4.1 Involvement of Phytophthora spp. in beech decline, site relations and interactions with climatic factors
This study demonstrated the occurrence of soil-borne Phytophthora species and typical disease symptoms at root, stem and crown level in most of the 134 beech stands investigated in Bavaria. Phytophthora infested sites covered the whole range of typical beech sites with pH (CaCl2) values between 3.3 and 7.0 and gritty-loamy, sandy-loamy, loamy, silty and clayey soil texture. Interestingly, many of the stands were growing on sites that hitherto were not believed to favour Phytophthora infections as the soils had either a very low pH (podzolic cambisols or podzols from sandstones, mylonite or granite) or a good vertical (rendzinas or sandy-loamy cambisols) or lateral drainage (steep slopes) thus preventing any waterlogging. Since the majority of the stands were randomly selected, a regular infestation of most beech stands in Bavaria can be suggested.
Phytophthora citricola and P. cambivora had the widest distribution and in pathogenicity tests have proven to be most aggressive to root systems and stem bark of beech. In soil infestation tests P. citricola and P. cambivora caused almost complete destruction of the fine root systems of young beech plants and 70 to 90% mortality within four months (Jung et al. 2003b), while P. pseudosyringae was markedly less aggressive (40% root rot, no mortality). Similar results were reported by Fleischmann et al. (2002). In underbark inoculation tests with logs of mature beech trees, P. cambivora and P. citricola caused bark necroses with a mean lesion size of 140 cm2 within 5 weeks (Brasier and Jung 2003). Stem inoculation tests with young beech trees revealed similar results. Here, P. gonapodyides and Py. undulatum were also shown being pathogenic to beech (Jung and Blaschke 1996).
Phytophthora cambivora and P. citricola are also widespread in declining oak stands across Europe (Jung et al. 1996, 2000; Hansen and Delatour 1999; Vettraino et al. 2002; Balci and Halmschlager 2003a,b; Jönsson et al. 2005), and were shown to be pathogenic to root systems and bark of Q. robur (Jung et al. 1996, 1999, 2002, 2003a,b; Brasier and Jung 2003). Moreover, P. cambivora is the major cause of the devastating Ink Disease of sweet chestnut (Castanea sativa) in Southern Europe (Vettraino et al. 2001, 2005), while P. cactorum and P. citricola are involved in the widespread decline and mortality of horse chestnuts (Aesculus hippocastanum; Werres et al. 1995; Jung and Blaschke 1996; Brasier and Jung 2006; Webber et al. 2006) and several Acer and Tilia species (Brasier and Jung 2006; Jung unpublished results). The high susceptibilty of the most common broadleaved tree species from Europe to P. cambivora, P. cactorum and P. citricola obviously indicates a lack of adaptation, which suggests a relatively recent introduction to Europe of these globally distributed pathogens (Erwin and Ribeiro 1996; Waterhouse and Waterston 1966b,c). For P. citricola, which was first described in 1927 from Citrus trees in Taiwan, the recent widespread finding of isolates in symptomless broadleaved forests in Nepal (Vannini et al. 2007), supports the hypothesis of a non-European origin. Also P. cambivora is believed to be introduced in Europe, results of an isozyme study of a worldwide collection of P. cambivora isolates suggesting an Australian origin (Oudemans and Coffey 1991). In order to definitely clarify the invasive status of P. cambivora, P. citricola and P. cactorum in Europe, molecular studies of the genetic variability of a global collection of isolates using AFLPs (Brasier et al. 1999; Cooke et al. 2005), nuclear gene-specific primers and mitochondrial gene-specific primers (Ioos et al. 2006) are urgently required. This has already been done for the aggressive oak-specific fine root pathogen P. quercina. A molecular study of the genetic variability of a European collection of isolates using AFLP markers demonstrated that P. quercina is unlikely to be native to Europe, and that it might have been introduced on several occasions (Cooke et al. 2005). This hypothesis was recently supported by the widespread finding of P. quercina in oak forests of the eastern USA (Schwingle et al. 2007).
