Forster, B.; Knizek, M.; Grodzki, W. (eds.) 1999: Methodology of Forest Insect and Disease Survey in Central Europe.
Proceedings ofthe Second Workshop ofthe IUFRO WP 7.03.10, April20-23, 1999, Sion-Chateauneuf, Switzerland.
Birmensdorf, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL) 175-180.
METHODOLOGY IN DISEASE SURVEY OF OAK FOREST IN FOREST- STEPPE OF RUSSIA
Nelly N. Selochnik Forest Science Institute
p/o Uspenskoye, 143030, Moscow region, Russia
For the last 16 years we have studied the role of pathological factors in oak decline by means of regular surveys of the forests in the russian forest-steppe and partially mixed forests, as well as monitoring on trial plots and mycological studies.
Before proceeding directly to oak diseases, we would like to consider some general problems of oak decline in Russia, and to emphasize the role of stress situations, predis- posing to fungal and other infections.
The Russian main oak massifs, such as Shipov and Tellerman forests (about 40 000 ha either), so called Tula-zaseks (abatis), some reserves and other oak stands are found in the forest-steppe ( 76.5% of oak forest areas). It should be mentioned, that in the Teller- man forest multidisciplinary biogeocenotic investigations have been continued for over 50 years (Osipov et al. 1989). Analysis of the relevant literature and our own surveys of oak forest ecosystems in the Russian Plain allows us to offer classification of oak degra- dation factors, appretiate the general pathological state of oak forests in the forest-steppe zone and try fmd out the causes of their decline in the last decades (Selochnik and Osipov 1996; Selochnik 1998a, 1999).
Among the factors not related to human activities are background processes, such as deaths of retarded trees in high density stands, drying-out of old age oaks or slower dying of oaks in inappropriate environmental conditions, for instance solonetz soils.
The most common type of drying-out is a periodical mass oak decline as a result of growth depression. Most often it is caused by a stress inducing combination of adverse abiotic and biotic factors in the natural environment (droughts, severe winters, crown defoliation by leaf-eating pests and diseases).
During 1983-1998 the author together with his colleagues surveyed about 30 forest massives in the forest-steppe zone and neithbouring regions, among which were stands, undergoing repeated catastrophic waves of decline in the past. However in this period we did not reveal either of extensive oak decline or typical foci of diseases, that could be the the primary source of oak decline. So we arrived at the conclusion, that the oak forests in the forest-steppe, severely damaged in the past, were able to recover due to oak's satel- lites and crown reconstruction in the remaining oak trees.
But in spite of generally satisfactory condition of oak stands in the Russian Plain in this period, in every of the 30 oak massifs surveyed a number of damaged oak stands were found, where the weakening and continued decline were related to the effects of an- tropogenic factors, which may be divided into two main groups: 1) poor forest manage- ment that fails to meet oak requirements; 2) human economic activities which disrupts directly or indirectly the habitat in the oak forest. Among the types of these activities, air pollution is of greatest importance. Especially harmful to oak forest were associations of factors, such as climatic stress, insect-induced defoliation and antropogenic burden.
The methodology in our survey of oak forests conditions included alsow annual de- tailed monitoring performed at the research station of the Forest Science Institute (the Tellerman oak forest in Voronezh province, about 650 km south of Moscow), where three waves of oak decline took place in the last 50 years (1940-s, 1960-s, 1970-s). The records were carried out in14 permanent trial areas (0.1-1.0 ha. in size each) in the three different types of oak stands, namely the upland goutweed-sedge type, flood-plain lily-of the valley dewberry type and solonetz type. The ages of the stands varied between 60 and 250 years. All the oak trees growing in the trial areas (over 1000) were marked individu-
ally in the past and examined annually during the period of observation. The trees. were evaluated visually and assigned one of the 6 following categories of state: 1 - apparently healthy; 2 - slightly weakened; 3 - severely weakened; 4 - declining; 5 -new dead stand- ing; 6 - old dead standing. The categorization was based on 24 different characteristics describing the state of the crown and stem (Selochnik and Kondrashova 1989).
Unfortunately my phytopathological studies began in 1983, when the last massive wave of oak decline in Tellerman forest (1975-1982) nearly ended. This accounts for the improvement in oak stands recorded in the following 10 years. At present the state of the trees under observation taken as a whole is continuously improving.
The oak decline syndrome, which we have observed in different zones, forest-types, age generations, and environmental conditions, is generally manifested by symptoms of sparsing of the crown, presence of dry branches and twigs, dry tops, yellowing of the foliage, water sprouts on the stems and branches. But these signs are not specific for the particular disease and they may reflect the effects of the environment constraints, antro- pogenic stresses, insect-defoliations and fungous diseases.
