Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands

Abstract

Most members of the oomycete genus Phytophthora are primary plant pathogens. Both soil- and airborne Phytophthora species are able to survive adverse environmental conditions with enduring resting structures, mainly sexual oospores, vegetative chlamydospores and hyphal aggregations. Soilborne Phytophthora species infect fine roots and the bark of suberized roots and the collar region with motile biflagellate zoospores released from sporangia during wet soil conditions. Airborne Phytophthora species infect leaves, shoots, fruits and bark of branches and stems with caducous sporangia produced during humid conditions on infected plant tissues and dispersed by rain and wind splash. During the past six decades, the number of previously unknown Phytophthora declines and diebacks of natural and semi-natural forests and woodlands has increased exponentially, and the vast majority of them are driven by introduced invasive Phytophthora species. Nurseries in Europe, North America and Australia show high infestation rates with a wide range of mostly exotic Phytophthora species. Planting of infested nursery stock has proven to be the main pathway of Phytophthora species between and within continents. This review provides insights into the history, distribution, aetiology, symptomatology, dynamics and impact of the most important canker, decline and dieback diseases caused by soil- and airborne Phytophthora species in forests and natural ecosystems of Europe, Australia and the Americas.

INTRODUCTION

The oomycete genus Phytophthora belongs to the Peronosporaceae, order Peronosporales, class Peronosporomycetes, kingdom Stramenipila (Dick 2001, Hulvey et al. 2010, Beakes et al. 2014, Thines & Choi 2016). Initially, based on phylogenetic analysis of ITS rDNA sequences from 50 Phytophthora species, the genus was structured in 10 phylogenetic clades (Cooke et al. 2000). Although increasing numbers of Phytophthora species and increasing numbers of nuclear and mitochondrial gene regions were used in subsequent phylogenetic studies, the basic structure of the genus remained unaltered (Martin & Tooley 2003, Kroon et al. 2004, 2012, Blair et al. 2008, Martin et al. 2014, Yang et al. 2017). However, recently the number of clades was expanded to 12 in order to accommodate the growing number of species in the P. quercina clade and the unique position of P. lilii (Rahman et al. 2015, Jung et al. 2017b). Several phylogenetic studies demonstrated that the genus Phytophthora is monophyletic with the 19 downy mildew genera residing within Phytophthora (Cooke et al. 2000, Kroon et al. 2004, Göker et al. 2007, Runge et al. 2011, Martin et al. 2014, Thines & Choi 2016). Recently, a closely related sister genus of Phytophthora, Nothophytophthora, which shares many phenotypic and ecological characters with Phytophthora, has been described from natural ecosystems in Asia, Europe and South America (Jung et al. 2017d).

Most Phytophthora (Greek for ‘plant destroyer’) species have a hemibiotrophic or necrotrophic lifestyle as primary plant pathogens, although for many aquatic Phytophthora species from phylogenetic Clades 6 and 9 a lifestyle as saprophytes and opportunistic necrotrophic pathogens seems likely (Erwin & Ribeiro 1996, Brasier et al. 2003, Jung et al. 2011, Nechwatal et al. 2013). In contrast, all c. 600 downy mildew species are host specific, obligate biotrophic plant pathogens (Göker et al. 2007, Runge et al. 2011, Beakes et al. 2012, Thines & Choi 2016). Phytophthora species are renowned as primary parasites on thousands of tree, shrub and crop species across the world. Depending on whether the lifecycle occurs mainly above- or below-ground a distinction is made between soilborne Phytophthora species causing fine root losses, root and collar rots and bleeding bark cankers, and airborne Phytophthora species causing leaf necrosis, shoot blights, fruit rots and also bleeding bark cankers (Erwin & Ribeiro 1996). However, several Phytophthora species have both a soil- and an airborne lifecycle. Phytophthora cactorum, for example, is causing root and collar rot in strawberries and a range of fruit and forest trees but can also infect the foliage and shoots of many ornamental plants and cause aerial bleeding cankers on European beech trees (Mircetich & Matheron 1983, Wilcox & Ellis 1989, Erwin & Ribeiro 1996, Jung 2009, Jung et al. 2016). In P. pseudosyringae the rate of sporangial caducity is highly variable between isolates enabling the pathogen to cause both fine root infections and aerial bleeding cankers on oaks, beech and other forest trees (Wickland et al. 2008, Jung et al. 2003b, 2013b, Jung 2009, Scanu & Webber 2016, Hansen et al. 2017).

It was estimated that, on a global scale, more than 66 % of all fine root diseases and more than 90 % of all collar rots of woody plants are caused by Phytophthora species (Tsao 1990). However, in many cases, abiotic factors or secondary pathogens instead of the primary Phytophthora pathogens are considered as the causal agents of disease. The reasons for such misidentifications are mainly based on the specific lifecycles of Phytophthora spp. Highly specific isolation methods are required in order to break dormancy of resting spores and exclude fungi and other oomycetes like Pythium or Phytopythium which are usually much faster growing than Phytophthora species (Ribeiro 1978, Tsao 1983, Erwin & Ribeiro 1996, Jung et al. 1996, De Cock et al. 2015). Phytophthora-specific isolation approaches include, amongst others, a wide range of specific baiting tests, Phytophthora-specific isolation media containing various antibiotics and fungicides, low or high incubation temperature depending on the Phytophthora species, leaching of polyphenols from necrotic bark samples, and drying and re-moistening of infested soil samples (Tsao 1983, 1990, Jeffers & Aldwinckle 1987, Erwin & Ribeiro 1996, Jung et al. 1996, 2013a, 2016, 2017c, Jung 2009). Another problem for Phytophthora isolations can be fluctuations of inoculum levels depending on the phase of the disease. When first symptoms become visible in the crown of a mature tree, the destruction of the fine root system is already in an advanced stage resulting in a continuous decrease of Phytophthora inoculum. As a consequence, a secondary disease process caused by high populations of secondary pathogenic and saprophytic fungi is masking the primary cause of the disease (Tsao 1990, Erwin & Ribeiro 1996, Jung et al. 1996). Similarly, isolation tests of Phytophthora species from bleeding bark lesions are only reliable at the active advancing lesion fronts whereas slightly older parts of the lesions are quickly colonised by secondary pathogenic fungi preventing the isolation of the primary Phytophthora pathogen (Erwin & Ribeiro 1996, Jung & Blaschke 2004, Jung 2009). In recent years, an array of highly sensitive, high-throughput, species-specific molecular detection methods have been developed, which facilitate the diagnosis of Phytophthora diseases significantly, and are particularly useful for routine screening of high numbers of samples for harmful and emerging Phytophthora pathogens (Schubert et al. 1999, Nechwatal et al. 2001, Schena et al. 2006, Martin et al. 2012, Scibetta et al. 2012, Sikora et al. 2012, Than et al. 2013, King et al. 2015, Schenck et al. 2016). Recent metagenomic approaches provide an efficient tool for large-scale surveys of Phytophthora diversity (Vettraino et al. 2012, Català et al. 2015, Sapkota & Nicolaisen 2015, Burgess et al. 2017).

