Compendium of Conifer Diseases, Second Edition by Scientific Societies

It was concluded that Taiwan probably lies within the natural range of P. lateralis. Port Orford cedar root disease was first reported in 1923 in nurseries growing ornamental cultivars of Port Orford cedar near Seattle, Washington, in the United States. It ultimately eliminated Port Orford cedar as a commercial ornamental tree in North America. In 1952, it was first reported on Port Orford cedar in its native range and has now spread throughout most of the forest areas in the U.S. states of Oregon and California where the tree grows. The annual loss in 1980–1989 was estimated at 2,100 m3, valued at US$2.3 million. Since that time, changes in international trade and protections implemented by the U.S. Department of Agriculture Forest Service have greatly reduced the harvest, and the loss, from federal lands. The ecological consequences of the loss of Port Orford cedar continue in sensitive ecosystems.

Symptoms and Diagnosis Port Orford cedar trees of all ages are killed rapidly. Trees are usually dead within 1 year of the first visible crown symptoms. P. lateralis colonizes the root phloem rapidly, growing to the root crown and on up the stem. A sharp demarcation between reddish infected phloem below and white healthy tissue above (Fig. 4) is visible until the stem starts to dry out or until secondary bark beetles (Phloeosinus sp.) create extensive larval galleries in the dying inner bark. Crown symptoms on yew develop more slowly, with several years elapsing between infection and death. The demarcation between living and dead phloem is visible in trees showing advanced symptoms, but infected tissue is seldom found far above ground. Field diagnosis is based on the distinctive demarcation between infected and healthy tissues in dying trees. The pathogen can be isolated from recently killed tissues, and commercial ELISA kits can be used to detect P. lateralis up to several years after tree death. DNA diagnostic tests are available. In Europe, where aerial infection is observed, the demarcation may appear on infected branches in the upper crowns of trees.

Disease Cycle P. lateralis thrives under cool conditions. In the Mediterranean climate of western North America, it is active through the mild, wet winters and inactive, or even dying, during the warm,

Fig. 4. Phloem lesion on Port Orford cedar caused by Phytophthora lateralis. (Courtesy E. Hansen–© APS)

dry, summer months. It is carried upslope in mud and debris and washes downslope in water. In the North American forests where Port Orford cedar grows, uphill transport is primarily along roads on vehicles and road-maintenance and logging equipment, while downslope movement occurs in streams and through overland flow during periods of heavy winter rains. Zoospores infect Port Orford cedar roots within 24 h of contact. In Europe, root infection is important, but new infections also are found on branches in the upper crowns (Fig. 5). Aerial infection apparently results from windblown sporangia. Longdistance transport in Europe has occurred via infected nursery stock. Chlamydospores and sometimes oospores (P. lateralis is homothallic) form within 2 weeks in infected roots and remain infective for at least 6 years. Resting spores are transported in mud on vehicles during wet weather. If soil is later dropped near healthy cedar roots, the cycle may begin again with germination of spores to produce sporangia that release zoospores during periods of soil saturation. Zoospores swim for only a few millimeters in saturated soil or on leaf surfaces but can be carried much greater distances in flowing or splashing water. They can remain motile for several hours.

Effects on the Forest The consequences of infection are dramatic. Infected Port Orford cedar invariably die, and the extensive system of logging roads in western North American forests has provided access for the pathogen to most of the Port Orford cedar native range. Many cedars survive, however, within the general area of introduction. Port Orford cedar grows in most locales as a minor component of the conifer forest, although it may be the predominant species in local areas, especially in wet places and on ultramafic soils (derived from old, metamorphosed rock high in several heavy metals). Mortality approaches 100% along infested streams and averages perhaps 25% adjacent to infested roads. Trees growing even a short distance away from these inoculum sources often remain healthy, however. Mortality levels away from roads and streams depend on the frequency and intensity of other soil-moving mechanisms, principally timber harvest and mining activity but also animals.

Fig. 5. Aerial infection of Port Orford cedar by Phytophthora lateralis in Scotland. (Reprinted, by permission. Crown Copyright, courtesy Forestry Commission. Licensed under the Open Government Licence)

Ecological effects are most evident in habitats where Port Orford cedar is the predominant tree species. The sensitive riparian habitat is often dramatically altered with death of the Port Orford cedar. With death of the overstory, several species of evergreen shrubs often assume dominance, with a resulting change in both structure and microenvironment of both the terrestrial and the aquatic communities. Distinctive plant community associations including many rare endemic species are found on the ultramafic soils characteristic of much of the region. Port Orford cedar is especially important as a dominant conifer on these soils if subsurface water is available. Disease incidence has not been high on these sites, primarily because timber volumes are low and therefore opportunities for introduction are reduced. Where present, however, the pathogen has a dramatic effect by killing what is often the only overstory species growing on the site. In the native C. obtusa forests of Taiwan, the pathogen is present in saturated soils and occasionally causes a foliage blight, but tree mortality has not been observed.

Disease Management The U.S. Forest Service has an active and aggressive program to stop the further spread of the pathogen, reduce inoculum levels in infested areas, and assure the continued viability of Port Orford cedar as a forest species in the region. All forest management activities in areas where Port Orford cedar grows are evaluated for their potential effects on the Port Orford cedar resource, and activities are modified or appropriate mitigating measures are undertaken, as necessary. Principal actions include road-use restrictions such as wet season or permanent closure, sanitation through equipment washing, and inoculum reduction by removing Port Orford cedar from the very vulnerable roadsides. Port Orford cedar trees vary in susceptibility to the pathogen, and trees that die more slowly than most or even appear to be immune have been identified. Resistance is genetically controlled, and selected trees are being propagated for the resistance breeding program. Seedlings from resistant parents are available and being planted in restoration programs in the forest. In landscape plantings, strict attention to sanitation is essential. In addition, great care must be exercised to assure healthy planting stock.

