Oak declines and diebacks in Europe and North America

Episodically recurring declines of oak (Quercus spp.) stands have been reported since the early 1900s in both temperate and Mediterranean regions of Europe and in the USA (Staley 1965, Delatour 1983, Ragazzi et al. 1989, Schütt 1993, Gottschalk & Wargo 1996, Abrams 2003). In Europe, the current phase of oak decline started in the 1980s and is still ongoing (Delatour 1983, Brasier et al. 1993, Jung et al. 1996, 2000, 2013b, Vettraino et al. 2002, Balci & Halmschlager 2003a, b). A wide range of abiotic and biotic factors, including frost, drought, air pollutants, decreased groundwater levels, silvicultural mismanagement, insect defoliators, bark borers, fungal species like Ophiostoma and Ceratocystis spp., bacteria, mycoplasma-like organisms and viruses, were discussed as predisposing and inciting factors of this phenomenon (Manion 1981, Delatour 1983, Nihlgård 1985, Nienhaus 1987, Oleksyn & Przybyl 1987, Oosterbaan & Nabuurs 1991, Siwecki & Liese 1991, Ahrens & Seemüller 1994, Schlag 1995, Ragazzi et al. 1995, Thomas et al. 2002). However, none of these potential agents accounted for more than local or regional decline episodes. Due to similarities in aetiology between Mediterranean oak decline and eucalypt dieback in Western Australia (WA) caused by P. cinnamomi (Shearer & Tippett 1989, this review), and earlier records of P. cinnamomi from declining chestnuts and oaks in Portugal (Lopes-Pimentel 1946, 1947, this review), the possible involvement of P. cinnamomi in Iberian oak decline was suggested in 1991 and soon after confirmed (Brasier et al. 1993). Another study demonstrated the association of several known and previously unknown Phytophthora species with declining oak forests in central Europe and temperate and Mediterranean regions of Italy and Slovenia (Jung et al. 1996). Numerous surveys in oak stands throughout Europe uncovered a diverse assemblage of Phytophthora taxa including eight known species, P. cactorum, P. ×cambivora, P. cinnamomi, P. cryptogea, P. drechsleri, P. gonapodyides, P. megasperma, P. syringae; and 14 previously unknown Phytophthora taxa, P. bilorbang, P. chlamydospora, P. europaea, P. gallica, P. multivora, P. plurivora, P. pseudosyringae, P. psychrophila, P. quercina, P. ramorum, P. tyrrhenica, P. uliginosa, P. taxon forest soil and P. taxon river soil (Brasier et al. 1993, Brasier 1996, Jung et al. 1996, 1999, 2000, 2002, 2003b, 2013b, 2017b, Robin et al. 1998, Gallego et al. 1999, Hansen & Delatour 1999, Sanchez et al. 2002, Vettraino et al. 2002, Balci & Halmschlager 2003a, b, Jönsson et al. 2003b, 2005, Moreira & Martins 2005, Brown & Brasier 2007, Jung & Nechwatal 2008, Corcobado et al. 2010, Camilo-Alves et al. 2013, Scanu et al. 2013, T. Jung, M. Horta Jung & S.O. Cacciola unpubl. data). Several of these Phytophthora species, including P. ×cambivora, P. cinnamomi, P. cryptogea, P. drechsleri, P. multivora, P. plurivora and P. ramorum, are introduced invasive pathogens in Europe whereas most other species are considered to be native or of cryptic origin (Jung et al. 2016, 2017b). Recently, the presence of P. cinnamomi and other Phytophthora species has also been demonstrated in declining oak stands in Western Algeria (H. Smahi & B. Scanu unpubl. data). Against the background of almost ubiquitous infestations of oak stands in European nurseries with P. cinnamomi, P. quercina, P. plurivora and 13 other Phytophthora spp. (Jung et al. 2016), the massive afforestation during the previous three decades, stimulated by both national and EU subsidy programmes, may have contributed to the widespread Phytophthora infestations of oak woodlands across Europe.

In Mediterranean regions, the most affected species are Quercus suber and Q. ilex and, to a lesser extent, Q. cerris, Q. faginea, Q. pubescens and Q. pyrenaica (Brasier et al. 1993, Gallego et al. 1999, Sanchez et al. 2002, Vettraino et al. 2002, Pérez-Sierra et al. 2013, T. Jung & M. Horta Jung unpubl. data). In temperate regions, stands of Q. petraea and Q. robur usually show similar disease incidences. Generally, in oak decline a rapid death of previously healthy-looking trees and a slow chronic decline and dieback are distinguished although there are gradual transitions between both scenarios (Delatour 1983, Brasier et al. 1993, Jung et al. 1996, 2000, Gallego et al. 1999, Vettraino et al. 2002, Camilo-Alves et al. 2013). Rapid or acute death of oaks occurs mainly in Mediterranean regions and is usually caused by an interaction between excessive root losses and collar rot cankers by P. cinnamomi and severe summer droughts (Brasier et al. 1993, Gallego et al. 1999, Sanchez et al. 2002, Scanu et al. 2013, Jung et al. 2013b). Affected trees and whole stands of Q. suber and Q. ilex rapidly develop crown dieback and often collapse within the same year (Fig. 3a–c). Bark lesions at main roots and the collar may occur in severely infected oak trees, with black exudates oozing from the outer bark and necrotic lesions and staining of the underlying phloem and xylem tissues (Fig. 3e, f), often girdling the stem. Chronic decline and dieback are characterized by a progressive crown thinning, branch dieback, leaf chlorosis and abundant pro- liferation of epicormic shoots (Fig. 3d). These crown symptoms are caused by extensive losses of both fine roots and lateral small woody roots and callusing cankers on suberized roots (Fig. 3g–i). The ability of the root system to absorb and transport water and nutrients is increasingly hampered, eventually leading to a slow death of the trees (Jung et al. 1996, 2000, 2013b, Jönsson et al. 2005). However, the interaction with several abiotic stress factors, including prolonged droughts, waterlogging, fluctuating water tables, sandy or shallow soils and unseasonal heavy rain, and opportunistic pathogens and pests, can accelerate the disease progress and cause rapid wilting and mortality of trees (Brasier et al. 1993, Jung et al. 1996, 2000, 2003a, Vettraino et al. 2002, Balci & Halmschlager 2003a, b, Jönsson et al. 2003a, 2005, Jönsson 2006, Moreira & Martins 2005).

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Fig. 3

Oak decline symptoms caused by Phytophthora spp. a. Extensive dieback and mortality of Quercus suber trees caused by P. cinnamomi in Portugal; b. progressive dieback and wilting of a mature Q. suber caused by P. cinnamomi and P. quercina in Sardinia (Italy); c. sudden death of a Q. ilex due to P. cinnamomi in a savannah-like ecosystem in Spain; d. Q. robur trees in Germany showing chlorosis, thinning and dieback of crowns, abundant proliferation of epicormic shoots, and mortality due to severe fine root destructions caused by P. plurivora and P. quercina; e. bleeding collar lesion with flame-shaped staining of the underlying xylem caused by P. cinnamomi on a mature Q. suber in Sardinia; f. root and collar rot caused by P. cinnamomi on a young Q. suber in a forest plantation in Sardinia; g, h. small woody roots of a mature Q. suber in Italy showing severe losses of fine roots and lateral roots and black necrotic lesions due to P. cinnamomi infections; i. small woody root of a mature Q. robur in Germany with severe losses of lateral roots and a callusing bark canker caused by P. plurivora and P. quercina. — Photos: a–d, i: T. Jung; e–h: B. Scanu.

The distribution of Phytophthora species and their impact on oak trees depends on the site conditions, in particular soil drainage and pH. In a study of fine root systems in 35 forest stands in Germany, the oak-specific P. quercina and other Phytophthora spp. were frequently detected in the rhizosphere of mature Q. robur and Q. petraea on sites with a mean soil-pH higher than 3.5 and sandy-loamy to clayey soil texture (Jung et al. 2000). In infested forests, crown transparency and several fine root parameters were significantly correlated. Oak trees with P. quercina and other Phytophthora spp. in their rhizospheres had significantly higher losses of fine roots and of small woody roots, reduced crown density and a threefold higher decline risk than oaks without Phytophthora. In contrast, no Phytophthora species could be recovered from forests on well-drained sandy to sandy-loamy soils with a mean pH below 3.9, and root and crown conditions of oak trees were not correlated in these non-infested stands (Jung et al. 2000). Also in Austria, Italy, Turkey and Sweden, significant associations between presence of P. quercina and decline of oaks were demonstrated (Vettraino et al. 2002, Balci & Halmschlager 2003a, b, Jönsson et al. 2005).

In soil infestation tests, P. cinnamomi, P. quercina, P. ×cambivora, P. plurivora and P. uliginosa caused severe losses of fine roots and small woody roots, necrotic root lesions and mortality of Q. ilex, Q. petraea, Q. robur and Q. suber seedlings (Jung et al. 1996, 1999, 2002, 2003a, b, 2017c, Robin et al. 1998, Gallego et al. 1999, Sanchez et al. 2002, Jönsson et al. 2003a, Pérez-Sierra et al. 2013, Corcobado et al. 2017).

The primary role of P. cinnamomi in the decline of oak woodlands across Mediterranean countries, including Portugal, Spain and southern regions of France and Italy was demonstrated by numerous studies (Brasier et al. 1993, Brasier 1996, Robin et al. 1998, Gallego et al. 1999, Sanchez et al. 2002, Vettraino et al. 2002, Moreira & Martins 2005, Camilo-Alves et al. 2013, Jung et al. 2013b, Scanu et al. 2013). For many years, P. cinnamomi was considered the only Phytophthora species associated with Mediterranean oak decline (Camilo-Alves et al. 2013). However, the Phytophthora diversity in Mediterranean oak ecosystems is considerably higher than previously assumed. Several other Phytophthora species have recently been isolated from declining Mediterranean oaks, including P. gonapodyides from Q. ilex in Extremadura (Spain), P. psychrophila, P. quercina and P. syringae from Q. ilex and Q. faginea in two protected areas in Italy and eastern Spain, and the newly described species P. tyrrhenica from both Q. ilex and Q. suber in Sardinia and Sicily (Corcobado et al. 2010, Pérez-Sierra et al. 2013, Linaldeddu et al. 2014, Scanu et al. 2015, Jung et al. 2017b). Pathogenicity of all these Phytophthora species to the respective oak species was demonstrated, and their involvement in the declines suggested. In addition, in co-infection experiments P. cinnamomi, P. gonapodyides and P. quercina caused severe mortality of young Q. ilex seedlings which might explain the widespread lack of seedling recruitment in Mediterranean oak forests (Corcobado et al. 2017).