Detailed descriptions and schematic illustrations of the lifecycles of airborne and soilborne Phytophthora species were given by several authors (Hickman 1958, Ribeiro 1978, Erwin & Ribeiro 1996, Jung 1998, Hansen et al. 2000, Agrios 2005, Grünwald et al. 2008). Both soil- and airborne Phytophthora species are able to survive unsuitable environmental conditions over several years with dormant resting structures (oospores, chlamydospores and hyphal aggregations) in the soil or in infected plant tissues. When environmental conditions become suitable (high moisture and temperature higher than the minimum temperature required by the respective Phytophthora species) the resting spores germinate by forming sporangia. In soilborne Phytophthora species, the sporangia release motile, biflagellate zoospores into the soil water which are then chemotactically attracted by a gradient of organic acids released from the elongation zone of young fine roots. In airborne species, the caducous sporangia are spread by wind and rain splash onto above-ground plant tissues where they either germinate directly or release zoospores. After penetrating the rhizodermis, exodermis or periderm of roots or the cuticle and epidermis of leaves, shoots and fruits Phytophthora grows as a hemibiotroph or necrotroph inter- and intracellular in the infected tissue with typical coralloid to irregular, non-septate hyphae. Nutrient depletion, competition by secondary antagonistic fungi or strong defence reactions by the host plant stimulate the production of resting structures. After decomposition of the necrotic tissue by saprophytes the resting spores are released into the soil, and the cycle starts again. Via the continuous production of sporangia on infected roots, leaves and fruits, Phytophthora pathogens can prolifically increase and disseminate their inoculum from initially very low levels during a relatively short time of favourable environmental conditions. Therefore, Phytophthora-induced fine root, leaf and fruit diseases are considered to be multicyclic (Ribeiro 1978, Erwin & Ribeiro 1996, Grünwald et al. 2008, Jung et al. 2013b). As a consequence of the root and bark damage caused by soilborne spp., the crowns of affected trees develop non-specific symptoms of drought and malnutrition, including increased crown transparency, sparse ramification and stunted growth of lateral shoots leading to whip-like branch structures and clustering of leaves at the end of branches, small-sized, often chlorotic foliage, wilting, dieback of branches, crown-dieback and eventually mortality (Erwin & Ribeiro 1996, Jung et al. 1996, 2000, 2013b, Jung 2009). However, in mature trees it can take decades of inoculum build-up and progressive destruction of the fine root system before the crowns begin to show visible symptoms (Ribeiro 1978, Tsao 1990, Erwin & Ribeiro 1996, Jung et al. 1996, 2000). Predisposing factors, such as waterlogging or planting of trees on sites not suitable for the species, as well as contributing factors which either reduce the vitality of the tree (e.g., extreme droughts or defoliations) or favour the pathogen (e.g., excess soil moisture following heavy rain, flooding or irrigation), can accelerate the disease process or make it possible in the first place (Davison 1988, Brasier et al. 1993, Marçais et al. 1993, Erwin & Ribeiro 1996, Jung et al. 1996, 2013b, Jung 2009). For European oak decline, a conceptual model was presented by Jönsson (2006) which included the complex interactions between soilborne Phytophthora species and various biotic and abiotic factors. Airborne Phytophthora diseases usually progress gradually upwards and in severe cases cause complete defoliation within a few months (Buddenhagen & Young 1957, Erwin & Ribeiro 1996, Durán et al. 2008). Extent and progress of soil- and airborne Phytophthora diseases are strongly depending on both long-term climatic and short-term weather conditions as demonstrated by the current declines and diebacks of oak and beech stands in Europe (Brasier et al. 1993, Brasier & Scott 1994, Jung et al. 1996, 2000, 2013b, Jung 2009, this review), the leaf fall disease of rubber in India and Malaysia (Agnihothrudu 1975, Erwin & Ribeiro 1996), the epidemics of P. ramorum on oaks and tanoaks in the western USA and on larch trees in the UK (Rizzo et al. 2002, 2005, Brasier et al. 2010, Grünwald et al. 2012a, Harris & Webber 2016, this review), and the needle cast and defoliation caused by P. pinifolia on Pinus radiata in Chile (Durán et al. 2008, this review).

In 1996, 50 Phytophthora species were known to science (Erwin & Ribeiro 1996). During the past two decades, more than 100 new Phytophthora species have been described or informally designated (Brasier 2009, Jung et al. 2011, 2017a, b, c, Hansen et al. 2012, Scanu et al. 2015, Yang et al. 2017, Burgess et al. 2018). This exponential increase has been caused by several factors:

• 1. more researchers have been studying Phytophthora diversity in natural ecosystems while research in the past had been focussed on agricultural crops. A conservative estimation predicted that there may be another 200–600 unknown Phytophthora species in natural ecosystems awaiting their detection (Brasier 2009);

• 2. phylogenetic analyses of nuclear and mitochondrial gene regions allow to discriminate complexes of morphologically similar but phylogenetically distinct species (Jung et al. 2003b, 2011, 2017b, c, Jung & Burgess 2009, Hong et al. 2009, 2011, Bezuidenhout et al. 2010, Rea et al. 2010, Ginetti et al. 2014, Henricot et al. 2014, Burgess et al. 2018);

• 3. the exponential increase in imports of living plants from overseas in combination with an outdated list-based plant biosecurity approach and notoriously understaffed plant protection services enables the continuous accidental introduction of exotic Phytophthora species (and other pests and pathogens) to Europe and other continents (Brasier 2008, Liebhold et al. 2012, Hantula et al. 2013, Santini et al. 2013, Eschen et al. 2015a, b, 2017, Jung et al. 2016); and

• 4. hybridisations between phylogenetically close Phytophthora species which due to geographic separation did not build up reproductive barriers and accidentally met after the introduction of one or both parents. Well-known examples of the latter are P. ×alni, P. ×cambivora, P. ×pelgrandis, P. ×serendipita and P. ×stagnum, all infecting woody plants, and undescribed hybrids in the complex of vegetable infecting Phytophthora species from Clade 8b (Brasier et al. 2004, Man in ‘t Veld et al. 2012, Bertier et al. 2013, Yang et al. 2014, Husson et al. 2015, Jung et al. 2017c).