Ramorum Disease of Larch Other names: Sudden larch death, ramorum dieback, sudden oak death Causal agent: Phytophthora ramorum Werres, De Cock, & Man in ’t Veld Hosts: Larix kaempferi, L. decidua, L. × eurolepis Distribution: Mainly western and southern United Kingdom (England, Scotland, Wales, Northern Ireland), the Republic of Ireland The introduced oomycete pathogen Phytophthora ramorum is well known as the cause of sudden oak death that affects evergreen oaks and tanoaks along 1,500 km of near-coastal forest in the U.S. states of California and Oregon. The same pathogen was also discovered in Europe during the 1990s within the ornamental nursery trade; but from 2003 onward, it has been found infecting rhododendron and broadleaf woodland trees outside nurseries in Great Britain. Initially, tree infections were infrequent, affecting mostly foliage or stems of Fagus, Nothofagus, Quercus, and Castanea spp. growing in the vicinity of infected rhododendron in southwest England. This changed in August 2009 when extensive dieback and mortality were observed in plantation-grown Japanese larch, Larix kaempferi, in southwest England and the causal agent was diagnosed as P. ramorum. Since then, around 20,000 ha of larch have been affected by the disease throughout the United Kingdom, and millions of trees have been felled for disease control.

Symptoms and Diagnosis Japanese, European (L. decidua), and hybrid (L. × eurolepis) larch are grown in the United Kingdom and Ireland for timber production; all are susceptible to infection by P. ramorum. The most conspicuous external symptoms are copious resin bleeding on the trunk, branches, and side shoots plus dieback of branches and sometimes the entire crown (Fig. 6). Phloem lesions are present under the resinous outer bark, often with deep pink to maroon red margins (Fig. 7), while older lesion areas are rusty brown to dark brown and the affected tissue is drier and less resinous. Foliage is also infected, and symptoms include

Selected References Betlejewski, F., Goheen, D. J., Angwin, P. A., and Sniezko, R. A. 2011. Port-Orford-cedar root disease. U.S. Dep. Agric. For. Serv. Pac. Northwest Reg. For. Insect Dis. Leafl. 131. Hansen, E. M., and Hamm, P. B. 1996. Survival of Phytophthora lateralis in infected roots of Port Orford cedar. Plant Dis. 80:1075-1078. Hansen, E. M., Goheen, D. J., Jules, E. S., and Ullian, B. 2000. Managing Port-Orford-cedar and the introduced pathogen Phytophthora lateralis. Plant Dis. 84:4-14. Hansen, E. M., Hamm, P. B., and Roth, L. F. 1989. Testing PortOrford-cedar for resistance to Phytophthora. Plant Dis. 73:791-794. Jules, E. S., Kauffman, M. J., Ritts, W. D., and Carroll, A. L. 2002. Spread of an invasive pathogen over a variable landscape: A nonnative root rot on Port Orford cedar. Ecology 83:3167-3181. Kliejunas, J. 1994. Port-Orford-cedar root disease. Fremontia 22:3-11. Robin, C., Piou, D., Feau, N., Douzon, G., Schenck, N., and Hansen, E. M. 2011. Root and aerial infections of Chamaecyparis lawsoniana by Phytophthora lateralis: A new threat for European countries. For. Pathol. 41:417- 424. Webber, J. F., Vettraino, A. M., Chang, T. T., Bellgard, S. E., Brasier, C. M., and Vannini, A. 2011. Isolation of Phytophthora lateralis from Chamaecyparis foliage in Taiwan. For. Pathol. 42:136-143. Zobel, D. B., Roth, L. F., and Hawk, G. M. 1985. Ecology, pathology, and management of Port-Orford-cedar (Chamaecyparis lawsoniana). U.S. Dep. Agric. For. Serv. Gen. Tech Rep. PNW-184.

(Prepared by E. Hansen and C. Robin)

Fig. 6. Dieback of entire larch crown caused by Phytophthora ramorum. (Reprinted, by permission. Crown Copyright, courtesy Forestry Commission. Licensed under the Open Government Licence)

gray black or purple discolored needles (Fig. 8), aborted bud flush, wilting and senescence of dwarf shoots, and needle loss. Larch trees can die rapidly, apparently within 2–3 years of infection, but this usually occurs when individual trees suffer multiple aerial infections on branches and stems. Other conifer species including Douglas-fir (Pseudotsuga menziesii), grand fir (Abies grandis), and western hemlock (Tsuga heterophylla) can also suffer stem and branch infections and show symptoms of resinosis and crown dieback but only when growing in close proximity to infected larch. These conifers are also infected in the main sudden oak death areas of western North America but only when growing beneath a canopy of infected tanoak. In addition to the striking symptoms, field diagnosis in larch is aided by the use of commercial serological kits that can confirm the presence of Phytophthora in infected bark or symptomatic needles. However, other Phytophthora spp. such as P. pseudosyringae or P. gonapodyides also occasionally cause bark lesions on Larix spp., so positive serological tests are not indicative of only P. ramorum infection.

