Beech decline in Central Europe driven by the interaction between Phytophthora infections and climatic extremes

During the past decade, and in particular after the wet year 2002 and the dry year 2003, an increasing number of trees and stands of European beech (Fagus sylvatica L.) in Bavaria were showing symptoms typical for Phytophthora diseases: increased transparency and crown dieback, small‐sized and often yellowish foliage, root and collar rot and aerial bleeding cankers up to stem heights of >20 m. Between 2003 and 2007 134 mature beech stands on a broad range of geological substrates were surveyed, and collar rot and aerial bleeding cankers were found in 116 (86.6%) stands. In most stands the majority of beech trees were declining and scattered or clustered mortality occurred. Bark and soil samples were taken from 314 trees in 112 stands, and 11 Phytophthora species were recovered from 253 trees (80.6%) in 104 stands (92.9%). The most frequent species were P. citricola, P. cambivora and P. cactorum. Primary Phytophthora lesions were soon infected by a series of secondary bark pathogens, including Nectria coccinea, and wood decay fungi. In addition, infected trees were often attacked by several bark and wood boring insects leading to rapid mortality. Bark necroses were examined for their probable age in order to determine whether the onset of the current Phytophthora epidemic was correlated to rainfall rates recorded at 22 Bavarian forest ecosystem monitoring stations. A small‐scale survey in nine Bavarian nurseries demonstrated regular infestations of all beech fields with the same range of Phytophthora species. The results indicate that (1) Phytophthora species are regularly associated with beech decline and may also be involved in the complex of ‘Beech Bark Disease’, (2) excessive rainfalls and droughts are triggering the disease, and (3) widespread Phytophthora infestations of nursery stock might endanger current and future silvicultural projects aiming on the replacement of non‐natural conifer stands by beech dominated mixed stands.     

Phytophthora root and collar rot of mature Fraxinus excelsior in forest stands in Poland and Denmark

In recent years, Common ash (Fraxinus excelsior) throughout Europe has been severely impacted by a leaf and twig dieback caused by the hyphomycete Chalara fraxinea. The reasons for its current devastating outbreak, however, still remain unclear. Here, we report the presence of four Phytophthora taxa in declining ash stands in Poland and Denmark. Phytophthora cactorum, Phytophthora plurivora, Phytophthora taxon salixsoil and Phytophthora gonapodyides were isolated from rhizosphere soil samples and necrotic bark lesions on stems and roots of mature declining ash trees in four stands. The first three species proved to be aggressive to abscised roots, twigs and leaves of F. excelsior in inoculation experiments. Soil infestation tests also confirmed their pathogenicity towards fine and feeder roots of ash seedlings. Our results provide first evidence for an involvement of Phytophthora species as a contributing factor in current decline phenomena of F. excelsior across Europe. Specifically, they may act as a predisposing factor for trees subsequently infected by C. fraxinea. Phytophthora species from ash stands also proved to be aggressive towards a wide range of tree and shrub species commonly associated with F. excelsior in mixed stands. Although damage varied considerably depending on the Phytophthora species/isolate–host plant combination, these results show that many woody species may be a potential source for survival and inoculum build‐up of soilborne Phytophthora spp. in ash stands and forest ecosystems in general.     

First records of soilborne Phytophthora species in Swedish oak forests

Thirty‐two oak stands in southern Sweden, 27 with predominantly declining trees and five with a higher proportion of healthy trees were investigated regarding the presence of soilborne Phytophthora species. Phytophthora quercina, an oak‐specific fine root pathogen, was isolated from rhizosphere soil samples in 10 of the 27 declining stands. Additionally, P. cactorum and P. cambivora were recovered from one stand each. No Phytophthora species were isolated from the healthy oak stands. The soil conditions at the sites from which Phytophthora spp. were recovered ranged from mesic sediments to moraines, with clayey to silty textures and with soil pH (BaCl₂) between 3.5 and 5.0. The results show that P. quercina is geographically widespread in oak stands in southern Sweden and indicate that this pathogen may be one of the factors involved in oak decline in Northern Europe as has already been shown for western, Central and parts of southern Europe.     