A Europe-wide survey, conducted in almost 2 000 nursery stands of 730 nurseries and in 2 500 young forest, horticultural and ornamental plantings, demonstrated widespread Phytophthora infestations. More than 80 % of the nursery stands in more than 90 % of the tested nurseries, and 2/3 of the tested young plantings were infested with in total 68 different Phytophthora species, of which 44 were unknown to science before 1990 (Jung et al. 2016). Based on these results, a calculation suggested that across Europe between 1990 and 2010 approximately 680 000 new afforestations with a total area of almost 5 million hectares had been established with Phytophthora-infested nursery stock. In the same period, the area of potentially Phytophthora-infested re-forestations may have exceeded 17 million hectares (Jung et al. 2016). Apart from only a few potentially native Phytophthora species from Clades 3 and 6, the vast majority of these 68 Phytophthora taxa are considered alien invasive pathogens in Europe, based on an accumulating body of indirect evidence. These include high aggressiveness towards native European tree, crop and ornamental plant species, occurrence in healthy, undisturbed natural ecosystems in other continents, presence of both mating types of heterothallic Phytophthora species in natural ecosystems of other continents, low genetic variability of European Phytophthora populations, and close phylogenetic relatedness to non-native Phytophthora species (Jung et al. 2016). Also in Australia and the USA, Phytophthora infestations of nursery stock are common (Hardy & Sivasithamparam 1988, MacDonald et al. 1994, Davison et al. 2006, Schwingle et al. 2007, Yakabe et al. 2009, Bienapfl & Balci 2014, Parke et al. 2014, Yang et al. 2014, Simamora et al. 2015).

The potentially high number of unknown Phytophthora species and the unknown origin of many known aggressive Phytophthora species in combination with the high Phytophthora-infestation rates of nursery stock and the increasing complexity, intensity and volume of the international plant trade (Brasier 2008, Dehnen-Schmutz et al. 2010, Drew et al. 2010, Liebhold et al. 2012, Jung et al. 2016, Chapman et al. 2017, Eschen et al. 2017) pose a serious threat to the health and sustainability of natural ecosystems, managed forests and crop production systems on a global scale.

Before 1950, the only known forest diseases caused by Phytophthora pathogens were ink disease of chestnuts in Europe and the USA and littleleaf disease of pines in the USA (Crandall et al. 1945, Zak 1957, Tainter & Baker 1996). During the past six decades, the number of previously unknown Phytophthora declines and diebacks of forests and natural ecosystems and the number of described species and informally designated taxa of Phytophthora have increased exponentially (Fig. 1; Brasier 2009). Most of these diseases are driven by exotic Phytophthora species which remain unnoticed in their native environment and often were unknown to science prior to their introduction to other continents. However, in their new environments they became invasive and threatened a non-adapted flora which due to a lack of co-evolution contains a high number of susceptible plant species (Shearer & Tippett 1989, Marks & Smith 1991, Erwin & Ribeiro 1996, Jung et al. 2000, 2013b, 2016, Rizzo et al. 2002, Shearer et al. 2004, Brasier 2008, Grünwald et al. 2012a). This review provides insights into the history, distribution, aetiology, symptomatology, dynamics and impact of the most important canker, decline and dieback diseases caused by soil- and airborne Phytophthora species in forests and natural ecosystems of Europe, Australia and the Americas.

Fig. 1.

Accumulated number of important Phytophthora declines and diebacks of forests and natural ecosystems over time; 1 = ink disease of Castanea sativa in Europe (observation of first typical symptoms in 1838); 2 = ink disease of Castanea dentata in the USA (observation of first typical symptoms in 1824); 3 = decline of Fagus sylvatica in the UK; 4 = littleleaf disease of pines in the USA; 5 = decline and mortality of Chamaecyparis lawsoniana in the Pacific Northwest; 6 = jarrah dieback in Western Australia (WA; observation of first typical symptoms in the 1920s); 7 = ink disease of C. crenata and chestnut hybrids in Korea; 8 = eucalypt dieback in Victoria (observation of first typical symptoms in 1935); 9 = kauri dieback in New Zealand; 10 = Mediterranean oak decline; 11 = Alnus mortality in Europe; 12 = temperate European oak decline; 13 = decline of F. sylvatica in mainland Europe; 14 = Sudden Oak Death in California and Oregon; 15 = mortality of Austrocedrus chilensis in Argentina (observation of first typical symptoms in 1948); 16 = oak decline in the Eastern USA; 17 = needle cast and defoliation of Pinus radiata in Chile; 18 = dieback of Eucalyptus gomphocephala in WA; 19 = dieback of E. rudis in WA; 20 = Sudden Larch Death in the UK; 21 = dieback of Nothofagus spp. in the UK; 22 = mortality of Juniperus communis in the UK; 23 = red needle cast of P. radiata in New Zealand; 24 = leaf and twig blight of Ilex aqufolium in Corsica and Sardinia; 25 = dieback of Mediterranean maquis vegetation.

SOILBORNE PHYTOPHTHORA DISEASES IN FORESTS AND WOODLANDS

Ink disease of chestnuts worldwide

Ink disease, caused by Phytophthora species, is one of the most destructive diseases affecting Castanea sativa worldwide. In Europe, typical symptoms were first reported in Portugal in 1838 (Crandall et al. 1945, Crandall 1950) and since then it has become widespread across the continent with an increase in incidences during the last decades (Vannini & Vettraino 2001, Vettraino et al. 2005, Černý et al. 2008, Jung et al. 2013b, Tziros & Diamandis 2014). In the United States, ink disease was the main problem of C. dentata before the chestnut blight epidemic (Crandall et al. 1945, Crandall 1950). Ink disease symptoms in the crown are best observed during the vegetative growing season. The trees initially show small-sized and chlorotic foliage followed by increasing transparency, defoliation and dieback of the whole crown, eventually leading to extensive dieback and mortality of trees (Fig. 2a–d). Dry leaves and fruits often persist on dead trees over the winter. These symptoms are caused by extensive root losses and dark-brown and flame shaped necrosis in the inner bark developing from the main roots into the collar (Fig 2e–g). Blue to black exudates, oozing from the necrotic tissues through cracks in the bark, are often visible on the stem, collar and roots. The disease was named after the black exudates from necrotic roots staining the surrounding soil (Fig. 2e). Infected chestnut stumps can lose their ability to resprout due to the destruction of the entire root system. Ink disease also occurs on chestnut seedlings in nurseries and new plantations which usually show a rapid or gradual wilting (Jung et al. 2016).