Several studies of Mediterranean oak decline have shown the interaction between P. cinnamomi and a combination of site factors, including the presence of shallow or compacted soils (Moreira & Martins 2005) and prolonged summer droughts (Brasier et al. 1993, Gallego et al. 1999). Mediterranean oak forests are delicate ecosystems, which are adversely impacted by human activities and global climate changes (Desprez-Loustau et al. 2010). The Mediterranean basin, which includes most of the natural range of Q. suber and Q. ilex, is considered one of the hot spots of future climate changes (Pachauri & Reisinger 2007). In this context, the predicted increase of P. cinnamomi activity with rising average temperatures (Brasier & Scott 1994, Brasier 1996, Burgess et al. 2017) could intensify root and collar rot incidences and further destabilise Mediterranean oak forests. Climate changes, in particular a rise of mean winter temperatures, a seasonal shift of precipitation from summer into wintertime, and a tendency towards heavy rain and prolonged droughts, have also been discussed as triggering factors for the current Phytophthora-related oak decline in temperate regions of Europe which, compared to previous oak decline episodes, is exceptional regarding its epidemic extent and long duration (Jung et al. 1996, 2000, 2003a, 2013b).

Also in the USA, episodes of oak decline with a symptomatology similar to European oak declines are occurring since decades (Staley 1965, Gottschalk & Wargo 1996, Abrams 2003). However, despite P. cinnamomi has been reported since the 1920s in North America, the involvement of Phytophthora species was not investigated conclusively (Balci et al. 2007). By the 1950s, P. cinnamomi was widespread in the north-eastern USA, but the significance of this species in tree health was only evaluated in connection with the demise of American chestnut (C. dentata). Today, in eastern US oak forests, P. cinnamomi is common, but due to its sensitivity to deep frost, its distribution is limited to below 40° northern latitude. In contrast, most other Phytophthora species are not restricted climatically but have a scattered distribution. The assemblage of Phytophthora species associated with oak stands includes P. cryptogea, P. europaea, P. quercetorum, P. pini, P. plurivora, P. ×cambivora and P. taxon ohioensis (Balci et al. 2007, 2008a, 2010, McConnell & Balci 2014b). Phytophthora cactorum and P. heveae occur only in southern oak forests (Meadows et al. 2011). All these species proved to be pathogenic to oaks in pathogenicity tests, but due to its widespread occurrence, P. cinnamomi has long been suspected as the main driver of oak decline in eastern US forests. Due to cold winter temperatures limiting canker development on stems, P. cinnamomi is mainly infecting the root system. Necrotic lesions on larger roots or bleeding stem cankers are only sporadically found on oaks in the southern USA, California and Mexico (Mircetich et al. 1977, Tainter et al. 2000, Wood & Tainter 2002, Balci et al. 2008b). Several recent studies investigated the role of P. cinnamomi in oak decline events in eastern US forests and provided insights into the epidemiology of the disease. Most significantly, both in the field and in pathogenicity tests P. cinnamomi-associated fine root losses were shown to be related to the propagule density of the pathogen. It was demonstrated that fine root losses are driving oak decline events in moist low-elevation stands where inoculum levels of the pathogen are higher and in areas like plant hardiness zones 6 and 7 where fine root regeneration is limited due to climatic constraints (McConnell & Balci 2014a, b).

Decline and mortality of Alnus species in Europe

In Europe, four Alnus species are indigenous. They are all characterised by having a symbiosis with the nitrogen-fixing actinomycete Frankia alni which is living in root nodules and enabling the trees to colonise extreme sites (Claessens 2003). The most widespread species is common alder (Alnus glutinosa) which, due to its ability to withstand permanently waterlogged conditions and prolonged flooding, typically colonises swamps and the banks and flood-plains along slow-flowing lowland streams. Grey alder (A. incana) is mainly distributed along fast-flowing white-water rivers and on dry rocky slopes, whereas the shrubby green alder (A. viridis) forms the subalpine tree line on heavy soils in the Alps and in the mountains of eastern Europe. The natural distribution of the Italian alder (A. cordata) is restricted to Corsica and southern Italy where it colonises moderately dry sites as a pioneer species. Alders have always been considered relatively non-problematic regarding their susceptibility to pests and pathogens. However, in 1993 a previously unknown lethal root and collar rot of A. glutinosa was recorded in southern Britain, which occurred mainly along riverbanks, but also in orchard shelterbelts and forest plantings (Brasier et al. 1995). In subsequent years, the disease was also found on A. incana and A. cordata, and in various countries including Austria, Belgium, Czech Republic, Croatia, Estonia, France, Germany, Hungary, Ireland, Italy, Lithuania, Norway, Poland, Portugal, Spain, Sweden, Switzerland and the Netherlands (Gibbs et al. 1999, 2003, Streito et al. 2002, Santini et al. 2003, Nagy et al. 2003, Jung & Blaschke 2004, Schumacher et al. 2006, Černŷ & Strnadová 2010, Solla et al. 2010, Jung et al. 2013b, 2016, Redondo et al. 2015, Trzewik et al. 2015, Kanoun-Boulé et al. 2016, M. Horta Jung & T. Jung unpubl. data). Affected trees show small-sized, sparse and often chlorotic foliage, a thinning and dieback of the crown, early and often excessive fructification, and eventually death (Fig. 4a, b). Young trees die within a few months while mature trees with large stem diameters take several years before they die (Gibbs et al. 1999, 2003, Streito et al. 2002, Jung & Blaschke 2004). Mortality rates can reach almost 100 % in permanently waterlogged swamps (Fig. 4a; Jung & Blaschke 2004), on sites with long retention of flood water such as oxbows and stretches behind bridges (Gibbs et al. 1999, Jung & Blaschke 2004) and in direct contact to slow-flowing stream water (Fig. 4b). A disease model, based on data from 35 rivers in north-eastern France, demonstrated that the disease incidence was increasing with decreasing distance of the stem base to the midwater line, with increasing river width, summer temperature of river water and clay content of the riverbank, as well as with slower water flow rates (Thoirain et al. 2007). Crown dieback and mortality are caused by root rot and collar rot lesions which can girdle the stem and extend up to 3 m from the stem base. Lesions are characterised by tarry or rusty exudate spots on the surface of the bark and flame-shaped orange-brown lesions of the inner bark (Fig. 4c–h). Along streams, waterborne inoculum, i.e. zoospores released from sporangia produced on infected alder tissues, is the main source of root and collar infections. Zoospores infect the collar region usually via the non-suberized adventitious roots and through the large lenticels (Gibbs et al. 2003, Jung & Blaschke 2004). During exceptionally high floods, infections can take place higher up the stem producing isolated aerial bark lesions (Fig. 4d). On non-flooded sites, above-ground bark lesions only develop when the pathogen progresses from infected main roots into the collar (Fig. 4f). If trees survive the first year after the infection occurred, lesions may progress in the following spring leaving the older parts sunken and surrounded by callusing tissues (Fig. 4f, i). Often the xylem underneath necrotic lesions shows a flame-shaped staining (Fig. 4j). Infected trees usually produce epicormic shoots in the vicinity of the bark lesions (Fig. 4g).

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Fig. 4

Symptoms of Phytophthora root and collar rot of Alnus spp. in Europe. a. Severe dieback and mortality of a mature A. glutinosa stand caused by P. ×alni in a seasonally flooded swamp forest in Bavaria, Germany; b. extensive dieback and mortality caused by P. ×alni in a riparian stand of A. glutinosa at Rio Alva in Portugal; c. bleeding bark lesion caused by P. ×alni on a surface root of mature riparian A. glutinosa in Portugal; d. bleeding aerial bark lesion on a riparian A. glutinosa at Rio Miño in Galicia, Spain, caused by simultaneous infections of P. ×alni and P. ×multiformis in 2 m stem height during an extreme spring flood; e, f. collar rot lesions caused by P. ×alni on A. glutinosa (e) and A. incana (f) planted on a non-flooded site in Bavaria, Germany, with rusty and tarry spots on the outer bark and flame-shaped, orange-brown necrotic lesions of the inner bark; inactive older lesion areas from the previous year are sunken and surrounded by callussing tissues (arrows); g. black exudates oozing from multiple collar rot lesions caused by P. ×multiformis during a severe flood on a riparian young A. glutinosa in Sardinia, Italy, reacting with the production of epicormic shoots; h. same tree as in (g) with multiple, fresh necrotic lesions of the inner bark caused by P. ×multiformis; i. inactive sunken collar rot lesion with surrounding callusing tissues (arrows) caused by P. siskiyouensis on a young A. cordata in the UK; j. flame-shaped staining of the xylem tissue underneath an active collar rot lesion caused by P. siskiyouensis on a young A. cordata in the UK. — Photos: a–f: T. Jung; g, h: B. Scanu; i, j: A. Pérez-Sierra.

The causal organisms of the unknown lethal rot on Alnus species were identified as a previously unknown swarm of interspecific hybrids originally described as Phytophthora alni s.lat. comprising three subspecies: P. alni ssp. alni (PAA), P. alni ssp. uniformis (PAU) and P. alni ssp. multiformis (PAM) (Brasier et al. 2004). Originally, it was hypothesised that P. ×cambivora and an unknown species close to P. fragariae were the progenitors of the hybrids (Brasier et al. 1999, 2004). However, allele-specific analyses of four single-copy nuclear genes and mtDNA of a European collection of isolates of PAA, PAM, PAU, P. ×cambivora and P. fragariae shed more light on the parental origin of the hybrids:

• 1. PAU is most likely a distinct non-hybrid species;

• 2. PAA resulted from a hybridisation between PAU and PAM; and

• 3. PAM is an ancient hybrid.

Thus, multiple hybridization events must have occurred (Ioos et al. 2006). These results were further confirmed using allele-specific real-time PCR for the quantification of allele copy numbers of three single-copy nuclear genes to assess ploidy levels, and flow cytometry for the determination of genome sizes (Husson et al. 2015). Consequently, the allotriploid PAA, the allotetraploid PAM and the diploid PAU were renamed as P. ×alni, P. ×multiformis and P. uniformis, respectively (Husson et al. 2015). It is suggested that P. ×multiformis and P. uniformis are of exotic, but different, origin and that the hybridisation that created P. ×alni occurred in a European nursery where both accidentally introduced parental species met (Brasier et al. 2004, Jung et al. 2017c). Interestingly, P. uniformis is common in streams and alder stands in Alaska and Oregon without causing noticeable damage (Adams et al. 2010, Navarro et al. 2015). Using a microsatellite analysis, Aguayo et al. (2013) demonstrated higher genetic diversity of P. uniformis isolates from Alaska compared to their European counterparts indicating a North American origin of this species.

