Analysis of spatial patterns of oak decline in cork oak woodlands in Mediterranean conditions

? Cork oak mortality is a recurrent problem in southwestern Portugal. Despite the perception of increasingly visible damage in oak woodlands on drought-prone sites, the role of the various environmental factors in their decline is not clear.

? To describe the spatial patterns of cork oak (Quercus suber L.) mortality, a cork oak mortality index (MI) was determined for each landscape feature (agroforestry system, soil type, slope and aspect) using a GIS approach. To achieve this goal, a logistic regression model was formulated analyzing interactions between landscape attributes and allowing a prediction of cork oak mortality.

? Maximum values of MI were found in (i) shrublands and open woodlands with shrub encroachment (MI 6 and 3, respectively), where competition for soil water between tree and understory increases; and (ii) on lower slopes in the rounded hilltops and smooth hillsides or shallow soils where access to groundwater resources during summer drought is difficult.

? The model highlighted the importance of the agroforestry systems on cork oak mortality and may be used to identify sensitive areas where mitigation actions should be employed in a scenario of increasing drought severity in these Mediterranean ecosystems.

     

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.     

Incidence of Phytophthora species in oak forests in Austria and their possible involvement in oak decline

A survey on the occurrence of Phytophthora species in oak ecosystems in Austria was conducted from April to May 1999 and in June 2000. The investigations were carried out at 35 study sites distributed throughout the zone of oak forests in eastern Austria. Four oak species, including Quercus robur, Q. petraea, Q. cerris and Q. pubescens were considered in the survey. Rhizosphere soil samples were taken from sample trees, which consisted of healthy and declining trees as indicated by their crown transparency. Young oak leaflets were used as baits to recover Phytophthora species. The assemblage of Phytophthora spp. detected in Austrian oak forests consisted of five species, including Phytophthora quercina, P. citricola, P. gonapodyides, P. europaea and P. syringae. P. quercina and P. citricola were isolated from 11 and seven sites, respectively, and were thus the most common and most widely distributed species. The three other species were recovered only sporadically. P. citricola could be separated into two morphologically and genetically well‐characterized types (A and B). Phytophthora species, in particular the common P. quercina and P. citricola occurred on sites showing a wide variety of soil types, soil textures and moisture classes. There was mild evidence for connection between deteriorating crown status and the presence of Phytophthora spp. Furthermore, significant differences in contents of magnesium, as well as calcium, aluminium, nitrogen and carbon at different soil depths (0–10, 10–20 and 20–40 cm) were detected between Phytophthora‐infested and Phytophthora‐free sites. The results of the present study provide circumstantial evidence that Phytophthora species are involved in oak decline at certain sites in Austria.     

The oak decline: a new problem in Italy

The Authors observed, in Italy, over a number of years, isolated and grouped trees of the genus Quercus that declined over one or more vegetative seasons. The spread was very fast; in fact the trees declined in the course of 2–3 vegetative seasons. A series of symptoms was observed: production of epicormic shoots, yellowing of leaves, laceration of the bark, bleeding from the trunk. Many fungi were isolated: Armillaria spp., Cephalosporium spp., Cladosporium spp., Cylindrocarpon spp., Diplodia mutila, Hypoxylon mediterraneum, Phoma cavae, Pbomopsis quercina, Sporotrix spp. Future research will attempt to ascertain the possible causes of the decline.     

Merchantable volume system for pedunculate oak in northwestern Spain

A model is required for accurate estimation of the merchantable volume of pedunculate oak (Quercus robur L.) trees in Galicia, northwestern Spain. Accordingly, the purpose of the present study was to obtain equations for predicting merchantable volumes and stem profiles of individual trees. For this reason, two compatible and four non-compatible volume systems were initially evaluated and fitted to data from 251 destructively sampled trees which were collected in stands located throughout the area of distribution of the species in Galicia. The outliers were removed to provide a data set of measurements from 3 090 sections, which was then available for fitting. A second-order continuous autoregressive error structure was used to account for autocorrelation. Comparison of the models was carried out using overall goodness-of-fit statistics and box plots of residuals against relative height or diameter class. The compatible volume system of Fang et al. [22] provided the best compromise in describing the stem profile and estimating merchantable height, merchantable volume and total volume and is therefore recommended for pedunculate oak stands in Galicia.     

