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Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. Forest. Pathol., 32, 277-307 ARTICLE in FOREST PATHOLOGY · JULY 2002 Impact Factor: 1.37 · DOI: 10.1046/j.1439-0329.2002.00291.x

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For. Path. 32 (2002) 277–307 2002 Blackwell Verlag, Berlin ISSN 1437–4781

Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe By F. M. Thomas1, R. Blank2 and G. Hartmann2 1

¨ kologie und Universita¨t Go¨ttingen, Albrecht-von-Haller-Institut fu¨r Pflanzenwissenschaften, Abt. O ¨ Okosystemforschung, Untere Karspu¨le 2, 37073 Go¨ttingen, Germany; E-mail: [email protected];

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Niedersa¨chsische Forstliche Versuchsanstalt, Abt. B (Waldschutz), Gra¨tzelstr. 2, 37079 Go¨ttingen, Germany

Summary Incidences of oak decline have occurred repeatedly during the past three centuries as well as in the most recent decades. On the basis of historical records and dendrochronological measurements, oak decline in Central Europe has been attributed to the single or combined effects of climatic extremes (winter frost, summer drought), defoliating insects, and pathogenic fungi. Starting from a literature review, we discuss the possible roles of various abiotic (air pollution, nitrogen eutrophication, soil chemical stress, climatic extremes, site conditions) and biotic factors (insect defoliation, borer attack, infection by pathogenic fungi, microorganisms) that have been related to oak decline. On the basis of investigations on Quercus petraea and Quercus robur at three different levels (from experiments with young trees to monitoring on a supraregional scale), we suggest a conceptual model of the interaction of abiotic and biotic factors responsible for the onset of oak decline. This model should be valid for Central European oak stands at more acidic sites (soil pH (H2O) £ 4.2; on soils with higher pH, pathogenic Phytophthora species may contribute to oak decline). The combination of severe insect defoliation in at least two consecutive years with climatic extremes is the most significant complex of factors in the incidence of oak decline. Combined with defoliation, summer drought or winter ⁄ spring frost or both have to occur within the same year or in consecutive years to trigger major outbreaks of decline. Important additional stress factors are the following: (1) hydromorphic site conditions which, particularly in the case of Q. robur, render the trees more susceptible to drought stress as a result of an impairment of root growth in the subsoil; and (2), possibly, excess nitrogen which, in combination with drought stress, results in distinct decreases in the foliar concentrations of allelochemicals in Q. robur, thereby probably making the trees more susceptible to insect defoliation. Air pollution, soil chemical stress (including excess manganese), and nitrogen-induced nutritional imbalance do not seem to be important causal factors in the complex of oak decline. On the basis of the model, the appearance of the most recent oak decline in North-western Germany can be adequately explained.

1 Introduction In addition to the European beech (Fagus sylvatica L.), oak (Quercus) species are – both economically and ecologically – the most important broad-leaved forest tree species in Europe. In its natural occurrence in Central Europe, the genus is almost exclusively represented by Q. petraea (Matt.) Liebl. (sessile oak) and Q. robur L. (pedunculate oak; with a large extension into Eastern Europe) with only minor contributions by Q. pubescens Willd. and Q. cerris L.; the latter two and the other important European oak species (Q. frainetto Ten., Q. ilex L., Q. suber L.) occur in the Mediterranean region or Eastern Europe (Meusel et al. 1965). Whether Q. petraea and Q. robur should be considered as two separate species or as two ecotypes within the same species is still subject to discussion. Support to an assessment of the taxa as two ecotypes within a common species is given by their pronounced ability to Received: 13.9.2001; accepted: 25.3.2002; editor: C. Delatour

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hybridize and by the lack of disjunctive expressions of morphological and genetic traits (e.g. Bacilieri et al. 1995; Kleinschmit et al. 1995; Bodeńe`s et al. 1997). However, both taxa can only be crossed to a limited extent, and both taxa can be well distinguished by a combination of several morphological parameters, with only a small portion of the trees taking an intermediate position that indicates real hybrids (Aas 1998). In addition, the different distribution of the taxa as well as the differences in their ecophysiological traits and responses are known from a large body of literature. In the present contribution, we keep to the conventional nomenclature of the taxa as two species, without ignoring their high genetic, physiological and morphological plasticity. During the past three decades, occurrence of oak decline has been recorded in many European countries (roughly, from east to west: Russia, Romania, Yugoslavia, Poland, Slovakia, Czech Republic, Hungary, Austria, Germany, the Netherlands, Sweden, UK, Belgium, France, Italy, Spain, Portugal; cf. Oleksyn and Przybyl 1987; Hartmann et al. 1989; Siwecki and Liese 1991; Andre´ and Laudelout 1992; Bayerische Akademie der Wissenschaften 1993; Luisi et al. 1993; Redfern et al. 1993; Ro¨sel and Reuther 1995; Gibbs and Greig 1997; Szepesi 1997; Barklund and Wahlstroem 1998; Sonesson 1999). In the Mediterranean region, mainly Q. ilex has been affected (Mu¨ller-Edzards et al. 1997), but decline has been also reported for deciduous oak species (Q. cerris, Q. frainetto, Q. pubescens and Q. robur) in Italy (Ragazzi et al. 1998), and for Q. suber on the Iberian peninsula (e.g. Sousa Santos and Moura Martins 1993). Thus, oak decline is widespread in Europe. However, the symptoms and causal factors may not be the same in all regions. The type of decline discussed in this paper prevails in North-western Germany. It is characterized by cyclic episodes of rapid mortality in local but widespread centres, followed by decreasing and slower mortality. Such episodes may last for up to 10 years and be sometimes preceded by a predisposing phase of reduced growth. In Northwestern Germany, they have occurred several times between 1910 and 1940 and after 1987 and 1997 (Hartmann et al. 1989; Hartmann and Blank 1998; Wachter 1999, 2001). This type is considered to be different from general forest decline, which is characterized by increased crown transparency of entire forest stands in big areas, but low mortality. This latter type is surveyed since more than 10 years by standardized European monitoring of crown condition (e.g. Mu¨ller-Edzards et al. 1997). According to this monitoring, the vast majority of oaks exhibits minor to medium crown transparency, and very low mortality rates (e.g. Eichhorn and Paar 2000). This monitoring provides data on average crown condition of large areas and on correlations of crown condition with potential stress factors (Klap et al. 2000). However, it does not satisfactorily represent the type of decline with high mortality in local centres, because these are often missed by the coarse and systematic sampling grid. Furthermore, the capacity of this monitoring to reveal temporal trends is presently limited to about 10 years. This is rather short in relation to the periods of 7–9 years (Altenkirch 1991) in which major causal factors such as gradations of defoliating insects or extreme weather conditions may occur. For these reasons, data from this monitoring system were not considered in this contribution. In the past two decades, several attempts have been made to explain the onset of oak decline by identifying the factors that trigger the outbreak of the damage (e.g. Delatour 1983; Hartmann et al. 1989; Hartmann and Blank 1992; Schu¨tt 1993; Schlag 1994; Hartmann 1996; Donaubauer 1998; Siwecki and Ufnalski 1998). In all of these studies, oak decline was not considered to be caused by a single factor but by complex interaction of several biotic and abiotic factors. However, evidence has been predominantly based on temporal and spatial coincidence of the factors and the occurrence of decline. Blank (1997) proposed a more mechanistic explanation, but lacked experimental evidence. Thus, up to now, a concise mechanistic explanation of the causal complex of oak decline is still lacking.

Causes of oak decline in Central Europe

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In this study, we attempt to contribute such an explanation by suggesting a conceptual model of the interaction of abiotic and biotic factors that are crucial to the onset of oak decline. This model is based on investigations that were performed at three different levels (from experiments with young trees to monitoring on a supraregional scale). The investigation has been conducted in Northern Germany on Q. petraea and Q. robur; therefore, the conclusions derived from these results apply to these two species and to regions with a climate similar to the temperate humid climate of Northern Germany, i.e. the majority of Central Europe. For our purposes, we define the region of Central Europe on the basis of the prevailing climatic conditions; it includes western Poland and Slovakia in the east, Austria and Switzerland in the south, North-eastern France in the west, and the British Isles and Denmark in the north. Initially, we describe the visible symptoms of oak decline, and continue by providing an overview, supplemented by our own results, of the abiotic and biotic factors that have been repeatedly considered to be part of the factorial complex of oak decline.

2 Symptoms of oak decline and occurrence of oak decline in historic time 2.1 Symptoms of oak decline The symptoms in declining oaks are as follows: crown thinning due to abnormally increased twig abscission and dieback of buds and branches in the upper canopy; remaining leaves arranged in tufts at the end of the shoots; discoloration or yellowing of the leaves in some cases; reduced leaf size; epicormic shoots; slime flux on the trunks; progressive necroses of bark and cambium and reductions in diameter growth (e.g. Hartmann et al. 1989; Hartmann and Blank 1992; Schlag 1994; Hartmann et al. 1995). The various symptoms do not necessarily occur synchronously and vary in their degree of expression. In the progressive course of the decline, part of the crown or the whole tree dies. Such dieback can affect single trees or groups of trees within stands, parts of stands and, rarely, whole stands. If the trees cannot recover, they die within one or some few years (cf. Bayerische Akademie Der Wissenschaften 1993; Schlag 1994; Block et al. 1995). Both oak species are subject to decline. In France, Poland and Germany, Q. robur is more severely affected than Q. petraea (e.g. Wachter 1999; Oszako 2000; Svolba and Kleinschmit 2000; Wachter 2001). In Northern Germany, after severe winter frost (1985–87) and insect defoliation, Q. petraea was as much affected as Q. robur (Hartmann et al. 1989; Hartmann and Blank 1992). Although it is part of the complex of symptoms related to oak decline, crown thinning due to increased twig abscission does not necessarily result in a complete decline of the tree. Rather, the active shedding of twigs from the crowns of mature oaks can be seen as a mechanism of acclimatization to drought stress resulting from conditions such as severe summer drought, preceding frost and ⁄ or insect defoliation, or impairment of root growth that reduce the water flow to the respective twigs (e.g. Thomas and Hartmann 1996; Klugmann and Roloff 1999). Under those conditions, twigs may be actively shed due to the activation of an anatomically differentiated abscission zone (Klugmann and Roloff 1999). If the environmental conditions improve, the loss of twigs may be compensated by a production of new ones in the following vegetation periods, and the crown may completely recover. On the other hand, continuation of adverse environmental conditions or even their aggravation by additional stress factors may prevent both the full integration of the xylem of already produced twigs into the hydraulic system of the tree and the formation of new shoots, and may result in a progressive decline of the crown (Klugmann and Roloff 1999).