Fig. 2.

Ink disease symptoms on Castanea sativa caused by Phytophthora spp. a. Extensive dieback and mortality caused by P. cinnamomi, P. ×cambivora and P. castanetorum in Portugal; b. patch dieback and mortality caused by P. ×cambivora in Portugal; c. chlorosis, microphylly, thinning, dieback and mortality of planted chestnut trees caused by P. cinnamomi in Chile; d. microphylly, severe thinning and dieback caused by P. cinnamomi and P. ×cambivora in Portugal; e. surface roots with bleeding lesions and black staining of surrounding soil caused by P. ×cambivora in Portugal; f, g. typical flame-shaped necrotic lesions of the inner bark caused by P. ×cambivora on the collar of a mature (f) and a young tree (g) in Italy. — Photos: a–e: T. Jung; f, g: B. Scanu.

The hybrid species P. ×cambivora has been the main species associated with ink disease in central and south-eastern Europe, while P. cinnamomi seems to be more widespread in Atlantic regions such as England and France and in the USA (Day 1938, Crandall et al. 1945, Crandall 1950, Vettraino et al. 2001, 2005, Martins et al. 2007, Černý et al. 2008, Jung et al. 2016). In Portugal, P. cinnamomi and P. ×cambivora often co-occur resulting in particularly high disease incidences and mortality rates (Fig. 1a, b) (Lopes-Pimentel 1946, 1947, T. Jung & M. Horta Jung unpubl. data). Due to its intolerance to low temperatures, the current distribution of P. cinnamomi in European forests is limited to areas with an average minimum soil temperature above 1.4 °C (Marçais et al. 2004, Vettraino et al. 2005). In accordance with the intensification of P. cinnamomi activity in Europe predicted by the CLIMEX model for increasing average temperatures (Brasier & Scott 1994, Burgess et al. 2017), P. cinnamomi is currently spreading in Italy to chestnut areas characterised by mild winters (Vettraino et al. 2005). Also in Chile, P. cinnamomi is currently threatening planted forests of C. sativa (Fig. 1c) (Jung et al. 2018). Several other Phytophthora species of minor impact were found associated with declining chestnuts in Europe, including P. cactorum, P. cryptogea, P. gonapodyides, P. megasperma, P. nicotianae, P. plurivora, P. pseudosyringae, P. sansomeana and P. syringae (Vettraino et al. 2005, Černý et al. 2008, Perlerou et al. 2010, Scanu et al. 2010, Jung et al. 2013b). The recently described P. castanetorum, a close relative of P. quercina, was isolated alongside other Phytophthora spp. from diseased chestnut trees in Italy and Portugal (Jung et al. 2017b). In Oregon, P. ×cambivora causes root rot, girdling basal stem cankers and mortality of golden chinquapin (Chrysolepis chrysophylla) which is closely related to the genus Castanea. The concentration of affected trees along roads suggests recent introduction and spread of the pathogen (Saavedra et al. 2007). In Japan and South Korea, P. castaneae (previously P. katsurae) was repeatedly found causing bleeding bark lesions and mortality of C. crenata and the chestnut hybrid C. crenata ×C. mollissima (Uchida 1967, Lee et al. 2009, Oh & Parke 2012). Phytophthora castaneae, together with P. cinnamomi, was also associated with bleeding bark lesions and mortality of Castanopsis carlesii in subtropical forests of Taiwan (Jung et al. 2017a).

Ink disease incidence is strictly related to climatic and site condition as well as human activities (Fonseca et al. 2004, Robin et al. 2006, Martins et al. 2007, Vannini et al. 2010). Heavy or continuous rain during the vegetative season, soil compaction and disturbance by tillage practices, physical restrictions to root expansion, poor soil fertility, vehicle movement along roads, and human recreational activities in forests are the main predisposing and contributing factors for disease development (Fonseca et al. 2004, Vannini et al. 2005, Martins et al. 2007). Planting of infested nursery stock and movement of contaminated substrates are the main pathways of short and long-distance inoculum dispersal (Jung et al. 2016). The existence of genetic variability in susceptibility to P. ×cambivora in C. sativa and resistance to P. cinnamomi in some clones of C. sativa and in many clones of the Euroasiatic chestnut hybrids C. crenata ×C. sativa and C. molissima ×C. sativa could provide the basis for a resistance screening programme necessary for a long-term management of ink disease in Europe (Robin et al. 2006, Miranda-Fontaíña et al. 2007, Costa et al. 2011, Santos et al. 2015, 2017a, b).

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).

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).

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).

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).

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).

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.

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.

Decline and dieback of European beech in Europe and the USA

European beech (Fagus sylvatica) is characterised by high shade tolerance and growth capacity, a wide climatic and geological amplitude ranging from atlantic to continental climate and from moderately dry to periodically wet soils with pH ranging from < 3 to > 7. Due to its high competitiveness, European beech would naturally dominate more than 50 % of the forests at hilly to mountainous sites in Western and Central Europe and in mountain areas of Eastern and Southern Europe (Walentowski et al. 2004, Ellenberg & Leuschner 2010).

Since the mid 1990s, forests and amenity stands of European beech across the entire natural range in Europe are increasingly threatened by a severe decline and dieback (Motta et al. 2003, Jung et al. 2003b, 2005, 2009, 2013b, Cacciola et al. 2005, Hartmann et al. 2006, Orlikowski et al. 2006, Brown & Brasier 2007, Munda et al. 2007, Vettraino et al. 2008, Černý et. al. 2009, Jung 2009, Schmitz et al. 2009, Stępniewska & Dłuszyński 2010, Telfer et al. 2015). Also in the USA and in Chile, European beech plantations experience a similar decline and mortality (Jung et al. 2005, 2018, Nelson 2009, Weiland et al. 2010). The symptoms are typical for Phytophthora diseases and comprise small-sized and often yellowish foliage, thinning and dieback of crowns, extensive losses of fine roots and lateral roots, collar rot, and aerial bleeding cankers along the stem up to the canopy (Fig. 9). A local epidemic with similar symptoms was recorded in the 1930s in the UK and could be associated to Phytophthora infections (Day 1938). Severe destructions of the fine root system are common in affected forests and lead to a slow chronic decline, whereas bleeding collar rot and aerial bark cankers have a scattered or patchy distribution and usually cause rapid mortality (Jung et al. 2005, 2009, 2013b).