Degradability of soils under oak and pine in Central Spain

The purpose of this research was to study the influence of the vegetation on the soil C pool of forests of pines (Pinus sylvestris) and oaks (Quercus pyrenaica), located in Central-Western Spain. Horizons from selected soils located in these forests were sampled, and the soil organic C (SOC) was determined. In addition, in vitro incubation experiments were carried out, under controlled conditions, to monitor the stability of SOC against the microbial activity. Soil humus fractions were isolated following a classical procedure of chemical fractionation using alkaline solutions, before and after the incubation experiment. A deeper O horizon was found under the pine forest than under oak one; however, higher SOC content was found in the oak site than that under pine one. During the in vitro mineralization process, a lower CO₂ production by the soil sample from pine forest was observed, in relation to that emitted by the oak soil. In addition, a lower humification degree was estimated for the soil humus under pines than for that under oaks. In conclusion, replacement of oaks by pines produced a decrease in SOC accumulation and a lower quality of humus in the forest soils.     

Requirements and biological aspects of Fusarium eumartii and its possible role in oak decline in North-eastern Italian oak forests

To determine a possible role of Fusarium eumartii in oak decline in different zones of Italy some requirements (temperature, substrates, pH) and some biological aspects (ability to produce phytotoxic metabolites, and pathogenicity) were studied in vitro and by inoculation tests on oak seedlings.     

Brenneria spp. and Rahnella victoriana associated with acute oak decline symptoms on oak and hornbeam in Iran

Decline diseases of forest trees are complex syndromes not attributable to single causal factors. In Iran, symptoms of decline disease have been observed in a number of native forest species including Quercus castaneifolia (chestnut‐leaved oak), Q. brantii (Persian oak) and Carpinus betulus (hornbeam). The symptoms are prevalent in the northern forests and the Zagros mountain forests. There are parallels between the disease in Iran and acute oak decline (AOD) reported in the UK, specifically the presence of weeping cankers, which have been attributed to a polybacterial complex wherein Brenneria goodwinii is considered a key necrogen. Based on the AOD symptomatology, and as a first step towards discovering potential causal agents of the stem weeping symptoms of affected trees in Iran, necrotic tissues were tested primarily for the presence of B. goodwinii. Symptomatic Q. castaneifolia and C. betulus from the Mazandaran Province and symptomatic Q. brantii from Kohgiluyeh and Boyerahmad Province were sampled. Isolation and culture on a selective medium yielded uniform bacterial colonies. Isolates were characterized using phenotypic and genotypic (DNA sequencing) tests. The isolates were phenotypically identical to members of Pectobacteriaceae and Yersiniaceae, specifically Brenneria and Rahnella spp. The nucleotide sequences of the 16S rRNA and housekeeping genes gyrB, infB and atpD (MLSA) amplified via PCR demonstrated that the isolates from the trees in Iran were indeed B. goodwinii, B. roseae subsp. roseae, Rahnella victoriana and an unknown species of Brenneria. Most bacteria isolated from non‐symptomatic trees were Gram‐positive, and Pseudomonas spp. were dominant, but bacterial species isolated from the diseased trees were not detected in healthy trees. Hypersensitivity response tests were positive, but inoculation on saplings was more variable with internal necrosis developing only once in the test period. Therefore, further testing is required. This is the first report of the incidence of B. goodwinii, B. roseae subsp. roseae, R. victoriana and Brenneria sp. associated with acute oak decline‐like symptoms on Q. castaneifolia, Q. brantii and C. betulus across the western forests of Iran and in the world.     

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.     

Treatment of oak decline using pressurized injection capsules of antifungal materials

Quercus ilex and Quercus suber trees growing at several sites in Extremadura, Western Spain, that were showing symptoms of oak decline were injected with potassium phosphonate, quinosol or carbendazim using a low-pressure method of trunk injection composed of a pressurized capsule system. A team of four people injected between 120 and 189 trees per day, depending upon the density of the undergrowth vegetation. This labour cost represented, approximately, 15–20% of the total cost of the treatment. The potassium phosphonate-injected trees showed a significant improvement in vegetative growth within 2 years of the injection treatment, and they also showed some recovery from the decline symptoms during the third year. Only one injection treatment of an average of 3.5 capsules (corresponding to 24.5 g phosphonic acid) per tree of approximately 36 cm in diameter, was necessary to reduce the disease severity significantly. Indirectly, these results corroborate the implication of Phytophthora cinnamomi in oak decline within Spanish Quercus woodlands.     

