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.     

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.     

Dormouse injuries predispose beech to infection by Neonectria ditissima

After awaking from winter hibernation, the Edible dormouse begins to feed by stripping the bark and the outer part of the xylem from the branches of both broadleaves and conifers. Natural or artificial wounds are essential for the penetration and colonisation of the tissues by the fungal pathogen Neonectria ditissima. This pathogen creates open cankers on beech branches and other broadleaves, which are frequently later infected by wood‐decaying fungi. Because of the high frequencies of both dormouse injuries and branch cankers in a large monospecific beech forest in northern Italy, field and laboratory investigations were conducted to verify whether rodent‐inflicted injuries on beech were a preferred infection point for the pathogen. These studies also examined the susceptibility to infection of the dormouse‐inflicted wounds over time, and the relationships between dormouse damage, Neonectria infection, and wood decay. The results showed a significant direct correlation between the percentage of infections and their proximity to the wounds, indicating that the parasite localises to sites where there are receptive dormouse injuries. In addition, the susceptibility of the wound was found to diminish with increasing age, disappearing in 120–150 days. The association between dormouse injuries, Neonectria cankers and wood decay was also found to cause approximately half of the frequent beech branch breakages during intense weather events.     

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.     

Characterization of Cylindrocarpon‐like species associated with litter in the old‐growth beech forests of Central Europe

Cylindrocarpon‐like fungi are globally distributed plant pathogens and have a wide range of host species. However, very little is known about the species that live in the topsoil of forests and their potential role in reducing the natural regeneration of tree species, particularly of forest trees that produce abundant fruit only once every few years. To enhance our understanding of the species that inhabit the topsoil, we studied the diversity and pathogenicity of Cylindrocarpon‐like fungi inhabiting the litter in old‐growth mixed‐beech forests in the Carpathians (Poland) and in the Alps (Austria), and in a managed beech stand in the Krakowsko‐Cz?stochowska Highland (Poland). The fungi inhabiting the beech litter were investigated using beechnuts and pine seedlings as bait. Isolates were identified based on morphology and DNA sequencing. The pathogenicity of the most common species was investigated by inoculating beech germinants. A wide range of Cylindrocarpon‐like fungi were associated with the beech litter: 718 cultures representing 12 species were isolated. Five taxa were identified down to species level: namely Ilyonectria crassa, I. pseudodestructans, I. rufa, Neonectria candida and N. obtusispora, and seven species were identified to genus level (Neonectria or Ilyonectria species). Ilyonectria destructans, which is considered to be the sexual morph of ‘Cylindrocarpon destructans’, was not found. There were qualitative and quantitative differences between the different forest sites in terms of Neonectria and Ilyonectria species composition in beech litter. The isolation frequency and species richness of Cylindrocarpon‐like fungi were greatest in beech litter taken from old‐growth mixed‐beech forests. Neonectria and Ilyonectria species were capable of killing beech germinants, suggesting that they may play a negative role in natural beech regeneration.     

Amino nitrogen and phenolic constituents of bark of American beech,Fagus grandifolia,and infestation by beech scale,Cryptococcus fagisuga

Concentrations of amino acids, total amino nitrogen, and phenols, ratio of phenol to amino nitrogen, and pH in the bark of American beech, Fagus grandifolia, were determined to see if these chemical constituents were correlated with susceptibility of trees to infestation by the beech scale, Cryptococcus fagisuga. The relationship of these bark constituents with scale infestation levels (none, light, and moderate), tree size (large vs. small trees), and bark shading was determined. Levels of some individual amino acids and total amino acid content in moderately infested trees were significantly higher than in uninfested trees. Large uninfested beech trees, which tend to be more readily infested by scale, had significantly higher concentrations of aspartic acid. Concentrations of phenol in the outer bark of both infested and uninfested trees were significantly higher than in the inner bark. However in bark infected by Nectria, phenol levels in the inner bark were significantly higher than in the outer bark.     

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.     

Bark phenolics of American beech (Fagus grandifolia) in relation to the beech bark disease1

The amount of total extractable phenols was determined for bark sections obtained from behind cankers naturally induced by Nectria coccinea var. faginata and from behind mechanically inflicted wounds on stems of American beech. Healthy bark from susceptible trees was found to contain a similar level of phenolics as bark from trees determined to be resistant to the beech bark disease. Six months after wounding, wound-altered bark from susceptible trees was found to be lower in phenols than woundaltered bark from resistant trees. Inoculation of wounds with N. coccinea var. faginata resulted in decreased phenolic levels in bark sections nearest the wound surface, and increased phenolic levels in sections nearest the vascular cambium, several mm distant. Phenolic levels in injured or infected bark appear to follow similar patterns as those resulting from injury or infection of xylem tissues.     