However, the precise role of fungous pathogens in oak decline is yet uncertain, and in various regions it is assessed rather differently. As for the Tellerman forest, the last phy- topathological studies (before we undertook our work here) were in 1940-s (V akin 1954), so we have attempted now to look into this intricate matter in our region, and investi- gated the distribution, pathogenicity and some problems in the ecology and biology of main oak diseases and their pathogens.
According to A.T. Yakin (1954) the main diseases of oaks were stem rots, caused by Basidiomycetes. Our analyses of fungal infestation in the oak stands of the Tellerman forest and other stands surveyed in the forest-steppe zone showed that shelf-fungi, which parasitized on living oak trees, such as Inonotus dryophillus, Phellinus robustus and in over-matured stands Laetiporus sulphureus, Inonotus dryadeus, Fistulina hepatica were unable to bring the tree to rapid death, and the disease could last for many years.
From the group of macromycetes fungi, Armillaria-complex was most commonly found on the oak trees. Some investigators believed that this pathogen was the primary infectious agent of the oak decline. So in our investigations we made a special emphasis on the A rmillaria disease. The methodology of studies included regular inspections of all the trees and stumps in the trial plots, digging down tree roots of different state catego- ries in various forest types and the value of fungus fructification. It was established, that the fungal infection was consistently present as rhizomorphs in the forest litter and stem base of virtually all the oak trees regardless of their state or oak stand type. However the rhizomorphs mass in the litter varied in different oak stand types. Measured by Pronos and Patton's method (1977), the mass of rhizomorphs in the litter did not correlate with the tree state category and ranged from 76 kg/ha in dry growth conditions (solonetz type) to 129 kg/ha in a flood plain (Selochnik and Kondrashova 1991).The basidia of Armil- laria appeared almost annually in the forest litter and on the stem root neck and were abundant, provided favourable temperature and moisture in the autumn. So, it may be supposed that Armillaria-complex is a regular member of the oak forest mycobiota. We have noted three phases in the mechanism of Armillaria colonizing the oak tree: phase 1 - epiphytic growth of rhizomorphs and sometimes of basidia on the surface of roots and root neck; phase 2 - ectotrophic growth o( fungal micelium in the bark (with occasional fruit bodies in wet conditions); phase 3 -penetration under bark and colonization of sap wood. Phases 1 and 2 did not injure healthy oak trees, because of being only superficial.
Phase 3 took place only in severely weakened and declined trees. We established alsow that harmfulness of honey agaric increased with oak age, and stem rot developed faster then root rot, which occurred after the crown decline (Selochnik and Kondrashova
1989). On the basis of root digging we worked out a scale of Armillaria-infection of oak
tree standing , where the tree state category was correlated to fungus colonization of stem, root neck and branch root (The table).
Among diseases induced by fungi-micromycetes we consider the oak mildew and vas- cular mycosis as most important. The pathogen of oak mildew Microsphaera alphitoides is the most widespread foliage fungus. The disease has wide occurrence in all the types of forest and age classes of oak stands, but mostly affects the secondary foliage growing out after severe insect defoliation. Under conditions of the Tellerman forest, oak mildew is more harmful for the oak trees of earley- foliated varieties in the light flood-plane stands, which regularly from year to year fall victims to defoliation by permanent insect complex ( Rubtsov et al. 1989; Selochnik et al. 1994; Selochnik and Romanovsky 1997).
In the upland oak forests, which are most valuable and productive, in the absence of the outbreaks or foci of insect-defoliators, the disease is not so damaging. However we have suggested for such stands a new forest technique to estimate a degree of leaf damage along the vertical profile of the canopy (Selochnik et al. 1994).
The evaluation of distribution and severity of oak mildew was carried out on felled model trees and branches from different parts of crowns. The average leaf samples were taken from different vertical layers and sides of trees (related to the cardinal points).
The degree of infestation of each leaf was determined by a 5-graded scale: 0 - no infec- tion, 1 - single small spot of thin fungus coating, 2 - infestation to 25% of leaf surface, 3 - to 50%, 4 - above 50%. Then the percentage of diseased leafs and the intensity of disease were estimated by a conventional method for the every layer. Similarly, the degree of insects leaf- eating was assessed. Using an equation relating the leaf-mass to d2H, the general mass of stand-foliage in every layer and then its infection and defoliation are obtained. Cutting of model trees of different Kraft's klasses enabled generalization of these data on the whole stand. It was established a clear tendency for mildew infection in high- density stands to increase in up-down direction. This meant less damage to the trees because of a relatively less mass of foliage in the lower crown, than in the upper and middle layers. Mildew infection of the most physiologically active layers in the crown (top and middle parts) of the trees in dominant classes I-II, with a slight degree of defo- liation by phyllophages was not serious (Selochnik et al. 1994).