Involvement of Phytophthora species in white oak (Quercus alba) decline in southern Ohio

This study was initiated to investigate the possible role of Phytophthora species in white oak decline (Quercus alba) in southern Ohio at Scioto Trail State Forest. Surveys demonstrated the presence of four species of Phytophthora including one novel species. By far, the most common species was P. cinnamomi; P. citricola and P. cambivora were isolated infrequently. In few instances, P. cinnamomi was isolated from fine roots and necroses on larger roots. No special pattern of incidence was found, but P. cinnamomi was more commonly isolated from greater Integrated Moisture Index values suggesting moist lower bottomlands favour this Phytophthora species. When tree crown condition was examined relative to the presence of Phytophthora, no significant association was found. However, roots of declining P. cinnamomi‐infested trees had 2.5 times less fine roots than non‐infested and healthy trees, which was significantly different. The population densities of P. cinnamomi from declining trees were significantly greater than from healthy trees, suggesting increased pathogen activity that has the potential to cause dieback and decline and possibly the cause of a reduced fine root amount found on declining trees.     

Review of oak stand decline with special reference to the role of drought in Poland

Declines in oak-forest ecosystems have been reported frequently throughout the world since the beginning of this century. They have been associated with the death of individual trees, of small groups of trees or of entire stands. In this paper, the phenomenon of oak decline is presented in the context of the local site conditions in selected countries. Oak decline is regarded as a result of the synergistic action between damaging agents, both biotic and abiotic. Periodic changes of the climate in selected experimental plots of Quercus robur stands in Poland were analysed by comparing Walter's climatic diagrams and annual growth rings. Climatic conditions have a major influence on the vigour of oaks. An increase in the frequency of dry years (especially when drought occurs at the beginning of the growing season, e.g. in May-June) has contributed to the complex phenomenon of oak decline.     

Susceptibility to Phytophthora cinnamomi of the commonest morphotypes of Holm oak in southern Spain

The four main morphotypes of Holm oak (Quercus ilex subsp. ballota) present in Andalusia (expansa, macrocarpa, microcarpa and rotundifolia) were infected with Phytophthora cinnamomi to determine their susceptibility to the root pathogen. No large differences were found among the four morphotypes in the infection of roots, which always showed a high degree of necrosis. However, the different responses of the foliage to infection separated the four morphotypes of Holm oak into three groups: very susceptible (microcarpa), susceptible (expansa) and moderately susceptible (rotundifolia and macrocarpa). The natural hybrid Q. ilex ballota–Q. faginea exhibited a low level of root and foliar symptoms when infected with P. cinnamomi. Quercus faginea could be considered as a source of resistance to P. cinnamomi in future breeding programmes.     

The oak buprestid beetle,Agrilus biguttatus (F.) (Col., buprestidae), a recent factor in oak decline in Europe

During last years, the populations of the oak buprestid beetleAgrilus biguttatus (Fab.) in Europe have increased. In several countries, the beetles’ attacks have become a new component in oak dieback. The larvae excavate galleries under the bark of weakened trees, which are killed through the girdling. Because of the difficult diagnosis it is necessary to draw more attention to the infestations. Therefore, this paper presents a review on the literature concerning the recognition of the infestations by the insect and its bionomics.     

Corresponding patterns of site quality,decline and tree growth in a sessile oak stand

This study focuses on two rarely studied aspects of oak decline: relations with site characteristics and effects on tree growth. The study was carried out in a 5.5 ha stand in Hungary which is strongly affected by oak decline. The nearly pure sessile oak (Quercus petraea) stand of mostly coppice origin was 90 years old at the beginning of the study. Within-stand site heterogeneity was described by the herbaceous vegetation. Four ecological site types were distinguished by the species composition of herbs, and characterized by the ecological indicator values of the species. Tree growth between 1987 and 1993 was measured, and tree vigour was estimated from visual characteristics five times between 1987 and 1993. Potential volume increment of declining trees was estimated with the growth rates of healthy trees of the same size. Volume increment loss caused by oak decline was also assessed. Significant positive relationships were found between tree vigour and tree size and between tree vigour and tree growth. The growth of seriously declining trees dropped to almost one-half of that of healthy ones. Growth reduction of living trees at the stand level amounted to 5.4%, whereas growth reduction of all trees, including those that died during the observation period, amounted to 19.9% of the potential growth. Tree size and growth were greater on better sites. A strong relationship was also found between tree vigour and site type, but sessile oak was more susceptible to decline at better sites.     

Ingrowth model for pyrenean oak stands in north-western Spain using continuous forest inventory data

In this paper, a two stage ingrowth model is presented for predicting periodic, 10 years ingrowth for pyrenean oak (Quercus pyrenaica Willd.) grown in medium to fully stocked coppice stands in north-western Spain. Data from the Spanish National Forest Inventory was used to develop the model, extracting the information from two inventories taken in 222 permanent plots. The first stage of the model predicts the probability of ingrowth occurrence, and in the second stage, the number of recruits is predicted using a conditional model. Both models were biologically realistic and presented logical behaviour. The ingrowth occurrence probability model was dependent on quadratic mean diameter and average height. The recruitment quantification model included stand density and average diameter as explanatory variables. Although the occurrence probability of ingrowth was predicted correctly in 71.7% of cases, the predictions of the number of recruitment are poorer, yielding a coefficient of determination of 0.358. The evaluation criteria included qualitative and quantitative examinations and a testing with independent data from another region. The proposed ingrowth model is the first to be developed for mediterranean oak species in Spain and is an essential feature in any stand growth system.     