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2.2 Lime-induced chlorosis symptoms at calcareous sites The symptoms of oak decline in its true sense have to be separated from chlorosis symptoms in Q. robur (far less frequently in Q. petraea) growing on calcareous soils, predominantly in solitary trees or in exposed trees at the margins of a stand (Hartmann 1996). In such trees, the symptomatic leaf yellowing (progressing from pale-green with a netlike chlorotic pattern to uniformly yellow) affects single branches, parts of the crown or the entire crown and is clearly different from leaf discoloration that sometimes occurs in oak decline syndrome, but is very typical for a lime-induced iron ⁄ manganese chlorosis (Hartmann et al. 1989; Hartmann et al. 1995). Although single branches or part of the crown may die, the trees often live for many years and only die after intense chlorosis has lasted for a long time. In an investigation on soil and leaves from stands of Q. robur exhibiting these symptoms, it was shown that the chlorosis syndrome was linked to a lime-induced manganese deficiency, enhanced by a short supply of (physiologically active) iron (Thomas et al. 1998). Thus, this type of chlorosis can be explained satisfactorily by edaphic site factors, and should not be confounded with the oak decline syndrome. 2.3 Occurrences of oak decline in historic times In Central Europe, episodes of oak decline have occurred repeatedly during the past three centuries. The earliest incidence that is verified by archival records took place in North-eastern Germany in 1739–1748 and was triggered by extremely severe frost in the winter of 1739–40 (Hausendorff 1940). Further episodes of oak decline were reported from Germany during the period from 1909 to 1940 (cf. Blank 1997; Wachter 1999). They were assumed to have been caused by a combination of the following factors: insect defoliation together with either winter frost, summer drought or flooding, and with powdery mildew (Microsphaera alphitoides Griff. et Maubl.). These agents of stress were then followed by attacks of pathogenic fungi (Armillaria) and borers (Agrilus) (Hartmann and Blank 1992; Hartmann 1996). During the past century, occurrences of oak decline have also been observed in other Central European countries (cf. Delatour 1983). In Poland, increased mortality of oaks was observed during and after a period from 1939 to 1942, when severe winter frost occurred. In the Netherlands (1921 and thereafter) and in Czechoslovakia (1947 and thereafter), oak decline occurred after severe drought whose impact was probably aggravated by ensuing infections with pathogenic fungi. In France (1921–26, 1942–50) and in the south of the UK (1920–24, 1958; cf. Gibbs and Greig 1997), episodes of oak decline presumably were triggered by combined effects of insect defoliation, frost and drought. These are the factors that, on the basis of dendrochronological analyses on several hundreds of oaks, have also been considered responsible for two recent outbreaks of oak decline in Northern Germany (Hartmann and Blank 1992; Blank 1997; Hartmann and Blank 1998).

3 Abiotic factors in the oak decline complex We group the main abiotic factors that have been considered to contribute to oak decline into the categories air pollutants, climatic extremes and site conditions. 3.1 Air pollutants Investigations on the effects of air pollutants on the vigour of oaks have concentrated on sulphur dioxide (SO2), ozone (O3) and nitrogen (N) compounds.


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3.1.1 Sulphur dioxide Between 1980 and 1992, SO2 emissions in Europe decreased by almost 40% (Rodhe et al. 1995). However, in some parts of Central Europe (e.g. at higher altitudes in the Ore Mountains, at the border between Saxony (Germany) and Bohemia (Czech Republic)), atmospheric SO2 concentrations still reached high levels in the mid-1990s (more than 100 lg m)3 in the winter months; Zimmermann et al. 1997). At such sites, coniferous forests prevail, with oak forests largely being confined to lower altitudes. Long-term exposure of trees to SO2 predominantly affects photosynthesis (e.g. Heber and Hu¨ve 1998), but Q. petraea and Q. robur are relatively tolerant to this chemical. Thus, fumigation of young Q. robur for up to 70 days with maximum SO2 concentrations of 470 lg m)3 did not result in a reduction of net photosynthesis, and the trees’ physiological mechanisms were capable of neutralizing the acid that was generated (Thomas and Runge 1992). Furthermore, in an extensive investigation carried out in the Danubian region, the direct effects of SO2 on the vigour of oak stands could be excluded (Ro¨sel and Reuther 1995). For these reasons, we do not consider SO2 to be an important factor in the complex of oak decline. 3.1.2 Ozone With respect to growth, it appears that distinct O3-induced effects are largely confined to fast-growing tree species (Ska¨rby et al. 1998). In these trees, exposure to O3 may lead to reductions in chlorophyll content, photosynthesis and biomass; alterations in carbon (C) allocation; and increased activity of the anti-oxidative system. In coniferous trees, chronic exposure to O3 increases the susceptibility to frost and drought (Schmieden and Wild 1995; Maier-Maercker 1998). Ozone effects are most pronounced when combined with nutrient deficiency and high light intensities (Schmieden and Wild 1995). Investigations on the effects of O3 on the slow-growing species Q. petraea and Q. robur are scarce. Long-term fumigation of Q. robur seedlings with elevated O3 levels, which can be reached for a few days during the summer (170 lg m)3), did not cause measurable lasting damage to photosynthetic CO2 uptake (Farage 1996). However, reductions in shoot and root biomass of Q. robur seedlings were found after a 2-year exposure to an O3dominated mixture of air pollutants in field-relevant concentrations (up to 130 lg O3 m)3; Ku¨ppers et al. 1994). In a study monitoring crown condition in Germany, typical visual symptoms of O3 damage to oak leaves, similar to those sometimes observed in the leaves of the beech (Fagus sylvatica), were not detected (cf. Hartmann et al. 1995; Hartmann 1996). So, there is no unambiguous evidence for O3 as a significant cause of the reported oak damage. According to Ska¨rby et al. (1998), the key effect of O3 on forest trees is an alteration in C allocation by restriction of phloem loading, thereby reducing the root:shoot ratio and predisposing the trees to drought stress. However, this effect is surely much less damaging than the effects of severe defoliation by insects, which causes enormous losses of C (see Section 4.1). For these reasons, we do not consider O3 to be a significant factor in the complex of damage to the oak. 3.1.3 Nitrogen compounds At the current atmospheric concentrations of gaseous N compounds, the impairment of the plants’ metabolism through direct uptake of these compounds by the shoot is improbable (in the case of nitrogen oxides, NOx; Segschneider 1995; Stulen et al. 1998) or occurs only in close vicinity to emission sources (in the case of ammonia, NH3; Fangmeier et al. 1994). Thus, direct effects of NH3 have only been reported – in isolated cases – from sites adjacent to NH3-emitting industrial plants in Eastern Europe. Long-distance transport of

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emitted N and its deposition occurs mainly in the form of ammonium (NH4+) or nitrate (NO3–). At high rates of N deposition, NH4+ is the predominant N compound. In almost every oak stand in Central and Northern Europe for which data were available (Ivens 1990), the calculated deposition of N originating from industry, traffic and agriculture reached or even exceeded the critical load for acidic, managed deciduous forests (15–20 kg N ha)1 a)1) and, in the long term, will lead to alterations in the forest-floor vegetation (Bobbink et al. 1992). These deposition rates also exceed the stands’ N demand for wood increment (10–15 kg N ha)1 a)1; Ulrich 1991a). The high rates of N input may – at least partly – be responsible for the increased growth of forest trees in several European countries during the past decades (Spiecker et al. 1996). In the large majority of cases, the throughfall fluxes of NO3– + NH4+ exceeded a threshold of 15 kg N ha)1 a)1, consequently highly increasing the risk of NO3– leaching from the soil (Gundersen 1992). Nitrification of N compounds and consecutive leaching of NO3– result in soil acidification and leaching of ÔbaseÕ cations (e.g. Ulrich 1991b). This may aggravate the soil acidification caused by acidic deposition (e.g. Ulrich 1995). A supply of excess N can affect the tree in the following ways: (1) by inducing nutrient imbalances, which might be aggravated by the reduction in the root:shoot ratio (a common response to increased N supply; Marschner 1995), and by the impairment of mycorrhization (Wallenda and Kottke 1998). These reactions, in turn, might increase the risk of drought stress in dry periods (Aber et al. 1989). (2) By increasing the trees’ susceptibility to freezing damage by decreasing their frost hardiness (cf. Skeffington and Wilson 1988). (3) By increasing the trees’ susceptibility to attacks from herbivorous insects due to a decrease in the concentrations of allelochemicals (cf. Scriber and Slansky 1981; Chapin 1991). (4) By aggravating soil chemical stress (see above). In the following, we discuss the significance of these alterations in the complex of oak decline. 3.1.3.1 Nutritional imbalances In a large number of investigations on oak stands in Europe, N deposition led to measurable effects on the nutritional status of the trees. In the majority of the investigated stands in Germany as well as in parts of Slovakia and Austria, the foliar N concentrations were above the normal level. This was, in part, accompanied by low concentrations of phosphorus (P), magnesium (Mg) and ⁄ or potassium (K) and led to increased ratios of N to the respective nutrients (Thomas and Bu¨ttner 1992; Ro¨sel and Reuther 1995; Thomas and Kiehne 1995). The Danubian study (Ro¨sel and Reuther 1995) revealed that, in Q. robur, the foliar P and K concentrations decreased and the N:P and N:K ratios increased with increasing crown thinning. In North-western Germany, the degree of foliation of Q. robur correlated with the foliar Mg concentrations (Thomas and Bu¨ttner 1998a). In North-eastern Germany, the leaves of damaged oaks showed decreased concentrations of calcium (Ca) and Mg (Heinsdorf 1996). However, in none of these cases could close correlations be detected between the nutrient status and the vigour of the investigated oaks. 3.1.3.2 Decrease of frost hardiness The effects of N supply on the frost hardiness of woody species are not uniform. Nitrogen fertilization may decrease frost hardiness (e.g. Pinus sylvestris, Aronsson 1980; Picea abies, Soikkeli and Ka¨renlampi 1984), increase it (Picea rubens, DeHayes et al. 1989; L’Hirondelle et al. 1992; Calluna vulgaris, Caporn et al. 1994), or have no effect at all (Picea abies, Wiemken et al. 1996). The N status of the plants prior to N fertilization obviously determines the likely effect (e.g. Larsen 1978). When plants are sufficiently or luxuriously supplied with N, an additional supply with N, especially in the form of NH4+,