Disease Cycle P. ramorum is an aerial pathogen, primarily infecting and causing symptoms on aboveground plant parts. The optimum temperature for growth is 20–25°C, but it is capable of significant

bark killing at 10°C, so it is active during mild winters as well as during the spring and fall. It is heterothallic, but populations in the United Kingdom consist only of the A1 mating type and oospores have not been observed. In contrast, both chlamydospores and sporangia form within a few days on infected larch needles. Across the wide host range of P. ramorum, some trees and shrubs have susceptible foliage that generates abundant sporangia and chlamydospores when infected; these plants are known as “sporulating hosts.” In other hosts, only lignified bark is attacked, resulting in lesions on branches and stems, but few, if any, sporangia are produced from these tissues. Until the spread to larch, Rhododendron ponticum was the major sporulating host driving the disease epidemic in Great Britain. However, larch has both susceptible needles and susceptible bark. Huge numbers of sporangia are generated from infected foliage (hundreds or even thousands can form on a single larch needle) (Fig. 9). This inoculum load leads to bark infections, not only causing the dieback and death of larch of all ages but affecting other nearby susceptible broadleaf and conifer species as well. Climate is another major driver of the P. ramorum epidemic in the British Isles. Mists and wind-driven rain can transfer spores from natural infections over a few kilometers, and mild, moist conditions favor sporulation and infection. The most conducive climate for disease development in Great Britain is in the maritime west. Years with above-average rainfall can result in a striking increase in disease development and larch mortality in the following spring and summer.

Effects on the Forest Larch is an important timber tree in Great Britain and makes up about 6% of the total tree cover. It is the only deciduous conifer, so it provides landscape, biodiversity, and recreational value. In large areas historically planted with larch, the effect of P. ramorum disease can be dramatic, with up to 95% of the trees symptomatic or dead and requiring wide-scale removal. This level of clear-felling can increase acidification and sedimentation within water courses and impact the ecology, especially in freshwater catchment areas.

Disease Management Fig. 7. Japanese larch with vivid pink coloration of the phloem at the edge of a Phytophthora ramorum lesion. (Reprinted, by permission. Crown Copyright, courtesy Forestry Commission. Licensed under the Open Government Licence)

P. ramorum consists of four largely clonal evolutionary lineages. When the pathogen was initially introduced into the United Kingdom and wider Europe, only the EU1 lineage was known, but in 2011 a fourth evolutionary lineage, EU2, was discovered in southwest Scotland and Northern Ireland. EU2 is genetically and behaviorally distinct from the more widespread

Fig. 8. Gray black, discolored larch needles infected by Phytophthora ramorum. (Reprinted, by permission. Crown Copyright, courtesy Forestry Commission. Licensed under the Open Government Licence)

Fig. 9. Phytophthora ramorum sporangia produced along the midvein of a larch needle. (Reprinted, by permission. Crown Copyright, courtesy Forestry Commission. Licensed under the Open Government Licence)

EU1. Both cause tree death, but EU2 is significantly more pathogenic to larch than EU1, suggesting it has the potential to cause even greater damage if it spreads beyond its current distribution. The presence of two lineages also suggests at least two separate introductions of P. ramorum into the United Kingdom, with the arrival of EU2 probably the more recent event. While P. ramorum remains a quarantine organism in Europe, disease surveillance and removal of infected sporulating hosts is required and enforced through Statutory Plant Health Notices. Host removal is an effective strategy for disease control but results in significant biosecurity and economic impacts for the forest industry and nurseries. The pathogen can also be spread in contaminated soil or leaf litter sticking to shoes of walkers or on tools and vehicles used on affected sites. Even after complete removal of affected larch stands, infected needles and soil remain persistent sources of P. ramorum inoculum and dictate future replanting decisions. Selected References

necrosis affecting the entire thickness of the phloem. Studies of infected A. chilensis have shown that necrosis also occurs in the sapwood, with invasion of the xylem occurring through parenchyma rays and spreading along the tracheids through the bordered pits. Aerial branch infections with no connection to the base of the tree are fairly frequently observed in the low-lying crown of J. communis in Great Britain. In both hosts, active lesions are bright chestnut brown, sharply demarcated from the pinkish white healthy tissue around them, and remain visible until the stem starts to dry out. The texture is as moist and flexible as the surrounding healthy phloem, differing only in color. Inactive lesions are dark brown, dry and hard, and almost indistinguishable from the outer bark. External symptoms include foliage desiccation and loss. When death is rapid, the foliage becomes pale before turning dark red to red brown. Resin exudation on the outer bark does not typically occur on infected J. communis but is often associated with lesions on A. chilensis. On this host, resin usually flows from a resin pocket in the phloem near the active margin of a necrotic lesion (Fig. 11).

Brasier, C. M., and Webber, J. F. 2010. Sudden larch death. Nature 466:824-825. Franceschini, S., Webber, J. F., Sancisi-Frey, S., and Brasier, C. M. 2014. Gene × environment tests discriminate the new EU2 evolutionary lineage of Phytophthora ramorum and indicate that it is adaptively different. For. Pathol. 44:219-232. Harris, A. R., and Webber, J. F. 2016. Sporulation potential, symptom expression and detection of Phytophthora ramorum on larch needles and other foliar hosts. Plant Pathol. 65:1441-1451. King, K. M., Harris, A. R., and Webber, J. F. 2015. In planta detection used to define the distribution of the European lineages of Phytophthora ramorum on larch (Larix) in the UK. Plant Pathol. 64:1168-1175. Rizzo, D. M., and Garbelotto, M. 2003. Sudden oak death: Endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1:197-204. Van Poucke, K., Franceschini, S., Webber, J. F., Vercauteren, A., Turner, J. A., McCracken, A., Heungens, K., and Brasier, C. M. 2012. Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biol. 116:1178-1191.