Multispecies Phytophthora disease patterns in declining beech stands

Decline diseases are typically caused by complex abiotic and biotic interactions and characterized by a suite of symptoms indicative of low plant vigour. Diseased trees are frequently infected by Phytophthora, but the complex interactions between pathogen, host and the heterogeneous forest environment mask a comprehensive understanding of the aetiology. In the present study, we surveyed European beech (Fagus sylvatica) stands in Swiss forests with recent increases in bleeding lesions for the presence of Phytophthora. We used a combined approach of analysing soil and bark samples from trees displaying bleeding lesions and trees free from bleeding lesions. Soil baiting revealed a higher prevalence of Phytophthora spp. around trees with bleeding lesions than around trees without bleeding lesions. For the bark samples from bleeding lesions, we used several detection methods. Phytophthora spp. were detected in 74% of the trees by an immunological on‐site diagnostic kit, in 64% by a specific PCR assay, and 38% by isolation on selective media. All samples tested were negative for P. ramorum using qPCR. Overall, nine Phytophthora species were identified by ITS sequencing, the most common of which were P. plurivora, P. gonapodyides, P. × cambivora and P. syringae. We identified distinct species in bleeding lesions and the rhizosphere of the same host tree which suggests a multispecies Phytophthora disease patterns in these declining beech. Among the recovered species, P. × cambivora and P. × serendipita were identified as hybrid genotypes with the former abundant in bleeding lesions.     

Comparative studies on the fine root status of healthy and declining spruce and beech trees in the Bavarian Alps and occurrence of Phytophthora and Pythium species

Investigations on root and crown status of spruce and beech were carried out on selected trees in the ‘Werdenfelser Land’ area (Bavarian Alps, Southern Germany). In addition, the association of fine root pathogens of the genera Phytophthora and Pythium with the trees’ rhizosphere was studied. In a variety of stands representing various site conditions, soil and root samples were taken from 12 spruce (Picea abies) pairs and eight beech (Fagus sylvatica) pairs. Each pair consisted of a healthy and a declining tree as indicated by crown transparency. The root status was characterized using a set of parameters, and correlations between crown and fine root status were observed. In spruce, most parameters decreased significantly with increasing crown transparency, whereas in beech, correlations were less pronounced. The total number of lateral roots per cm small root (diameter 2–5 mm) was significantly lower in both species for declining trees compared to healthy trees. Pythium spp. were isolated from 15 of 24 soil samples taken from under spruce, and from eight of 16 samples from under beech. Phytophthora citricola was found in two beech stands only. Among the isolated species, Pythium anandrum, Pythium inflatum and Pythium acrogynum were identified according to morphological features. After polymerase chain reaction‐restriction fragment length polymorphism analysis, residual Pythium isolates were assigned to four different groups. No crown transparency‐dependent differences in isolation frequency were found. In soil infestation tests, all species tested caused root damage on both young spruce and beech plants, with P. citricola being the most aggressive pathogen. Additionally, Pythium‐infected beeches showed severe leaf chloroses and necroses. Due to their low isolation frequency, Phytophthora spp. are not considered to play a major role in the decline of spruce and beech in the investigated area. Pythium spp., however, were isolated frequently, showed pathogenicity towards the fine roots of spruce and beech, and are therefore considered to be at least contributing factors in the decline of Bavarian mountain forests.     

Involvement of Phytophthora spp. in chestnut decline in the Black Sea region of Turkey

Chestnut blight caused by Cryphonectria parasitica is a serious disease of Castanea sativa in the Black Sea region of Turkey. During disease surveys, dieback and decline symptoms were observed on trees without apparent blight and ink disease symptoms. Black necroses, similar to those caused by Phytophthora infections, were noted on some of the chestnut coppices and saplings in one nursery in Ordu and led to an investigation into this disease complex. Only symptomatic plants showing dieback symptoms were investigated. Soil samples together with fine roots were collected from two directions, north and north‐east, approximately 150 cm away from the main stems. Phytophthora spp. were baited with young chestnut leaves. Three Phytophthora spp., P. cambivora, P. cinnamomi and P. plurivora, were identified from 12 soil samples collected from 73 locations, while from the nurseries, only P. cinnamomi was obtained. Phytophthora cinnamomi was the most common species, obtained from seven locations in five provinces and from four nurseries having similar symptoms mentioned above in different locations. Phytophthora cambivora and P. plurivora were less frequently obtained, from three to two stands, respectively. Phytophthora cinnamomi and P. cambivora were the most aggressive species when inoculated at the stem base on 3‐year‐old chestnut saplings, killing six saplings of eight inoculated in 2 months. The three Phytophthora species were first recorded on chestnut in Black sea region of Turkey with the limited samples investigated in a large area about 150 000 ha chestnut forest.     