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increases the demand for C compounds in the N assimilation. This may result in decreased concentrations of soluble carbohydrates and ⁄ or cyclitols, which are important in the development of frost hardiness. In January or February, within or after a period of permanent frost, the frost hardiness of living bark tissue of mature Q. petraea and Q. robur which exhibited a significantly decreased C:N ratio in the bark was significantly lower than that in trees with higher C:N ratios (Thomas and Blank 1996). However, this was found in only one instance in Q. petraea and Q. robur, respectively. In Q. robur, for January and February, a significant correlation was found between the C:N ratios and an index of frost hardiness (decreasing frost hardiness with decreasing C:N ratios; Thomas and Blank 1996). Since the investigations of trees with normal and low C:N ratios had to be performed in different stands, and since, in the case of Q. robur, the sampling date had been preceded by a mild weather period, effects of site conditions and of the climatic regimes on the frost hardiness could not be excluded. Therefore, an experiment with young oak trees, which had been grown with different N supply and were in a state of maximum frost hardiness at the time of investigation, was conducted under controlled conditions. In this experiment, no distinct effects of excess N on the frost hardiness of the bark tissue were detected (Thomas and Ahlers 1999). Therefore, it was concluded that excess N – at least in fully hardened trees – affects the frost hardiness of the bark tissue only slightly, and that N effects are overridden by the course of temperature during the period prior to sampling. 3.1.3.3 Decreased concentrations of allelochemicals Some allelochemicals produced by the secondary metabolism of the plants are important in the plants’ defence against herbivores. They include phenolic compounds and their derivatives, e.g. tannins. In comparison with other deciduous tree species of Central Europe, the oak species have particularly high tannin concentrations (e.g. Heldt 1996). Uptake of excess N results in a decrease in the production of phenolic compounds in, among others, Betula pendula (Lavola and Julkunen-Tiitto 1994), Fagus sylvatica (Balsberg Pa˚hlsson 1992), Acer saccharum and Populus tremuloides (Kinney et al. 1997). In an experiment with young Q. petraea and Q. robur under controlled conditions, cultivation with excess N resulted in slightly, but significantly decreased concentrations of total phenolic compounds (Q. robur) and a reduction of the protein precipitation capacity (Q. petraea; Thomas and Schafellner 1999). The same results, however, were obtained from trees which had, in the summer prior to harvesting, been subjected to a drought stress, which was intensive enough to cause reductions in height growth, for 2 months. In Q. robur, but not in Q. petraea, a combination of excess N and drought led to the most severe reduction in tannin concentration and protein precipitation capacity and in the ratios of tannins and protein precipitation capacity to foliar N (Thomas and Schafellner 1999). In several tree species, the performance of phyllophagous insects increases at reduced concentrations of foliar allelochemicals (Picea abies, Schafellner et al. 1994; Ha¨ttenschwiler and Schafellner 1999; Pinus sylvestris, Holopainen et al. 1995; Populus tremuloides, Kinney et al. 1997; Pseudotsuga menziesii, Joseph et al. 1993), and at increased ratios of foliar N to protein precipitating compounds (Picea abies, Schafellner et al. 1996). Therefore, we hypothesize that a combination of increased N supply and summer drought also increases the risk of severe insect defoliation in stands of Q. robur. 3.1.3.4 Aggravation of soil chemical stress In terms of the total deposition in oak stands, NH4+ may constitute the largest fraction of the acidic deposition (Thomas and Bu¨ttner 1998b). The nitrification of the deposited NH4+ leads to an acidification of the system if the NO3– produced is not taken up by

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vegetation. The generation of acidity due to such nitrogen transformation can contribute considerably to acid loading in oak ecosystems (Van Breemen et al. 1987; Tietema et al. 1992; Thomas and Bu¨ttner 1998b). Excess NO3– and SO42–, accompanied by cations, are leached from the soil. Significant losses of Ca2+ and Mg2+ from oak ecosystems, triggered by air pollution, have been established, for example, in Hungary (Jakucs 1985), Austria (Berger and Glatzel 1994), and Germany (Thomas and Bu¨ttner 1998b). However, these studies, as well as investigations in the UK (Freer-Smith and Read 1995), have provided no indications that soil chemical stress acts as a causal factor of the current damage to the oak. In two case studies on oak stands with considerable decline (Thomas and Bu¨ttner 1998b), the parameters of soil acidification (pH; fractions of Al3+ and of H++ Fe3+ in the cation exchange capacity; molar ratios of Ca2+:Al3+, Mg2+:Al3+, Ca2+:H+, [Na+ + K+ + Ca2+ + Mg2+]:Al3+) measured in the declining areas of the stand were not less favourable, but, in some cases, even more so than in the healthy areas, and generally were out of the critical ranges of the respective parameters in which the trees might be damaged. In conclusion, soil chemical stress does not seem to have substantially contributed to the recent oak decline, but a continuing input of acidifying N compounds is regarded as a risk to future ecosystem stability due to a steady loss of ÔbaseÕ cations and an aggravation of nutritional imbalances. Generally, deposition of acidic air pollutants with a high N content may be the main cause of the distinct increase in Mg deficiency in Central European forest ecosystems during the last few decades (Katzensteiner and Glatzel 1997). 3.2 Climatic extremes Summer drought and severe frost in mid-winter are presumed to be involved in the outbreak of oak decline. 3.2.1 Summer drought Generally, European oak species exhibit morphological and physiological adaptations that enable them to postpone desiccation and increase desiccation tolerance. Morphological adaptations that help to postpone desiccation are a deep-reaching root system (Ko¨stler et al. 1968); hairs on the undersurfaces of the leaves (e.g. in Q. pubescens) which increase the boundary layer resistance and therefore reduce transpiration; and the ability of mature trees to shed twigs (cladoptosis; Klugmann and Roloff 1999), thereby reducing the transpiring leaf area. Postponement of desiccation is also achieved, as an acclimatizational reaction, by an increase in the ratio of fine roots to leaves upon the exposure to drought (Thomas 2000; Thomas and Gausling 2000). As a physiological mechanism to postpone desiccation, transpiration is effectively controlled by a delicate regulation of stomatal conductance, thereby decreasing the risk of embolism that otherwise would considerably reduce the hydraulic conductivity in the shoots of those ring-porous species (Cochard et al. 1992, 1996). Stomatal closure induced by drought stress results in a reduction of photosynthesis (Epron et al. 1992) and, finally, in the cessation of shoot growth; in Q. robur, shoot growth ceases at higher (less negative) leaf water potentials than in Q. petraea (Vivin et al. 1993). Desiccation tolerance is increased by osmotic adjustment, i.e. the lowering (values become more negative) of the osmotic pressure of the leaf cells by concentrating osmotically active compounds to a greater extent than could be explained solely by water loss (Hinckley et al. 1980; Kozlowski et al. 1991). However, this reaction loses importance with increasing drought stress, in which morphological reactions (increase in the ratio of fine roots to leaves) become more pronounced (Thomas 2000; Thomas and Gausling 2000).


