal we want to achieve.     

Morphological evaluation of cork oak (Quercus suber): Mediterranean provenance variability in Tunisia

Twenty-six provenances (2 340 plants) of cork oak (Quercus suber spp.) originating from Portugal, Spain, Italy, Morocco, Algeria, and Tunisia were tested for genetic variation among and within provenances by growth traits. Seven morphometrical characters were measured in 90 plants from each provenance. Analysis of variance showed highly significant differences for all characters. The phenotypic coefficient of differentiation reached 0.24 for the form and 0.22 for height, thus revealing a strong structuring between the provenances. Comparative study of growth among the provenances revealed more vigorous growth and better survival rate for those from Morocco, Spain, and Portugal, which may constitute better materials for afforestation. Furthermore, this variability appeared to be geographically structured and would be mainly genetically controlled, as cork oak provenances were cultivated under the same environmental conditions. Our results should be helpful for guide forest managers in afforestation.     

Modelling cork oak production in Portugal

The layout of 32 permanent plots in the most important cork production regions of Portugal and the measurement of the most representative tree parameters were performed for statistically sound cork weight modelling. The establishment of cork weight equations is presented for the different cork oak study areas considered alone or grouped according to the most representative tree parameters. For the presented cork weight models was chosen independent variable the total stripping surface (artmax). For the selection criteria five statistic were used, including PRESS, APRESS and Mallows's statistic. The crossvalidation of the best classified models was performed and to discuss the importance of the “study area” factor, a regression analysis with “dummy” variables was performed.     

Temporal effects dominate land use as factors affecting soil nematode communities in Mediterranean oak woodlands

We analysed the soil nematode community within three different montados (agricultural, pastoral and forestry uses), focusing on temporal variation. Nematodes were classified into trophic groups (bacterivores, fungivores, omnivores, predators and plant-parasitic nematodes (PPN)) and we calculated the maturity index for free-living taxa (MI), maturity index for plant-parasitic taxa (PPI) and the nematode channel ratio (NCR). Temporal variations were most evident during winter when there was a rise in the abundance of the five functional groups. Concordantly, there was a simultaneous increase of soil moisture and organic matter, due to litter decomposition. Fungivore abundance was highest in the forest and the temporal occurrence and abundance of many PPN genera was largely determined by land use. Land management was responsible for differences in plant community structure and composition, thus plant diversity increased from the agricultural to the forestry use. Because the montado shows great temporal variability in vegetation structure our results of MI, PPI and PPI/MI ratio explain the significant changes in the nutritional status over time, with the highest values recorded in the spring. NCR is a good indicator of energy efficiency in the soil decomposition process. Its lowest values were attained in the forest, where the slow-growing plant species favoured a lower activity of the bacterial energy channel and a prevalence of the fungal-based decomposition energy channel. Nematode composition reflected plant succession, changes in decomposition in the soil food web and temporal variations in the structure of soil.     

Variables influencing cork thickness in Spanish cork oak forests: A modelling approach

In this study, we evaluate the influence of different variables on cork thickness in cork oak forests. For this purpose, first we fitted a multilevel linear mixed model for predicting average cork thickness, and then identified the explanatory covariates by studying their possible correlation with random effects. The model for predicting average cork thickness is described as a stochastic process, where a fixed, deterministic model, explains the mean value, while unexplained residual variability is described and modelled by including random parameters acting at plot, tree, plot × cork harvest and residual within-tree levels, considering the spatial covariance structure between trees within the same plot. Calibration is carried out by using the best linear unbiased predictor (BLUP) theory. Different alternatives were tested to determine the optimum subsample size which was found to be appropriate at four trees. Finally, the model was applied and its performance in the estimation of cork production was tested and compared with the cork weight model traditionally used in Spain.     

Assessing foraging strategies of herbivores in Mediterranean oak woodlands: a review of key issues and selected methodologies

Montados are agro-silvo-pastoral ecosystems, typical of the Southwest Iberian Peninsula, of high socio-economic and conservation importance, where grazing is a dominant activity. Montados are characterized by an open tree canopy of Quercus sp. and a diverse undercover of shrubs and grasslands that constitute the plant food resources for grazing animals. Plant food resources of Montados are highly variable, both spatially and seasonally, in quantity and quality. Reliable and easy to use methods to monitor grazing are necessary to allow proper understanding of foraging strategies of grazing animals and to set sustainable grazing management. We describe the main characteristics of the plant food resources available for grazing animals, striking its variability, and revise the potential of using N-alkanes and saliva proteome methods to assess foraging strategies in Montados. In a scenario of dynamic multiple choices, we discuss the use of n-alkane methodology for the simultaneous estimation of diet composition and voluntary intake and saliva proteome as a mean of increasing the knowledge on diet adjustments.     