Modelling above and below ground carbon dynamics in a mixed beech and spruce stand influenced by climate

Tree growth and carbon dynamics are important issues especially in the context of climate change. However, we essentially lack knowledge about the effects on carbon dynamics especially in mixed stands. Thus, the objective of this study was to test the effects of climatic changes on the above and below ground carbon dynamics of a mixed stand of Norway spruce (Picea abies [L.] Karst.) and European beech (Fagus sylvatica L.) by means of scenario simulations. To account for the typical tree interactions in a mixed-species stand a spatial explicit tree growth model based on eco-physiological processes was applied. Three different climate scenarios considering altered precipitation, temperature, and radiation were calculated for an unthinned and a thinned stand. The results showed significant changes of above and belowground biomass over time, especially when temperature and radiation were increased additionally to decreased precipitation. The reduction in biomass increments of Norway spruce were more attenuated above than below ground. In contrast, the results for beech were the opposite: The belowground increments were reduced more. These results suggest a shift in the species contribution to above and belowground biomass under dryer and warmer conditions. Distinct effects were also found when thinned and unthinned stands were compared. A reduced stand density changed the proportions of above and below ground carbon allocation. As a main reason for the changed growth reactions the water balance of trees was identified which lead to changed biomass allocation pattern. This article belongs to the special issue “Growth and defence of Norway spruce and European beech in pure and mixed stands”.     

Beech bark disease: an evaluation of the predisposition hypothesis in an aftermath forest

The beech bark disease (BBD) complex affecting American beech consists of the scale insect, Cryptococcus fagisuga, and one or more pathogenic fungi of the genus Neonectria. Following extensive above‐ground mortality of mature beech, stands can be defined by a characteristic set of conditions that are termed the aftermath zone. A long‐standing hypothesis states that C. fagisuga is a necessary predisposing factor for Neonectria infection. Although some evidence supports this in the killing front, the relationship has not been examined in the aftermath zone and other predisposing factors have been proposed. Using quantitative, tree‐level data, we found no significant relationships between C. fagisuga and Neonectria spp. in aftermath stands of central New York State. We propose that the pathosystem operating in the aftermath zone differs from that in the killing front in that C. fagisuga may not be the sole predisposing factor.     

Endophytische Pilze in Blättern und Ästen gesunder und geschädigter Buchen (Fagus sylvatica L.)

Endophytic fungi in leaves and twigs of healthy and diseased beech trees (Fagus sylvatica L.). Endophytic fungi were isolated from surface-sterilized leaves and twigs of healthy and diseased trees. Three fungal species could be isolated frequently: Apiognomonia errabunda, Diaporthe eres and Bisporella sp. D. eres occurred in leaves of healthy trees more frequently, than in those of diseased trees. It has been hypothesized, that less capacity of water and nutrient uptake of diseased trees is responsible for this effect. A mutualistic symbiosis of A. errabunda and D. eres with beech trees is supposed and discussed.     

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.     

Feinwurzelmasse und Mykorrhiza von Altbuchen (Fagus sylvatica L.) in Waldschadensgebieten Bayerns

Feeder root biomass and mycorrhizae of old beech trees (Fagus sylvatica L.) in bavarian forest die-back areas . The feeder root biomass (roots = 2 mm diameter) and the quantity of mycorrhizae of apparently healthy and diseased old beech trees were determined in 7 stands in Bavaria. Canopy die-back correlated with reduction of the feeder root biomass and of mycorrhizae in the topsoil. In the deeper layers of the soil (below 50 cm) there were nearly no differences between the decline classes lor these parameters. The feeder root damage described were encountered in all stand types. For that reason, such damage can be considered, at least for comparable stands, as a general symptom of above ground diseased old beech trees.     