(Prepared by J. F. Webber and C. M. Brasier)

Mal del Ciprés Other name: Mountain cypress disease Causal agent: Phytophthora austrocedri Gresl. & E. M. Hansen (syn. P. austrocedrae Gresl. & E. M. Hansen) Hosts: Austrocedrus chilensis, Juniperus communis Distribution: Southwestern South America, southern Chile and Argentina (Patagonia) in native A. chilensis forests; northern Great Britain in native J. communis woodlands

Fig. 10. Necrotic lesion caused by Phytophthora austrocedri on Austrocedrus chilensis extending from a root up the bole. (Cour tesy M. P. Floria– © APS)

Austrocedrus chilensis, native and endemic to southern South America, and Juniperus communis, which has a broad circumpolar boreo-temperate distribution in the northern hemisphere, are very susceptible to Phytophthora austrocedri. The pathogen has also been reported affecting planted individuals of Chamaecyparis spp. in Scotland, and laboratory studies have demonstrated the susceptibility of two other South American native members of Cupressaceae (Fitzroya cupressoides and Pilgerodendron uviferum). The origin of P. austrocedri has not been determined, but current evidence suggests that it was introduced into the ecosystems where it has been reported.

Symptoms and Diagnosis A. chilensis and J. communis trees of all ages are affected and can die rapidly or slowly. The main symptoms of P. austrocedri in naturally infected trees are necrotic basal lesions that extend from killed roots up to 1 m up the stem (Fig. 10) with

Fig. 11. Resin flow at the base of an Austrocedrus chilensis tree from traumatic resin channels formed in response to Phytophthora austrocedri infection. (Cour tesy E. Hansen–© APS)

Field diagnosis in both A. chilensis and J. communis is based on the distinctive demarcation between infected and healthy tissues in diseased trees. The pathogen can be isolated from fresh necrotic lesions, and a quantitative real-time PCR assay specific to P. austrocedri has been developed to confirm the presence of the pathogen in a range of environmental samples, including bark, foliage, soil, and water. Commercial ELISA kits can also be used to detect Phytophthora spp. in dead tissue.

Disease Cycle P. austrocedri thrives under cool conditions; is active through the mild, wet winters of Patagonia; and is inactive, or even dies, during the warm, dry, summer months. In the cool, mainly maritime climate of northern Great Britain, the pathogen appears to be active all year round. It readily produces sporangia when soil is saturated. Inoculum is most likely transported in soil, debris, and water along roads on vehicles, through the forest by livestock movement and recreational traffic, and by rivers and streams. Oospores are produced in infected tissues and can be transported, even during dry periods, causing new infections if dropped near healthy host trees, because resting spores may germinate to produce sporangia that release zoospores during periods of soil saturation.

Effects on the Forest In Argentina, A. chilensis forms mainly pure stands (60%) but also forms mixed stands with Nothofagus spp. (about 39%) and Araucaria araucana (less than 1%). Since most affected forests are pure, the impact of the disease is devastating because it affects the entire ecosystem, altering forest structure and functionality, microclimate, and ecosystem processes. Generally, mortality of A. chilensis progresses gradually, generating a heterogeneous “patchwork” where dead, symptomatic, and asymptomatic trees coexist. In areas with conditions favorable for the pathogen, mortality initially shows a dispersed pattern (Fig. 12), gradually becoming clustered when the incidence is high, eventually leading to the death of most trees. By contrast, in areas with conditions unfavorable for the pathogen, the disease initially occurs in clusters, usually associated with specific microsite conditions, for example, waterways, roads, and paths. In Great Britain, J. communis is one of only three native conifer species and accordingly holds great ecological value, existing in fragmented, pure, upland stands in which the majority of trees are mature. P. austrocedri is regarded as the greatest single threat to the future of J. communis in Great Britain because it is now widely distributed on this host across the north of the country, particularly in the Scottish Highlands and the Lake District of northern England where J. communis is most populous (Fig. 13). Observations suggest that the disease tends to start along watercourses and in poorly drained areas before spreading outward across each site. Some A. chilensis trees can survive P. austrocedri attack and are able to begin to wall off old, inactive lesions with callus tissues. In Great Britain, healthy individuals of J. communis have been observed in pockets of high mortality, but it is not known whether these trees have natural resistance to the pathogen.

Disease Management

Fig. 12. Phytophthora austrocedri killing Austrocedrus chilensis in Patagonia, Argentina. The disease started at the base of the hill, near the banks of the Corcovado River, and is progressing uphill. (Cour tesy A. Greslebin–© APS)

Management actions are aimed mainly at preventing further spread of the pathogen. For example, in Argentina the valuable millennial F. cupressoides forests are protected. Principal actions include restrictions on the use of trails and movement of livestock and the imposition of biosecurity protocols such as disinfecting footwear and equipment. Research on genetic resistance in both A. chilensis and J. communis has recently started, with the aim of finding genetically resistant individuals for propagation in restoration programs.