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Since a reduction in shoot growth and therefore in the assimilating leaf area is connected with exposure to drought, drought stress may render the trees more susceptible to other stress factors via a decrease in photosynthate and carbohydrate reserves (e.g. Dreyer 1994). This might be the reason for the reduced frost hardiness (Thomas and Ahlers 1999) and the reduced foliar concentrations of allelochemicals (Thomas and Schafellner 1999) in previously drought-stressed oak seedlings and, thus, can contribute to damage even before marked symptoms of desiccation are visible. This might be particularly important in regions with a subcontinental to continental climate. Generally, Q. robur is considered to have a greater water requirement (Le´vy et al. 1992) and to be more sensitive to drought stress (Cochard et al. 1992; Vivin et al. 1993) than Q. petraea. Drought was considered to be one of the main factors causing the recent outbreaks of oak decline in Poland (Siwecki and Ufnalski 1998), the Danubian region (Ro¨sel and Reuther 1995), France (e.g. Landmann et al. 1993; Bre´da 2000) and the UK (Mather et al. 1995). In North-eastern France, a close inverse correlation was found between soil water deficit and radial growth in the period from 1964 to 1994; the correlation was closer for Q. robur than for Q. petraea (Bre´da 2000). In Central and North-western France (Le´vy et al. 1992), Q. robur was also more severely affected by summer droughts than was Q. petraea growing in the same stands. In part, this was attributed to inappropriate silvicultural management, which had led to the cultivation of Q. robur at sites that are unfavourable to this species. Even in cases of severe summer drought, however, drought stress was not assumed to be the sole factor leading to oak decline but rather as a factor that weakens the vigour of the trees and, in combination with unfavourable site conditions, renders them susceptible to additional factors such as insect pests and pathogenic fungi (Landmann et al. 1993; Siwecki and Ufnalski 1998). 3.2.2 Winter and spring frost The degree of frost hardiness during winter varies between and within species as well as between organs and tissues of the plant, and depends, for example, on the preceding temperature regime and the plant’s nutritional status (e.g. Sakai and Larcher 1987). Generally, Q. robur is considered to be less susceptible to frosts in mid-winter and late winter than Q. petraea (e.g. Ellenberg 1996). Severe winter frost is regarded as one of the causal factors of oak decline in Eastern and Central Europe and in Southern Sweden and may have had a synchronizing effect on the occurrence of decline in the 1980s (Balder 1992; Landmann et al. 1993; Ro¨sel and Reuther 1995). The impact of frost on the vigour of oaks is particularly severe under the continental climate at the north-eastern boundary of their distribution in Europe, to the west of the Ural Mountains (Yakovlev 2000). In Southern Sweden, frost damage to roots, enhanced by only thin snow covers, is seen as the initial cause of oak decline (Barklund and Wahlstroem 1998). In Northern Germany, up to 20% of the damaged oaks exhibited necroses in the living bark of their trunks, which presumably were caused by three consecutive cold winters in the mid-1980s (Hartmann and Blank 1992). Minimum air temperatures of )18 to )24C occurred repeatedly in January and February in three consecutive winters (1985–87) and, in 1987, even lasted until March, i.e. during periods when the living bark tissue already becomes dehardened (Thomas and Blank 1996). The necroses mainly occurred at the southern (sun-exposed) sides of the trunks. Investigations on mature Q. petraea revealed that, in late winter, oscillations between warming of the trunk surface by radiation during the day and cooling at night result in more frequent changes between daily maximum temperatures above and minimum temperatures below 0C in the bark tissue. This leads to a premature reduction in frost hardiness and makes the bark tissue on the southerly exposed sides of the trunks susceptible to freezing damage

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resulting from deep frost in late winter (Thomas et al. 1996). Effects of excess N on frost hardiness have already been discussed in Section 3.1.3.2. Spring frost can cause damage to oaks mainly in two different ways. To ensure water supply to the newly generated leaves, the formation of the large earlywood vessels must be completed before the leaves emerge (Zimmermann 1983); accordingly, in Central European oaks, earlywood apparently is established by the end of April (Bre´da and Granier 1996). Since the water in the xylem generally freezes between 0 and )2C (Lambers et al. 1998), spring frost which can reach temperatures considerably below that threshold (see below) can cause the water to freeze in those vessels. When the frozen water in the vessels thaws after bud break at a time when the leaves are already active with transpiration, transpiration will reduce the pressure in the xylem, and dissolved gas will form gas bubbles which ultimately will lead to embolism of the vessels and, thus, to blockage of water transport (Zimmermann 1983). In addition, spring frost can damage the expanding leaves, which are very susceptible to frost stress (Sakai and Larcher 1987). Spring frost is assumed to occasionally contribute to the complex of oak decline (Hartmann and Blank 1998). It may cause severe visible damage extending up to the upper crowns of mature oaks. This was documented in 1991 by CIR aerial photography in oak stands of a lowland region of North-western Germany, where flushing of oaks started around 14 April, and minimum temperatures of )5.5 to )6.4C on 21 April caused complete defoliation in 53% of the oaks. In 1996, on 6 May, spring frost of )3 to )9C occurred in the same region, where most serious oak decline occurred thereafter. 3.3 Site conditions In this section, we concentrate on the discussion of the role of hydromorphic soils in the complex of oak decline. The role of soil chemical stress has already been discussed in Section 3.1.3. Particularly in Q. robur, close correlations were found between soil water relations and tree health. In the Netherlands (Oosterbaan 1991), North-western Germany (Ackermann and Hartmann 1992), France (Nageleisen 1993) and the Danubian region (Ro¨sel and Reuther 1995), oak decline was found to be increased at hydromorphic sites with fluctuating water tables. This is somewhat surprising, since Q. robur generally is considered to be less sensitive to waterlogging than Q. petraea (Belgrand and Le´vy 1985; Oberdorfer 1994; Ellenberg 1996). However, most probably it is the intermittent soil moisture conditions rather than a steadily high water level in the soil that makes the trees more susceptible to stress. Normally, hydromorphic soils also are soils with high clay content. At those sites, which are regarded as the typical sites for the cultivation of Q. robur, the rooting in the subsoil is impaired (e.g. Thomas and Hartmann 1996, 1998). In old oaks, this impairment seems to be even worse than in young ones, since old oaks, in contrast to oaks of less than 100 years, were found to be unable to extend their roots into recently drained soil (Becker and Le´vy 1986). Thus, in dry periods of the growing season, the stronger restriction of the fine roots to the more superficial soil layers, and the rather negative soil matric potentials in the clay-rich subsoil that develop under desiccation, increase the risk of severe drought stress to the trees (Thomas and Hartmann 1996, 1998). On acidic and weakly drained soils, high concentrations of manganese (Mn2+) can severely impair the growth of plants (manganese toxicity, e.g. Horst 1988). With respect to forest trees, this has been shown for Picea abies (Ga¨rtner et al. 1990) and Pseudotsuga menziesii (Scho¨ne 1992; Kaus and Wild 1998). In analyses of samples from oak stands on hydromorphic soils (cf. Thomas and Bu¨ttner 1998b), we found maximum Mn2+ concentrations of 0.14 mm (and one extremely high value of 0.3 mm) in soil solutions, and maximum foliar Mn concentrations of 0.08 mmol g)1 dry matter (¼ 4.6 mg Mn g)1 dry matter). In order to assess the effects of high Mn2+ concentrations in the substrate on


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growth and gas exchange of oaks, we grew oak seedlings for 6 months on two types of nutrient solution with high Mn2+ concentrations (0.24 mm, representing the upper threshold of Mn concentrations in acidic forest soils under aerobic conditions; Schachtschabel et al. 1992; and 1.2 mm), and compared the response of the seedlings with the performance of control plants grown on a customary Mn2+ concentration (0.0024 mm). Toxicity symptoms such as dark spots on the leaf blade, chloroses and wilting were found at 0.24 mm Mn2+ (at mean foliar Mn concentrations in the first flush of 13–16 mg g)1 dry matter), but stomatal conductance and root growth were only impaired at the highest Mn2+ concentration (1.2 mm), whereby Q. petraea was more severely affected than Q. robur. Shoot growth and leaf mass were not affected at all. Therefore, it is concluded that both oak species are rather resistant against high Mn2+ concentrations of the substrate, and that high Mn2+ concentrations in the soil do not substantially contribute to oak decline. 3.4 Impacts of abiotic factors on mycorrhiza Investigations on the mycorrhiza of declining oaks are scarce. In a Polish study, Q. robur with more severe symptoms of decline exhibited reduced mycorrhizal colonization (Przybyl and Pukacka 1995); whereas in an Italian investigation (Causin et al. 1996), the correlation between the decline intensity of Q. robur and mycorrhizal parameters was less clear. In the Czech Republic, in oak stands exhibiting severe leaf loss, the percentage of active mycorrhizal root tips was negatively correlated with the degree of leaf loss; this was considered to be caused by the influence of air pollutants (Fellner and Peskova 1995). Distinct reductions in mycorrhization were also found in the surroundings of industrial complexes in North-eastern Hungary and were thought to be caused by air pollutants (SO2, NOx, NH3; Holes and Berki 1988). However, it remains unclear whether the impairment of mycorrhization is essential in the interaction of factors resulting in the decline, or if it occurs concomitantly and in parallel to the interaction of factors that are more important in the onset of damage. Thus, the role of mycorrhiza in the oak decline complex is far from being understood. 3.5 Conclusions on the importance of the various abiotic factors From the investigations on the role of abiotic factors in the complex of oak decline, the following conclusions can be drawn: No substantial contributions to the recent outbreaks of oak decline by gaseous air pollutants such as SO2, ozone and gaseous N compounds have been found. The increased N input into oak forests leads to nutrient imbalances in the trees, may aggravate soil acidification, and results in an increased output of NO3– and ÔbaseÕ cations from the system; but there are no close correlations between these features and the vigour of the trees. Definitive effects of excess N on the frost hardiness of the bark were not observed. It is hypothesized that excess N does not reduce frost hardiness in fully hardened trees. In combination with drought, excess N leads to reduced concentrations of allelochemicals in leaves of Q. robur. This may render the trees more susceptible to insect defoliation; however, further investigations are necessary to confirm this hypothesis. Severe summer drought makes the trees more susceptible to adverse effects exerted by additional stress factors (e.g. winter frost). Severe winter frost causes damage to the living tissue of the bark; especially in late winter, the southern (sun-exposed) sides of the trunk are more prone to bark damage. Spring frost may occasionally also contribute to the causal complex by induction of xylem embolization or by causing damage to the expanding leaves. Intermittent soil moisture, particularly on clayey soils, impairs the fine-root growth in the subsoil and renders the trees more susceptible to drought stress during dry periods in summer. This was more obvious in stands of Q. robur than in those of Q. petraea.

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In the past three decades, climatic extremes seem to have occurred more frequently. In continental regions, their expression is often more extreme. This may explain the fact that, during this period, the first reports on oak decline came from the eastern parts of Europe (Schume and Huber 1995).