One of the most significant results from the studies on the causes of oak decline, re- lates to the assessment of the possible role of vascular mycosis. We carried out mycologi- cal analyses on specimens of branches, cuttings and cores from about 1500 healthy to dead trees in the Tellerman forest and some other massifs of the Middle-Russian Plain.
Since the external signs of disease are nonspecific and similar to those of oak decline syndrome described above, we made emphasis on internal characteristics of wood and mycological analyses. Internal signs of the disease are brown or black spots, streaks, ne- croses on a cross-section and longitudinal lines along the stem or branches. But even these signs are not always sufficient to identify the disease as vascular mycosis and reveal the pathogen's presence because the causative organisms of vascular mycosis in our in- vestigations first of all were present in living trees, sometimes without signs of disease.
Thus, those behaved as endophytic fungi - members of the forest mycobiota. Our data agree with suggestions about an endophytic existense of some fungi in oak tissues (Butin
1987; Balder 1989; Halmschlager 1993). On the other hand, internal signs alone are not adequate to identify the vascular mycosis, because the same symptoms may be induced by other fungi. Inparticular, we isolated apart from Ophiostoma species, species of Fusarium, Cylindrocarpon, Cladosporium and others. Thus it is necessary to confirm the disease ].Jy identifying the pathogens in every case.
We d_eveloped an express method for vascular mycosis diagnosing, using the technique of taking the cores. It was used in mycological practise where the cores are placed on an artificial nutrient medium (Knighten and Maxwell1971). However this technique is rather time-consuming and makes it more difficult to identify pathogens. So we used
steril test tubes with wet strips of filter paper within as wet cameras for cores, taken by an increment hammer, sterilized with alcohol . The cores were then incubated at 23-25°C and viewed with a binocular microscope (x 16-32) every 3 days. Under the favorable conditions of a natural nutrient medium, typical coremia of Graphium sp. could appear in 3 days, and perithecia of Ophiostoma sp. -in 7 days, but sometimes these sporulations might appeared much later, during about a month. The same and even better results were obtained by placing hewings into wet cameras of petry dishes, providing more air and better environment for fungi. But because the hewings are harmful to the tree, we took the hewing only from declining or dead trees.
In view of identification difficulties with the teleomorph stage we tried to recognize these on the anamorphs. Judging from the anamorphs ( fungi of the species Graphium, Hyalodendron, Rhinotrichum, Cephalosporium, Verticillium), teleomorphs belonged to Ophiostoma roboris, 0. walachicum and 0. kubanicum, reported by many russian investi- gators (Shcherbin-Parfenenko 1953; Minkevich 1962; Kryukova and Plotnikova 1985;
Selochnik 1998b ). Two of them ( 0. roboris and 0. valachicum), according to european scientists (Hunt 1956; Gibbs 1981;Kowalski and Butin 1989; Przybyl and de Hoog 1989;
Brasier 1993 and others),clously related tosaprotrophic species Ophiostoma piceae, which is a weak pathogen at most. In the USSR it was indicated only as a habitant of the conif- erous species (Potlaichuk and Shchekunova 1985) , so this issue needs further studies.
As for species 0. kubanicum, there is evidence of its more pathogenic and aggressive properties and its distribution in the south-east of Russia (Krykova and Balder 1993).
So, in the light of numerous studies performed in Europe, there is every reason to sug- gest, that in Russia, with regard to the vascular mycosis, apart from more aggressive fungous species and strains in the arid south-east of the country, we are dealing with a variable, ubiquitous sapwood-discolorating fungus, colonizing both deciduous and conif- erous species, manifesting its pathogenic features only under stress conditions.
In total, considering all the principal oak diseases in a complex with their correspond- ing environmental factors, we may conclude, that in the european part of Russia oak decline is not a specific disease, because of its multiple etiology. And on every single oc- casion it is useful to establish the source of a predisposing stress, and the vascular disease should be identified by means of mycological examination.
References
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Table. Degree of honey agaric infestation in different categories of oak trees
Evidence of Tree state category
infection 1 2 3 4 5
Rhyzomorphs on Only epyphytic on the root neck Penetrate the bark Penetrate the bark
stem and ascend the stem
I
No No or only epiphytic No, or only There is the foci of fungus penetration I
Rhysomorphs on epiphytic, or on dry under the bark
root branches sides, mechanical
damages, in sites of insects nibbles
Rot on root neck No Only ectotrophic The fungus penetrate the kambium and The sapwood rot
growth in the bark the sapwood spreads up the stem
Rot on root No No Ectotrophic growth There is the foci of The sapwood rot on
branches in the bark, in the fungus penetration all or major part of
sapwood - on dry under the bark, not root branches sides , mechanical nessesary on wounds
injuries, and in the and injuries; partial sites of insects nibbles rot of sapwood