Fig. 9.

Decline and dieback symptoms caused by Phytophthora spp. on Fagus sylvatica. a. Scattered mortality and patch dieback and chlorosis (arrow) due to root and collar rot and aerial bleeding cankers caused by Phytophthora plurivora and P. ×cambivora in a mountain forest in the Bavarian Alps. Germany; b. severe dieback and mortality due to root and collar rot caused by P. ×cambivora in Austria; c. chlorosis, microphylly, thinning and dieback due to root losses caused by P. cactorum and P. plurivora in Bavaria; d. small woody roots with extensive losses of lateral roots and fine roots caused by P. cactorum and P. plurivora in Bavaria; e. bleeding collar rot lesion and aerial bleeding canker caused by P. ×cambivora in a mountain forest in the Bavarian Alps; f. bleeding collar rot lesion caused by P. ×cambivora in a Swedish forest; g. collar rot lesion with orange- to dark-brown exudates on the outer bark and flame-shaped lesion front in the inner bark caused by P. plurivora in Sweden. — Photos: all T. Jung.

Several independent surveys in 17 European countries showed that more than 80 % of the almost 300 beech stands growing on a wide range of geological substrates with soil pH ranging from 3.3 to 7.8 were infested with in total 15 Phytophthora taxa. Most widespread were P. ×cambivora, P. plurivora and, in urban situations, also P. cactorum. Phytophthora ×cambivora was frequently encountered on acidic heavy soils, while P. plurivora was more common in calcaric soils. Other species had a scattered distribution like P. chlamydospora, P. europaea, P. gonapodyides, P. pseudosyringae, P. psychrophila, P. quercina, P. syringae, P. tubulina and P. uliginosa, or were restricted to areas with mild winters like P. cinnamomi in Portugal and the UK (Jung & Blaschke 1996, Balci & Halmschlager 2003a, Jung et al. 2003b, 2005, 2013b, 2017b, Motta et al. 2003, Cacciola et al. 2005, Hartmann et al. 2006, Orlikowski et al. 2006, Brown & Brasier 2007, Munda et al. 2007, Vettraino et al. 2008, Černý et. al. 2009, Jung 2009, Schmitz et al. 2009, Stępniewska & Dłuszyński 2010, Telfer et al. 2015). The airborne pathogens P. kernoviae and P. ramorum exclusively occurred in the UK where the humid climate allows the continuous production of caducous sporangia on infected foliage of adjacent Rhododendron ponticum plants and their aerial dispersal onto neighbouring beech stems where they cause extensive bleeding lesions (Brasier et al. 2005, Brown & Brasier 2007, Jung et al. 2013b). In the eastern USA, P. cactorum, P. plurivora and its close relative P. pini (previously P. citricola I) are causing root and collar rot and mortality on mature F. sylvatica in amenity plantings (Jung et al. 2005, Weiland et al. 2010). Phytophthora cactorum, P. ×cambivora, P. kernoviae, P. plurivora and P. ramorum proved to be highly aggressive to the bark and root systems of both mature and young beech trees (Fleischmann et al. 2002, Brasier & Jung 2003, Jung et. al. 2003b, 2017b, Brown & Brasier 2007, Vettraino et al. 2008, Weiland et al. 2010). In Europe, all five species are considered as exotic invasive pathogens (Jung 2009, Jung & Burgess 2009, Jung et al. 2013b, 2016).

Detailed investigations in Germany, Austria and the UK showed that aerial bleeding cankers on stems of mature beech trees are in most cases not following the classical pattern of the phenomenon ‘Beech Bark Disease’. The latter is considered as complex interaction of predisposing drought stress, colonisation of the bark by the scale insect Cryptococcus fagisuga, infection of the colonised bark by the secondary parasite Neonectria coccinea and, eventually, invasion of the stem by wood decay fungi (Parker 1974, Lonsdale & Wainhouse 1987). However, this aetiology is apparently restricted to young pole-stage stands (Lonsdale & Wainhouse 1987) while in mature stands Phytophthora pathogens are the primary disease agents (Jung et al. 2005, 2013b, Brown & Brasier 2007, Jung 2009). Both soilborne Phytophthora species, in particular P. plurivora, P. ×cambivora and P. gonapodyides, and the airborne P. cactorum, P. kernoviae, P. pseudosyringae and P. ramorum can infect stem bark and shoots of beech via rain- or wind-splash dispersal of sporangia or progression from root lesions into the collar (Jung et al. 2005, 2013b, Brown & Brasier 2007, Jung 2009, Nechwatal et al. 2011). After establishment in the bark, Phytophthora pathogens can spread non-symptomatically in the xylem causing multiple aerial cankers along the stem (Brown & Brasier 2007).

The onset of the Phytophthora epidemics in Austria, Germany and Sweden was triggered by the succession of continuously wet conditions during the growing season followed by extreme drought in the same or the following year (Jung 2009, Jung et al. 2013b, T. Jung, T. Corcobado & T. Cech unpubl., T. Jung & J. Witzell unpubl. data).

A large-scale survey of nursery stands and young plantings of F. sylvatica in Europe revealed that 80 % of the nursery stands and almost 100 % of the plantings tested were infested with 9 and 11 Phytophthora species, respectively (Jung et al. 2016). Most common were P. ×cambivora, P. plurivora and P. cactorum demonstrating the importance of the nursery pathway for the spread of this devastating disease into beech stands.

AIRBORNE PHYTOPHTHORA DISEASES OF FORESTS AND WOODLANDS

Dieback and mortality of Nothofagus species in the UK and Chile

The genus Nothofagus is native to the Southern Hemisphere, where it constitutes an important component of temperate rainforests and mountainous forests (Kirkpatrick & DellaSala 2011, Tecklin et al. 2011) and represents an important economic and silvicultural resource (Heenan & Smissen 2013). Since the early 1900s, several Nothofagus species have been planted in the UK due to their fast growth and high wood quality (Danby 1991, Webber et al. 2011). Apart from very occasional infections by P. ramorum (Webber 2008), no other pests and pathogens have been recorded on Nothofagus. However, in 2009 severe dieback and mortality of Nothofagus trees, associated with bleeding cankers on stems and main branches, were reported in the UK (Scanu et al. 2012). Due to the similarity to aerial cankers caused by P. ramorum on F. sylvatica trees in the UK (Brown & Brasier 2007) this pathogen was initially thought to be the causal agent of this new disease outbreak. However, isolations from necrotic bark tissues revealed the presence of a homothallic Phytophthora species that was subsequently identified as P. pseudosyringae (Scanu & Webber 2016).