The severe deteriorations of the crown structure of beech trees observed in most stands of this study and at the Forest Condition Monitoring Plots of the Bavarian State Forestry (Anonymous 2003, 2004, 2006a) are the result of a long-term degeneration of the crowns, which is indicative for long-term problems in the root system. Considering the high aggressiveness of Phytophthora species to roots and bark of beech, their regular association with declining beech trees as shown by this study and by investigations in north-western Germany and Belgium (Hartmann and Blank 1998; Hartmann et al. 2006; Schmitz et al. 2007), and the similarity of root and crown symptoms of declining beech and oak trees, it seems likely that Phytophthora species are strongly involved in the widespread chronic decline of beech as was shown for European oak decline (Brasier et al. 1993; Jung et al. 1996, 2000, 2003a; Gallego et al. 1999; Vettraino et al. 2002; Balci and Halmschlager 2003a,b; Jönsson et al. 2005). Likewise, an interaction between a progressive destruction of beech fine root systems with increasing age and decreasing regeneration capacity, climatic extremes, in particular heavy rain and droughts, site conditions, and secondary fungi and insect pests is suggested. In addition, on many sites several Phytophthora species, i.e. P. cambivora, P. citricola, P. cactorum and P. gonapodyides caused collar rot and aerial bark cankers in beech trees, leading to a rapid dieback of the trees. Moreover, these primary necroses are usually invaded by a series of secondary bark pathogens and wood rotting fungi, exacerbating the damages and predisposing the trees to storm damages. However, detailed studies on the fine root status of declining and healthy beech trees on a wide range of site conditions, and on the correlation between root and crown condition as done for European oak decline (Jung et al. 2000; Vettraino et al. 2002; Balci and Halmschlager 2003a) are required before final conclusions on the involvement of Phytophthora species in beech decline can be drawn.
In contrast to the slow and chronic decline of the preceding decade, beech stands across Bavaria experienced a sudden and strong increase of crown damages and mortality levels in 2003 and 2004 (Anonymous 2003, 2004). The sudden dieback coupled with the presence of Phytophthora collar rots and aerial cankers in supposedly non-conducive soils/sites, raises the question of the triggering factors. Since in most stands the majority of the Phytophthora-induced bark lesions could be dated back to the extremely wet year 2002, and extensive fine root losses were observed in most of the sampled stands the following hypothesis seems feasible: the extremely high precipitations in spring, late summer and autumn 2002 (Fig. 8) led to prolonged favourable conditions for the continuous production and spread of Phytophthora zoospores even on well-drained soils. As a consequence, multicyclic fine root infections (Erwin and Ribeiro 1996) in the wet soils caused an extensive destruction of the fine root systems of beech trees. Moreover, due to the low tolerance of beech to waterlogging (Ellenberg 1986; Kölling et al. 2005; Felbermeier and Mosandl 2006) and the high inoculum pressure Phytophthora species were able to invade suberised root and stem bark of mature trees on many sites. In 2003, the weakened and predisposed beech stands were faced with the strongest drought of the past 100 years (Fig. 8; Anonymous 2003, 2004). As a consequence, the necessary regeneration of the reduced fine root capacities was inhibited, and beech trees in most stands were suffering from extreme drought stress leading to premature leaf fall (Anonymous 2003), predisposing the trees to attacks by secondary fungi and bark beetles, and resulting in severe crown dieback and increased mortality levels.
The feasibility of this hypothesis is also supported by the observation made in this study and in the Forest Condition Monitoring (Anonymous 2003, 2004) that in stands with a high disease incidence of beech other hardwood species with higher tolerance to Phytophthora spp., i.e. Common ash (Fraxinus excelsior L.), and hornbeam (Carpinus betulus L.), were much less affected by the 2003 drought.
Interactions between Phytophthora infections, floodings and droughts are well known and generally accepted as triggers of epidemics (Duniway 1977, 1983; Brasier et al. 1993; Erwin and Ribeiro 1996; Brasier and Jung 2003; Jung et al. 2003a; Jung and Blaschke 2004). For oak decline in Central Europe and parts of Western and Northern Europe Jung et al. (1996, 2000) suggested that the epidemic extent and its long duration are due to long-term changes of climatic conditions in the second half of the 20th century, i.e. a continuous increase of mean winter temperatures, a seasonal shift of precipitation from summer into wintertime, and a tendency to heavy rain (Schönwiese et al. 1994; Rapp and Schönwiese 1995; Hennegriff et al. 2006). For many regions of Central Europe and in particular southern Germany current models of climate change are predicting a further intensification of these climatic trends (Anonymous 2006b,c; Hennegriff et al. 2006). Therefore, a proliferation of Phytophthora damages may be expected, increasing the instability and vulnerability of forest ecosystems dominated by beech and other tree species susceptible to Phytophthora, i.e. oak, alder, maple, lime, fir and pine species. Recently, a model was developed showing that due to climate change the distribution and local impact of P. cinnamomi and a range of other forest pathogens, i.e. Biscogniauxia mediterranea, Cryphonectria parasitica, Melampsora spp., and Sphaeropsis sapinea will significantly increase in France at the end of the 21st century (Desprez-Loustau et al. 2007). For P. cinnamomi a significant extension of the pathogen’ s activity and distribution in wide parts of Europe was already shown by the model of Brasier and Scott (1994).