Insights into the potential host range of Phytophthora foliorum

During a survey for Phytophthora ramorum undertaken in north‐west Scotland in early 2016, Phytophthora foliorum was found infecting foliage of the invasive shrub Rhododendron ponticum. Prior to this, P. foliorum had only been reported from foliage of hybrid azaleas in nurseries in California and Tennessee and from azalea plants in an ornamental nursery in Spain. No other hosts were known, and much of the behaviour of P. foliorum remained enigmatic. The species is classified in Phytophthora Clade 8c, with closest relatives, P. ramorum and Phytophthora lateralis, both of which are highly damaging tree pathogens. To explore the threat that P. foliorum might pose to trees, its growth–temperature responses on agar media and ability to cause lesions in the living bark of various hosts were contrasted with the behaviours of P. ramorum and P. lateralis. Phytophthora foliorum proved faster growing and more tolerant of temperature extremes than the other Phytophthora species. Comparisons of bark colonization initially focussed on R. ponticum and larch species Larix decidua and Larix kaempferi as all three are significant hosts of P. ramorum in the UK. Further experiments included another P. ramorum host, Fagus sylvatica (European beech), and the main host of P. lateralis, Chamaecyparis lawsoniana (Lawson cypress). Findings suggested that as well as being a significant pathogen of R. ponticum, damage caused by P. foliorum to both species of larch and beech was very similar to that of the EU1 lineage of P. ramorum, although growth in host tissue was also influenced by season.     

Parasitic association of the mycetophagous wood nematode,Bursaphelenchus fraudulentus with the honey fungus Armillaria ostoyae

Honey fungi, Armillaria spp. are common and economically important pathogens of a wide range of tree species grown both in the forest and orchard cultures worldwide. Our field research in 73 forest stands across Poland has shown a common association of the mycetophagous wood nematode, Bursaphelenchus fraudulentus with Armillaria‐infected trees. The data reported here provide the first insight into the parasitic interaction of a nematode and Armillaria ostoyae. In laboratory conditions, B. fraudulentus reproduced on A. ostoyae, caused substantial damage to its mycelium and, finally, killed the whole colony within a short time. In ageing cultures, the nematode produced resting (dauer) juveniles. After artificial inoculation to Armillaria‐infected trees, the nematode population persisted under the bark, continued feeding and mass reproduction on the mycelium, and dispersed over the mycelial fans. The ability of B. fraudulentus to develop and reproduce on the surface and inside the fungal rhizomorphs suggests that these structures could facilitate the nematode dispersion in the environment. Since B. fraudulentus is not pathogenic to the host tree, its parasitic association with A. ostoyae may contribute to natural regulation of this fungus in the environment. The observed characteristics of this nematode suggest that it could potentially be used as a biocontrol agent of honey fungi in forest and orchard trees.     

Dutch elm disease pathogen transmission by the banded elm bark beetle Scolytus schevyrewi

Dutch Elm Disease (DED) is a vascular wilt disease of Ulmus species (elms) incited in North America primarily by the exotic fungus Ophiostoma novo‐ulmi. The pathogen is transmitted via root grafts and elm bark beetle vectors, including the native North American elm bark beetle, Hylurgopinus rufipes and the exotic smaller European elm bark beetle, Scolytus multistriatus. The banded elm bark beetle, Scolytus schevyrewi, is an exotic Asian bark beetle that is now apparently the dominant elm bark beetle in the Rocky Mountain region of the USA. It is not known if S. schevyrewi will have an equivalent vector competence or if management recommendations need to be updated. Thus the study objectives were to: (i) determine the type and size of wounds made by adult S. schevyrewi on branches of Ulmus americana and (ii) determine if adult S. schevyrewi can transfer the pathogen to American elms during maturation feeding. To determine the DED vectoring capability of S. schevyrewi, newly emerged adults were infested with spores of Ophiostoma novo‐ulmi and then placed with either in‐vivo or in‐vitro branches of American elm trees. The inoculation of trees via feeding wounds was successful 30% of the time for in‐vivo trials and 33% for in‐vitro trials. Although the infection rate of DED has declined in Colorado over the past 10 years, the disease is still present in urban elms. While it appears that S. schevyrewi is another vector of the DED pathogens, it appears that S. schevyrewi is no more efficient than S. multistriatus. Thus, management programs that remove elm bark beetle breeding sites, rapidly remove DED‐infected elms and include the planting of DED‐resistant elms should continue to be effective management tactics.     