In pathogenicity tests, P. ×alni was significantly more aggressive to the bark of mature A. glutinosa logs than P. ×multiformis and P. uniformis (Brasier & Kirk 2001). Phytophthora ×alni, P. ×multiformis and P. uniformis were shown to be non-pathogenic to a range of other tree species indicating their host specificity to Alnus spp. (Brasier & Kirk 2001, Santini et al. 2003). In a comparative pathogenicity trial with different Alnus spp., the ranking of susceptibility to P. ×alni was A. glutinosa > A. incana and A. cordata > A. viridis > A. rubra (Jung & Blaschke 2006). Despite being only moderately aggressive to European alder species in pathogenicity trials, P. uniformis is primarily driving the root and collar rot epidemic of A. glutinosa and A. incana in Sweden and in the Bavarian Alps, Germany (Jung & Blaschke 2004, Redondo et al. 2015). This is most likely due to the significantly higher frost tolerance of P. uniformis compared to P. ×alni (Černý et al. 2012, J. Schumacher & T. Jung unpubl. data).

In Bavaria, root and collar rot and extensive mortality of A. glutinosa and A. incana was found in riparian forests along more than 20 000 km of rivers and streams. In the catchments of 58 of 60 river systems studied in detail, the primary source of inoculum could be traced back to numerous, young infested alder plantings established on the riverbanks or on forest sites draining into the rivers (Jung & Blaschke 2004). A similar association was found in 26 river systems in Austria (Jung et al. 2009, 2013b). The presence of the disease in more than 800 young forest and riparian alder plantings in Bavaria (Jung & Blaschke 2004), and the findings of P. ×alni and P. uniformis in 20 and 6.3 %, respectively, of the 64 nursery fields of Alnus spp. examined in seven European countries (Jung et al. 2016), clearly demonstrated that the rapid spread and the epidemic extent of this disease in Europe was primarily driven by the widespread planting of infested nursery stock. A range of other Phytophthora species, including P. cactorum, P. gonapodyides, P. lacustris, P. plurivora and P. polonica, are occasionally isolated from small root and collar lesions of Alnus spp. without playing a significant role in this epidemic (Gibbs et al. 2003, Jung & Blaschke 2004, Belbahri et al. 2006, Kanoun-Boulé et al. 2016). However, the recent finding of the introduced pathogen P. siskiyouensis causing collar rot and mortality of A. cordata in the UK (Fig. 4i, j) might pose an additional threat to alder stands in Europe. Phytophthora siskiyouensis was previously reported causing collar rot lesions on planted trees of A. glutinosa and A. cordata in Victoria, Australia, and in California, respectively, and from A. rhombifolia and A. rubra in riparian forests in Oregon (Smith et al. 2006, Rooney-Latham et al. 2009, Sims et al. 2015a). In underbark inoculation tests, P. siskiyouensis caused similar lesion lengths on A. rubra as P. uniformis (Navarro et al. 2015).

Variation in susceptibility of alder trees to P. ×alni, observed both in the field and in pathogenicity tests, could be the basis for a successful resistance screening programme which would allow sustainable long-term management of diseased alder stands. For example, in Bavaria, susceptibility of A. glutinosa trees, growing in permanent or seasonal contact to infested water on the banks of five rivers with long disease history, was tested and significantly higher tolerance to P. ×alni was found in many healthy-looking trees as compared to declining trees with root and collar rot symptoms (Jung & Blaschke 2006). Also in Belgium, considerable variation in susceptibility to P. ×alni was found among A. glutinosa trees randomly selected along 34 watercourses (Chandelier et al. 2016).

Decline and mortality of Chamaecyparis lawsoniana in Europe and North America

Chamaecyparis lawsoniana (Lawson’s cypress or Port-Orford-cedar, POC) has a limited geographical distribution in humid regions of south-western Oregon and northern California. It grows on a wide range of soil types and sites as a major overstorey component in mixed forests with Abies concolor, A. magnifica, Notholithocarpus densiflora, Pinus monticola, Pseudotsuga menziesii, Tsuga heterophylla and Sequoia sempervirens at altitudes from sea level up to 2 000 m (Zobel et al. 1985, Jimerson et al. 2001). POC is also one of the most common ornamental trees worldwide used for amenity plantings, shelterbelts and in hedgerows. The first reports of diseased POC came in 1923 from an ornamental nursery in Seattle, USA, outside of the natural range of the species, and since the early 1950s decline and mortality have been observed in natural forest stands in Oregon. The association with a previously unknown Phytophthora species, P. lateralis, was established by Tucker & Milbradt in 1942. Phytophthora lateralis is a soilborne pathogen which abundantly produces chlamydospores enabling its survival during dry and hot summers. Homothallic production of oogonia containing oospores was mentioned in the original description (Tucker & Milbradt 1942) but the sexual stage could not be confirmed in later studies (Hansen et al. 2000, Brasier et al. 2012). Phytophthora lateralis is a slow growing low-temperature species reproducing and infecting in the Pacific Northwest (PNW; California to British Columbia) mainly during cool and wet conditions in spring, autumn and summer (Hansen et al. 2000). Phylogenetically, P. lateralis is the closest known relative of P. ramorum, the causal agent of ‘Sudden Oak Death’ in California and Oregon and ‘Sudden Larch Death’ in the UK (Brasier et al. 2012, Yang et al. 2017). Phytophthora lateralis is highly aggressive to POC (Hansen et al. 2000, Robin et al. 2015). The only other tree species occasionally infected by P. lateralis in forests in Oregon is Taxus brevifolia but its susceptibility to the pathogen is much lower compared to POC (Murray & Hansen 1997, Hansen et al. 2000). Similar to P. cinnamomi in WA, the main pathway of P. lateralis in the USA is along roads and paths with infested soil particles adhering to tyres of vehicles and boots (Hansen et al. 2000, Goheen et al. 2012). Once introduced to a forest, P. lateralis shows efficient and rapid spread downhill and along rivers and streams (Hansen et al. 2000, Jimerson et al. 2001, Jules et al. 2002). Phytophthora lateralis has spread throughout the total natural range of POC causing a devastating decline with high mortality rates, which can reach more than 90 % on riparian sites with devastating effects on stream ecology (Hansen et al. 2000, Jimerson et al. 2001, Jules et al. 2002).

Outside the PNW, P. lateralis was for the first time isolated from POC in a nursery in France and the infestation was considered eradicated (Hansen et al. 1999). However since 2005, P. lateralis has been causing severe decline and mortality of thousands of C. lawsoniana trees growing in shelterbelts in Brittany, France (Robin et al. 2011). Soon after, P. lateralis has also been recovered from declining POC and C. pisifera trees at numerous sites in forests, parks and shelterbelts in England, Scotland and Northern Ireland (Green et al. 2013, Schlenzig et al. 2014). In Europe and the Pacific Northwest, the symptoms of POC decline include chlorosis, wilting and bronzing of foliage, thinning and dieback of the crown and finally death of affected trees (Fig. 5a, b) (Hansen et al. 2000, Robin et al. 2011, Green et al. 2013). These crown symptoms and mortality are caused by root rot and basal stem lesions with resinous exudates on the outer bark and flame-shaped red-brown necrosis of the underlying phloem and cambium (Fig. 5c–e; Hansen et al. 2000, Robin et al. 2011, Green et al. 2013). While seedlings get killed within a few weeks, large trees usually die within one year after appearance of first crown symptoms (Hansen et al. 2000). In both Brittany and the UK, P. lateralis was also isolated from aerial bark lesions on stems and branches, and in Brittany also from necrotic foliage suggesting aerial infections (Robin et al. 2011, Green et al. 2013). Foliage infections and aerial bark cankers on stems and large branches, supposedly originating from rain and wind splash inoculum, were also observed earlier in the USA (Roth et al. 1957). In a Scottish nursery, P. lateralis was isolated from pale-green discoloured foliage of declining seedlings of Thuja occidentalis originally imported from a nursery in France (Schlenzig et al. 2011). In the Netherlands, P. lateralis was detected on POC nursery stock (Brasier et al. 2012).

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Fig. 5

Symptoms of Port-Orford-cedar (Chamaecyparis lawsoniana) decline and mortality caused by Phytophthora lateralis in the UK (a–e) and of kauri (Agathis australis) dieback caused by P. agathidicida in New Zealand (f–h). a, b. Shelterbelts of C. lawsoniana containing recently dead trees with sparse brown foliage (white arrows) and declining trees with chlorotic foliage and increased transparency (red arrows); c. C. lawsoniana stem with resinous exudates indicating necrotic lesion of the inner bark caused by P. lateralis; d. flame-shaped reddish brown inner bark lesion on a C. lawsoniana caused by P. lateralis, extending from the main roots to more than 1 m stem height; e. flame-shaped reddish brown lesion front caused by P. lateralis on a C. lawsoniana tree (detail from d); f. mature A. australis in a diverse kauri forest showing advanced thinning and dieback of the crown; g. massive stem of a mature A. australis with tongue-shaped resinous bark lesion caused by P. agathidicida, extending from the main roots up to 2 m stem height; h. resin exudations marking the front of the inner bark lesion caused by P. agathidicida on a mature kauri stem (detail from g). — Photos: a–e: A. Pérez-Sierra; f–h: T. Jung.

Due to the high aggressiveness of P. lateralis to POC and the occurrence of several endemic Chamaecyparis species in eastern Asia with comparatively high resistance to P. lateralis, an Asian origin of this pathogen has long been suggested (Tucker & Milbradt 1942, Zobel et al. 1985, Hansen et al. 2000). Recently, P. lateralis was isolated at several sites in natural, high-altitude cloud forests of Taiwan from soil in wet seeps and from necrotic foliage of mature C. obtusa var. formosana with generally healthy crowns and non-damaged fine root systems (Brasier et al. 2010, 2012, Webber et al. 2012). A population genetic study using microsatellites demonstrated that isolates from France, the Netherlands and the majority of the UK isolates were identical to isolates from the PNW, whereas the Taiwanese isolates belonged to two distinct evolutionary lineages, designated as TWJ and TWK. Several isolates from Scotland constituted a separate UK lineage which might have resulted from a hybridisation between the PNW and the Taiwanese lineages (Vettraino et al. 2017). The lineages also show considerable phenotypic and morphometric differences (Brasier et al. 2012). In all lineages short preformed sporangial pedicels occur enabling aerial spread and infections of foliage and bark (Brasier et al. 2012). In comparative underbark shoot-dip and root-dip inoculation trials the PNW and TWJ lineages showed higher aggressiveness to POC than the TWK and the UK lineages (Robin et al. 2015). Based on the results of these studies, it was concluded that the European PNW isolates were recently introduced from the USA with infested nursery stock (Vettraino et al. 2017). The exact origin of the PNW lineage in Asia still remains to be found.