The reason because beech decline was observed markedly later than oak decline even though beech is more susceptible to Phytophthora root and bark infections than Q. robur (Jung and Blaschke 1996; Brasier and Jung 2003; Jung et al. 2003b), can be explained by interactions with site factors and defoliating insects. The main distribution of Q. robur is on sites that are prone to Phytophthora infections, i.e. riparian sites and sites with heavy soils and high or fluctuating water tables. In contrast, beech is less tolerant to heavy soils and high water tables and largely avoids these sites. Therefore, it is not surprising that Phytophthora forest damage started in oak stands on Phythophthora-conducive sites despite of the lower susceptibility of the dominant tree species. Furthermore, oak decline is a complex phenomenon. Results of several studies have clearly shown that dieback of oak stands requires the interaction of fine root losses by Phytophthora, insect defoliations and climatic extremes (Jung et al. 2000; Hartmann and Blank 2002; Thomas et al. 2002). Oaks are highly susceptible to various defoliating caterpillars and gradations and total stand defoliations occur periodically (Hartmann and Blank 1992, 2002; Thomas et al. 2002) while severe defoliations of beech stands are extremely rare (Kölling et al. 2005).
During the last five years root and collar rot of beech has been found in most parts of Europe and the eastern USA, and several Phytophthora species were recovered from symptomatic beech trees in Austria (P. cambivora, Cech and Jung 2005; P. citricola and P. cactorum Jung and Cech, unpublished), the Czech Republic (P. citricola, Jung and Jankowski, unpublished), Italy (P. pseudosyringae, Motta et al. 2003; Diana et al. 2006; P. cactorum, Jung, Vettraino and Vannini, unpublished; P. cambivora, Belisario et al. 2006), the Netherlands (P. pseudosyringae, Man In’t Veld, pers. com.), Romania (P. cambivora, Jung and Chira, unpublished), Switzerland (P. cactorum, P. citricola and P. syringae, Jung, unpublished), Turkey (P. cambivora, Balci and Halmschlager 2003b), the United Kingdom (P. cambivora, P. citricola, P. gonapodyides, P. ramorum and P. kernoviae sp. nov., Brown and Brasier 2007; P. pseudosyringae, Denman et al. 2007), and the USA (P. inflata,Jung et al. 2005; Hudler et al. 2006). In north-western Germany P. cambivora and P. pseudosyringae are causing a widespread severe dieback of whole beech stands on both periodically waterlogged and base-rich sites (Hartmann and Blank 1998; Hartmann et al. 2006). Also, in Belgium, P. cambivora was recently recovered from bark cankers of beech trees in 19 out of 49 declining stands, and the involvement of Phytophthora infections in beech decline was also suggested (Schmitz et al. 2007). However, large-scale investigations on pathogen and disease distribution in these countries are required before general conclusions on the involvement of Phytophthora species in beech decline on a European scale can be drawn.
4.2 Aerial bark cankers and possible involvement of Phytophthora species in the complex of ‘Beech Bark Disease’
In 40 stands, aerial bleeding cankers were found on mature beech trees that were similar to those described from ‘Beech Bark Disease (BBD)’. In Europe, BBD is generally considered as a complex interaction of predisposing drought stress, subsequent colonisation of the bark by the scale insect Cryptococcus fagisuga, infection of the colonised bark by the weak parasite Nectria coccinea and, finally, invasion of the stem by wood decay fungi (Parker 1974; Lonsdale and Wainhouse 1987;Butin 1996). However, there has been much controversy over the relative importance of scale insects, N. coccinea and abiotic factors in disease development (Lonsdale and Wainhouse 1987). Surprisingly, in 31 of the 34 Bavarian stands where bleeding cankers had been examined in detail, Phytophthora species could be isolated from actively growing margins of the necroses. In most cases N. coccinea or its anamorph C. candidum were following the active lesion front at a distance of a few centimeters. In most stands no scale insects could be found. This is consistent with observations of Lonsdale (1980) who reported that most cases of BBD affecting mature stands in the United Kingdom occurred in the absence of significant scale populations. The data from the current study support the role played by Phytophthora species in the complex aetiology of BBD in Europe, maybe as the primary pathogen in mature stands. This may have been overseen in the past simply because specific methods for the detection of Phytophthora spp. were not used. This is supported by the finding of Paucke (1966) who observed increased incidences of BBD in Eastern German beech forests associated with increasing soil moisture, and by the observations of higher disease frequencies in depressions (Wood and Nimmo 1962).
