Risk analysis of Phytophthora ramorum establishment in the Mediterranean area

Eduardo Moralejo & Enrique Descals.
Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB), c/Miquel Marquès, 21, 07190 Esporles, Balearic Islands, Spain; vieaemr@uib.es

The newly described plant pathogen, Phytophthora ramorum Werres et al. (2001), is the causal agent of extensive oak and tanoak mortality in central coastal California since 1995 (Rizzo et al. 2002), as well as those of Rhododendron leaf and twig blight and Viburnum stem canker in nurseries in Europe since 1993. This oomycete is causing important economic and ecological damage in California. International concern has risen because of the risk of spread in natural vegetation in other areas of the USA and Europe. In the last two years international co-operation on research of P. ramorum biology has grown and as a result of this the first International Science Symposium on Sudden Oak Death (SOD) was held in Monterey, California, in December 2002. Some of what was presented in Monterey, including our own laboratory research, is cited here in our discussion on the risk of establishment of P. ramorum on natural vegetation in the Mediterranean area.

Might P. ramorum Become Established In Natural Vegetation In The Mediterranean Basin?

Forecasting the establishment of an introduced wide-host range pathogen in a new area is risky. But an overview from classical plant pathogen epidemiology may offer some assistance. For a disease to occur and develop optimally, a combination of three factors must concur: an infective pathogen, susceptible plant(s), and a favorable environment, mainly with regard to the climate (Agrios 1997).

P. ramorum is a pathogen (introduced or native) recently emerging in California due to the concurrence of these three conditions at the right place and time. And this is not the first case nor perhaps the last one to occur. P. cinnamomi dieback in Australia is a good example of an invasive disease that has caused a dramatic ecological impact (Weste & Marks 1987). It has also been reported to cause oak mortality in the southwestern part of the Iberian Peninsula (Brasier 1992) and threatens important endemic plants in Cape Town, South Africa. Coincidentally, both large-scale diseases affecting entire ecosystems are caused by exotic Phytophthora spp., in distant Mediterranean climates and vegetation type areas.

The Pathogen: Pathways To Natural Vegetation

The first requirement for disease development has been fulfilled: P. ramorum has already been found in several localities in the Mediterranean area; it has been isolated from imported ornamental Rhododendron spp. (Moralejo & Werres 2002) in garden centers in Majorca (Balearic Islands), Spain and from Rhododendron spp. and Viburnum spp. in France (SODSS, Delatour et al. 2002). A wider distribution area within Spain and other European Union Mediterranean member states is expected when the results of official surveys are published later in 2003.

Imported ornamental rhododendrons from European nurseries seem to be the common pathway of entrance of P. ramorum into Majorca and maybe other regions of Spain. The inoculum might spread from garden centers to natural vegetation either through direct transmission or, more probably, through infected plants transplanted to private gardens. Fortunately rhododendrons are not a popular plant in eastern Spain because they are not well adapted to calcareous soils and summer drought and heat. However, rhododendrons are usually set in garden centers alongside other laurophyllous ornamentals such as Arbutus unedo, which is known to be highly susceptible in laboratory inoculations. In addition, Viburnum tinus is an important nursery plant in Spain as well as a widespread native plant around the Mediterranean. Inside garden centers there is a high risk of P. ramorum spreading to alternative potential hosts and from these back to the nurseries, where they are propagated. Much care should be taken, because these could be a new undetected source of P. ramorum and a new pathway for the pathogen reaching natural vegetation. Furthermore some Mediterranean potential hosts are extensively grown in official nurseries for reforestation programs.

Potential Hosts In Natural Vegetation

From our preliminary in vitro inoculation trials several Mediterranean plants proved to be susceptible to the P. ramorum A1 mating type strain (Figs. 1 & 2). The widely distributed species Arbutus unedo, Pistacia lentiscus, Ceratonia siliqua, Rhamnus alaternus, Lonicera implexa, and occasionally Olea europea are highly susceptible to the pathogen which causes extensive blight 7 days' after inoculation of detached leaves (SODSS, Moralejo & Hernández 2002). In addition, fruits of these species, except those of C. siliqua, are susceptible, and a high number of sporangia were produced when inoculated with zoospores. Furthermore, UK Forest Commission pathogenicity tests using both American and European strains of P. ramorum have found that Quercus ilex is among the most susceptible European forest species (SODSS, Brasier et al. 2002). To date, it seems that there is no significant difference in the degree of in vitro pathogenicity between American A2 and European A1 mating type strains (SODSS: Brasier et al. 2002; de Gruyter et al. 2002). These preliminary results create great concern, because evergreen oak forests and woodlands are among the most widespread forest ecosystems in the Mediterranean Basin.