Floristic diversity of valonia oak silvopastoral woodlands in Greece

Valonia oak (Quercus ithaburensis subsp. macrolepis (Kotschy) Hedge and Yaltirik), a deciduous species grown in the xerothermic conditions of the east Mediterranean zone of Europe, forms woodlands of open canopy that permits adequate light to reach the ground thus sustaining an exceptionally rich flora. In Greece, these woodlands are mainly used for livestock grazing and considered important silvopastoral systems. Nowadays, most of them are abandoned and degraded as a result of inappropriate management. For the effective evaluation and sustainable management of these woodlands and the establishment of reliable monitoring systems, a detailed analysis of their plant diversity characteristics across Greece is needed. This paper aims at determining and comparing floristic diversity measures as well as at assessing the impact of human activities on vegetation and floristic diversity of the most characteristic valonia oak silvopastoral woodlands of Greece. It was found that the truncated log-normal model adequately predicts the species abundance data for eleven out of the twelve woodlands. From the statistical comparison of the diversity indices Q-statistic, Berger–Parker dominance index and Shannon-Wiener measure of equitability, three groups of these woodlands can be distinguished (a) the high-richness group of Pentalofos, Lesvos, Lakonia and Thesprotia, (b) the medium-richness group of Kriti Island, Alexandroupoli, Strofylia and Galaxidi, and (c) the low-richness group of Kea Island, Amfilohia, Almyros and Lilaia. However, the Rényi’s diversity ordering diagram showed that, generally, in low levels of entropy inconsistency is the rule and no clear pattern of diversity is extracted reflecting the impact of complex factors. Among them, those related to management seem to mostly determine plant diversity of valonia oak silvopastoral woodlands, with abiotic factors having an occasionally supporting role. Changes of species richness and evenness due to livestock grazing as well as acorn and wood harvesting are further discussed.     

Occurrence of Phytophthora cinnamomi in cork oak forests in Italy

An increasing decline and mortality of cork oak trees have been recently observed in central Italy and Sardinia Island. Following surveys conducted in three declining cork oak forests, a Phytophthora species was consistently isolated from soil samples collected from trees displaying different level of decline. Based on morphological features, growth rates at different temperatures and analysis of DNA sequences of the ITS region, all isolates were identified as Phytophthora cinnamomi Rands. This pathogen caused large brownish lesions on inoculated freshly cut branches of cork oak. It was re‐isolated from all infected tissues. These findings represent the first report of P. cinnamomi on cork oak trees in Italy.     

Etiology of oak decline in Spain

In different areas of Extremadura, Western Spain, soil samples were taken at the bottom of holm oak (Quercus ilex) trees that were showing decline symptoms. Half of each sample was sterilized, and acorns were sown in both sterilized and nonsterilized soil samples. The resulting seedlings were used as baits for the isolation of fungi. Seedlings growing on the natural, nonsterilized substrate were characterized by having a lower vegetative growth than the ones growing on the sterilized soil samples, and most of them died. Phytophthora dnnamomi was consistently isolated from their roots. Fusarium oxysporum was also isolated as well as different species of Pythium, although to a lesser extent. Pathogenicity tests were performed on holm oak seedlings with five different isolates of P. chinnamomi, with F. oxysporum, Pythium and with a mixture of the three fungi. All the inoculated seedlings with P. chinnamomi developed root rot and grew slowly, and 35.7% of them died up to the end of the experiments. P. chinnamomi was consistently isolated from their roots, indicating that this fungus is the causal agent of holm oak decline. However, F. oxysporum caused similar symptoms on oak seedlings as P. chinnamomi, and was isolated also from the roots, although its frequency was lower than that of. P. cinnamomi.     

Mediterranean cork oak wooded grasslands: synergies and trade-offs between plant diversity,pasture production and soil carbon

Mediterranean wooded grasslands that emerge from silvopastoral activities are multifunctional systems that result in high biodiversity and offer ecosystem services such as forage production and soil carbon sequestration. During 3 years, ten grazed wooded grassland fields were studied in the Berchidda–Monti long-term observatory, located in NE Sardinia, Italy, with the aim of exploring the synergies and trade-offs between biodiversity and selected ecosystem services. Positions below and outside the canopy of three cork oak trees in each field were randomly selected to compare seasonal pasture production, pasture utilization rate by animals, botanical composition, biodiversity indicators (Shannon index and plant species richness) and soil organic carbon. In autumn, dry matter production of pasture was similar in the two positions; in two winters out of three it was greater below the trees than outside, and in spring it was greater outside than below the trees. While plant species richness and Shannon index were not significantly influenced by the position, the overall wooded grassland plant species richness was 31% higher than that outside of the tree crown. The soil organic carbon content in the 0–40-cm soil layer was also higher below the trees. Our findings highlight that if the main purpose of the wooded grasslands is to provide forage for grazing animals rather than conserving and/or enhancing plant diversity and soil fertility, the presence of trees constrains the overall forage productivity, although the greater forage availability in winter under the trees can contribute to improve the seasonal distribution of forage production.     