The detection of heritable genetic resistance to the PNW lineage of P. lateralis in the natural population of POC (Hansen et al. 1989) stimulated a successful long-term resistance screening programme (Hansen et al. 2000, 2011, Oh et al. 2006, Sniezko et al. 2006, 2011). Using stem-dip and root-dip infection trials resistance was found in 1 600 of 12 000 trees tested (Oh et al. 2006). In greenhouse trials survival rate of seedlings and rooted cuttings from resistant parent trees varied between 25 and 100 % compared to 0–10 % survival of seedlings from susceptible parents (Sniezko et al. 2006). In a long-term outplanting trial on a high disease impact site, seedlings and rooted cuttings from the five most resistant families showed after 16 years 20–80 % survival compared to less than 8 % in progenies from the three most susceptible families (Oh et al. 2006). Several POC families resistant to the PNW lineage of P. lateralis were also challenged with the UK, TWJ and TWK lineages and no breakdown of resistance was observed (Robin et al. 2015). These results are promising regarding the re-establishment of this important tree species on dieback sites. The successful POC resistance screening programme could serve as a role model for the management of other Phytophthora diseases of forest trees.

Kauri dieback in New Zealand

Kauri (Agathis australis), a particularly long-lived ancient conifer species in the Araucariaceae, can reach 5 m stem diameter and up to 50 m height. Naturally, it grows widely on the North Island of New Zealand as a keystone species in diverse, mixed lowland forests below 600 m altitude together with other conifers, including Dacrycrydium cuppressinum, Phyllocladus trichomanoides, Podocarpus totara, P. laetus and Prumnopitys ferruginea (Nicholls 1976, Wardle 1991, Steward & Beveridge 2010). Due to excessive logging in the past, the current distribution of kauri is largely fragmented and relatively pristine old growth stands occupy less than 5 % of the pre-European area (Ahmed & Ogden 1987).

In 1972, Phytophthora isolates were recovered from a dying kauri stand on the Great Barrier Island off the coast of the North Island and morphologically identified as P. heveae (Gadgil 1974). Apparently, not much attention had been paid to managing this local disease outbreak until dieback and mortality of kauri stands were observed 30 years later on the North Island (Beever et al. 2009, Scott & Williams 2014, Bellgard et al. 2016). Symptoms include thinning, chlorosis and dieback of crowns (Fig. 5f), fine root losses and tongue-shaped collar rot lesions with abundant resin exudations extending several meters up the trunk and also into the main roots (Fig. 5g, h) (Beever et al. 2009, Bellgard et al. 2016). A homothallic Phytophthora species, informally designated as Phytophthora taxon Agathis (PTA) and later described as P. agathidicida, was consistently isolated from necrotic bark lesions and from rhizosphere soil (Beever et al. 2009, Scott & Williams 2014, Weir et al. 2015). Although the smooth-walled oogonia of P. agathidicida resemble those of P. heveae, multigene phylogenetic analysis placed it closer to P. castaneae within Phytophthora Clade 5, together with P. cocois from Hawaii and P. heveae (Weir et al. 2015, Yang et al. 2017). Since its closest relatives P. castaneae and P. heveae are of Southeast Asian and Australasian origin (Arentz 1986, Brown 1999, Ko et al. 2006, Jung et al. 2017a) it is likely that P. agathidicida is also indigenous to this area (Beever et al. 2009, Weir et al. 2015, Bellgard et al. 2016). One original isolate, obtained in 1972 from a dying kauri tree on the Great Barrier Island, could be assigned to P. agathidicida and in 2006 this pathogen could again be isolated from kauri collar rot at this original outbreak site (Beever et al. 2009). It is assumed that P. agathidicida did not spread from the Great Barrier Island to kauri stands of the North Island but has rather been present there for decades and collar rot and dieback symptoms have simply been overseen (Beever et al. 2009). A reassessment of the dieback area on the Great Barrier Island revealed an annual rate of disease extension of approximately 3 m, comparable to P. cinnamomi in Western Australia (Strelein et al. 2006, Beever et al. 2009). Other Phytophthora species like P. cryptogea, P. kernoviae, P. multivora and P. nicotianae are occasionally recovered from kauri soils, while P. cinnamomi is widespread in kauri forests. Although in general P. cinnamomi is not associated with kauri dieback it can be infrequently associated with scattered mortality of individual kauri trees under particularly favouring conditions for the pathogen (Podger & Newhook 1971, Beever et al. 2009, Waipara et al. 2013, Horner & Hough 2014). In both underbark inoculation and soil infestation trials, P. agathidicida showed much higher aggressiveness to A. australis than P. cinnamomi, P. cryptogea and P. multivora, causing large girdling lesions and high mortality (Horner & Hough 2014). Recent surveys demonstrated a wide distribution of collar rot, dieback and mortality of kauri throughout much of the natural range in the North Island, and P. agathidicida has been isolated at many sites from collar rot lesions confirming this pathogen being the causal agent of this epidemic (Waipara et al. 2013, Scott & Williams 2014). Phytophthora agathidicida infects trees of all ages and, besides killing mature trees, poses a serious threat to kauri regeneration, hence, resulting in the long-term in an altered forest composition from kauri-dominated forests to forests dominated by Podocarpus spp., D. dacrydioides and P. trichomanoides (Beever et al. 2009, Bellgard et al. 2016).

Decline and mortality of Austrocedrus chilensis and Juniperus communis in Argentina and Europe

Austrocedrus chilensis (Cordilleran cypress or Chilean cedar) is a dioecious evergreen conifer, member of the Cupressaceae, and native to the mountains of South Chile and South Argentina. It grows in a wide range of soil types and under different environmental conditions between S36°30’ and S43°35’ latitude on the eastern slopes of the Andes in Argentina and between S32°39’ and S44° latitude on the western slopes of the Andes in Chile (Veblen et al. 1995). Besides its ecological importance, A. chilensis is valued for its high timber quality and straight stems used for construction and woodworking (La Manna & Rajchenberg 2004). Decline and mortality of Cordilleran cypress, commonly known as ‘mal del ciprés’, was first detected in 1948 (Havrylenko et al. 1989, Greslebin et al. 2005) and has since spread throughout its whole range in Argentina. Chlorosis, progressive withering, defoliation, and finally the death of affected trees characterise the decline. Trees can die rapidly and in these cases the foliage turns from chlorotic to red. Such epidemics cause high mortality at landscape level (Fig. 6a–d). Earlier studies discussed several hypotheses regarding the causal agents of the decline including root infections by Pythiaceous pathogens, root decay by basidiomycete fungi, lack or dysfunction of mycorrhizae of Cordilleran cypress, global warming, droughts, and poor drainage and increased precipitation (Havrylenko et al. 1989, Rajchenberg et al. 1998, Filip & Rosso 1999). Although several studies of biotic and abiotic factors tried to elucidate the origin and causes of this decline, it was not before 2007 that a previously unknown Phytophthora species, P. austrocedri (synonym P. austrocedrae), was first described and associated with the mortality of A. chilensis in Argentina (Greslebin et al. 2007). Phytophthora austrocedri is a homothallic species with very slow growth and a low optimum growth temperature of 17.5 °C. It was placed in Clade 8 where the most closely related species are the soilborne P. syringae and P. obscura, both causing root rots, cankers and foliar and shoot blights on numerous trees and ornamentals (Grünwald et al. 2012b). Phytophthora syringae and P. ×cambivora were occasionally recovered from the rhizosphere of declining trees but are not involved in the decline (Greslebin et al. 2005, 2007). Phytophthora austrocedri was isolated from roots and from collar and stem lesions of symptomatic A. chilensis trees. Lesions extend from the roots up the trunk and are characterised by resin exudations at the surface of the bark and brown, flame-shaped lesions of the underlying phloem and cambium (Fig. 6e). Sometimes, a staining of the superficial sapwood underneath bark lesions can be observed. Pathogenicity tests on seedlings, saplings and adult trees demonstrated high aggressiveness of P. austrocedri to A. chilensis confirming the association of this pathogen with the decline in Argentina (Greslebin & Hansen 2010). The virtually clonal population structure of P. austrocedri and its aggressive behaviour on Cordilleran cypress, strongly suggested that it is an alien invasive pathogen in Argentina (Vélez et al. 2013).

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Fig. 6

Decline and dieback symptoms caused by Phytophthora austrocedri on Austrocedrus chilensis in Argentina (a–e) and on Juniperus communis in the UK (f, g). a. Extensive mortality of A. chilensis at landscape level; b. decline, dieback and mortality of A. chilensis at stand level; c. A. chilensis trees with thinning and dieback of crowns; d. healthy, declining chlorotic and dead A. chilensis (from right to left); e. mature A. chilensis stem with flame-shaped necrotic lesion of the inner bark; f. long-dead and recently killed J. communis with red-brown foliage; g. tongue-shaped orange-brown lesion extending from the main roots into the collar of a mature J. communis. — Photos: a–d: T. Jung; e–g: A. Pérez-Sierra.

Juniperus communis (common juniper) is another dioecious evergreen conifer from the Cupressaceae, with a wide holarctic, boreo-temperate distribution ranging from N30° in North Africa to northern Asia, North America and Europe (Preston et al. 2002, Thomas et al. 2007). In 2010, first reports of a serious decline of common juniper came from a National Nature Reserve in northern England (Britain). By 2013, the disease was detected at 19 sites in northern England and Scotland. Dead and dying juniper trees are scattered throughout the affected areas, mainly concentrated on wet, flat ground but also extending uphill across drier slopes. Affected trees and shrubs show fading green colour, reddening or browning foliage on individual branches or the whole crown, and eventually defoliation and tree death (Fig. 6f). Crown symptoms and mortality are caused by orange-brown tongue-shaped lesions in the phloem at the stem collar and along upper roots (Fig. 6g). In some cases, a distinct yellowing of healthy phloem in advance of the lesion margin can be observed on infected trees. Phytophthora austrocedri was confirmed as the cause of this dieback and mortality (Green et al. 2012). This pathogen was also identified on two other non-native conifer species in the UK, Xanthocyparis nootkatensis (Nootka cypress or Alaskan yellow cedar) (Green et al. 2016) and POC, both like A. chilensis and J. communis from the Cupressaceae family. British isolates from different geographical sites were analysed and also showed limited genetic diversity (Green et al 2015). In Germany, a single isolate of P. austrocedri was obtained from a young J. horizontalis ‘Glauca’ in a nursery (Werres et al. 2014).