Genetic diversity and bark physiology of the European beech (Fagus sylvatica): a coevolutionary relationship with the beech scale (Cryptococcus fagisuga)

In 1994 and 1995, the degree of infestation by the beech scale (Cryptococcus fagisuga Lind.) was recorded on 120 beech trees (Fagus sylvatica L.) in the Pless Forest near G?ttingen, Germany. Simultaneously, the trees were characterized genetically and compounds of primary and secondary metabolism of beech bark were analyzed. A correlation was established between beech scale infestation and the genotype of the host trees, based on gene locus A of isocitrate dehydrogenase (IDH-A). The fraction of infested beech trees was higher in the heterozygous genotype A2A3 group than in the homozygous genotype A2A2 and A3A3 groups, whereas the fraction of beech trees with decreasing infestation from one year to the next was lower in the heterozygous genotype A2A3 group than in the homozygous genotype A2A2 and A3A3 groups. Concentrations of soluble carbohydrates, protein amino acids and proanthocyanidins were determined in the inner and outer bark of trees with differing degrees of infestation. The results indicate that the defense reaction of beech against infestation by beech scale comprises multiple processes in which nutrient availability to the beech scale is reduced by concentration shifts and by the formation of inhibiting compounds.     

Pathogenicity of ophiostomatoid fungi on Picea abies in Slovenia

Pathogenic fungi can survive and develop in living plants, often causing diseases in the host. Some theories speculate that pathogenic ophiostomatoid fungi provide benefits to its vectors – bark beetles – by overcoming the tree's defence mechanisms. This study reports the results of an experiment in south‐eastern Europe in which mature and seedling Norway spruce trees were artificially inoculated with various ophiostomatoid fungi. The aim of the experiment was to determine the relative virulence of ophiostomatoid fungi by assessing the ability of the fungi to stimulate host tree defence mechanisms through inoculation experiments. Experiments were performed by inoculation of Picea abies in seedling and mature trees. The following fungi were used in low‐density and seedling inoculations: Ophiostoma ainoae, O. brunneo‐ciliatum, Grosmannia cucullata and an unidentified Leptographium sp., O. bicolor, O. fuscum, O. piceae, G. penicillata and G. piceiperda. Endoconidiophora polonica was used in mass and seedling inoculations. Various characteristics such as host vitality, blue stain, lesion and resin outflow were measured before and after the trees were felled. E. polonica caused blue stain, induced large lesions and killed some of the mature trees and seedlings, confirming earlier reports that it is a strong wound pathogen. Only E. polonica, Leptographium sp. and O. ainoae caused blue stains in the sapwood of inoculated seedlings. In low‐density inoculations, G. piceiperda induced intense necrosis and had higher values for all the characteristics monitored. Some of the other ophiostomatoid fungi showed a moderate level of pathogenicity. Fungi with the capacity to stimulate a host defence mechanism could play a role in the establishment of bark beetle populations.     

Diversity and spatio-temporal dynamics of dead wood in a temperate near-natural beech forest (<Emphasis Type="Italic">Fagus sylvatica</Emphasis>)

The diversity, spatial patterns and temporal dynamics of dead wood were examined within the near-natural beech forests (Fagus sylvatica) of Serrahn (North-eastern Germany). Data were collected in an 8 ha sample plot and in two permanent plots (0.36 and 0.25 ha) that had been established at the end of the 1960s. The mean volume of dead wood was 94 m³ ha⁻¹, amounting to 14% of the total volume of all trees. The dead wood displayed a large variation in dead wood type, tree size and decay class. Standing dead wood accounted for about one-third of the total dead wood volume. The densities of standing dead trees were about 10% of the densities of the living trees over a wide range of diameters. The overall spatial distribution of dead trees exhibited a random pattern. Among the different dead wood types, standing entire dead trees and uprooted trees deviated from this pattern by displaying a significantly aggregated pattern. In the permanent plots a high mortality of overstorey trees was observed (1.3% year⁻¹) and the average amount of dead wood increased greatly from 2.9 to 111.6 m³ ha⁻¹ over the 35-year observation period. The near-natural beech forests of Serrahn have experienced a long period of low human interference. Nevertheless, our results suggest that the structure and dynamics of dead wood are strongly affected by the last major disturbance events that took place at the end of the Middle Ages. Information about the forest history is therefore a basic requirement when interpreting the results obtained in near-natural forests.     