4 Biotic factors in the oak decline complex The biotic factors discussed in the context of oak decline comprise defoliation by insect larvae, attack by bark beetles, pathogenic fungi, and microorganisms. 4.1 Defoliation by insect larvae Various investigations have supplied evidence that defoliation by the larvae of phyllophagous insects plays a predominant role in the outbreak of oak decline. From North-western Germany, more than 20 local incidences of oak decline between 1909 and 1947 as well as two more recent ones (1987, 1996) have been reported. Most of them, including the last two, are documented to have been closely preceded by insect defoliation (Blank 1997; Hartmann and Blank 1998; Wachter 1999, 2001). Damage due to severe defoliation has not only been reported from Central Europe (Poland, Siwecki 1989; Germany, Hartmann and Blank 1992; Block et al. 1995; France, Landmann et al. 1993), but also from countries of Eastern Europe (Russia, Rubtsov 1996; Romania, Donita et al. 1993; Hungary, Varga 1993). The most important defoliating insects are Operophthera brumata L., Tortrix viridana L. and, in warmer regions, Lymantria dispar L. Defoliation in two or more consecutive years rather than one single defoliation event is thought to be a significant causal factor of decline. However, even one single defoliation caused by L. dispar might be sufficient to considerably reduce the vigour of the trees (e.g. Lobinger 1999). In stands of Northern Germany that were part of a long-term provenance experiment started in 1951 (57 provenances of Q. robur, 62 of Q. petraea), severe defoliation by insect larvae in 1996 led to increased mortality in the following years (Svolba and Kleinschmit 2000). On average, Q. robur has been more severely affected than Q. petraea, but the intraspecific differences between the provenances were larger than the differences between species. There was a significant correlation between the time of leaf emergence and the extent of decline, which, however, only explained a relatively small portion of total variation. It was hypothesized that the differences between the species were due to the better adaptation of Q. petraea to dry and nutrient-poor sites (Svolba and Kleinschmit 2000). Defoliation reduces the assimilating leaf surfaces and causes loss of photosynthate. These effects are most severe if caused by larvae of L. dispar, which feed much longer (until July) than the other defoliators. In this case, due to the large depletion of carbohydrate reserves, the regeneration of foliage by formation of replacing shoots is also impaired; thus, the loss of carbohydrates can be compensated only to a rather limited extent. As a result of defoliation, root starch content is substantially lowered or even depleted. Tree survival may then be critically dependent on the starch reserves present at the time of defoliation (Wargo 1996). This severe reduction in carbohydrate reserves presumably is responsible for the strong reduction or even complete lack of latewood formation, which was observed after defoliation in consecutive years (Hartmann and Blank 1992; Rubtsov 1996; Blank 1997). Additionally, severe defoliation can result in a reduced production of root biomass (Kozlowski et al. 1991; Block et al. 1995), which also renders the tree more susceptible to drought stress. In an experiment with saplings of Q. petraea and Q. robur under controlled conditions, a drastic reduction in fine-root biomass was observed at the end of the second year of the investigation period, following artificial defoliation in the


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spring of both years (Gieger and Thomas 2002). In addition, in the defoliated specimens of Q. robur, the daily amount of water transpired per unit leaf area was increased (Gieger and Thomas 2002). Thus, important mechanisms of acclimatization to drought, i.e. the enhancement of fine-root growth and reduction in stomatal conductance, were impaired, particularly in Q. robur. From the more superficial rooting pattern of oaks at hydromorphic sites (see Section 3.3), it becomes evident that severe defoliation at such sites makes the trees even more susceptible to drought stress in dry periods. In studies on the importance of waterlogging, defoliation and drought as damaging factors to Q. robur in experimental plots in Romania, the highest tree mortality was caused by a combination of waterlogging and repeated defoliation (Donita et al. 1993). In South-western Germany, oak decline after repeated defoliation was most intensive at sites with a high groundwater level (Delb 1999). In North-western Germany, the most recent and most severe decline of Q. robur was preceded by three consecutive years of insect defoliation and an extraordinary spring frost, and occurred during a period of spring and summer drought. It was hypothesized that defoliation, together with climatic extremes, and the impairment of root growth – especially on hydromorphic sites – have triggered this decline (Hartmann and Blank 1998). In this complex of primary causal factors, insect defoliation is considered to be most important because of its overriding effect in reducing the trees’ carbohydrate supply. Since the diameters of earlywood vessels and width of latewood rings in adult trees were found to be drastically reduced, an impairment of hydraulic conductance has also been postulated (Blank 1997; Hansen 1999; Gieger and Thomas 2002), but could not be confirmed in potted saplings after experimental defoliation (Gieger and Thomas 2002). In three oak stands in North-western Germany, insect defoliation was proven to have a stronger effect on latewood reduction than climatic factors (Blank and Riemer 1999). Since a close correlation exists between the concentrations of carbohydrates, especially of sugars, and the frost resistance of plant tissue (e.g. Sakai and Larcher 1987), severe defoliation can lead to reduced frost hardiness as a result of the reduction in carbohydrate reserves (see above). The bark of mature Q. petraea and Q. robur, which had been defoliated by insects in the preceding summer, was less frost resistant (Thomas and Blank 1996). This finding was corroborated by investigations on approximately 20-year-old trees of Q. robur, which had been artificially defoliated in two consecutive years: in the following winter, the frost hardiness of the bark tissue was significantly lower than in nondefoliated trees (Fig. 1; Meyer 2001). 4.2 Infestations by borers and bark beetles Detailed analyses of several hundred oak trees in Northern Germany have shown that the borer Agrilus biguttatus Fabr. (Buprestidae) is the first and most important of the secondary insect pests, which attack oaks that are weakened by effects of other biotic or abiotic stress factors (Hartmann et al. 1989; Hartmann and Blank 1992). Other Buprestidae species may also be involved (e.g. Agrilus sulcicollis, Coraebus undatus; Veldmann and Kontzog 2000). The borer may even attack trees with scarcely visible damage symptoms. The larvae produce galleries in the living bark and the cambial zone. In early phases of the attack, the insect may be repelled and the damage often heals, although a certain impairment of water transport due to irregular earlywood tissue may remain; but in repeated attacks, more extended larval galleries can lead to girdling and ultimately kill the tree (Hartmann 1996). Infestations by Agrilus have been known for many years (e.g. Strohmeyer 1912; Wachtendorf 1955); but their typical symptoms (zig-zagging larval galleries under the outer bark, D-shaped exit holes in the bark) may often have been overlooked, or their importance may have been underestimated. Meanwhile, it is evident that A. biguttatus is present nearly all over Europe, possibly with increasing numbers and

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T

Fig. 1. Indices of injury determined after artificial freezing at )30C (I)30) of bark tissue from approximately 20-year-old specimens of Q. robur (means ± standard errors), and daily minimum air temperatures (Tmin) measured at a meteorological station in the region during winter 2000 ⁄ 01. The trees had not been defoliated (control), or had been artificially defoliated in the spring of both years (1999 and 2000) prior to the investigation of frost hardiness. Lower I)30 values indicate higher frost hardiness and vice versa. Between the treatments, the I)30 values differ significantly for the entire investigation period (indicated by the different letters in the legend; repeated measures analysis of variance; p < 0.05), and for the date in February when tested separately for each date of measurement (indicated by the asterisk; analysis of variance, p < 0.05). The broken horizontal line marks 0C. (Data from Meyer 2001; temperature data from Deutscher Wetterdienst 2001)

population densities (Gibbs and Greig 1997; Moraal and Hilszczanski 2000). Once activated by primary weakening and mortality of oaks, it continues attacking and killing trees for many years even if primary factors such as insect defoliation and climatic extremes are no longer active (Hartmann and Blank 1992, 1998). Other coleopterans such as Scolytus intricatus Ratz and Dryocoetes villosus (Scolytidae) only appear rather late in the decline process, in branches and on the stems of declining oaks. The postulated role of S. intricatus as a vector of tracheomycosis-like diseases could not be confirmed (Hartmann and Blank 1992).

4.3 Pathogenic fungi 4.3.1 Phytophthora species Recently, root pathogens of the genus Phytophthora have been found in declining oak stands and have since been discussed in the context of oak decline. In the Mediterranean region, the well-known and very aggressive species Phytophthora cinnamomi, which attacks fine roots, is – in combination with drought – considered responsible for the decline of Quercus suber and Q. ilex (Brasier 1996; Robin et al. 1998). However, P. cinnamomi does not survive the winter temperatures found in Central Europe. Several Phytophthora species have been isolated from rhizosphere soil of stands with declining oaks in Central, Southern and South-eastern Europe (France, Germany, Switzerland, Italy, Slovenia, Hungary), and from necrotic fine roots of oaks. Phytophthora quercina and P. citricola were among the most frequently recovered species (Jung et al. 1996; Hansen and Delatour 1999; Jung et al. 2000). These findings confirm the generally widespread occurrence of Phytophthora species in forest soils, probably even in stands