Recently, Henricot et al. (2017) compared Argentinian, British and German isolates of P. austrocedri to clarify the epidemiological and evolutionary relationships between them. Morphological and physiological parameters did not differ significantly between the different populations and in cross-infection experiments both Argentinian and British isolates were pathogenic to the two main hosts A. chilensis and J. communis. However, phylogenetic analyses of sequences from two mitochondrial and five nuclear gene regions showed that all British isolates were near identical but phylogenetically distinct from the Argentinian and German isolates which share the same genotype. These results indicate that British isolates and Argentinian/German isolates of P. austrocedri constitute two evolutionarily distinct lineages originating from the same as-yet-unidentified source population (Henricot et al. 2017).

At the end of 2017, a new case of P. austrocedri was reported on a new host, Cupressus sempervirens (Italian cypress) in northern Iran (Mahdikhani et al. 2017). The symptoms in affected trees were consistent with those reported on other hosts and included bronzed foliage and an orange-brown lesion in the phloem around the collar. To date, decline and canker diseases caused by P. austrocedri have been reported from three continents, South America, Europe and western Asia, and so far the host range has been confined to the Cupressaceae family.

Diebacks of natural ecosystems in Australia

Apart from tropical regions in north-eastern Queensland and cool-temperate Tasmania, the climate in Australia is characterised by hot and dry summers and relatively low annual precipitations. In the south-west of WA, soil temperatures during summer often exceed 30 °C, and soil water potentials and soil water contents often drop below -6 Mpa (-60 bar) and 1 %, respectively (Shearer & Tippett 1989, Lamont & Bergl 1991, Enright & Lamont 1992, Collins et al. 2011). Although such conditions are generally not believed to favour survival, spread and infection via zoospores of soilborne oomycetes, Australia hosts an impressive diversity of Phytophthora species. Since 2009, 19 previously unknown Phytophthora species were described from natural ecosystems in WA, including P. amnicola, P. arenaria, P. bilorbang (previously P. taxon oak soil), P. balyanboodja, P. boodjera, P. condilina, P. constricta, P. cooljarloo, P. elongata, P. fluvialis, P. gibbosa, P. gregata, P. kwongonina, P. litoralis, P. mooyotj, P. multivora, P. pseudorosacearum, P. thermophila and P. versiformis (Scott et al. 2009, Rea et al. 2010, 2011, Jung et al. 2011, Crous et al. 2011, 2012, 2014, Aghighi et al. 2012, Simamora et al. 2015, Paap et al. 2017, Burgess et al. 2018). A metagenomic survey of Phytophthora diversity at 640 natural sites across Australia demonstrated presence of 68 Phytophthora phylotypes, of which 21 were potentially new taxa and another 25 were previously not found in natural ecosystems or were new introductions to Australia (Burgess et al. 2017). With presence at 44.7 and 34.2 % of the sites, respectively, P. multivora and P. cinnamomi were by far the most common species. Interestingly, these two introduced wide-host range pathogens also have the most deleterious impact on Australian natural ecosystems.

During the long isolation from other continents, a diverse and largely endemic flora evolved in Australia which, due to a lack of co-evolution, contains a high proportion of plant species susceptible to non-native introduced Phytophthora species. Alone in the south-western Botanical Province of WA, 40 % of the 5 710 endemic plant species from 39 families are susceptible to P. cinnamomi (Shearer et al. 2004). Recently, pathogenicity of P. cinnamomi and 21 other Phytophthora taxa from WA, most of them recently described or informally designated new species, to seven native plant species from WA, including Eucalyptus marginata (jarrah), Banksia grandis, B. littoralis, B. occidentalis, Casuarina obesa, Corymbia calophylla (marri) and Lambertia inermis, was demonstrated (Belhaj et al. 2018). Eucalyptus marginata and the three Banksia species were susceptible to the highest number of Phytophthora taxa whereas C. calophylla showed the highest resistance to all 21 Phytophthora taxa (Belhaj et al. 2018). Australia has a long history of diebacks of various eucalypt forests, Banksia woodlands and heathlands, which are particularly severe in the Mediterranean climates of WA (Shearer & Tippett 1989, Shearer & Dillon 1995, 1996, Shearer et al. 2004) and Victoria (Weste & Marks 1987, Marks & Smith 1991, Laidlaw & Wilson 2003, Weste 2003, Cahill et al. 2008). In WA, the most widespread forest type is the dry sclerophyll jarrah forest which is largely dominated in the overstorey by E. marginata, while the understorey contains a diverse flora mainly from the Proteaceae, Dilleniaceae, Epacridaceae, Fabaceae and Xanthorrhoeaceae (Shearer & Tippett 1989). First symptoms of dieback and mortality in the jarrah forest were reported during the 1920s but it took 40 years until the association with the presence of P. cinnamomi in the rhizosphere was established (Podger et al. 1965, Podger 1972, Shearer & Tippett 1989). Fifty years of intense research has produced a rich body of knowledge on the aetiology, site relations and dynamics of jarrah dieback and numerous other diebacks in WA and eastern Australia, the ecology, host range and pathways of P. cinnamomi, and the role that other Phytophthora spp. are playing. Although P. elongata, P. gibbosa, P. gregata, P. litoralis, P. multivora, P. thermophila and P. versiformis can cause local dieback and mortality of understorey species and sometimes also of E. marginata (P. multivora, P. elongata), the dieback of the jarrah forest is mainly driven by two clonal lineages of P. cinnamomi from the A2 mating type (Shea 1975, Shea et al. 1982, Shearer & Tippett 1989, Dobrowolski et al. 2003). The main pathway of P. cinnamomi in the jarrah forest and other natural ecosystems in WA is the accidental transport of infested soil adhering to vehicles and boots and the use of infested gravel material for building of forest roads (Shea et al. 1983, Shearer & Tippett 1989, Marks & Smith 1991). A few months after the introduction of P. cinnamomi to a site, first symptoms of chlorosis and wilting appear on highly susceptible understorey species, in particular B. grandis, Xanthorrhoea preissii and Macrozamia riedlei, hence, they are used as indicator species for presence of P. cinnamomi (Shea 1979, Shearer & Tippett 1989). The pathogen usually moves through the forest via zoospores and root-to-root contact with more or less sharply defined infection fronts (Weste & Marks 1987, Shearer & Tippett 1989). An extensive study at 55 sites across WA using aerial photography demonstrated mean disease progression rates of 1.4 m per year for uphill extension and 9.5 m per year across slopes (Strelein et al. 2006). Downhill progression is much faster reaching up to 400 m per year in Victoria (Weste & Law 1973). After several years, the majority of midstorey and understorey species are affected by dieback and mortality and highly susceptible species can be eliminated while the E. marginata overstorey shows severe thinning, chlorosis, wilting and dieback of the canopy and mortality of scattered trees or in groups up to several hectares in size (Fig. 7a) (Podger 1972, Shearer & Tippett 1989, Jung et al. 2013a). Although in jarrah the rate of symptom expression is varying depending on the site conditions, other tree species, in particular marri and bullich (E. megacarpa) can persist much longer. In E. marginata, P. cinnamomi causes excessive fine root losses, which interact with the extreme summer droughts leading to gradual decline and eventually dieback and mortality (Podger 1972, Shea 1975, Crombie et al. 1987, Shearer & Tippett 1989). In addition, P. cinnamomi can infect large woody roots and produce bark lesions, which on sites with impeded drainage due to a concrete lateritic hardpan close to the surface may girdle the vertical roots just above the lateritic layer resulting in acute wilting and mortality (Shea et al. 1982, Tippett et al. 1983, Shearer & Tippett 1989). Collar infections on jarrah are rare and mostly restricted to waterlogged sites or young trees (Fig. 7f; Shearer & Tippett 1989). Burgess et al. (1999) demonstrated increased susceptibility of jarrah stems to P. cinnamomi infection under conditions of root hypoxia. About 20 % of the 64 000 km² covered by the jarrah forest are already infested by P. cinnamomi and the structural and floristic changes it caused are unprecedented (Fig. 7a). Recently, it has been shown that P. cinnamomi survives the hot and dry summer conditions in WA within infected fine roots and small woody roots of woody host and non-host species and annual herbs. Particularly thick-walled oospores produced by selfing of the A2 mating type, stromata-like hyphal aggregations and intracellular hyphae encased by callose sheaths (lignitubers) serve as long-term survival structures, while the thin-walled chlamydospores enable short-term survival between consecutive rain events (Crone et al. 2013, Jung et al. 2013a).

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Fig. 7

Diebacks of natural ecosystems caused by Phytophthora spp. in the south-west of Western Australia (WA). a. Severe dieback and mortality of jarrah (Eucalyptus marginata) forest with extensive elimination of the previously diverse understorey caused by P. cinnamomi; b. high mortality of tuart (E. gomphocephala) on calcaric sandy soils in the Swan Coastal Plain caused by extensive fine root losses due to P. multivora infections; c. severe dieback and mortality of riparian flooded gum (E. rudis) stand within the jarrah forest caused by P. elongata and P. multivora; d. extensive dieback and collapse of a Banksia woodland caused by P. cinnamomi; e. dieback and mortality of mature red tingle (E. jacksonii) caused by P. cinnamomi and P. cryptogea in a humid relic forest at the south coast of WA; f. girdling collar rot lesion caused by P. cinnamomi on a young E. marginata in the jarrah forest; g. bleeding collar rot lesion caused by P. cinnamomi on a mature Banksia grandis tree in an open Banksia woodland. — Photos: all T. Jung.

Across its native range and in particular in the Swan coastal plane south of Perth, tuart (E. gomphocephala) forests, growing on dry and sandy limestone sites, are suffering for almost 20 years from a severe decline characterised by thinning and dieback of the crowns and high mortality rates (Fig. 7b; Edwards 2004, Archibald 2006, Scott et al. 2009). Several environmental factors have initially been considered responsible for tuart decline until a firm association with the previously undescribed pathogen P. multivora was established (Scott et al. 2009). In pathogenicity tests, P. multivora demonstrated high aggressiveness to the fine root system of E. gomphocephala (Scott et al. 2012). In the tuart forest, P. multivora causes progressive fine root losses which exacerbate the severe drought stress during summer on the sandy soils predisposing affected trees to attacks by stem borers (Scott et al. 2009). Other tree species like Agonis flexuosa (peppermint) are also affected, but to a lesser extent (Scott et al. 2009). Phytophthora multivora has a wide host range in WA and in other continents whereas in South Africa it is widespread in natural ecosystems without causing visible disease symptoms suggesting long-term coevolution (Scott et al. 2009, Oh et al. 2013, Jung et al. 2016). The acidophilic P. cinnamomi is generally absent from these calcaric sites in WA and, hence, is not involved in tuart decline. Also in the south-west of WA, riparian gallery forests of flooded gum (E. rudis) along many rivers and streams are showing since the 1970s increasingly severe thinning and dieback of crowns with high levels of mortality (Fig. 7c). For a long time, attacks by psyllids and leaf miners and various environmental factors, including rising salinity levels of river water due to agricultural mismanagement, have been discussed as causal agents, but a satisfactory disease aetiology was not established (Curry 1981, Abbott 1999, Yeomans 1999, Clay & Majer 2001). However, recently P. elongata and P. multivora were regularly isolated along many rivers from the rhizosphere of dying riparian E. rudis trees with extensive fine root losses (Edwards et al. 2010). It seems likely that this widespread devastating decline is driven by root damage caused by these invasive Phytophthora species interacting with other biotic and abiotic factors including insect defoliations, droughts and salinity. Phytophthora elongata has a clonal population structure in WA and its origin is still unknown. It was most likely introduced to the jarrah forest during the 1970s with infested nursery stock used for rehabilitation plantings of mine sites, and subsequently spread into streams and river systems (Rea et al. 2010).