Conversion of single-layered Scots pine monocultures into close-to-nature mixed hardwood forests: effects on parasitoid wasps as pest antagonists

In the north Saxon lowlands (near Torgau), effects of conversion of pure pine stands (Pinus sylvestris L.) into mixed stands by planting deciduous trees [Fagus sylvatica L. and Quercus petraea (Matt.) Liebl] were investigated on parasitoid wasps as pest antagonists. The effects of planting deciduous trees in pine stands were investigated using the strategy of space-for-time substitution including advanced plantations of beech and oak of different age classes. Wasps were captured at 4-week intervals by ground photoeclectors (GPE, n=6, 1 m²) and flight-interception traps (FIT, n=8), placed in the tree crown layer during the vegetation period (April–October) of 2000. A total of 32,479 parasitoid wasps belonging to 30 families were caught in the traps. Fifty-nine percent of individuals were representatives of families relevant as antagonists of forest insect pests: Ichneumonidae, Braconidae, Pteromalidae, Eulophidae, Mymaridae, Trichogrammatidae, and Scelionidae. Compared to the pure pine stand, individual numbers of most families of parasitoid wasps were statistically significantly higher in mixed stands with deciduous trees. The clearest promoting effects of deciduous trees on parasitoid wasps were manifested in the oldest age classes of advanced beech and oak plantations. Oak exerted stronger effects than beech. This applied especially to the tree crown layer, the stratum with the highest spatial correlation between important phytophagous pine pests and relevant parasitoids. The increased structural diversity of the stands and the broader spectrum of potential hosts are regarded as key factors for the promoting effects of advanced plantings of deciduous trees in pine stands on the community of parasitoid wasps.     

Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees

Soil‐borne species of Phytophthora were isolated from 19 of 30 examined oak forest areas in Italy. The frequency of isolated Phytophthora spp. (35.2%) was significantly correlated with soil pH and longitude of the sites. Eleven Phytophthora species were detected. Phytophthora cambivora, P. cinnamomi and P. cactorum were recovered from sites in central and southern Italy whereas P. quercina was isolated in the northern and central part of the country. Phytophthora citricola occurred all over Italy. Phytophthora quercina was the only species significantly associated with declining oak trees.     

Phytophthora pseudosyringae associated with the mortality of Nothofagus obliqua in a pure stand in central‐southern Chile

Mortality of Nothofagus trees in the southern‐central Chile region has been observed for over 30 years. A field survey conducted in 2013 detected partial defoliation and bleeding cankers on Nothofagus obliqua in a pure stand in the Nahuelbuta coastal ranges of the Biobío region. A Phytophthora sp. was isolated from stem cankers and soil samples around symptomatic N. obliqua trees: All isolates were identified as Phytophthora pseudosyringae. These isolates were pathogenic on 1‐year‐old N. obliqua and Nothofagus alpina, and on detached twigs of adult N. obliqua and Nothofagus dombeyi trees. This paper is the first to report association and pathogenicity of P. pseudosyringae with N. obliqua, N. alpina and N. dombeyi native to the Biobío region of Chile. The potential of P. pseudosyringae to cause damage in natural Nothofagus stands in Chile must be determined.     

Field survey,isolation, identification and pathogenicity of Phytophthora species associated with a Mediterranean‐type tree species

Corymbia calophylla (marri), a keystone tree species in the global biodiversity hot spot of southwestern Australia, is suffering decline and mortality associated with a canker disease caused by the endemic fungus Quambalaria coyrecup. Phytophthora species are frequently isolated from the rhizosphere of C. calophylla, and a hypothesis is that Phytophthora root infection is predisposing C. calophylla to this endemic canker pathogen. Field surveys were conducted in both anthropogenically disturbed and undisturbed C. calophylla stands, from where a total of 100 rhizosphere soil samples, from both healthy and cankered trees, were collected. Phytophthora species were isolated from 26% of the samples collected, with Phytophthora incidence significantly higher on disturbed stands than in natural forests (73% and 27%, respectively). Five Phytophthora species were recovered, including P. cinnamomi, P. elongata, P. multivora, P. pseudocryptogea and P. versiformis. Under‐bark inoculations with the Phytophthora isolates caused significant lesion lengths in excised C. calophylla stems. Corymbia calophylla response to pot infestation trials in the glasshouse varied between Phytophthora species and isolates, with isolates of P. cinnamomi and P. multivora causing a significant reduction in seedling root volume and often leading to seedling death. This study demonstrates that root disease caused by Phytophthora species, especially P. cinnamomi and P. multivora, has the ability to adversely affect C. calophylla health. This study leads the way to do a dual inoculation trial with the canker pathogen Q. coyrecup, and different Phytophthora species to investigate if Phytophthora root infection predisposes C. calophylla to this canker disease.     