In the California coastal range, P. ramorum has been reported to produce three diseases in redwood forests, mixed evergreen forests, and oak woodland ecosystems (Rizzo et al. 2002): girdling canker on some Fagaceae, and foliar blight as well as twig dieback on many understory shrubs and trees, including tanoak, redwood and Douglas-fir. The distinction of three diseases proposed by Hansen (SODSS, 2002) in the same ecosystem provides clues for understanding the epidemiology of the SOD syndrome in California and Oregon, and focuses on the possibility of P. ramorum becoming established in other plant communities in the USA and Europe without causing tree mortality and thus, going undetected.

Hygrophilous trees form redwood forests and mixed evergreen forests above 36º latitude on the California coast without equivalent ecosystems in the Mediterranean Basin. However, the Californian oak woodland and Mediterranean holm oak woodland and forest occupy an equivalent habitat, with a similar canopy structure and understory shrubs belonging to the laurophyllous and sclerophyllous type of vegetation (Dallman 1998).

The Environment

To date, the SOD epiphytotic is limited to the fog belt along the Pacific coast of California and Oregon where special climatic conditions within the Mediterranean climate pattern are produced. The Mediterranean climate is characterized by mild, rainy winters and hot, dry summers. In those areas affected by SOD, rain precipitation ranges from 600 to 2000 mm, and the dry season usually extends from june to november although summer temperatures are attenuated because of the cooling effect of oceanic currents and fog. The role of the climate in SOD epidemiology is beginning to be understood; P. ramorum seems to produce a polycyclic plant disease with a 3 to 5 month overseason stage during the dry season. The propagative stage initiates soon after the first seasonal rains and extends throughout the rainy season. The number of sporangia in the environment reaches a maximum at the end of the rainy season. (SODSS, Davidson et al. 2002). Although drought hinders transmission of the disease it does not compromise inoculum survival on infected tissue.

Many areas around the Mediterranean Basin have a rainy season, which is as long or longer than that found in California; therefore, climatic conditions are expected to produce more disease cycles throughout the year if P. ramorum become established. However, the effect of heat long exposures on P. ramorum is unknown. Therefore, the most important fact is whether the pathogen can survive the hot dry summer.

Conclusions

Preliminary research indicates that P. ramorum might become established in the Mediterranean evergreen oak forest. Its success or failure will basically depend, in order of priority, on (i) the ability to survive prolonged heat in the form of chlamydospores or mycelium in infected tissue or in soil, (ii) the degree of susceptibility of understory shrubs and its capacity to produce a large number of sporangia on aerial lesions, (iii) the plant community structure, (iv) and the susceptibility of evergreen and deciduous oaks, and other forest trees. Consequently we believe that priority research on this issue should focus on assessing chlamydospore survival; screening the susceptibility of Mediterranean flora, especially trees, by means of in vitro tests; determining numbers of sporangia per unit leaf area as compared with those found on bay laurel in California; analyzing climatic conditions and plant community components; and developing a risk model of P.ramorum establishment throughout the Mediterranean Basin.

Acknowledgements

We are grateful to the "Direcció General de Biodiversitat de la Conselleria de Medi Ambient, Govern Balear" for the financial support provided.

References

Agrios, G. N. (1997) Plant pathology. 4th edition. Academic Press.

Brasier, C. M. (1992) Oak tree mortality in Iberia. Nature 360, 539.

Dallman, P. R. (1998) Plant life in the world's Mediterranean climates. Oxford University Press.

Moralejo, E. & Werres, S. (2002) First Report of Phytophthora ramorum on Rhododendron sp. in Spain. Plant Disease 86, 1052

Rizzo, D. M., Garbelotto, M., Davidson, J. M., Slaughter, G. W., & Koike, S. T. (2002) Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease 86, 205-214.

SODSS, Sudden Oak Death Science Symposium, Monterey, California (2002) http://danr.ucop.edu/ihrmp/sodsymp/present.html.

Werres, S., Marwitz, R., Man in't Veld, W. A., De Cock, A. W., Bonants, P. J., De Weedt, M., Themann, K., Ilieva, E. & Baayen, R. P. (2001) Phytophthora ramorum sp., a new pathogen on Rhododendron and Viburnum. Mycological Research 105, 1155-1165.

Weste, G. & Marks, G. C. (1987) The biology of Phytophthora cinnamomi in Australasian forests. Annual Review of Phytopathology 25, 207-229.