In WA, highly diverse Banksia woodlands and Kwongan heathlands constitute the climax vegetation in the northern and southern sandplains and on other sites too dry for supporting forest growth. In these ecosystems P. cinnamomi and many other Phytophthora spp. are causing fine root losses in susceptible plant species leading to dieback and bleeding collar lesions (Fig. 7g) which may girdle the plants resulting in acute wilting and mortality (Fig. 7b; Scott et al. 2009, Shearer et al. 2009, Rea et al. 2011, Jung et al. 2013a). Pathogenicity of 22 Phytophthora taxa to three Banksia species and L. inermis was recently demonstrated (Belhaj et al. 2018). While the invasive P. cinnamomi usually moves through these ecosystems in clearly visible infection fronts with high mortality rates, potentially indigenous species like P. arenaria from Clade 4, P. constricta from Clade 9, P. balyanboodja, P. condilina, P. cooljarloo, P. kwongonina and P. pseudorosacearum from Clade 6a and P. gibbosa, P. gregata, P. litoralis and P. thermophila from Clade 6b cause scattered or patchy dieback which is usually associated with episodic, unseasonal heavy rain events (Rea et al. 2011, Jung et al. 2011, Burgess et al. 2018).

In the humid south-western-most corner of WA, a tertiary relic forest dominated by particularly tall and long-lived tree species like karri (E. diversicolor), red tingle (E. jacksonii), yellow tingle (E. guilfoylei), Rates tingle (E. brevistylis) and marri is growing in a small area which is mostly protected within the Walpole-Nornalup National Park. For about a decade, numerous red tingle trees are suffering from a severe dieback and mortality which is associated with root infections by P. cinnamomi and P. cryptogea (Fig. 7e; T. Jung unpubl.). Due to the small natural habitat of red tingle this disease might threaten the survival of this endangered iconic tree species in nature.

In Victoria, severe diebacks occur in eucalypt forests and Banksia woodlands, in particular in the Grampians, in East and South Gippsland, the Wilsons Promontary and the Brisbane Ranges National Parks (Marks & Smith 1991). Symptomatologies, disease aetiologies, dynamics and site relations are largely similar to the situation in WA (Weste & Marks 1987, Marks & Smith 1991, Wilson et al. 2000, Weste 2001, Cahill et al. 2008). A 30-years study at 13 sites in representative eucalypt forests, woodlands and heathlands across Victoria demonstrated a gradual decline of P. cinnamomi inoculum to very low levels with progressing elimination of highly susceptible plant species from infested sites and their natural replacement by highly resistant species. After 20–30 years, substantial regeneration and survival of 30–40 previously eliminated susceptible plant species like Xanthorrhoea australis was observed, while the crowns of affected overstorey trees showed no recovery (Weste 2003). Future surveys are needed to assess whether the ecosystem recoveries will be sustainable or whether P. cinnamomi inoculum levels will increase again resulting in new dieback cycles.

In the tropical rainforests of northern Queensland, an extensive Phytophthora survey revealed presence of 10 Phytophthora species at 55 % of the 1 897 sites tested. More than 13 000 isolates were obtained of which 86 % and 9 % were P. cinnamomi and P. heveae, respectively. The remaining isolates belonged to P. boehmeriae, P. castaneae, P. citricola s.lat., P. cryptogea, P. drechsleri, P. meadii, P. nicotianae and P. palmivora (Brown 1999). Phytophthora cinnamomi was more frequently isolated from dead and dying than from healthy forests, and at nine sites this pathogen was associated with patch dieback of rainforest trees. All other Phytophthora spp. showed no association with disease (Brown 1999). The absence of large-scale dieback of forests might be explained by the constantly warm and humid climate which is favouring the trees more than P. cinnamomi, or indicate long-term coevolution between the flora and the pathogen, which could have spread from New Guinea to Queensland via a landbridge during the pleistocene. However, the presence of the A1 mating type at only four of the 646 sites infested by P. cinnamomi does not support the latter hypothesis, since in Papua New Guinea the A1 mating type is more widespread and considered an ancient introduction whereas the A2 mating type was most likely introduced in modern times (Arentz 1983, 2017, Arentz & Simpson 1986).

A recent survey in the diverse Gondwana rainforests of southern Queensland and northern New South Wales demonstrated the presence of eight Phytophthora species, including P. cinnamomi, P. cryptogea, P. frigida, P. heveae, P. macrochlamydospora, P. multivora, the previously unknown P. gondwanensis and another unknown Phytophthora taxon (Scarlett et al. 2015). Due to their wide host ranges and their high virulence, P. cinnamomi and P. multivora might pose a serious threat to the Gondwana rainforests which contain more than 200 rare and endangered plant species (Crous et al. 2015, Scarlett et al. 2015). Also in New South Wales, both P. multivora and P. cinnamomi were recovered from declining trees of the ‘living fossil’ Wollemia nobilis (Wollemi pine) in its only natural site and their high aggressiveness to this critically endangered tree species has been demonstrated (Puno et al. 2015).

Decline and dieback of the Mediterranean maquis vegetation

Mediterranean-type ecosystems, with their characteristic and unique climatic regimes of mild wet winters and warm and dry summers, occur just in five regions of the world: California, Central Chile, the Mediterranean Basin, South Africa and south-western and South Australia (Peel et al. 2007). These Mediterranean climate regions harbour a remarkable and globally significant level of plant diversity and endemism, accounting for almost 20 % of all plant species in the world (Myers et al. 2000, Cowling et al. 2006). In response to the climate, similar woody, shrubby plants, with evergreen sclerophyll leaves, have developed in communities of varying density. The names for the shrub vegetation vary by region because of language and plant structure, including ‘maquis’ and ‘garrigue’ in the Mediterranean Basin, ‘chaparral’ in California, ‘matorral’ in Chile, ‘fynbos’ or ‘renosterveld’ in South Africa and ‘mallee’ scrubs and shrublands and ‘kwongan’ heathlands in Australia.

The maquis vegetation in the Mediterranean Basin is characterised by scrub, sparse grass and scattered evergreen trees with a maximum size of 2–3 m, which differ in structure and species richness depending on local conditions (Spano et al. 2013). Since 2010, in the National Park of La Maddalena archipelago, off the northern coast of Sardinia, extensive dieback and mortality of a wide range of plant species, typical of the Mediterranean maquis in the archipelago as well as in other maquis sites in Sardinia, has been recorded across slopes downhill of roads and trekking paths (Fig. 8a, b) (Scanu et al. 2015). The main species affected are Arbutus unedo, Asparagus albus, Cistus sp., Erica spp., Juniperus phoenicea, J. oxycedrus, Pistacia lentiscus and Rhamnus alaternus (Scanu et al. 2015). Amongst the most susceptible species, J. phoenicea, J. oxycedrus and A. unedo show a wide range of symptoms including partial or complete dieback of the crown and abnormal production of epicormic shoots, and reddening or browning of drying foliage on dying and recently dead trees and shrubs (Fig. 8c, d). Crown symptoms are associated with extensive losses of both lateral small woody roots and fine roots, opening cankers and the presence of basal phloem lesions extending from the main roots up the stems (Fig. 8e). Root and collar rot on juniper trees and shrubs frequently occurs in low-laying areas with seasonal waterlogging. In wetlands, other tree/shrub species like P. lentiscus and R. alaternus also show severe crown thinning, dieback of single branches and mortality (Fig. 8b, f), which are caused by root and collar rot. Ground layer species such as A. albus (Fig. 8g) and Cistus spp. are also commonly affected showing chlorosis, wilting and dieback.

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Fig. 8

Decline and dieback symptoms on maquis vegetation caused by Phytophthora spp. in the Mediterranean basin. a. Extensive dieback and mortality of shrub species due to P. cinnamomi; b. Pistacia lentiscus showing severe dieback and mortality caused by P. ornamentata; c. mature tree of Juniperus oxycedrus with severe wilting and red discoloration of the foliage; d. large orange-brown lesion extending from the main root into the collar of a mature J. phoenicea; e. young Arbutus unedo recently killed by P. cinnamomi; f. chlorosis, wilting and dieback of Rhamnus alaternus caused by P. cinnamomi; g. chlorosis, wilting and dieback of Asparagus albus caused by P. asparagi. — Photos: a–c, e–g: B. Scanu; d: T. Jung.

An unexpected high diversity of Phytophthora species has been found associated with the decline and dieback of this diverse ecosystem. In total 10 Phytophthora species were isolated from rhizosphere soil samples collected from declining Mediterranean maquis vegetation and stream catchments in the National Park of La Maddalena archipelago, including P. asparagi, P. bilorbang, P. cinnamomi, P. crassamura, P. gonapodyides, P. melonis, P. ornamentata, P. parvispora, P. pseudocryptogea and P. syringae (Scanu et al. 2015). The most common species detected were P. asparagi and P. bilorbang, both from Clade 6 (Jung et al. 2011, Aghighi et al. 2012). While P. bilorbang appears to be a common species in natural environments (Aghighi et al. 2012, Sims et al. 2015b), P. asparagi was previously only reported from horticultural and ornamental plants (Cunnington et al. 2005, Saude et al. 2008, Jung et al. 2016). Likewise, also P. melonis was previously only known from agriculture causing a severe disease of members of the Cucurbitaceae in Asia (Ho et al. 2007). This suggests the possible introduction of both P. asparagi and P. melonis with infested plant material (Moralejo et al. 2009, Jung et al. 2016). Two previously unknown species, P. crassamura and P. ornamentata have been described from J. phoenicea and P. lentiscus, respectively, in Sardinia (Scanu et al. 2015). While P. crassamura is widespread across continents with different climatic conditions (Brasier et al. 2003, Burgess et al. 2009), P. ornamentata seems to be restricted to the Mediterranean Basin (Scanu et al. 2015), although it has recently been detected from C. calophylla plants in Australia (G.E.St.J. Hardy pers. comm.). In pathogenicity trials, all Phytophthora species demonstrated pathogenicity to J. phoenicea and P. lentiscus (Scanu et al. 2015). On J. phoenicea the most aggressive pathogens were P. asparagi and P. bilorbang, killing 50 % and 37.5 % of inoculated plants, respectively, while P. cinnamomi caused 100 % mortality on P. lentiscus. Phytophthora asparagi, P. crassamura, P. bilorbang, P. melonis and P. ornamentata were also highly aggressive to P. lentiscus (Scanu et al. 2015).