Fig. 13. Native juniper, Juniperus communis, killed by Phytophthora austrocedri in Great Britain. (Reprinted, by permission. Crown Copyright, courtesy Forestry Commission. Licensed under the Open Government Licence)

Selected References Green, S., Elliot, M., Armstrong, A., and Hendry, S. J. 2014. Phytophthora austrocedrae emerges as a serious threat to juniper (Juniperus communis) in Britain. Plant Pathol. 64:456- 466. Green, S., Hendry, S. J., MacAskill, G. A., Laue, B. E., and Steele, H. 2012. Dieback and mortality of Juniperus communis in Britain associated with Phytophthora austrocedrae. New Dis. Rep. 26:2. Greslebin, A. G., and Hansen, E. M. 2010. Pathogenicity of Phytophthora austrocedrae on Austrocedrus chilensis and its relation with mal del ciprés in Patagonia. Plant Pathol. 59:604- 612. Greslebin, A. G., Hansen, E. M., and Sutton, W. 2007. Phytophthora austrocedrae sp. nov., a new species related to Austrocedrus chilensis mortality in Patagonia (Argentina). Mycol. Res. 111:308-316. La Manna, L., and Matteucci, S. D. 2012. Spatial and temporal patterns at small scale in Austrocedrus chilensis diseased forests and their effect on disease progression. Eur. J. For. Res. 131:1487-1499. La Manna, L., and Rajchenberg, M. 2004. The decline of Austrocedrus chilensis forests in Patagonia, Argentina: Soil features as predisposing factors. For. Ecol. Manage. 190:345-357. La Manna, L., Matteucci, S. D., and Kitzberger, T. 2008. Abiotic factors related to the incidence of Austrocedrus chilensis disease at a landscape scale. For. Ecol. Manage. 256:1087-1095. Mulholland, V., Schlenzig, A., MacAskill, G. A., and Green, S. 2013. Development of a quantitative real-time PCR assay for the detection of Phytophthora austrocedrae, an emerging pathogen in Britain. For. Pathol. 43:513-517. Vélez, M. L., Cotzee, M. P. A., Wingfield, M. J., Rajchenberg, M., and Greslebin, A. G. 2014. Evidence of low levels of genetic diversity in Phytophthora austrocedrae population in Patagonia, Argentina. Plant Pathol. 63:212-220. Vélez, M. L., Silva, P. V., Troncoso, O. A., and Greslebin, A. G. 2012. Alteration of physiological parameters of Austrocedrus chilensis by the pathogen Phytophthora austrocedrae. Plant Pathol. 61:877-888.

(Prepared by A. Greslebin, S. Green, and M. L. Vélez)

Daño Foliar del Pino Causal agent: Phytophthora pinifolia Alv. Durán, Gryzenh. & M. J. Wingf. Host: Pinus radiata Distribution: Chile, from the Maule region to the Los Ríos region Sporangia of Phytophthora pinifolia are formed abundantly in soil water but are generally absent in culture. They are borne on predominantly unbranched sporangiophores and are nonpapillate and subglobose to ovoid. They release zoospores and occasionally germinate directly with apical elongations. Free

sporangia with pedicels are occasionally observed in medium immersed in soil water and are usually released after the liquid medium is stirred. Colonies on carrot agar and V8 juice agar are white with fluffy aerial mycelia and rosaceous borders. Optimal temperature for growth is about 25°C. Colonies rarely completely cover the plates, reaching a maximum diameter of 50 mm on carrot agar in 4 weeks. Hyphae are coralloid with unusual single spherical swellings, sometimes with radiating hyphae. In detached leaves, sporulation of the pathogen occurs from the stomata (Fig. 14). Oospores of the pathogen have not been observed in different culture media, on needles under field conditions, or after mating with other species and isolates.

Symptom and Infection Development The most characteristic symptom of daño foliar del pino is resinous bands, which can appear black, on infected pine needles (Fig. 15A). Symptoms progress to include a general discoloration of the needles and a grayish appearance of the tree crowns (Fig. 15B), which turn brown at the end of spring as the affected foliage dies. Rapid death of infected needles is characteristic of daño foliar del pino, followed by defoliation of the trees affected. Symptoms are commonly observed from autumn to late spring, coinciding with the main rainy season. Dead needles remain attached to the branches until November or December, and they fall from the branches during strong winds, which occur repeatedly in the affected area. Superficial bark cankers can develop from infected needles, especially epicormic fascicles (Fig. 15C). The pathogen can survive at low levels during the summer in the litter on the ground because it is difficult to detect.

Disease Management Current management of daño foliar del pino in areas with high risk of infection includes three main strategies: selection of sites where conditions are less conducive for disease development, selection of tolerant genetic material, and application of chemicals, such as phosphates and fungicides. Sites with low risk have been identified. Between 2004 and 2015, areas with different levels of daño foliar del pino incidence were surveyed annually by air and on the ground. Areas totaling about 150,000 ha have been determined to have severe disease incidence. A climatic model estimates the length of time with relative humidity greater than 90%, conditions favorable for P. pinifolia infection, across the landscape. The model identifies specific areas of Arauco province that are more favorable for infection by P. pinifolia. Aerial surveys confirm the correlation between the number of days favorable for infection and the planting sites with different levels of historical damage. Tolerant plants have been selected by the evaluation of young clones growing under the foliage of adult P. radiata with severe

Fig. 14. Phytophthora pinifolia sporangia forming from stomata on Pinus radiata needles. (Cour tesy E. Sanfuentes– © APS)

infections. The selection of tolerant genetic material is a longterm strategy; however, it is already providing useful results. Fungicides such as mefenoxam (phenylamides), metalaxyl, and salts of phosphorous acid (phosphite) have been selected as the most effective in reducing infection by P. pinifolia. Currently, the strategy includes one application of mefenoxam in the nurseries just before planting and three manual applications of phosphite for 3 consecutive months during the first 3 years after planting. The use of these fungicides in young plantations consistently reduced the mortality caused by daño foliar del pino. An advantage with phosphites is their translocation between phloem and xylem. In addition, phosphites in Chile are still registered as fertilizers and have a low environmental impact and few restrictions. Adult plantations are treated with mefenoxam or metalaxyl when they have a high level of infection and are near roads.