Nothofagus obliqua and N. alpina are the main species affected in the UK. Both species are affected by severe dieback and mortality of mature and young trees (Fig. 10a–c). At early stages, trees show symptoms of crown thinning, wilting and branch dieback (Fig. 10b, c), which are often associated with abundant proliferation of epicormic shoots on stems and branches. These symptoms are caused by up to 2 m long bleeding bark lesions on the main stem (Fig. 10d). Necrotic lesions often progress deep into the xylem (Fig. 10e) resulting in multiple bleeding aerial lesions along the stem and in branches, which may girdle the trunk and branches entirely, causing branch and crown dieback and wilting foliage. Up to 60 discrete lesions can be observed on a single tree and these can reach 16 m above ground level (Scanu & Webber 2016). In the canopy, shoot blight and necrosis on small branches, twigs and leaves are common (Fig. 10f–i). During dry conditions, lesion growth on small branches and twigs ceases, resulting in sunken cankers with cracking bark (Fig. 10f) and necrotic underlying xylem tissues. Although the pathogen was detected in rhizosphere soil samples, symptoms of root infection are largely absent (Scanu & Webber 2016).

Fig. 10.

Disease symptoms caused by Phytophthora pseudosyringae on Nothofagus spp. in the UK. a, b. Severe dieback and mortality of N. obliqua and N. alpina in mixed plantations in the UK; c. N. obliqua trees showing severe thinning, wilting and dieback of the crown and recent mortality; d. large, aerial bleeding canker with red-brown flame-shaped phloem lesion on the main stem of N. obliqua; e. deep xylem lesion on N. obliqua; f. sunken canker with cracking bark on a young N. alpina twig; g, h. N. obliqua twigs with dark necrotic bark lesions and orange-brown discoloration of the underlying necrotic phloem tissue (h); i. N. obliqua leaves with necrotic lesions resulting from aerial infections. — Photos: all B. Scanu.

Field observations and the high sporulation rate of P. pseudosyringae on Nothofagus foliage strongly indicate that aerial bark infections occur directly through penetration of intact bark with caducous sporangia produced on infected foliage and dispersed by wind and rain (Scanu & Webber 2016). At infected sites, aerial lesions are often observed on other host plants, including F. sylvatica and Vaccinium myrtillus (Beales et al. 2009, Denman et al. 2009b), most probably due to massive airborne inoculum coming from infected overstorey Nothofagus trees (Scanu & Webber 2016). Phytophthora pseudosyringae is characterised by having partial caducity of sporangia ranging from 10 to 90 % (Jung et al. 2003b). This enables the pathogen to be aerially dispersed and cause foliar and bark infections, as well as being a soil, water and root inhabitant. Previously in Europe, P. pseudosyringae was shown to be mainly involved in root and collar infections of alder, beech, chestnut and oak trees (Jung et al. 2003b, Cacciola et al. 2005, Denman et al. 2009b, Jung 2009, Scanu et al. 2010). However, in the humid forests of northern California and south-western Oregon, P. pseudosyringae has a similar lifestyle as P. ramorum, causing foliar infections on Umbellularia californica and aerial bark cankers on Notholithocarpus densiflorus and Quercus agrifolia (Wickland et al. 2008).

More recently, P. pseudosyringae has been detected associated with dieback and partial defoliation of N. obliqua in its natural range in central southern Chile (Fajardo et al. 2017). Main symptoms were similar to those reported from Nothofagus in Britain, with typical bleeding stem lesions and crown dieback, but twig and foliage infection were absent (Fajardo et al. 2017). Disease incidence seems to be lower in Chile compared to the UK (10 % vs up to 70 %). In inoculation trials under the bark of mature logs, and in zoospore inoculation trials of detached leaves, N. obliqua was highly susceptible to P. pseudosyringae isolates from the UK, while N. alpina was less susceptible (Scanu & Webber 2016). In both stem inoculation and soil infestation trials, isolates of P. pseudosyringae from Chile were highly aggressive to stems and roots of both N. obliqua and N. alpina (Fajardo et al. 2017). Nothofagus dombeyi was also shown to be susceptible to P. pseudosyringae in artificial inoculation experiments, although no natural infection has been reported so far (Fajardo et al. 2017).

The severity of P. pseudosyringae outbreaks on Nothofagus in the UK and its recent detection in native Nothofagus in South America, and the presence of P. pseudosyringae in the international nursery trade (Jung et al. 2016) highlight the risk of further spread of the pathogen into the Gondwanan Nothofagus forests in Chile, New Zealand and Tasmania. Previous records of Phytophthora spp. infecting Nothofagus spp. in their countries of origin include P. cinnamomi, associated with severe dieback and mortality of Nothofagus trees in the southern highlands of Papua New Guinea (Arentz 1983), and P. citrophthora and P. nicotianae, causing dieback of N. macrocarpa seedlings in a nursery in Chile (Valencia et al. 2011). Many natural forest ecosystems in the temperate regions of the southern Hemisphere, in particular in Chile, Argentina, New Guinea, Tasmania and New Zealand, are climatically favourable for inoculum production, spread and infections by airborne Phytophthora species (Scanu & Webber 2016), which may pose a serious risk to these native forests.

‘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.

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).

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).