Factors influencing the dispersion of Arceuthobium oxycedri in Central Spain: evaluation with a new null model for marked point patterns

The dwarf mistletoe, Arceuthobium oxycedri, is found on populations of Juniperus oxycedrus, in central Spain. This species can have negative effects on the physiology of its host, including mortality. Understanding the mechanisms that control its distribution and dispersal is critical to assessing its potential for spread. We assessed dwarf mistletoe distribution within a population of J. oxycedrus, including infected and uninfected host individuals. A new null model of parasitic dispersion was built using two dispersal kernel forms that were simulated with lower and upper envelopes for second‐order functions to summarize a point pattern, such as Ripley's K, nearest‐neighbour distribution and pair correlation functions. Nine dispersal scenarios were constructed with half‐bandwidth kernels (10, 20, 30 m) and initial population of infected trees (P₀ = 05, 10 and 20). These scenarios were compared with the observed pattern and evaluated using the goodness‐of‐fit test. Significant differences at short distance (r < 10 m) were found between the observed pattern and simulated patterns, corresponding to the range of seed dispersal of the dwarf mistletoe. Interactions between infected and uninfected hosts patterns at all scales were identified, suggesting that A. oxycedri uses other mechanisms in addition to ballistic seed shooting as secondary dispersal agents to spread to distances greater than 20 m. Given that the seed characteristics facilitate dispersal by adhesion, we infer that spread between host individuals is amplified by seed transport by birds or small mammals.     

La variabilité de la sensibilité du Hêtre (Fagus sylvatica L.) à Nectria coccinea,un des agents de la maladie de l'écorce

Variability of Fagus sylvatica susceptibility to Nectria coccinca, one of the agents of beech bark disease . N. coccinea was inoculated into wounds of young beeches raised from seeds of 6 bark diseased trees and 6 healthy ones in the same stand of the forest of Lyons. Classifieation of the progenies, according to the size of the necrosis, is in good agreement with the health of the mother trees. N. coccinca susceptibility of beech has a genetic origin.     

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.     

Lesion formation and host response to infection by Armillaria ostoyae in the roots of western larch and Douglas‐fir

The process of lesion formation and host response to natural infection by Armillaria ostoyae were studied in the roots of western larch (Larix occidentalis) and Douglas‐fir (Pseudotsuga menziesii ssp. glauca) trees in the three age classes, 6–8, 18–19 and 85–95 years. The characteristics of lesions on infected roots were recorded and bark samples were dissected from infection points and lesion margins in the field and stored in liquid nitrogen for macroscopic study in the laboratory. Infection in the roots of 6‐ to 8‐year‐old trees advanced freely, overcoming any host resistance, quickly girdling the root collar and killing the trees. In 18‐ and 19‐year‐old trees, however, 43% of infections on western larch and 27% of the infections on Douglas‐fir roots were confined to lesions bounded by necrophylactic periderms with multiple bands of phellem. Host response was similar in 85‐ to 95‐year‐old trees, but the percentage of confined lesions was higher than in younger trees. The results suggest that larch shows resistance to A. ostoyae at a younger age and with greater frequency than Douglas‐fir.     

A twig blight of understorey European beech (Fagus sylvatica) caused by soilborne Phytophthora spp.

During and after prolonged periods of rainfall in late spring, blighted young twigs of European beech (Fagus sylvatica) were frequently observed in several beech stands in south‐western and southern Germany. Long and short shoots of young understorey trees or lower branches up to 1.5 m above the soil level were affected. Symptoms also occurred regularly on twigs in heights up to 2 m and more above the ground. Necroses usually expanded within the current year’s tissue and often also reached into the previous year’s wood. Ponding rain water in the stands or along forest roads or open soil seemed to promote the disease. Of a total of 54 symptomatic twigs collected in four stands, 37 revealed Phytophthora isolates, of which 33 were P. plurivora and four were P. cambivora. Both species caused extensive lesions on beech twigs in laboratory pathogenicity tests. Patterns of the disease indicated that these pathogens, generally considered soilborne species, in most cases are transmitted from the soil to above‐ground parts of the trees via rain splash. In larger heights, however, other vectors such as snails might be responsible for transmission. Although Phytophthora spp. are well known as causal agents of seedling blight as well as root and cambium rot and aerial bleeding cankers of mature beech, to our knowledge this is the first report of a twig blight in beech associated with soilborne Phytophthora spp. In particular in periods of high precipitation, this disease might pose an additional threat to Central European beech forests, especially endangering the success of artificial and natural regeneration of beech in affected stands.