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without any actual symptoms of decline. Tests on pathogenicity using oak seedlings have demonstrated the potential virulence of Phytophthora, especially that of the recently discovered new species P. quercina (Jung et al. 1996, 1999). In an investigation of oak stands in Southern Germany, Phytophthora-infected oaks had higher levels of fine-root damage and a higher crown transparency than oaks without Phytophthora (Jung et al. 2000). On the other hand, Phytophthora infection did not necessarily result in the death of the tree (Jung et al. 2000), and the wilting toxin which was isolated from Phytophthora cultures and was proven to induce leaf wilting in oak seedlings (Jung et al. 1996) could not be isolated from leaves of declining oaks in the field. A survey of 35 oak stands in Southern Germany indicated that the possible contribution of Phytophthora to oak decline is confined to sandy-loamy to loamy, silty or clayey soils with a mean pH (CaCl2) > 3.4 (pH (H2O) > 4.2; Jung et al. 2000). The presence of a certain minimum amount of water for a sufficiently extended time period is a precondition of the development of Phytophthora and a successful infection of oak roots by this pathogen. This may be the reason for the finding of more pronounced Phytophthora infection on soils with higher clay contents. On the basis of the results obtained up to the present time, Jung et al. (2000) proposed a ÔPhytophthora-mediated oak declineÕ, at sites with a mean soil pH (CaCl2) > 3.4, which – after long periods without any above-ground signs of damage – can be recognized by visible crown symptoms when root death caused by Phytophthora outweighs the production of new fine roots. This state may be induced by prolonged periods of waterlogging. The fine-root system then passes into a progressive course of destruction, which is connected with crown dieback. The weakened tree is rendered more susceptible to additional stress factors such as summer drought, frost, severe defoliation and Agrilus attack, the combination of these factors ultimately killing the trees. The combination of waterlogging, severe insect defoliation in two consecutive years (1994 and 1995) and Phytophthora infection was assumed to be responsible for dramatic oak dieback in an approximately 50-year-old oak stand in Southern Germany in 1996 (Jung et al. 2000). In North-western Germany, 343 oaks in 37 stands showing decline symptoms were surveyed for presence of Phytophthora species in their upper rhizosphere using Jung’s methods (Jung et al. 1996). Phytophthora quercina and, less frequently, other Phytophthora species [P. cambivora, P. citricola, P. syringae and P. europaea sp. nov., P. psychrophila sp. nov., Jung et al. (2002)] were found in 49% of the stands and in 15% of all trees, at soil pH (CaCl2) of 3.5–4.6 (Hartmann and Blank, in preparation). For North-western Germany, these results seem to confirm the findings from the southern part of the country (see above), however, at a lower frequency level that is probably due to lower soil pH and the prevalence of more sandy soils. In both areas, investigations in 30 and 51%, respectively, of the studied oak stands showing decline failed to yield Phytophthora species. These preliminary results suggest that Phytophthora species, although being widespread in Central-European oak stands, may not necessarily and at all sites contribute to the complex of oak decline. In North-western Germany, high isolation rates (50–70%) of Phytophthora spp. were only found on few sites with exceptionally high base and clay contents in the upper soil layers. This suggests that Phytophthora spp. may find optimal conditions for epidemic development only in very restricted areas in this region. This view of a limited role of Phytophthora in CentralEuropean oak decline is in line with the results of a recently concluded European research project on the role of root pathogens in oak decline. It was stated that, although P. quercina was frequently associated with declining oaks in several countries, no general relation was observed between oak decline and the presence of Phytophthora species in the soil; that factors additional to Phytophthora probably have to be active to drastically threaten the health of oaks; and that, in many cases, oak decline occurs without any impact of Phytophthora (Delatour 2001).

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4.3.2 Other potentially pathogenic fungi As a primary root pathogen, Collybia fusipes (Bull. ex Fr.) Quel. is a common cause of root rot in North-eastern France (Marçais et al. 2000). It grows as a parasite in the outer bark of roots, especially of mature Q. robur and Q. rubra, and eventually may penetrate into the inner bark; at which time, the central part of the root system may be destroyed (Marçais et al. 1999). In a study conducted in Central and North-eastern France, the presence of basidiomes of C. fusipes was always connected with significant root infections; however, tree decline was severe only in the case of heavily infected roots, and, in some of the stands investigated, even a severe root infection did not cause severe tree decline (Marçais et al. 2000). Thus, generally, the correlations between root damage and symptoms of tree decline were only weak, probably because surviving and ⁄ or adventitious roots can take over the function of the diseased ones (Marçais et al. 1999, 2000). Locally, however, C. fusipes may play a significant role in the complex of oak decline. But this assessment can not be confirmed for Northern Germany: in more than 60 oak stands investigated during the past 12 years, fruiting bodies of C. fusipes were observed in only one stand of sessile oak on loess over calcareous parent rock (Hartmann 1996). Therefore, no systematic investigation of root rot caused by this fungus was conducted in that region. In Central France, the parasitic species Armillaria mellea (Vahl: Fr.) Kumm., which attacks roots with an intermediate diameter (5–20 mm) at some distance from the trunk, was associated with declining trees of Q. robur, mainly on hydromorphic sites; but it did not seem to be involved in initial stages of decline (Guillaumin et al. 1985). Armillaria gallica Marxm. and Romagn. (syn. A. bulbosa (Barla) Romagn.) was only detected in later stages of decline, when it invaded the base of dying trees (Guillaumin et al. 1985). On sandy and more acidic sites in the Netherlands, the parasitic species A. ostoyae (Romagn.) Herink was found to occur most frequently on oak (Termorshuizen and Arnolds 1994). In North-western Germany, unidentified mycelium of Armillaria spp. was found only at a low frequency in roots of oaks in the early stage of dying after insect defoliation. Later, after secondary Agrilus attack, fruiting bodies of the mainly saprophytic species A. gallica and A. cepistipes Velen frequently occurred on dead trees (Hartmann, unpublished). Thus, Armillaria species may often be late saprophytic colonizers rather than primary causal factors of oak decline. Powdery mildew (Microsphaera alphitoides Griff. et Maubl.) has reached Europe not before the first decade of the twentieth century, but has quickly spread over the entire distribution area of oaks in Europe thereafter (Krahl-Urban 1959). It causes heavy infestation and substantial loss of foliar assimilation capacity only if the presence of young leaves coincides with a high inoculum potential of fungal conidiospores. This combination occurs normally during a short period in early summer. After insect defoliation, young foliage is regenerated later in summer, when high conidial concentrations are also present. Thus, the period of mildew infection is prolonged and the foliage of insect-defoliated oaks is reduced further by mildew. This seems to have also contributed to the most recent decline in North-western Germany (see Section 5). Further weakly pathogenic fungi, which are not discussed here in detail, may contribute to late phases of decline, but have no importance in the primary causal complex (Hartmann et al. 1989; Kowalski 1991; Kehr and Wulf 1993; Donaubauer 1998). Among these, Ophiostoma spp., which colonize sapwood, were postulated by some authors to cause tracheomycosis in oak. This could not be confirmed by pathogenicity tests with O. querci (Georgevitch) Nannf. on seedlings of Q. robur (Simonin et al. 1994; Oszako 1997). Any contribution of American oak wilt, caused by Ceratocystis fagacearum (Bretz.) Hunt., to European oak decline can also be excluded ( Schlag 1994; Donaubauer 1998).


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4.4 Bacteria and viruses Observations indicating a contribution of phytoplasm (mycoplasma-like organisms; MLO) to oak decline (Ahrens and Seemu¨ller 1994) have been contradicted by investigations that failed to prove correlations between these organisms and damage to the oak (e.g. Schlag 1995). Viruses are able to induce symptoms of damage to oak leaves (e.g. Bu¨ttner and Fu¨hrling 1996), but it is improbable that they contribute to oak decline (Schlag 1994). 4.5 Conclusions on the importance of the various biotic factors From the investigations on the role of biotic factors in the complex of oak decline, the following conclusions can be drawn: Severe defoliation by caterpillars in consecutive years is a factor that weakens the tree to a considerable extent by depletion of carbohydrate reserves and impairment of fine-root growth. The effects are even more pronounced at hydromorphic sites where waterlogging and high clay contents additionally impair the root growth in the subsoil. In cases exhibiting a combination of both conditions, the risk of trees suffering drought stress in dry periods is greatly increased. In the ensuing winter, the frost hardiness of the bark is decreased by defoliation in the preceding vegetation periods. Collybia fusipes is a primary pathogen and is apparently of regional importance. Infection of fine roots by Phytophthora species, in particular by P. quercina, can weaken the tree at sites with pH (CaCl2) > 3.4 and – in combination with hydromorphic site conditions, climatic extremes (drought, frost) or insect defoliation – contribute to the decline. Among the secondary organisms, the borer Agrilus biguttatus occurs as the earliest one in the progression of decline and has the greatest impact on the vigour of the tree. Armillaria spp. more often seem to be late saprophytic colonizers rather than primary pathogens.

5 A conceptual model of the interaction of abiotic and biotic factors in the emergence of oak decline In Fig. 2, we present a conceptual model of the interaction of abiotic and biotic factors that are crucial in the emergence of oak decline. This model is based on investigations which had been performed at three different levels: (1) under controlled conditions by experiments with young trees; (2) on a local scale (in centres of oak decline) by case studies on water and nutrient relations in mature oak stands; and (3) on a supraregional scale (including centres of oak decline) by monitoring crown condition, soil water relations (on a site level) and nutrient status (on a tree level) of mature oak stands. The investigations were carried out in Northern Germany on Q. petraea and Q. robur. An overview of the approaches and the publications of the main results is given in Table 1. The model is restricted to the occurrence of oak decline at more acidic sites (pH (H2O) 6 4.2) since, at sites with a higher pH, infestation by Phytophthora species can be assumed to be involved in the onset of oak decline, and we feel that the interaction of these pathogens with additional abiotic and biotic factors still has to be more thoroughly investigated before including it in a model of oak decline. In the model, the three factors Ôinsect defoliationÕ, Ôsummer droughtÕ and Ôwinter ⁄ spring frostÕ are considered to be decisive causal factors for past as well as present occurrences of oak decline; this is done on the basis of archival evidence, symptom and tree-ring analyses, experiments, case studies and monitoring. Since, normally, at least two of these factors (always including defoliation) have to occur simultaneously to trigger decline, the following discussion focuses on the combined effects of these factors. Subsequently, the