Needle cast and defoliation of Pinus radiata in Chile

Pinus radiata (Monterey pine) has a scattered limited natural distribution along the Pacific coast of central California and Baja Californica in Mexico (Rogers 2004, Rogers et al. 2006). On a global scale, it is one of the most common plantation trees in Mediterranean regions, in particular in Australia, Chile, New Zealand, South Africa and Spain (Rogers et al. 2006, Richardson et al. 2007). In 2004, a needle cast and defoliation disease, named ‘Daño foliar del pino’, was reported for the first time from 70 ha coastal P. radiata plantations in the Arauco province of central Chile (Durán et al. 2008). By 2006, the affected area had increased to almost 60 000 ha, with varying levels of damage. In 2007 the disease area decreased to less than 2 000 ha and has remained at that level (Durán et al. 2008, 2010, Ahumada et al. 2013). Currently, the disease occurs between Constitución and Valdivia, exclusively in areas with high humidity during most of the year due to their proximity to the Pacific coast (Ahumada et al. 2013). ‘Daño foliar del pino’, one of the most important foliar diseases affecting Monterrey pine, is caused by the previously unknown P. pinifolia which was the first Phytophthora species reported to cause needle infections on Pinus spp. (Durán et al. 2008). The pathogen has only been found in Chile where it exclusively affects P. radiata (Durán et al. 2008, 2010, Ahumada et al. 2012, 2013). The considerable variation of disease incidences and affected areas over the years is related to the El Niño cycle and has been explained using favourable days calculated with the Hyre model. With 141 d, the peak of favourable conditions was recorded in 2006, which correlated with the highest disease incidence recorded until now, while each of the following years had less than 60 favourable days coinciding with low incidence of the disease (Ahumada et al. 2013). Due to the lack of preformed sporangial pedicels, P. pinifolia is not a true airborne species. However, as in P. constricta in Western Australia, sporangia break off with relative ease enabling an aerial lifestyle (Durán et al. 2008, Rea et al. 2011). Phytophthora pinifolia survives non-favourable dry conditions in infected needles on the ground. After onset of humid conditions in spring or early winter, the pathogen infects needles on lower branches via sporangia formed on infected needles on the ground and spreading via rain and wind splash onto healthy needles. If humid conditions persist, P. pinifolia produces new sporangia on infected needles causing multicyclic infections and moving gradually up in the canopy (Fig. 13a–f) (Durán et al. 2008). In seedlings and trees younger than three years old, total defoliation occurs frequently resulting in plant death. In addition, the pathogen can progress in the shoots and the stem causing girdling lesions, leading to quick death of the trees. In trees older than three years the infection progress and the symptoms are similar but bark lesions are not girdling the stem and mortality is rare (Ahumada et al. 2012). On trees older than six years, the disease can affect all needles except those less than one year old (Fig. 13c–f). Needle infection is usually characterized by the presence of a black band (translucent areas) and a pale-green to greyish discolouration (Fig. 13g) turning brown at the end of spring (Ahumada et al. 2013). Long-dead needles have a pale greyish colour (Fig. 13e). The symptoms are generally best observed during the rainy season, from May to November, but heavy rain at the end of summer can induce an early appearance of symptoms.

Fig. 13.

Needle cast and defoliation caused by Phytophthora pinifolia on Pinus radiata in the Valdivian region of Chile. a. Mature plantation with extensive red-brown discolouration of infected foliage; b. mature plantation with largely defoliated crowns due to massive needle infections by P. pinifolia; c. extensive defoliation of mature crowns resulting from the progressive browning and shedding of infected needles which started at the lowest branches and spared only the youngest needles; d. recently killed tree with severe defoliation; e. dying young tree in a dense stand with greyish discolouration of infected needles; f. upper crown typically showing transparency due to shedding of older infected needles, pale-green discolouration of freshly infected needles and uninfected, dark-green young needles; g. needle showing typical black bands (translucent areas; arrow) within the pale-green to greyish area of infected tissue. — Photos: a–f: T. Jung; g: A. Durán.

Since 2008, another needle disease, named Red Needle Cast, with similar symptoms and disease aetiology has been reported in P. radiata plantations in New Zealand. However, in this case the airborne Phytophthora species P. pluvialis from Clade 3 was shown to be the causal agent (Dick et al. 2014).

Phytophthora pinifolia belongs to Clade 6, which contains mostly aquatic species and opportunistic soil- and waterborne pathogens of woody plants (Jung et al. 2011, Burgess et al. 2018). Currently, the only known foliage-infecting member of Clade 6 is P. pinifolia (Durán et al. 2008, Burgess et al. 2018). An amplified fragment length polymorphism (AFLP) analysis demonstrated a clonal population structure of P. pinifolia in Chile indicating a single clonal introduction of the pathogen (Durán et al. 2010). A character shared between P. pinifolia and many other Clade 6 species is the sterile breeding system (Durán et al. 2008) which is responsible for maintaining the clonal population structure of P. pinifolia in Chile and reduces the ability of the pathogen to adapt to changes in P. radiata resistance.

An integrated management approach for the needle disease caused by P. pinifolia includes the selection of tolerant P. radiata clones, species replacement in high-risk areas and fungicide application (Ahumada et al. 2013). Using a disease model, areas with high, medium and low risk of disease development have been identified. In high-risk areas, P. radiata plantations are being replaced by alternative species, in particular Eucalyptus spp., while in medium-risk areas tolerant P. radiata clones are planted. Alternatively, fungicides like mefenoxam and metalaxyl (phenylamides) and the fungi-static potassium phophite have proven suitable for disease control, reducing symptoms by up to 90 % and plant mortality to less than 5 % (Ahumada et al. 2013). Fungicides are mainly applied in one- or two-years old plantations to reduce the heavy infection pressure.

Despite the significantly reduced disease incidence since the peak in 2006 and the development of successful management strategies (Ahumada et al. 2013), P. pinifolia continues to be an important threat to the P. radiata industry worldwide. In Chile, the introduction of new genotypes or the appearance of mutations in the existing clonal population (Durán et al. 2010) could produce new pathotypes able to overcome the current genetic resistance or pesticide effectiveness, as has been reported for other Phytophthora spp. (Gisi & Cohen 1996, Goodwin et al. 1996). Since the origin of P. pinifolia is still unknown, the pathogen also poses a serious threat to natural populations of P. radiata and other pine species in their native ranges (Widmer & Dodge 2015).

CONCLUDING REMARKS

Concern about Phytophthora pathogens in natural and forest ecosystems began in the 1960s in Australia, where the invasive P. cinnamomi has been spreading for more than one century threatening some of the world’s richest plant communities in Western Australia and Victoria (Podger et al. 1965, Podger & Newhook 1971, Shearer & Tippett 1989, Marks & Smith 1991, Shearer et al. 2004, Hardham 2005). During the past 60 years, the detection of previously unknown Phytophthora diseases in natural and semi-natural ecosystems has increased exponentially (Fig. 1). Since the 1990s, the finding of P. cinnamomi and many other soilborne Phytophthora spp. involved in the oak declines in southern and central Europe (Brasier et al. 1993, Jung et al. 1996, 2000), the discovery of the airborne P. ramorum causing ‘Sudden Oak Death’ in the western USA (Rizzo et al. 2002), the resurgence of chestnut ink disease and the widespread alder mortality across Europe due to the P. ×alni hybrid complex (Vettraino et al. 2001, Brasier et al. 2004, Jung & Blaschke 2004, Husson et al. 2015), have raised the interest by many plant pathologists for this important diseases causing genus. Consequently, in 1999 the International Union of Forestry Research Organizations (IUFRO) Working Party 7.02.09 ‘Phytophthora Diseases of Forest Trees’ (https://www.iufro.org/science/divisions/division-7/70000/70200/70209/) was established which has subsequently become the main platform for researchers studying all aspects of Phytophthora pathogens and the diseases they are causing in forests and other natural woody ecosystems. This review provides the first comprehensive overview of the history, distribution, aetiology, symptomatology, dynamics and impact for the main diseases caused by Phytophthora species on woody host plants in natural ecosystems on a global scale, hence giving a baseline from which to identify and compare similar disorders in the future.