Selected References Ahumada, R., Rotella, A., Poisson, M., Durán, A., and Wingfield, M. J. 2013. Phytophthora pinifolia: The cause of daño foliar del pino on Pinus radiata in Chile. Pages 159-165 in: Phytophthora: A Global Perspective. Plant Protection Series No. 2. K. Lamour, ed. CAB International, Wallingford, U.K. Ahumada, R., Rotella, A., Slippers, B., and Wingfield, M. J. 2012. Potential of Phytophthora pinifolia to spread via sawn green lumber: A preliminary investigation. South. For. 74:1- 6. Durán, A., Gryzenhout, M., Slippers, B., Ahumada, R., Rotella, A., Flores, F., Wingfield, B. D., and Wingfield, M. J. 2008. Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathol. 57:715-727. Guest, D., and Grant, B. 1991. The complex action of phosphonates as antifungal agents. Biol. Rev. 66:159-187. Sanfuentes, E., Casanova, A., and González, G. 2012. Epidemiología del daño foliar del pino (DFP) y ciclo biológico de Phytophthora pinifolia: Bases para una estrategia de control integrado. Universidad de Concepción, Concepción, Bío Bío Region, Chile. http:// www.cfrd.cl/~pgodoy/proyecto_patfor_f_A.pdf

(Prepared by E. Sanfuentes)

Red Needle Cast Other name: Phytophthora needle cast Causal agent: Phytophthora pluvialis Reeser, W. Sutton, & E. Hansen Hosts: Pinus radiata, Pseudotsuga menziesii, Pinus patula Distribution: New Zealand; Oregon, U.S.A. Red needle cast emerged as a new disease on Pinus radiata plantations in New Zealand in 2008, where it was associated with abnormal winter needle cast. Red needle cast is caused by Phytophthora pluvialis, which has been shown to infect only the needles of the tree. Discrete, olive-colored lesions, each often with a narrow, dark, resinous mark or band, develop after infection and result in rapid needle senescence and premature defoliation. The disease has been termed “red needle cast” in New Zealand because affected trees have a reddish appearance prior to needle cast. P. pluvialis was first isolated from baited streams, soil, and canopy drip samples in mixed tanoak (Notholithocarpus densiflorus) and Douglas-fir (Pseudotsuga menziesii) forests in the U.S. state of Oregon. In Oregon, P. pluvialis has been isolated rarely from tanoak and more recently from Douglas-fir. In New Zealand, the pathogen has since also been recovered from Douglas-fir and Pinus patula foliage. Preliminary analysis of the genetic diversity of P. pluvialis indicates high diversity in the Oregon population in contrast to the New Zealand population. This, along with the recovery of several other Phytophthora spp. closely related to P. pluvialis in Oregon, suggests a potential origin of the species in the Pacific Northwest.

Symptoms and Diagnosis

Fig. 15. Symptoms caused by Phytopthora pinifolia in Pinus radiata. A, resinous bands in needles; B, foliage discoloration; and C, superficial canker in the stem. (A and B, courtesy J. Stone– © APS; C, courtesy E. Hansen–© APS)

The symptoms of red needle cast closely resemble those of daño foliar del pino, which is caused by Phytophthora pinifolia. However, P. pinifolia and P. pluvialis are not closely related, residing in Phytophthora clades 6 and 3, respectively. Red needle cast in radiata pine is most commonly observed in trees that are 10 years old or older when canopy closure limits air movement and maintains conditions suitable for disease development (Fig. 16). Juvenile trees are capable of developing symptoms, but this occurs most commonly in areas of high inoculum pressure close to older infected stands. Early symptoms (distinct resinous bands that extend to pale olive khaki lesions) are most commonly observed in the basal portion of the needle near the fascicle sheath. However, lesions may be observed anywhere on the needle shaft, especially under high inoculum

pressure. Following lesion extension, the resinous mark may or may not be identifiable. Needles senesce quickly following infection and are readily cast, often before the needle blade is completely necrotic. Repeated cycles of infection and casting occur throughout the wet season, giving the canopy a reddish appearance from autumn until spring with a successively thinner crown. Infection of Douglas-fir by P. pluvialis results in chlorotic needle mottling, low needle retention, and canker development on seedlings. In New Zealand’s plantations, Douglas-fir defoliation has been most evident in trees adjacent to radiata pine plantations with established red needle cast. In Douglas-fir in Oregon, disease appears to be most severe in trees on stand edges and at the bases of slopes (Fig. 17). Disease appears to spread upward into the crown. Severely impacted branches are bare of needles until spring budburst. The new growth is often reduced. While laboratory inoculations indicate young needles are susceptible, needles in the new flush are retained on the trees in the field, because the environmental conditions during the late spring and summer months are generally not suitable for disease development. By the end of summer, trees often appear to have returned to health. However, close inspection shows the loss of previous years’ foliage, which is normally retained by P. radiata for 2–4 years. Symptoms of red needle cast on both P. radiata and Douglasfir can be observed in the field. Diagnostics, confirming infection by P. pluvialis, can be done by either isolating the pathogen from diseased needles, with highest recoveries achieved with carrot- and pea-based selective agar, or with species-specific qPCR primers. The P. pluvialis species-specific primers can amplify DNA from symptomatic needles or from commercially available Phytophthora ELISA kits that have tested positive with needle lesions.