Phytophthora cinnamomi was isolated from R. alaternus showing severe dieback and wilting (Scanu et al. 2015) and together with its closest relative P. parvispora, this pathogen was also isolated from A. unedo, another common species in Mediterranean maquis ecosystems (Scanu et al. 2014a). Also in Portugal, P. cinnamomi has been isolated from declining and wilting A. unedo plants in Mediterranean maquis vegetation (T. Jung & M. Horta Jung unpubl. data). Phytophthora cinnamomi was also found causing a severe decline and mortality of Erica umbellata, a small heather species native to the western Iberian Peninsula and northern Morocco, in a protected natural area in Extremadura (Spain) (Acedo et al. 2013). Several understory Ericaceae and Cistaceae scrubs commonly occurring in declining Mediterranean oak stands in Spain and Portugal were also found to be infected by P. cinnamomi (Brasier et al. 1993, Moreira & Martins 2005). These plant species are suspected to act as a reservoir of pathogen inoculum, contributing to the spatial distribution of P. cinnamomi (Moreira & Martins 2005). The frequent detection of P. cinnamomi from Mediterranean plant species in recent years indicates that this pathogen is currently spreading into the maquis vegetation ecosystems. Against the background of a predicted increase of P. cinnamomi activity under current climate change projections (Brasier & Scott 1994, Burgess et al. 2017), the severe destructions of the root system caused by P. cinnamomi in pathogenicity tests on A. unedo, E. umbellata, J. phoenicea and P. lentiscus (Acedo et al. 2013, Scanu et al. 2014a, 2015) suggest that this polyphagous pathogen has the potential to threaten the native maquis vegetation in the Mediterranean basin on a large scale.

‘Sudden Oak Death’ and ‘Sudden Larch Death’ in the USA and the UK

‘Sudden Oak Death’ (SOD) is one of the most destructive epidemics of forest trees worldwide. This disease was first recorded in 1995 in Marine County, California, and subsequently spread across the relatively narrow coastal strip from Monterey county in central California to south-western Oregon (Goheen et al. 2002, Rizzo et al. 2002). In this area grow diverse temperate rainforests with an overstorey dominated by conifers like Sequoia sempervirens, Abies grandis, Pseudotsuga menziesii and Tsuga heterophylla and a mid- and understory layer of various broadleaved tree species including Notholithocarpus densiflorus (tanoak), Quercus agrifolia (coast live oak), Umbellularia californica (California bay laurel), Acer macrophyllum, Alnus rubra and Arbutus menziesii (Abrams & Ferris 1960, Knapp 1965, Lanner 1999).

The disease rapidly reached epidemic proportions in forests and in urban-forest interfaces in California, with a large number of N. densiflorus, Q. agrifolia, and to a lesser extent Q. kellogii and Q. parvula trees showing severe wilting and high mortality (Fig. 11a). First reports from forests in Oregon came in 2002 (Goheen et al. 2002). The causal organism was the heterothallic airborne pathogen P. ramorum which was first described from ornamental Rhododendron spp. and Viburnum tinus in Europe (Werres et al. 2001). The scale of devastation in California prompted national and international regulatory actions and local eradication efforts (Rizzo et al. 2005, Grünwald et al. 2012a, Hansen et al. 2012). Within a decade, extensive research had produced a rich body of knowledge on disease aetiology, infection biology, host range, pathways and population structure of P. ramorum. Over the last 20 years, the host list of P. ramorum has grown continuously exceeding to date 150 host species ranging from herbaceous plants and ferns to woody shrubs and trees (Grünwald et. al. 2012a). Extensive pathogenicity trials in Oregon demonstrated that 80 % of 49 native tree and shrub species tested were susceptible to P. ramorum (Hansen et al. 2005). Host lists, distribution of the pathogen in California and any new research findings are periodically updated on the web page www.suddenoakdeath.org.

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Fig. 11

Sudden Oak Death and Sudden Larch Death symptoms caused by Phytophthora ramorum in the USA (a–e) and in the UK (f, g), respectively. a. Severe wilting and mortality of tanoaks (Notholithocarpus densiflorus) in a mixed coastal forest with Sequoia sempervirens in California; b. necrotic lesions on leaves of California bay laurel (Umbellularia californica) in California; c. necrotic lesions on tanoak shoot in California; d. bleeding bark lesions on a tanoak stem in California; e. tanoak stem in California with multiple red-brown necrotic lesions of the inner bark; f. severe defoliation and mortality of a Japanese larch (Larix kaempferi) plantation in the UK; g. phloem lesion on a branch of a Japanese larch in the UK showing brown discoloration of older necrotic parts and a maroon-red advancing margin. — Photos: a, b, d: T. Jung; c, e: Y. Balci; f, g: A. Pérez-Sierra.

While the host list is extensive, the susceptibility and role of different hosts in disease development varies considerably and relatively few plant species are actually killed by P. ramorum. One important distinction is that between the ‘leaf or sporulation hosts’ and ‘canker hosts’ which are dead-end hosts due to the inability of P. ramorum to produce sporangia on infected bark (Garbelotto et al. 2003, Davidson et al. 2005, Rizzo et al. 2005, Grünwald et al. 2008). Several plant species like N. densiflorus fall into both categories. In the humid coastal forests of northern California and south-western Oregon, P. ramorum demonstrates the typical multicyclic infection pattern of Phytophthora diseases. The pathogen is infecting with its caducous sporangia and zoospores the leaves and young shoots of a wide range of herbaceous and woody species, causing necrotic lesions and shoot blight (Fig. 11b, c). On infected necrotic and symptomless tissues prolific numbers of sporangia are produced and dispersed via rain and wind splash onto other leaves, branches and stems (Rizzo et al. 2002, 2005, Grünwald et al. 2008, Denman et al. 2009a). Infectious propagules are produced readily on petioles and leaves in the crowns and are spread aerially as demonstrated by the isolations of P. ramorum from canopy drip baited in rainwater traps (Davidson et al. 2005, Hansen et al. 2012). Efficient aerial spread and infections occur within 10 m distance of an infected host (Davidson et al. 2005, Hansen et al. 2008), although the sporadic appearance of isolated disease outbreaks suggests that long-distance dispersal of sporangia with strong blowing winds and fog may sometimes incite new disease foci in distances of more than 4 km from infected trees (Peterson et al. 2015).

Foliar infections, in contrast to bark cankers, do not usually result in plant death, thus plant species that have susceptible foliage only are not eliminated, enabling continuous inoculum production (Garbelotto et al. 2017, Lione et al. 2017). Due to its common occurrence in coastal forests and the high sporulation capacity of P. ramorum on its leaves, California bay laurel is the main driver of inoculum build-up and, hence, the epidemic in California, whereas infected tanoak leaves are the most important source of inoculum in south-western Oregon (Davidson et al. 2005, Rizzo et al. 2002, 2005, Hansen et al. 2008, Peterson et al. 2015). The existence of genetically identical P. ramorum populations in forests separated by distances exceeding 50 km, strongly indicates long-distance spread of the pathogen via infested nursery stock and infested substrate adhering to boots and tyres (Davidson et al 2005, Mascheretti et al. 2008, Filipe et al. 2012, Grünwald et al. 2012a). Long-term survival and long-distance spread in infested soil particles is achieved with thick-walled chlamydospores produced abundantly in infected plant tissues (Werres et al. 2001, Rizzo et al. 2002, Shishkoff 2007, Grünwald et al. 2008). Phytophthora ramorum can also be isolated from soil and streams, but propagules in such ecological niches are not contributing to disease development (Peterson et al. 2014). On stems and branches of N. densiflorus, Q. agrifolia and other oak species, P. ramorum sporangia cause infections leading to bleeding cankers with red-brown lesions of the underlying phloem and cambium (Fig. 11d, e). Due to multiple cankers girdling large branches and the stem, affected trees die within a short time, often in considerable numbers (Fig. 11a).

Using data on host susceptibility, host species distribution and reproduction, dispersal, and climate suitability of P. ramorum, Meentemeyer et al. (2004) developed a rule-based model of P. ramorum establishment and spread risk in California plant communities. This model demonstrated high accuracy when spread risk predictions were compared to data about presence, absence and severity of the disease from field surveys. In 2017, citizen science – based SOD Blitz surveys documented in California a three-fold increase in infection rates following the ending of a long period of drought in 2015 (Meentemeyer et al. 2015, Anonymous 2017). This increase in disease incidence during the wet years 2016 and 2017 and the recovery of susceptible tree species during the preceding long-lasting drought are correlated with the El Niño-Southern Oscillation (ENSO) cycle, an ocean-atmosphere phenomenon which originates in the tropical Pacific (Ropelewski & Halpert 1987, 1989). This is highlighting the importance of climatic parameters in the development of disease epidemics by airborne Phytophthora pathogens like P. ramorum.

Two other airborne Phytophthora species, P. nemorosa and P. pseudosyringae, are widely distributed in forests in California and Oregon. Both species cause leaf necrosis on foliar hosts like California bay laurel and cankers on oaks and tanoaks indistinguishable from the symptoms caused by P. ramorum. However, cankers associated with P. nemorosa and P. pseudosyringae are less common, have a scattered distribution and much lower mortality levels compared to P. ramorum, possibly suggesting host-pathogen coevolution (Wickland et al. 2008, Hansen et al. 2012, Kozanitas et al. 2017). Results from a population genetic AFLP analysis supported this hypothesis for P. nemorosa while P. pseudosyringae appears to be of European origin (Linzer et al. 2009).