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Fig. 2. Conceptual model of the interaction of the significant abiotic and biotic factors in the onset of oak decline in Central Europe at acidic sites (pH (H2O) £ 4.2). The most significant factors are framed with bold lines. The sizes of the arrows symbolize the importance of the respective factor combinations

factors Ôexcess NÕ and Ôchemical stress exerted by the soilÕ are also discussed, with special reference to combined effects. 5.1 Insect defoliation In the majority of cases, repeated insect defoliation is involved in the occurrence of severe episodes of oak decline. The reduction in the quantity of photosynthate caused by defoliation results in a decreased production of fine roots (Block et al. 1995; Gieger and Thomas 2002). Under conditions of summer drought, this leads to a severely diminished water uptake, thus triggering severe drought stress and, finally, resulting in desiccation damage. The reduction in the quantity of photosynthate also diminishes frost hardiness. Thus, the combined effects of insect defoliation and ensuing winter frost can still be considered to be an important causal complex for the occurrence of oak decline. 5.2 Summer drought Under the climatic conditions prevailing in our region, summer drought without the action of additional factors is not considered an important causal factor, but only a weakening (ÔpredisposingÕ) or intensifying factor in oak decline. An exception is provided by sites with intermittent soil moisture, where summer drought can be regarded as a causal factor – or, at least, as an aggravating factor – for damage to Q. robur. Thus, the hypothesis that this species is more prone to damage at such sites can be upheld. In the case of the sessile oak, however, evidence for the existence of such a relationship has not been found (Thomas and Hartmann 1996, 1998). 5.3 Winter and spring frost The bark necroses caused by deep frost in late winter at the southerly exposed sides of the trunks of mature oaks result from premature dehardening of the tissue due to increased irradiation (Thomas et al. 1996). The frost hardiness of the living bark tends to be

Investigated parameters

Growth, water relations Growth, gas exchange

Waterlogging

Excess Mn

Crown condition N deposition, crown condition, foliar nutrient concentrations

Hydromorphic sites

Excess N, nutrient imbalance

Supraregional scale (including mature stands in centres of oak decline)

Pools and concentrations of nutrients in the soil; input-output budgets; indicators for soil chemical stress; foliar nutrient concentrations

Excess N, nutrient imbalance; soil chemical stress

Thomas and Bu¨ttner (1992), (1998a); Thomas and Kiehne (1995)

Ackermann and Hartmann (1992)

Thomas and Bu¨ttner (1998b)

Thomas and Hartmann (1996), (1998)

Thomas and Blank (1996); Thomas et al. (1996)

Frost hardiness Soil and tree water relations

Excess N, defoliation

Hartmann et al. (1989); Hartmann and Blank (1992); Blank and Riemer (1999)

Sprenger (2001)

Schmull and Thomas (2000)

Thomas and Ahlers (1999); Thomas and Schafellner (1999); Gcocos (2000); Thomas (2000); Thomas and Gausling (2000); Gieger and Thomas (2002)

Source

Symptom analysis, tree ring analysis

Hydromorphic sites, drought

Primary and secondary organisms

Local scale (mature stands in centres of oak decline)

Growth, water relations, photosynthesis, frost hardiness, allelochemicals

Defoliation, drought, excess N (single or in combination)

Controlled conditions (experiments with young trees)

Levels of investigation and causal factors

Table 1. Methodical approaches to investigations on single and combined effects of various stress factors causing the onset of oak decline, and citations of published results that form the basis of the model presented in Fig. 2

Causes of oak decline in Central Europe 295

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diminished by preceding summer drought (Thomas and Ahlers 1999) as well as by insect defoliation during the preceding spring (Thomas and Blank 1996; Meyer 2001). Therefore, the hypotheses that the combined effects of summer drought and ensuing winter frost as well as the combined effects of insect defoliation and ensuing winter frost constitute important causal factors for the onset of oak decline can be upheld. Spring frost amplifies the effects exerted by repeated insect defoliation, and, as a result of embolization of earlywood vessels, renders the trees more susceptible to desiccation damage. 5.4 Excess N In Northern Germany, nutrient imbalances in the leaves of mature oaks due to excess N are widespread (Thomas and Bu¨ttner 1992, 1998a; Thomas and Kiehne 1995). However, the hypothesis that these nutrient imbalances are connected with the observed oak decline could not be confirmed (Thomas and Kiehne 1995; Thomas and Bu¨ttner 1998a). Nevertheless, continued high N inputs carry the risk that the oak stands will cease to function as sinks for N, and that the N output from the systems will increase (Thomas and Bu¨ttner 1998b). In comparison with other factors (temperature course during winter, preceding summer drought), excess N only slightly affects the frost hardiness of the bark (Thomas and Blank 1996; Thomas and Ahlers 1999). Thus, the hypothesis that excess N markedly reduces the frost hardiness could not be confirmed. However, especially in combination with summer drought, excess N results in diminished concentrations of allelochemicals in the leaves of Q. robur (Thomas and Schafellner 1999). Based on this result, the new hypothesis is formulated that the combined effects of excess N and summer drought distinctly increase the risk of insect defoliation to this species. This hypothesis still has to be tested in stands of Q. robur in the field. The general trend of increased growth of European oaks during the past decades (Spiecker et al. 1996) may be at least partly attributed to higher N nutrition. So far, there is no evidence that this general and continuous phenomenon has influenced local and episodic oak mortality. 5.5 Chemical stress exerted by the soil All existing case studies have failed to provide evidence for the contribution of chemical stress exerted by the soil to the current oak decline (Thomas and Bu¨ttner 1998b). However, a continued input of acidifying N compounds carries the risk of ecosystem destabilization in the future due to a progressive loss of ÔbaseÕ cations and an aggravation of nutrient imbalances. Increased Mn concentrations of soil and leaves were not found to play a decisive role in the onset of the present oak decline (Thomas and Bu¨ttner 1998b; Sprenger 2001). 5.6 Combination of factors responsible for the recent oak decline in North-western Germany The model in Fig. 2 is a tentative one. However, our investigations provide a sounder basis for the assessment of the effectiveness of individual factors and factor combinations for the onset of the present oak decline than has previously been possible. On the basis of this model, the onset of the recent and severe oak decline that occurred in Northwestern Germany in summer 1997 (Hartmann and Blank 1998) can also be explained. The damage was concentrated on sites that are characterized by intermittent soil moisture. We consider the following combination of factors to be responsible for the outbreak of decline:


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1 very warm and dry periods in the summers of 1994 and 1995, whose effects may have been aggravated by a relatively dry vegetation period of 1996; 2 severe insect defoliation in three consecutive years (1995–97); 3 unusual spring frost in 1996 (cf. Section 3.2.2) and severe winter frost in late December of 1996 and early January of 1997 (below )15C). After its onset, the decline may have been intensified by severe drought in the late summer of 1997. Although it is, in principle, impossible to present clear evidence for the general existence of specific cause-effect relationships, the results presented here indicate that the investigated factor combinations, which were shown to be effective, distinctly increase the probability of oak decline. Therefore, these results can be used as a basis for the application of measures within the framework of forest management.

6 Consequences for the forest management Man can only influence the occurrence and intensity of the factors leading to oak decline to a very limited extent. Therefore, the occurrence of a respective combination of these factors very probably will also result in oak decline in the future. Especially on hydromorphic sites, oak decline can result in a long-term change of the forest structure. The decline of the trees leads to lowered transpiration rates and therefore to even more extreme hydromorphic conditions. Under such conditions, natural regeneration of the oak can be prevented due to suppression by grasses and sedges (Molinia coerulea, Deschampsia caespitosa, Carex spp., Juncus spp.) that are better adapted to waterlogging and take advantage of the increased supply of light and nutrients and of higher temperatures at the forest floor after tree dieback. Such a situation has been observed in South-western Germany after the occurrence of high oak mortality following severe defoliation (Delb 1999). Since the number of mature oaks has been reduced to such a great extent, a sufficient mast of acorns is not to be expected during the next few years. Thus, in the long term, the oak forest may be replaced by a community that is dominated by more waterlogging-tolerant trees such as birch (Betula pendula), pine (Pinus sylvestris) or alder (Alnus glutinosa) (Delb 1999). This may lead to an increased diversity of tree species, but to a decrease in the overall species diversity. Thus, the consequences of oak decline may be so severe and longlasting that it seems to be important to prevent them by appropriate control and management measures. As has been discussed in the previous sections, severe defoliation in consecutive years distinctly increases the risk that both Central European oak species will undergo a decline episode. This is particularly true for Q. robur since this species, after defoliation, apparently is more prone to mortality than Q. petraea (Wachter 1999; Svolba and Kleinschmit 2000; Wachter 2001; cf. Sections 2.1 and 4.1). Hence, in cases where the conservation of the stand structure has the highest priority for economic or ecological reasons, measures for forest protection should be taken to diminish the effects of defoliation. This also includes the control of defoliators by spraying. A study in Southwestern Germany has shown that spraying against Lymantria dispar can prevent a severe defoliation and, thus, prevent the decline of mature stands dominated by Q. robur even under critical site and weather conditions (intermittent moisture, drought; Block et al. 1995; Delb 1999). With regard to the control of Operophthera brumata and Tortrix viridana, clear evidence of successful prevention of increased oak mortality is still lacking. Since, in any case, spraying is critical due to side-effects and hardly calculable factors in planning and application (weather, coincidence of leaf emergence and hatching of larvae, delayed effect of pesticides), the elaboration of reliable criteria for the recognition of