Stand factors influencing Pinus halepensis decline in north‐western Spain

Although decline of Aleppo pine was observed long ago and several climatic and biotic factors have been previously associated with this complex process, site factors involved in this decline remain poorly understood. The objective of the work described here was to identify site factors associated with canopy condition. Canopy condition was estimated both by a visual estimation of defoliation, and by an indirect estimation of leaf area index (LAI) and other stand‐ and light‐related parameters through the analysis of hemispherical photographs. A high percentage of damaged trees (81%) along with high levels of defoliation in plots (up to 53%) and trees (up to 85%) were recorded. Regression models showed that the site factors associated with defoliation were basal area, age, crown depth and elevation, while those associated with LAI were diameter at breast height, tree density and canopy openness. Analysis of hemispherical photographs proved to be a useful method for LAI estimation, but not for estimation of defoliation due to heterogeneous defoliation patterns caused by fungal pathogens detected in the study area. Soils and climatic conditions were common to all plots, so their influence could not be tested, but poor soil conditions and climatic restraints are known in this area, including low soil productivity, frequent summer droughts and high numbers of frost days. The results obtained suggest that several factors were associated with the decline of Pinus halepensis, including age, basal area, canopy openness, diameter, height and tree density. These factors can influence canopy condition, and thus, they might be acting as predisposing factors for the decline. The modulation of these factors is possible if suitable forest management strategies are applied, which could lead to a decrease of the decline incidence.     

Identification and distribution of Armillaria species associated with an oak decline event in the Arkansas Ozarks

Forests in the Ozark Mountains of northern Arkansas recently experienced a widespread oak decline event. Armillaria, a root rot fungus, has been associated with other oak decline events and may have been an important contributing factor to tree mortality in this event. Although Armillaria has been identified from the Ozark Mountains in Missouri, it has never been investigated in the Arkansas Ozarks. Molecular diagnostic techniques were used in this study to identify species of Armillaria present on roots removed from dead trees of two common oak species, northern red oak, Quercus rubra L., and white oak, Q. alba L., from three geographic areas and on three topographic positions – ridges, south‐ and west‐facing benches. Armillaria(A. mellea, A. gallica or A. tabescens) was identified from 31% of root samples taken from 102 trees in seven of nine sample plots. Armillaria mellea, occurred most often (20 samples, both oak species on seven plots) followed by A. gallica (10 samples, northern red oak only on four plots), and A. tabescens occurred twice (on northern red oak in a single plot). Thus, all three Armillaria species occurred on northern red oaks while A. mellea was the only species recovered from white oaks. Results varied by topographic position with samples from tree roots on ridges having the fewest positive identifications, one of 29. West‐facing benches had the highest positive samples with 20 of 41 testing positive and trees on south‐facing benches were intermediate with 11 of 32 samples from infected trees. This study documents the occurrence of three species of Armillaria in the Arkansas Ozarks and their association with oak mortality resulting from an oak decline event coupled with a red oak borer, Enaphalodes rufulus, outbreak. Further, it documents some potential variation in host/pathogen combinations and forest site conditions.     

The role of yellow lupin (Lupinus luteus) in the decline affecting oak agroforestry ecosystems

Phytophthora cinnamomi is a soilborne pathogen causing root rot in Mediterranean Quercus species growing in ‘dehesa’ rangeland ecosystems. Recently, it has been reported causing wilting and death of Lupinus luteus (yellow lupin), a spontaneous plant in southern Spain rangelands, but also frequently sowed for livestock grazing. In soils artificially infested with P. cinnamomi chlamydospores and planted with different cultivars of yellow lupin, a significant increase in the density of propagules was detected in comparison with the initial levels of inoculum and with the infested but not planted soil (control). In oak‐rangelands in which yellow lupine was planted, isolation and counting of colonies of P. cinnamomi from soil samples have shown the ability of this plant to maintain or even increase the inoculum density and thus facilitate the infection of trees. Results suggested that cultivation of yellow lupin in oak‐rangeland ecosystems should be avoided whether oak trees are affected by root disease caused by P. cinnamomi or not. This leguminous plant can act as an inoculum reservoir or even enhance inoculum soil levels available for oak root infections, exacerbating the oak decline severity in the region.