Although P. ramorum was detected in Europe in the early 1990s, its impact has long been restricted to Rhododendron spp., Viburnum spp. and other ornamentals in nurseries and amenity plantings (Werres et al. 2001, Ivors et al. 2006, Vercauteren et al. 2010, Jung et al. 2016). Using a climate matching model (CLIMEX) revised according to the Californian risk ranking model of Meentemeyer et al. (2004) to Europe, a high risk of P. ramorum infections has been predicted for the Atlantic regions along the western parts of the British islands, Portugal, Spain and North-western France (Anonymous 2007). In accordance with this prediction, P. ramorum has since 2003 been causing aerial bleeding lesions on individual trees of F. sylvatica, Aesculus hippocastanum and Q. rubra growing in close proximity to heavily infected R. ponticum foliage in the UK (Brasier et al. 2004, Denman et al. 2006, Brown & Brasier 2007, Webber 2008). In August 2009, in south-western England, extensive mortality on mature and juvenile Japanese larch (Larix kaempferi) was detected for the first time and found being associated with P. ramorum but not with infected Rhododendron foliage (Brasier & Webber 2010, Webber et al. 2010). The disease rapidly reached epidemic proportions and was soon named ‘Sudden Larch Death’ (SLD) (Brasier & Webber 2010). Larch trees (Larix spp.) are fast growing deciduous conifers from the family Pinaceae which are distributed in all cold-temperate and boreal zones of the northern hemisphere. In the UK, Japanese larch, European larch (L. decidua) and their hybrid (L. ×leptolepis) are all grown commercially for their durable timber with high mechanical strength and decay resistance. In 2010, the disease was also detected on Japanese larch in Scotland, Wales and Northern Ireland, and in 2011 P. ramorum was confirmed on European larch and on hybrid larch across the UK. This was the first record of P. ramorum causing lethal infection on a commercially important conifer species anywhere in the world. By the end of 2013, more than 3 million trees growing on over 10 000 hectares had been felled or were under notice to fell (Forest Research, unpubl. data). In Northern Ireland, it was recently demonstrated that the felling and removal of larch trees significantly reduces the inoculum of P. ramorum in the soil and successfully eradicates the pathogen from infested sites (O’Hanlon et al. 2017). SLD has a serious impact on the UK larch industry. Landowners suffer from significant losses through the destruction of immature crops, implementation of biosecurity measures and decreased timber values as the market is flooded with surplus supplies of felled larch (Harris 2014).

Initial symptoms of SLD on affected trees include purple or pale needle discolouration, wilting of short shoots, aborted buds, defoliation, dieback of branches or death of the entire crown (Fig. 11f). Crown symptoms are most pronounced in autumn. Resin bleeding can be observed on bark lesions of lateral shoots, branches and trunks of affected trees with brown discoloration and a deep pink to maroon-red margin of the underlying necrotic phloem (Fig. 11g) (Brasier & Webber 2010, Webber et al. 2010). On infected needles of all three larch species, P. ramorum produces very high numbers of 800 to almost 1 800 sporangia per cm² making larch the best of all sporulation hosts known to date (Harris & Webber 2016). This massive sporulation on the infected needles is driving multicyclic infections of needles and bark resulting in rapid and large-scale mortality of larch (Fig. 11f). In addition, sporangia from infected larch needles cause massive infection pressure on other tree species growing under-neath or adjacent to infected larch trees (Brasier & Webber 2010, Harris & Webber 2016). Underneath infected larch trees, P. ramorum infections have been detected on broadleaved woody species such as Betula pendula, C. sativa, F. sylvatica, Nothofagus spp. and R. ponticum, and on other conifers such as Abies procera, A. grandis, Picea sitchensis, P. menziesii and T. heterophylla (Brasier & Webber 2010, Webber et al. 2010, Harris & Webber 2016). Climate and weather play a key role in the distribution and intensity of the disease on larch.

Initially, apart from the UK, the Republic of Ireland had been the only other country where larch trees were suffering from P. ramorum infections. However, in 2017, P. ramorum was for the first time detected affecting Japanese larch in mainland Europe in Brittany (France) (http://ephytia.inra.fr/fr/C/24935/Forets-Phytophthora-ramorum).

Phytophthora ramorum resides, together with P. lateralis, P. foliorum and P. hibernalis, within phylogenetic Clade 8c (Werres et al. 2001, Grünwald et al. 2008, Yang et al. 2017). There are four known clonal lineages named after the continent of their first appearance as EU1 and EU2 from Europe and NA1 and NA2 from North America (Ivors et al. 2006, Grünwald et al. 2008, Van Poucke et al. 2012). All European isolates of the EU1 and EU2 lineages belong to the A1 mating type while the North American NA1 and NA2 lineages contain exclusively A2 isolates (Brasier & Kirk 2004, Werres & Kaminski 2005, Vercauteren et al. 2011). In interlineage pairing tests of A1 and A2 isolates the mating frequency is extremely low and the resulting oospores have aberrant genome sizes and unusually high abortion rates, suggesting the presence of reproductive barriers (Brasier & Kirk 2004, Boutet et al. 2010, Vercauteren et al. 2011, Franceschini et al. 2014). This is supported by the results of a coalescence analysis indicating that the EU1, NA1 and NA2 lineages are separated since 165 000–500 000 yr (Goss et al. 2009). The apparent lack of sexual reproduction explains the clonal structure of the P. ramorum populations in Europe and the USA. In North America, three of the four known clonal lineages of P. ramorum are currently recognised: NA1, NA2 and EU1. The NA1 lineage most likely arrived in California in the 1990s via infected nursery stock imported from an unknown exotic origin, and has since spread throughout California and southwest Oregon as primary driver of the SOD epidemic (Grünwald et al. 2012a). Interestingly, the Oregon outbreak could genetically not be linked to the Californian NA1 population and, apparently, originates from a separate introduction of infested nursery plants (Prospero et al. 2007, Mascheretti et al. 2008, Grünwald et al. 2012a). The NA2 lineage was most likely introduced to nurseries in the PNW and occurs only infrequently in Californian forests (Ivors et al. 2006, Goss et al. 2011, Grünwald et al. 2012a). The EU1 lineage was introduced from Europe to the PNW where it is thriving in ornamental nurseries and eventually spread to California (Goss et al. 2011, Grünwald et al. 2012a). In the UK, the majority of the isolates from larch belong to the widespread EU1 lineage, while the EU2 lineage occurs currently only in Northern Ireland and in a small area in south-western Scotland (Van Poucke et al. 2012). The EU2 lineage shows faster growth and tolerates higher temperatures than the EU1 lineage (Franceschini et al. 2014). In addition, the EU2 lineage is also significantly more aggressive to larch bark tissue than the EU1 lineage (Harris et al. 2015) and, therefore, is likely to kill affected trees more rapidly (King et al. 2015). In 2016, P. ramorum was detected in several streams running through diverse mountain forests in northern Vietnam. Extensive mating tests demonstrated that the Vietnamese population contained both mating types, which together with the absence of apparent leaf symptoms and bleeding stem lesions in these forests suggest potential endemism of P. ramorum to Southeast Asia (T. Jung, M. Horta Jung, C.M. Brasier unpubl. data).

Leaf and twig blight of Ilex aquifolium in Europe and North America

Native to Atlantic regions of Europe and to southern Europe and western Asia, English holly (Ilex aquifolium) is an important component of the understorey vegetation in temperate Fagaceae forests and in cool and humid mountain ecosystems in Mediterranean regions (Pignatti 1982). This species is also widely planted as an ornamental plant and in hedgerows across Europe, and it is grown extensively in the PNW, USA for the production of holly cuttings and young trees.

In 1954, a previously unknown Phytophthora species was consistently isolated from black leaf spots, twig blight, berry infections and limb and trunk cankers of English holly orchards in Oregon and later also Washington, which were previously attributed to ascomycete fungi like Diaporthe crustosa, Vialaea insculpta and Fusarium spp. (Buddenhagen & Young 1957). This new species was described as P. ilicis, and a detailed description of the disease aetiology was given by Buddenhagen & Young (1957). In severe cases, the whole crown became completely defoliated with leaf shedding starting from the lower branches. No root or collar infection of P. ilicis were reported and the pathogen has never been detected from river water (Hansen et al. 2017).

Thirty years later, P. ilicis was recovered from Ilex spp. in parks and gardens of the UK, where it caused infections along hedges, and also from symptomatic nursery stock (Strouts et al. 1989). The pathogen was considered introduced to the country, probably during the 20th century (Tubby & Webber 2010). More recently, the pathogen has been reported causing twig blight on ornamental I. aquifolium in Galicia, Spain (Pintos et al. 2012) and in Germany from nursery plants (https://gd.eppo.int/reporting/article-5866).

Based on these reports, the geographic distribution of P. ilicis seemed to be restricted to cool-temperate regions (Buddenhagen & Young 1957, Strouts et al. 1989, Pintos et al. 2012). However, a recent study demonstrated the widespread occurrence of P. ilicis on I. aquifolium in natural forests of the Tyrrhenian islands Corsica and Sardinia (Scanu et al. 2014b). The symptomatology matches previous descriptions in the USA and Europe, including severe defoliation of the whole crown (Fig. 12a) and bleeding cankers on the main stem and branches (Fig. 12b). Necrotic twig lesions are often observed around the axillary node (Fig. 12c, e) and where the petiole is inserted (Fig. 12f), most likely due to the accumulation of zoospores produced by sporangia that emerge through stomata on the leaf surface and by growth of the pathogen through the petiole (Scanu et al. 2014b). Black leaf spots occur in the early decline stages (Fig. 12g), starting from branches close to the ground. Necrotic twig lesions develop as cankers with brownish orange, suberized and cracking epidermal tissues during the dry season (Fig. 12d, e). In these tissues, P. ilicis forms oospores, which allow the pathogen to survive dry summer conditions and germinate in the following wet season. Having caducous sporangia and a low optimum temperature for growth of 20 °C, P. ilicis infections occur mainly during the cool rainy period, from October to May, while the disease is completely inactive during summer (Buddenhagen & Young 1957, Scanu et al. 2014b).

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Fig. 12

Disease symptoms caused by Phytophthora ilicis on Ilex aquifolium in mountain forests of the Mediterranean islands Corsica and Sardinia. a. Mature trees showing complete defoliation and severe dieback; b. bleeding stem canker; c. fresh twig lesion around an axillary node and dead infected leaves; d. inactive twig canker with cracking surface due to the production of brown suberised tissue during the dry season; e. necrotic twig lesion originating from the progression of P. ilicis from the infected leaf through the petiole into the twig; f. leaf necrosis and progression of P. ilicis through the petiole into the twig; g. black necrotic leaf spots indicating multiple fresh infections. — Photos: all B. Scanu.

Since all previous records of the species worldwide came from horticultural, parks, gardens and nurseries, the widespread distribution of P. ilicis in natural ecosystems of Corsica and Sardinia strongly indicates endemism of this pathogen in the Mediterranean basin (Scanu et al. 2014b, Hansen et al. 2017). This hypothesis is supported by the fact that two close relatives of P. ilicis, P. pseudosyringae and P. psychrophila, are most likely also native in Europe (Jung et al. 2002, 2003b, 2016, Linzer et al. 2009, Pérez-Sierra et al. 2013, Hansen et al. 2017).

The authors are grateful to the Czech Ministry for Education, Youth and Sports and the European Regional Development Fund for financing the Project Phytophthora Research Centre Reg. No. CZ.02.1.01/0.0/0.0/15_003/0000453.