Relationships among beech bark disease,climate, radial growth response and mortality of American beech in northern Maine,USA

A majority of beech forests across Maine first experienced beech bark disease (BBD) from 1935 to 1960 when sap feeding by an introduced beech scale insect, Cryptococcus fagisuga, allowed lethal fungal infections primarily by Neonectria ditissima and/or Neonectria faginata. Beech stands along the Maine–Quebec border in northern Maine were excluded from this initial killing phase presumably due to cold winter temperatures that inhibited scale survival. However, a sharp increase in beech mortality after 2002 occurred in previously uninfected border stands and stands long affected by BBD. Beech mortality averaged 50% across northern Maine during 2003–2006. To identify plausible stresses that could explain the mortality, a dendropathological study was conducted from 2005 to 2006 in northern Maine that quantified temporal and spatial relationships between possible stressors with beech mortality and growth decline. Nineteen sets of high‐ and low‐mortality plots were located randomly across four bioregions. Increment cores were taken from both beech trees (n = 565) and associated tree species (n = 450). A growth change index of increments was used to evaluate beech responses to biotic and climatic stresses. A prolonged period of relatively mild winters without temperatures lethal to scale insect (Neonectria was found infecting weakened trees across the region. Drought, beech scale and Neonectria are plausible explanations for the episode of high beech mortality in northern Maine. This is the first report of a major killing phase of beech within the BBD ‘aftermath’ forests.     

Effects of root trenching of overstorey Norway spruce (Piceaabies) on growth and biomass of underplanted beech (Fagussylvatica) and Douglas fir (Pseudotsugamenziesii) saplings

In Central Europe, the conversion of pure Norway spruce stands (Picea abies [L.] Karst.) into mixed stands with beech (Fagus silvatica L.) and other species like e.g. Douglas fir (Pseudotsuga menziesii [Mirb.] Franco) is accomplished mainly by underplanting of seedlings beneath the canopy of overstorey spruce trees after partial cutting treatments what means exposure to shade and below-ground root competition by the overstorey to the seedlings. Particularly about the second factor, our knowledge is limited. Therefore, we carried out a below-ground competition exclusion experiment by root trenching and investigated the effects on soil resources, growth, and biomass partitioning of underplanted beech and Douglas fir saplings under target diameter and strip cutting treatments. The exclusion of overstorey root competition by trenching increased the soil water potential in the second year that had a fairly dry growing season and led to significantly higher foliar concentrations of most nutrients, particularly in Douglas fir, indicating an amended nutrient supply. Both improvements were accompanied by an increase in length and diameter increment of the underplanted saplings, appearing in both species only after having surpassed a species-specific threshold light value (Douglas fir 16% of above canopy radiation, beech 22%). We also found significant interactions between trenching and light for specific fine root length and further biomass and morphological parameters. Judged by the much steeper increase in height and diameter growth with increasing light after release from below-ground competition, Douglas fir saplings appeared to be more sensitive to root competition than beech saplings what conforms to older findings for beech. According to our results, a strip cutting seems to be more appropriate than a target diameter cutting treatment to replace a pure spruce stand by a mixed stand with beech and Douglas fir.     

Regeneration growth in different light environments of mixed species, multiaged, mountainous forests of Romania

Growth of regenerating trees in different light environments was studied for the mountainous, mixed-species forests in the Carpathian Mountains of Romania. The primary species in these mixtures were silver fir (Abies alba Mill.), European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst). Seedlings/saplings of these species were selected and measured in different stands from two different geographical locations. Regenerating trees were measured for height and diameter growth during the summer of 2002. For each seedling/sapling, percentage of above canopy light (PACL) and stand basal area (BA) were used to assess available and occupied growing space respectively. Regeneration growth was compared against these two variables and regression relationships were developed. Using these models, we predicted the dynamics of regeneration as both growth and species composition. Our results showed that in low-light environments (PACL<20–35%; BA>30 m²/ha), shade tolerant fir and beech clearly outcompeted the spruce. Therefore, in dense stands, spruce could be eliminated by the shade tolerant species. For intermediate levels of cover (PACL=35–70%; BA=15–35 m²/ha) the spruce grew at comparable rates as the beech and fir. All three species showed similar growth rates in open conditions (PACL>80–90%; BA<15–20 m²/ha) with the spruce having a tendency to outgrow the others. However, in terms of establishment, such conditions favor spruce and inhibit fir and beech.