Three of the four Phytophthora species recovered from aerial cankers, i.e. P. citricola, P. cambivora and P. gonapodyides, are not able to produce caducous sporangia and thus the mechanism which enables these pathogens to reach 20 m stem height is unknown. Recently, however, Brown and Brasier (2007) demonstrated the presence of both airborne and soilborne Phytophthora species including P. citricola, P. cambivora and P. gonapodyides in non-symptomatic xylem tissue between isolated aerial cankers suggesting that Phytophthora species are able to spread within trees via xylem vessels. The occurrence of sequential multiple aerial cankers following the fibre course in many Bavarian stands strongly supports this hypothesis. However, it cannot be excluded that animal vectors may also be involved. In many stands of this study several species of snails, and in particular the vineyard snail (Helix pomatia), were frequently observed sucking at the exudates from Phytophthora cankers. Microscopical findings of typical oospores in fresh exudates from P. citricola cankers on beech in two Bavarian stands (data not shown) suggest that snails might act as vectors of Phytophthora. This is in accordance with results of El-Hamalawi and Menge (1996) who found oospores and sporangia of P. citricola in the exudates from aerial cankers of avocado in Californian plantations, and proved experimentally that these structures are taken up by snails and transported up-stem where new cankers were formed. Moreover, the bark beetle T. bicolor was often observed to establish breeding galleries in fresh Phytophthora lesions on beech, and it seems feasible that this parasite is able to pass Phytophthora onto healthy trees while establishing sister broods. The feasibility of this pathway was shown for the sudden death of cocoa in Papua New Guinea caused by Phytophthora palmivora cankers (Prior 1986).
4.3 Infestation of nurseries
Fagus sylvatica is the most important tree species in new silvicultural concepts aiming on the replacement of non-natural pure conifer stands by mixed forests, in order to increase the ability of the ecosystems to withstand the threats by predicted climatic changes (Ammer et al. 2005; Kölling et al. 2005; Fritz 2006). Hence, there is an increasing demand for nursery-grown beech plants, and the regular infestations with multiple Phytophthora species of beech fields in Bavarian nurseries are awkward. The majority of the beech fields were infested with the same Phytophthora species responsible for the widespread dieback of mature beech stands, i.e. P. cactorum, P. cambivora and P. citricola. These findings confirmed the results of surveys of nursery fields of beech and other tree species in northern Germany, and nursery fields of alder in Bavaria and eastern Germany (Themann et al. 2002; Jung and Blaschke 2004; Hartmann et al. 2006; Schumacher et al. 2006). Also in Poland nursery fields of beech and other tree species were regularly found to be infested with several Phytophthora species (Orlikowski et al. 2004, 2006). The environmental risk of the presence of multiple Phytophthora species in most nursery fields is evident. The impact of a spread of Phytophthora species into beech forests via infested nursery stock was investigated by Hartmann et al. (2006) in five afforestations on former agricultural land in northern Germany. Eight to 15 years after planting more than 70% of the beech trees were suffering from root and collar rot caused by P. cambivora and high mortality occurred. The devastating impact of a large-scale use of infested nursery stock on natural ecosystems was demonstrated by the root and collar rot epidemic of alders in Europe caused by P. alni and its subspecies (Gibbs et al. 2003; Jung and Blaschke 2004).
In conclusion, the results of this study demonstrate that (1) Phytophthora species are regularly associated with beech decline, (2) the succession of excessive rainfalls and droughts is triggering the disease, and (3) Phytophthora species may be involved in the complex of ‘Beech Bark Disease’. The high susceptibility of the most competitive tree species of Central Europe to non-native, well-established Phytophthora species and the large-scale decline and dieback of beech stands are a serious threat to European forestry and arboriculture. The widespread Phytophthora infestations of nursery stock are likely to undermine any current and future silvicultural projects aiming on the replacement of pure conifer stands by beech dominated mixed stands. Therefore, management concepts for the production of non-infested nursery stock, the silvicultural treatment of declining mature beech stands and the control of the disease in the field are urgently required at a European scale.