Differences of raw cork quality in productive cork oak woods in Sicily in relation to stand density

Differences of raw cork quality, in terms of thickness and porosity, were observed in productive cork oak (Quercus suber L.) stands in the Nebrodi and Iblei mountains of Sicily in relation to stand density. Five study areas were chosen across a range of different stand density satisfying specific sampling requirements among two managed cork oak woods.Analysis of variance using Fisher–Snedecor‘s F test (p < 0.05) were used to identify statistically significant differences of cork quality and sylvicultural, dendrometric and cork stripping parameters between study areas within each stand. Relationships between cork quality and sylvicultural and dendrometric parameters were also tested using Pearson's correlation coefficient (r). Results shown that sylvicultural practices are a key factor influencing cork quality: statistically significant differences in cork thickness and crown area were observed between areas at different stand density; positive correlations were found between cork thickness and crown area in lower density study areas favouring a significant vegetative activity; negative correlations were found between parameters of cork stripping (cork stripping coefficient, cork stripping surface, maximum height of cork stripping) and cork thickness. No correlations were found between cork porosity and dendrometric or sylvicultural parameters, demonstrating the probable genetic origin of cork porosity. Results shown that cork quality parameters and stand attributes may be used in sustainable management models of cork oak forests.     

Birds as predators of cork and holm oak pests

The recent decline of Mediterranean oak woodlands in SW Iberian Peninsula is related to insect pests which affect both cork oak (Quercus suber) and holm oak (Quercus rotundifolia). We identified twenty-six bird species as potential regular predators of twenty major pests by reviewing the diet of breeding, wintering and resident species in this ecosystem. Foraging guilds are strongly associated with predation at distinct stages of the pests’ life-cycle: ground-foragers prey on overwintering pupae and larvae of seed-borers, tree-foragers prey on eggs, larvae and pupae of defoliating and wood-boring pests, and aerial-sweepers prey on airborne imagines. Bird predation can cover the complete life-cycle of pest species because different species may be complementary due to a dissimilar exploitation of foraging niches and periods. Small generalist tree-foraging passerines are important pest predators given their high densities and widespread distribution in Mediterranean oak woodlands, but management practices can have a significant negative effect in their populations.     

Litter flammability in oak woodlands and shrublands of southeastern France

Characterizing the flammability of litter fuels is of major importance for assessing wildland fire ignition hazard. Here we compared the flammability of litter within a mosaic of Quercus suber (cork oak) woodlands and shrublands in a Mediterranean fire-prone area (Maures massif, southeastern France) to test whether the characteristics and the flammability of litter vary with the vegetation types. We tested experimentally the ignitability, the sustainability, the combustibility and the consumability of undisturbed (=non-reconstructed) litter samples with a point-source mode of ignition. Although the frequency of ignition was similar between all the vegetation types, we distinguished four groups having litter of specific composition and flammability: low and sparse shrublands dominated by Cistus species, medium shrublands with cork oak, high Erica shrublands with sparse cork oak woodlands, and mixed mature oak woodlands with Q. suber, Q. ilex and Q. pubescens. As these vegetation types corresponded to a specific range of past fire recurrence, we also tested the effect of the number of fires and the time since the last fire on litter flammability. Litters of plots recurrently burned had low ability to propagate flames and low flame sustainability. We discuss how the recent fire history can modify vegetation and litter flammability, and thus the fire ignition hazard.     

Low temperature during winter elicits differential responses among populations of the Mediterranean evergreen cork oak (Quercus suber)

Populations of cork oak (Quercus suber L.) were assessed for seasonal and inter-population variability in, and temperature responses of, the ratio between light-induced variable and maximum fluorescence of chlorophyll, Fv/Fm, considered a surrogate for the maximum photochemical efficiency of photosystem II (PSII). Seedlings from 10 populations throughout the distribution range of Q. suber in the Mediterranean basin were grown in a common garden in central Spain. The Fv/Fm ratio of dark-adapted leaves was measured at dawn every month for 2 years. Air temperature was recorded at a nearby climatic station. During the summer, when maximum air temperatures reached 40 degrees C, there were no significant differences in Fv/Fm among populations, but significant differences were seen during the winter. In colder months, Fv/Fm ranged in all populations between 0.5-0.6 and 0.2-0.3 in 2001 and 2002, respectively. The variance explained by the population effect was greatest during winter months, especially in 2002, reaching a peak value of 10% when minimum air temperature was below -10 degrees C. Populations originating from warmer sites showed the largest decline in Fv/Fm between the end of 2001 and the beginning of 2002. Thus, a negative linear relationship was established between mean annual temperature at the population source and population mean Fv/Fm recorded in the coldest month in 2002 and normalized by the Fv/Fm spring measurement.