Host and Habitat Index for Phytophthora Species in Oregon

Introduction

Phytophthora species are known as pathogens of agricultural crops or invasive pathogens destroying forests, and their prominent inclusion in various host-pathogen-indices reflects this importance. It is increasingly evident, however, that Phytophthora species are abundant in streams in healthy forests and widespread in forest soils causing cryptic diseases, in addition to their more traditional roles as aggressive pathogens. While their ecology in non-agricultural ecosystems remains poorly understood, we now know that a numerous and diverse, nutritionally complex community of Phytophthora species is present in a variety of associations with forests and forest trees.

In this contribution we compile existing records from available sources of reliably identified Phytophthora species from forests and forest trees in Oregon, USA. The results are summarized by host and habitat in Tables 1-3. A searchable version of this information may be found in the Forest Phytophthoras of the World Disease Finder (select USA-Oregon). Details of specifically documented isolates, including locations and available cultures and Genbank acquisitions, as well as citations are included in the supplemental spreadsheet. We have included isolations from soil and streams in forests that are often not associated with any specific disease symptoms. Our goal is to inventory forest Phytophthora species, not forest diseases. On the other hand, we have included records from forest trees growing outside the forest, as Christmas trees or in the urban landscape, for example. The result is, we hope, a more accurate representation of the ecological amplitude of Phytophthora species and a more complete record of the sources from which they may be spread.

Sources

For this report we attempted to compile all reliable records from all sources. Most records were from three large programs or projects. The OSU Plant Disease Clinic database extends across many years and includes records from all hosts and the entire state. Most samples to the Clinic came from diseased plants grown as agricultural or horticultural crops, and many Phytophthora isolations were identified only to genus; these were not included here. Those from forest related sources with specific identification were included, however, and identified by “Pc”. Another major source continues to be the Sudden Oak Death control program in this state. While diagnosis focused on P. ramorum, and was concentrated in one county in the SW corner of the state, all Phytophthora species encountered in plants, soil, and streams were cultured and identified, leading to many new records. Many of theseresults were published and sources are cited here. The third main source of records was an ongoing survey of the Phytophthora species associated with declining alder trees along streams in western Oregon. This has resulted in several thousand Phytophthora isolates from alder roots and stems as well as associated soil and adjacent streams. This work is not yet published. In addition, there were many reports from systematic surveys of Phytophthora species in forest tree nurseries and Christmas tree plantations. Unfortunately, morphological identification methods available at the time could not distinguish problem species reliably and many of these records were thus excluded.

Criteria for Inclusion

Phytophthora species: All records are based on isolations in culture, and identifications of all problematic species were confirmed with molecular sequencing methods. Older records of species that lack distinctive morphology were not included unless confirmed by recent sequencing of original isolates. Many records originally identified as P. drechsleri, P. citricola, P. cryptogea, and P. megasperma in particular were thus excluded. This especially affected the host and location records from forest tree nurseries, since nursery pathology research in Oregon largely predated availability of molecular tools.

Species concepts in Phytophthora continue to evolve. The range of variability in morphology as well as DNA sequence is not clearly established for many species. We have adopted a population based phylogenetic species concept that is tolerant of minor variations in sequence and morphology, so long as isolates are consistent with norms for the species, and in the same terminal DNA sequence clade. Sometimes single isolates or even populations of isolates differ from named species in more troublesome ways. In this work, these are named for the closest established relative, but a “note” is added in the appendix Table. In a few cases it is clear that a population represents an as yet undescribed species. These are designated P. taxon xxxx. P. taxon ceanothus, for example, would be identified as P. citrophthora based on ITS sequence alone, but isolates are homothallic.

Habitats and Hosts: All records are from western Oregon (west of the crest of the Cascade Mountains). We have not deliberately excluded the eastern 2/3 of the state; there simply are no forest Phytophthora records from that part of the state. There are extensive forests on the ‘eastside,’ but these are drier forests with fewer hardwoods, and there have been no stream surveys in these areas as yet. “Forest” in our usage is a plant community dominated by trees at maturity. We include records from all plant species growing in the forest, as well as from forest soil and forest streams. “Forests” are often disturbed and may be found at various stages of ecological succession. In Oregon, many forests originated from planting after harvest of the previous stand. They are almost always comprised of species native to Oregon. “Christmas tree plantations” and “Seed orchards” are cultivated plantations of forest tree species managed for specific products. The “Urban” habitat refers to trees planted in cities, usually in parks or as street trees. In some cases the host species are not native to Oregon.

In forest nurseries trees, and sometimes shrubs and other native plants, are intensively managed to produce stock for transplanting to forest sites for regeneration of the forest after harvest or other disturbance. In general, we have not included records from horticultural nurseries, regardless of the plant species. The decision is rather arbitrary and the distinction is sometimes vague, however. Chamaecyparis lawsoniana illustrates the ambiguity. We have included landscape records for this species that is widely planted as an ornamental, but we have not included horticultural nursery records despite the role of the horticultural nurseries in the establishment and spread of Phytophthora lateralis in the state.

Results and Discussion

Thirty-two Phytophthora species, including described but not formally named taxa, have been identified associated with 25 host species from Oregon forests or forest trees (Tables 1 and 2). This total includes 19 species recovered from forest streams, and 19 from forest soils, generally in the absence of noticeable disease on associated vegetation. A total of 29 Phytophthora species were identified from the various environments in forests (Table 3). Fourteen species came from cultivated and urban environments. Only three species were unique to the latter, however, including P. ilicis, known only from cultivated holly (Ilex), P. sansomeana and P. taxon ceanothus from forest nurseries (Table 3).

The sampling that produced these lists is not systematic, however, and very uneven. Only in tanoak forests of Curry County was the full range of habitats sampled. Two large studies focused on forest stream sampling, so the list from that habitat is perhaps most complete, but this work still covers only a small portion of the state, including streams in 12 of the 19 counties in western Oregon. Three species, P. gonapodyides, P. taxon oaksoil, and P. lacustris (Nechwatal et al. 2012) were recovered from streams in 13 counties. The most widespread species causing root disease or bole cankers was P. lateralis on Port Orford cedar in landscape plantings throughout the state as well as on forest trees in its limited native range (Tucker and Milbrath 1942), and P. cambivora, which is widespread but uncommon on a number of forest trees (Saavedra et al. 2007). Other widespread species were P. ilicis, only on holly in commercial plantations and landscapes (Buddenhagen and Young 1957), and P. cinnamomi on several hosts, although uncommon. In contrast, eleven species are reported from only 1 county. Some, such as P. ramorum on Notholithocarpus are locally abundant (Hansen et al. 2008), while others seem to be rare, known only from one or a few records. The overall forest Phytophthora record reflects the relative health of Oregon forests despite the potential susceptibility of the tree species evident from the records from nurseries and Christmas tree plantations.

Douglas-fir (Pseudotsuga menziezii) provides an interesting example. It is by far the most important forest tree in Oregon, dominating forest sites in much of the state including the 19 counties in western Oregon that were most regularly sampled in these surveys. Only one Phytophthora species (P. ramorum) is reported from this host growing in forests, although in nurseries and Christmas tree plantations at least five other species cause disease. In contrast, tanoak (Notholithocarpus densiflorus) is host to at least 11 Phytophthora species in the forests of SW Oregon where it grows (Reeser et al. 2008, Reeser et al. 2011a)

Acknowledgements

We thank the Oregon Department of Forestry and the USDA Forest Service, Pacific Southwest Experiment Station and Southwest Oregon Forest Insect and Disease Center for participation in, and support of, this work.