Phytophthoras in European forests: Their rising significance

Clive Brasier

Before 1990. An epidemic of ink disease (root and collar rot) of European chestnut, Castanea sativa, caused by the introduced pathogens P. cinnamomi and P. cambivora, occurred in central and southern Europe in the 1920s-1940s. Today, the disease remains very active and widespread. Research on chestnut resistance is in progress. In the 1960s-1970s P. cinnamomi caused an epidemic on trees and woody ornamentals within the European horticulture trade and consequently in gardens. P. cinnamomi also damaged plantation American red oak, Quercus rubra, in southwest France. Generally, Phytophthora species caused local damage to a wide range of other broadleaved and coniferous hosts.

Since 1990 the picture of Phytophthora species in European forests has changed considerably, with a number of prominent new developments.

Cork oak mortality: In 1991 the aggressive, introduced root pathogenP. cinnamomiwas shown to be involved in the continuing and widespread mortality and decline of two evergreen oak (or live-oak) species in southern Europe, Quercus suber (cork oak) and Q. ilex (holm oak). The disease is concentrated in southern Spain and Portugal. Infected trees may die rapidly (known locally as sudden death) or slowly. There may be a significant interaction with drought. Other woody species in these oak ecosystems are also susceptible. Research on cork oak resistance is in progress.

Deciduous oak dieback: In the mid-1990s, a range of root-infecting Phytophthora species were shown to be associated with classic oak dieback; a widespread complex disease (also involving climatic and soil effects) of deciduous oaks such as Q. robur across central and northern Europe. The associated Phytopthoras included well-known species such as P. cambivora and P. citricola, plus a raft of previously unknown species such as P. quercina sp. nov. Some studies show a strong relationship between crown dieback symptoms and the presence of Phytophthora species. The associated Phytophthoras probably have different ecologies, and their role in forests remains little understood. Several are believed to be invasive.

New hybrid alder Phytophthora species: In 1993 a new collar-rot disease of European alders (Alnus spp.) was reported in the UK. A Phytophthora was isolated and shown to comprise a swarm of hybrids between two Phytophthora species: P. cambivora and a Phytophthora close to P. fragariae. Both these 'parent' species were probably introduced into Europe. Neither is a pathogen of alder; i.e., the hybridization event may have led to a new host specificity. The event is probably recent and it has been suggested that it occurred in a nursery environment. The hybrids are now spreading across Europe, probably mainly via infested planting stock. They threaten the future of riparian and plantation alders in many areas. However, the threat to alder populations elsewhere in the world is unknown.

Phytophthora ramorum sp. nov.: P. ramorum., cause of Sudden Oak Death in the USA, is also spreading in Europe on rhododendrons and viburnums within the ornamental nursery trade. There is no evidence to date that P. ramorum is attacking trees in Europe. Tests of the pathogen's ability to infect bark and foliage of European native and plantation trees are underway. Preliminary results indicate there may be more susceptible, less susceptible, and resistant tree species. The European and U.S. populations of P. ramorum appear to differ somewhat in their behavior and molecular fingerprints. Hence the European and US outbreaks are probably unrelated. (http://danr.ucop.edu/ihrmp/sodsymposium.html)

Many new Phytophthoras: In addition to the hybrid alder Phytophthora species and P. ramorum, at least ten other new Phytophthora species have been obtained recently from European trees or forests. Their discovery reflects a growing awareness of the threat posed by Phytophthora species to forest ecosystems (before 1990 only about 50 Phytophthora species were known to science). Some may be native Phytophthora species, some may be introduced aliens, and some may be new hybrids. As with the alder Phytophthora and P. ramorum, their ecology, their host range, and the threat they pose to trees on other continents have yet to be fully evaluated.

Spread by planting stock: Since 1990 evidence has accumulated that infested nursery stock plays a significant role in introducing alien Phytophthora species into Europe and in spreading them from nurseries into forests. The problem may be exacerbated by the common use in nurseries of fungistatic (not fungicidal) chemicals. This can allow Phytophthora-infected but healthy looking plants to be sold or exported. Furthermore, Phytophthora species may thrive under intensive nursery regimes, even occurring on 'non-hosts'; i.e., host species they would not usually infect in the field. As many as five different Phytophthora species have been isolated from a single potted nursery alder seedling. This indicates a considerable potential for evolution - via hybridization between species - of entirely new or genetically modified forest Phytophthora species - such as the new alder Phytophthora - in nurseries.

Influence of climate change: Climate models constructed in the 1990s indicate that predicted levels of global warming and climatic instability could favor some forest Phytophthora species such as P. cinnamomi, increasing their activity and spread in parts of Europe (and worldwide). Corresponding climatic stress on trees, such as oaks, could also render hosts more susceptible to Phytophthora species. These types of interaction, along with the introduction of aggressive alien Phytophthora species, may further exacerbate existing disease problems such as cork oak mortality and deciduous oak decline.

Phytopthora species and European forests: Some outstanding ecological issues

• Alien, invasive Phytophthora pathogens that could endanger European forests and natural ecosystems continue to enter Europe.
• Alien Phytophthora species are a threat because native European trees may have little resistance to them.v
• Invasive Phytophthora species may not only cause acute epidemics, but also be the basis of long-term forest declines, loss of biodiversity, and degradation of entire ecosystems.
• Infested but visibly healthy nursery stock has been implicated in the introduction or spread of many alien Phytophthora species in Europe.
• In time, alien Phytophthora species may gradually adapt and become able to attack new hosts.
• Alien Phytophthora species may also hybridize with resident Phytophthora species to produce new or modified Phytophthora species and new tree diseases.
• Global warming may further exacerbate these problems.
• Ecology, diversity, and general biology of native and alien Phytophthora species in European forests are poorly understood.

References

Brasier, C.M. 1999. Phytophthora pathogens of trees: Their rising profile in Europe. Forestry Commission Information Note 30. HMSO, London. 6 p.

Brasier, C.M. 2000. The role of Phytophthora pathogens in forests and semi-natural communities in Europe and Africa. In: Hansen, E.M. and Sutton, W., eds. Phytophthora diseases of forest trees. Forest Research Laboratory, Oregon State University Press: 6-13.

Brasier, C.M. and Jung, T. [In press]. Progress in understanding Phytophthora diseases of trees in Europe. Australasian Plant Pathology.

Delatour, C., ed. 2001. Report on European Community Project: Long-term dynamics of oak ecosystems: assessment of the role of root pathogens and environmental constraints as interacting decline inducing factors ('Pathoak'). European Community, Brussels. 115 p.

Gibbs, J.N., Van Dijk, C., and Webber, J.F. [In press]. Phytophthora disease of alder in Europe. Forestry Commission Bulletin. HMSO, London.