of June–August, and the needles are cast within 4 weeks of infection. Severe disease can almost completely defoliate affected trees, but recovery is common, with the new-year’s flush of foliage largely unaffected. Work in New Zealand shows that in the presence of water, infection is established within 18 h. From 5 days postinoculation, mycelial mats and hyphal swellings can be observed on the needle surfaces, acting as wicks to retain moisture. After 6–7 days, masses of sporangia are produced from the stomata and exude across the needle surface (Fig. 18). The sporangia are moderately caducous in culture and may be more so upon infection, though the role of sporangia in the spread of disease is not clear at this time. Masses of evacuated sporangia have been observed on needles collected from the field, indicating direct release and spread of zoospores by rain splash and water runoff. However, sporangia may have a role in the spread of the pathogen under drier conditions. Limited infection occurs in the absence of persistent moisture. The role of inoculum on the forest floor is not clear, and there is no evidence of root or collar infection associated with red

Disease Cycle P. pluvialis is an aerial pathogen known to infect P. radiata and Douglas-fir. The disease cycle is closely associated with rainfall, and in New Zealand the inoculum can be detected from canopy drip traps from March (autumn) to December (early summer) following periods of persistent rain. In Oregon, the pathogen is recovered in late winter and early spring. The timing of symptom development is strongly dependent on local climatic conditions, and low levels of infection can continue into early summer in some areas. Fog has also been associated with red needle cast in New Zealand, where clear fog lines delineate the extent of disease on elevated coastal fog-prone sites. Disease expression generally peaks in the winter months

Fig. 17. Red needle cast, caused by Phytophthora pluvialis, on Douglas-fir in the U.S. state of Oregon’s Coast Range. (Cour tesy E. Hansen–© APS)

needle cast in the field. Stem and trunk cankers have not been observed on P. radiata in association with red needle cast. While reduced growth has been noted in severely impacted sites in New Zealand, infection in P. radiata has not been observed to extend from the needle into the growing shoot and tree mortality has not been observed. While oospores of P. pluvialis are produced quickly in culture, they have not been commonly found in infected tissues. Thus, the potential role of oospores in the survival of the pathogen is yet to be clarified. Hyphal swellings are produced readily in liquid culture and are observed on the needle surfaces under wet conditions in association with sporangia or in advance of sporangia development.

Effects on the Forest In New Zealand, P. pluvialis has been detected in stands throughout the North Island and down to Westland in the South Island, with timing, expression, and impact varying considerably among regions and across years. In heavily impacted regions, significant defoliation events from red needle cast have been cyclical. While not yet studied in depth, this polycyclic disease development is believed to be associated with both favorable weather and a buildup in canopy density, providing sufficient susceptible host tissue. The variation in disease expression has made quantification of growth reduction associated with red needle cast difficult. Quantification of growth reduction in one area of high disease pressure showed there was an annual incremental growth decrease of approximately 35% in the year following severe disease. However, over the 3-year period of the study, the average growth reduction was 16% per annum, with no notable loss of growth in the third year. In some areas or years, the incidence of red needle cast is very low and unlikely to result in significant reductions in tree growth.

Disease Management As with many Phytophthora diseases, phosphite (phosphorous acid) has been shown to be effective in the control of infection of P. radiata by P. pluvialis as have copper-based fungicides, such as copper oxychloride, and phenylamide metalaxyl-M. Breeding for resistance is a long-term option for management of red needle cast in P. radiata plantations. Field and laboratory screening has shown that resistance to needle loss caused by red needle cast is heritable, and screening is underway to identify resistance within P. radiata breeding lines currently in use in New Zealand. Breeding for resistance to P. pluvialis is considered the most promising long-term response to mitigate the effects of red needle cast in production forestry.

Hansen, E. M., Reeser, P., Sutton, W., Gardner, J., and Williams, N. 2015. First report of Phytophthora pluvialis causing needle loss and shoot dieback on Douglas-fir in Oregon and New Zealand. Plant Dis. 99:727. Hood, I. A., Williams, N. M., Dick, M. A., Arhipova, N., Kimberley, M. O., Scott, P. M., and Gardner, J. F. 2014. Decline in vitality of propagules of Phytophthora pluvialis and Phytophthora kernoviae and their inability to contaminate or colonise bark and sapwood in Pinus radiata export log simulation studies. N.Z. J. For. Sci. 44:7. https://nzjforestryscience.springeropen.com/articles/10.1186/ s40490- 014- 0007- 6 Reeser, P. W., Sutton, W., and Hansen, E. M. 2013. Phytophthora pluvialis, a new species found in mixed tanoak-Douglas-fir forests of western Oregon, U.S.A. North Am. Fungi 8(7):1-8. Rolando, C., Gaskin, R., Horgan, D., Williams, N., and Bader, M. K.-F. 2014. The use of adjuvants to improve uptake of phosphorous acid applied to Pinus radiata needles for control of foliar Phytophthora diseases. N.Z. J. For. Sci 44:8. https://nzjforestryscience.springeropen.com/articles/10.1186/s40490- 014- 0008-5 Schoedel, B., and Avila, F. J. 2008. Specific immunodetection of Phytophthora ramorum and P. kernoviae. (Abstr.) Phytopathology 98:S141.