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endangered stands and increased risk of defoliation is indispensable (Hartmann and Blank 1998). The risk of damage to Q. robur at hydromorphic sites in regions that may be more frequently subjected to extended periods of intense drought is particularly high; this is also a result of the higher water requirement of this species. In France, the extension of Q. robur into areas and to sites that are inappropriate for this species because of its higher susceptibility to drought stress probably is a reason for distinctly increased rates of decline after severe drought (e.g. Le´vy et al. 1992; Bre´da 2000). This extension of Q. robur is due to its growth rates, which are – especially in young stages – generally higher than that of Q. petraea (cf. Krahl-Urban 1959) and may enable the species to outcompete Q. petraea; and to management practices that favoured Q. robur in coppice systems and in coppice with standards that were widespread systems of forest management in past centuries. In those areas, in the long term, Q. robur should be replaced by other species, e.g. by the more drought-tolerant Q. petraea. This species, which is less sensitive to Collybia fusipes and less prone to insect defoliation, also seems to be better suited to cope with the expected longterm increase in temperature due to global climate change (Becker et al. 1994). Management plans, particularly in areas with relatively low amounts of annual precipitation and on sites that are prone to frequent periods of soil water deficits, should include intensive thinning and coppice cutting to reduce stand leaf area index and stand transpiration. This will result in an improved water budget and reduce the intensity of water deficit, thus lowering the risk of oak decline (Bre´da 2000; Dreyer et al. 2001). In some parts of France, the increasing age of oak stands due to limited harvest poses an additional risk by rendering the trees more susceptible to decline-inducing factors. Often, this problem is related to a conversion of standards with coppice into high stands. At those sites, management procedures should aim to reduce the risk of decline by maintaining an adequate age-class distribution. In addition to hydromorphic sites, root growth may also be impaired at those sites subjected to soil compaction due to the use of forestry machinery. Thus, soil compaction is seen as an additional stress factor, which may well contribute to oak decline on a local scale (Gaertig et al. 1999). Therefore, forest management schemes should aim to reduce the use of heavy machinery on soils that are prone to compaction due to their texture or water relations. A long-term increase in temperature and extended warm and dry periods may result in an increase of the frequency and the intensity of attacks by the borer Agrilus biguttatus. Therefore, the recognition of its activity and a timely sanitary felling is recommended to prevent further losses due to secondary borer attack (Hartmann and Kontzog 1994; Hartmann and Blank 1998). To minimize infestation by Agrilus, it has been recommended that oak stands should be underplanted with beech or hornbeam in order to make the microclimate of the stand less favourable to the beetle (Hartmann and Blank 1998). However, this may increase competition for water among the oaks and the underplanted species. As damage has often (not always) been found to be higher among suppressed trees (Delb 1999; Habermann unpubl.), better silvicultural treatment, including changes from pure oak stands to mixed stands, may help reduce future damage. Acknowledgements We thank our colleagues at the Forest Research Station of Lower Saxony (Niedersa¨chsische Forstliche Versuchsanstalt), Go¨ttingen: Dr. Gerhard Bu¨ttner, Dr. Ulrike Kiehne; and at the University of Go¨ttingen, Albrecht von Haller Institute of Plant Sciences, Section Ecology and Ecosystem Research: Thomas Gieger, Ulrike Ahlers, Christiane Bartels, Tanja Brandt, Thomas Gausling, Gabriele Gcocos, Christine Hilker, Gabriele Meyer, Michaela Schmull, Stefan Schrader, Katharina Sporns and Susanne Sprenger for their cooperation. We also thank numerous foresters in Northern Germany for their kind support in our field investigations. The study was partly funded by the German Ministry of Education and Research (Bundesministerium fu¨r Bildung und Forschung), Project no. 0339382 A. The authors are responsible for the content of the publication.


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Re´sume´ Facteurs abiotiques et biotiques et leurs interactions, comme causes du de´pe´rissement des cheˆnes dans le centre de l’Europe Des de´pe´rissements de cheˆnes ont eu lieu pe´riodiquement durant les trois sie`cles passe´s comme durant les rećentes dećades. D’apre`s les mentions historiques et des observations dendrochronologiques, le de´pe´rissement des cheˆnes dans le centre de l’Europe a e´te´ attribue´ a` l’effet simple ou combine´ d’extreˆmes climatiques (froids hivernaux, sećheresses estivales), de de´foliations par les insectes, et de champignons parasites. Dans le pre´sent article, nous discutons du roˆle possible de facteurs abiotiques (pollution atmosphe´rique, eutrophisation azoteé, stress chimique du sol, extreˆmes climatiques, conditions stationnelles) et de facteurs biotiques (de´foliations entomologiques, attaques de xylophages, infection de champignons parasites, et autres microorganismes) qui ont e´te´ associe´s au de´pe´rissement des cheˆnes. Sur la base des recherches reáliseés a` trois niveaux diffe´rents sur Quercus petraea et Q. robur (depuis des expe´riences sur jeunes plants jusqu’au suivi supra re´gional), nous proposons un mode`le conceptuel d’interactions entre les facteurs abiotiques et biotiques responsables de l’initiation du de´pe´rissement. Ce mode`le devrait eˆtre valide pour les cheˆnaies du centre de l’Europe sur sols acides (pH(H2O) £ 4,2, des Phytophthora ssp. pouvant contribuer au de´pe´rissement sur les sols a` pH plus e´leve´). Les de´foliations entomologiques se´ve`res pendant au moins deux anneés consećutives et les extreˆmes climatiques, constituent la combinaison de facteurs la plus significative dans l’apparition du de´pe´rissement. La sećheresse estivale ou les geleés hivernales ou printanie`res, ou les deux, doivent avoir lieu la meˆme anneé que la de´foliation, ou les anneés suivantes, pour qu’un de´pe´rissement majeur se de´veloppe. D’autres facteurs additionnels de stress sont: (1) les conditions d’hydromorphie qui rendent les arbres (particulie`rement Q. robur) plus sensibles au stress hydrique a` cause d’une moindre croissance racinaire dans le sol profond; (2) e´ventuellement l’exce`s d’azote qui, combine´ au stress hydrique, induit une reélle diminution des concentrations foliaires en me´tabolites secondaires chez Q. robur, ce qui rend probablement les arbres plus sensibles aux de´foliations entomologiques. La pollution atmosphe´rique, le stress chimique du sol (y compris l’exce`s en mangane`se), et les de´se´quilibres nutritionnels induits par l’azote ne semblent pas intervenir de façon importante dans le processus de de´pe´rissement. Sur la base du mode`le, le de´pe´rissement le plus rećent apparu dans le nord-ouest de l’Allemagne peut eˆtre explique´ de façon satisfaisante.

Zusammenfassung Abiotische und biotische Faktoren und ihre Wechselwirkungen als Ursachen fu¨r das Eichensterben in Mitteleuropa Eichensterben-Episoden traten wiederholt in den letzten zweihundertfu¨nfzig Jahren wie auch in den letzten Dekaden auf. Auf der Grundlage historischer Aufzeichnungen und dendrochronologischer Untersuchungen wurde das Eichensterben in Mitteleuropa auf einzelne oder kombinierte Auswirkungen klimatischer Extreme (Winterfrost, sommerliche Trockenheit), Entlaubung durch herbivore Insekten und Befall mit pathogenen Pilzen zuru¨ckgefu¨hrt. Im vorliegenden Beitrag wird auf der Basis einer Literaturu¨bersicht die Rolle verschiedener abiotischer (Luftverschmutzung, Stickstoff-Eutrophierung, bodenchemischer Stress, Witterungsextreme, Standortsbedingungen) und biotischer Faktoren (fraßbedingte Entlaubung durch Insektenlarven, Borkenka¨fer, pathogene Pilze, Mikroorganismen) diskutiert, die mit Eichensterben in Verbindung gebracht wurden. Vor dem Hintergrund von Untersuchungen, die auf drei unterschiedlichen Ebenen (von Experimenten mit Jungbaümen bis zum Monitoring im u¨berregionalen Maßstab) an Quercus petraea und Q. robur durchgefu¨hrt wurden, wird ein Modell der Wechselwirkungen abiotischer und biotischer Faktoren bei der Entstehung des Eichensterbens vorgestellt. Dieses Modell gilt fu¨r mitteleuropaïsche Eichenbesta¨nde an sta¨rker sauren Standorten (pH (H2O) £ 4,2; auf Bo¨den mit ho¨herem pH-Wert ko¨nnen Phytophthora-Arten zum Eichensterben beitragen). Eine Kombination von Kahlfraß in aufeinanderfolgenden Jahren und Witterungsextremen ist bei der Entstehung von Eichenscha¨den die bedeutendste. Von den drei Faktoren Kahlfraß, sommerliche Trockenheit und Winter- bzw. Spa¨tfrost mu¨ssen mindestens zwei zeitgleich oder kurz nacheinander auftreten, um schwerwiegende Episoden von Eichensterben auszulo¨sen. Schadversta¨rkende Stressfaktoren sind wechselfeuchte Standortsbedingungen, die, insbesondere bei Q. robur, die Anfa¨lligkeit der Baüme fu¨r Trockenstress aufgrund der Beeintra¨chtigung des Wurzelwachstums im Unterboden erho¨hen, sowie mo¨glicherweise u¨berschu¨ssiger Stickstoff, der, in Kombination mit Trockenstress, bei Q. robur zu einer drastischen Abnahme der Konzentration sekunda¨rer Pflanzenstoffe in den Bla¨ttern fu¨hrt und somit die Baüme wahrscheinlich anfa¨lliger fu¨r fraßbedingte Entlaubung macht. Luftverschmutzung, bodenchemischer Stress (einschließlich u¨berschu¨ssiges Mangan) und Stickstoff-induziertes Na¨hrstoffungleichgewicht scheinen im Ursachenkomplex des Eichensterbens keine wesentliche Rolle zu spielen. Auf der Grundlage des vorgestellten Modells la¨sst sich die Entstehung der ju¨ngsten Eichenscha¨den in Nordwestdeutschland angemessen erkla¨ren.

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