(Prepared by N. Williams and E. Hansen)

Kauri Root and Collar Rot Other name: Kauri dieback Causal agent: Phytophthora agathidicida B. S. Weir, Beever, Pennycook, & Bellgard Host: Agathis australis Distribution: North Island of New Zealand New Zealand kauri, Agathis australis, is an iconic, ancient southern conifer belonging to the family Araucariaceae (Fig. 19). To Māori, the indigenous people of New Zealand, kauri holds a very significant place in their creation mythology, and iconic trees have their own names, for example, Tane Mahuta, “the God of the Forest.” With approximately 1% left in oldgrowth, kauri has a listing of “conservation dependent” with the International Union for Conservation of Nature. Kauri is now threatened by the introduced soilborne pathogen Phytophthora agathidicida, a newly described species in clade 5. Other hosts are not known, and the origin of the pathogen has not been determined. Kauri dieback was first reported in 1972 on Aotea (Great Barrier Island), associated with regenerating “ricker” kauri. It was not recognized on the mainland

Selected References Ahumada, R., Rotella, A., Slippers, B., and Wingfield, M. J. 2013. Pathogenicity and sporulation of Phytophthora pinifolia on Pinus radiata in Chile. Australas. Plant Pathol. 42:413- 420. Dick, M., Williams, N., Bader, M., Gardner, J., and Bulman, L. 2014. Pathogenicity of Phytophthora pluvialis to Pinus radiata and its relation with red needle cast disease in New Zealand. N.Z. J. For. Sci. 44:6. https://nzjforestryscience.springeropen.com/articles/10.1186/ s40490- 014- 0006-7 Dungey, H. S., Williams, N. M., Low, C. B., and Stovold, G. T. 2014. First evidence of genetic-based tolerance to red needle cast caused by Phytophthora pluvialis in radiata pine. N.Z. J. For. Sci. 44:31. https://link.springer.com/article/10.1186/s40490- 014- 0028-1 Durán, A., Gryzenhout, M., Slippers, B., Ahumada, R., Rotella, A., Flores, F., Wingfield, B. D., and Wingfield, M. J. 2008. Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathol. 57:715-727. Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society, St. Paul, MN.

until 2006. Since 2009, via delimitation surveys instigated by a multiagency government response, it has been shown that the disease is distributed throughout the natural range of kauri except Little Barrier Island and the Hunua Ranges in the Auckland Region. Kauri represents a climax, keystone taxon, and the ecological consequences of the loss of kauri impact a range of specialist epiphytes and vertebrates.

Symptoms and Diagnosis The symptoms of kauri dieback include crown decline and resin production at the collar (Fig. 20). However, these symptoms represent the chronic phase of the disease, with initial fine-root infections occurring many years before the onset of aboveground symptoms. The disease trajectory is purportedly dependent upon environmental factors, tree age, and inoculum density. Trees of all ages are killed. P. agathidicida parasitizes the secondary (cork) cambium, growing from the root crown on up the stem and forming lesions that are evident through the exudation of resin (Fig. 20). A demarcation between brownish, infected phloem below and white healthy tissue above is visible when the outer bark is removed. Field diagnosis in kauri is based on crown decline symptoms, gummosis at the collar, the presence of necrotic fine roots, and potentially a strong demarcation between necrotic and healthy tissues, advancing from the large leader roots to the root crown in a dying tree. The pathogen can be isolated from recently killed tissues by removing the outer bark and plating the cork cambium to Phytophthora-selective media. Commercial ELISA kits have not proved to be reliable, possibly because the resin-laden plant material confounds the polarity of the membrane. Soil bioassays in which a drying and wetting phase is employed followed by baiting with cedar needles and germinated lupine radicles are routinely used. A real-time PCR-based assay has been developed for soil and plant material, and a species-specific fluorescent in situ hybridization assay is available to assist in visualizing the infection process in planta.

Disease Cycle P. agathidicida can infect plants across a broad temperature range and can be recovered from soil (via soil bioassay) throughout the year. It is carried in mud and plant debris and washes downslope in water. In recreational parks, transport has been primarily along trails, while downslope movement occurs in streams and potentially through overland flow during periods of heavy winter rains.

Oospores (P. agathidicida is homothallic) formed after 3 months in deliberately inoculated kauri seedlings, and P. agathidicida can be recovered from soil after at least 9 years. It is hypothesized that resting spores are transported in mud on footwear during wet weather. Wild boars (Sus scrofa) are fond of foraging under kauri trees for giant kauri snails and earthworms and are considered potential vectors. This has resulted in the culling of boars and other vertebrates.

Effects on the Forest The consequences of kauri dieback are visually dramatic. However, significant plot-level studies commenced only in 2011, so the ecological consequences are not yet well studied. Standing dead trees are quickly attacked by pinhole borers, leaving bleached stagheads. Because kauri is no longer logged, trees have protected status. The advisability of using recently killed trees for cultural purposes remains unresolved, because the timber of the lower bole may be a pathway for inoculum dissemination. Distinctive plant associations with up to 36 species, including many rare endemic epiphytic species, exist in or on kauri (Fig. 21). The pathogen removes one of the canopy dominants to be potentially replaced by other canopy members of the closely related Podocarpaceae family, e.g., tanekaha (Phyllocladus trichomanoides), rimu (Dacrydium cupressinum), and kahikatea (Dacrycarpus dacrydioides).

Disease Management The New Zealand central government has initiated and coordinates a joint agency response to kauri dieback. “Keep Kauri Standing” is the program developed to stop the further spread of the disease by containing the pathogen in infested areas and, if necessary, restricting access to certain diseased forest areas. All forest management and concessionaire activities in kauri forests are evaluated for their potential effects on the kauri resource, and activities are modified or appropriate mitigating measures are undertaken as necessary. Principal actions include trail-use restrictions, such as wet season or permanent closure and/or renovation of elevated boardwalks (Fig. 19), and sanitation measures such as washing of boots (Fig. 22).