Most of the diseases presented in this review are caused by exotic invasive Phytophthora pathogens with a clear link between the ‘plants-for-planting’ pathway and subsequent impacts in natural ecosystems (Jules et al. 2002, Jung & Blaschke 2004, Brasier 2008, Chadfield & Pautasso 2012, Jung et al. 2016). There is an accumulating body of indirect and partly also direct evidences that P. cinnamomi, P. lateralis, P. plurivora and P. ramorum originate from Southeast and eastern Asia (Shearer & Tippett 1989, Brasier et al. 1993, 2010, 2012, Chang et al. 1996, Hansen et al. 2000, 2012, Jung et al. 2000, 2016, 2017a, b, c, Rizzo et al. 2002, Shearer et al. 2004, Goss et al. 2009, Hardham 2005, Jung 2009, Jung & Burgess 2009, Brasier & Webber 2010, Webber et al. 2010, 2012, Franceschini et al. 2014, Arentz 2017). Also for P. agathidicida in New Zealand P. austrocedri in Argentina and the UK, P. acerina and P. cactorum in Europe, P. elongata in Australia, P. kernoviae in the UK, P. multivora in Australia and Europe, P. pinifolia in Chile, P. ×cambivora in Europe and North America, and for the parents of P. ×alni, i.e., P. ×multiformis and P. uniformis, the high aggressiveness to native woody species, low genetic variability of pathogen populations and co-existence with healthy native vegetation in other continents, respectively, indicate exotic origin (Crandall et al. 1945, Jung et al. 2000, 2002, 2003b, 2016, 2017b, c, Brasier & Kirk 2001, Vettraino et al. 2001, 2005, Jung & Blaschke 2004, 2006, Brasier et al. 2005, Greslebin et al. 2007, 2010, Saavedra et al. 2007, Beever et al. 2009, Jung 2009, Scott et al. 2009, Durán et al. 2010, Rea et al. 2010, Green et al. 2013, Vélez et al. 2013, Ginetti et al. 2014, Henricot et al. 2014, Scott & Williams 2014, Weir et al. 2015). Recently, several studies identified the international plant trade as the main pathway for the introduction of invasive forest diseases into North America and Europe (Liebhold et al. 2012, Santini et al. 2013, Chapman et al. 2017). Accordingly, Jung et al. (2016) demonstrated almost ubiquitous infestations of nurseries and young plantings across Europe with a wide range of Phytophthora species. This study and similar results from Australia and the USA (Hardy & Sivasithamparam 1988, MacDonald et al. 1994, Davison et al. 2006, Schwingle et al. 2007, Yakabe et al. 2009, Bienapfl & Balci 2014, Parke et al. 2014, Yang et al. 2014, Simamora et al. 2015) leave no doubt that plant production facilities are the major source of Phytophthora spread into the wider environment. Due to the application of fungicides or fungistatic chemicals, nursery plants infected by Phytophthora spp. often appear visually symptomless and, hence, pass unnoticed through the phytosanitary controls acting as ‘inoculum reservoirs’ in the nurseries and resulting in accidental Phytophthora spread (Pérez-Sierra & Jung 2013, Bienapfl & Balci 2014, Migliorini et al. 2015, Jung et al. 2016). Another danger, arising from the intensified international nursery trade, is the accidental encounter of closely related allopatric Phytophthora species, which due to geographic separation have not build up reproductive barriers and readily hybridise. Such interspecific hybrids may differ in host range and virulence from the parental species as demonstrated by P. ×alni (Brasier & Kirk 2001, Brasier et al. 2004, Husson et al. 2015), thus making predictions about the potential effects of an ongoing invasion even more difficult.

Once introduced to a new suitable environment, a Phytophthora pathogen will inevitably spread, actively via root-to-root infection and with motile zoospores in soil and surface water and passively through the movement of infested soil or infested water. Therefore, the control and management of Phytophthora pathogens and diseases are mainly focused on the prevention of their introduction, and on slowing down their spread once they are introduced. Prevention of primary Phytophthora introductions can be achieved by testing nursery stock using classical isolation methods, sensitive high-throughput molecular detection methods and temporary outplanting in quarantine-facilities. When managing natural ecosystems, the only cost-effective and ethically acceptable approach is the use of plants from certified pathogen-free production facilities (Parke & Grünwald 2012). Preventative system approaches for the production of Phytophthora-free nursery stock in nurseries have been repeatedly suggested by the scientific community to the regulators (Brasier 2008, Parke & Grünwald 2012, Jung et al. 2016). Parke & Grünwald (2012) highlighted the importance to define the hazards for Phytophthora contamination within a nursery and employ best management practices to reduce the risk of infestation for all pathogens and pests. This systems approach demonstrated to improve the control of pathogens and pests in nursery production and prevent the movement of exotic pathogens or pests in the nursery trade. Training nursery growers to identify early symptoms minimizes risks. Thermo-sterilisation of potting media and the filtering or disinfestation of irrigation water also helps to reduce the risk of Phytophthora introductions (Stewart-Wade 2011, Pérez-Sierra & Jung 2013).

The current approach to prevent the movement of pests and pathogens via the nursery trade is mainly based on international plant biosecurity protocols, including certification, endpoint inspections for list-based pests and pathogens, and quarantine measures. However, these methods have largely failed to prevent the arrival of invasive and exotic pathogens (Brasier 2008, Liebhold et al. 2012, Santini et al. 2013, Jung et al. 2016, Eschen et al. 2017). For plants moving through the nursery trade, a phytosanitary certificate, indicating the production facility is free of regulated Phytophthora spp., is mandatory. In the absence of a certificate, a visual inspection of plants has to be performed (Brasier 2008). However, visual inspections of symptoms are costly and often ineffective, especially since they are based on lists of known harmful species despite the fact that the majority of introduced aggressive Phytophthora species were unknown to science before they caused serious damages in their new environments. In addition, the regular use of fungicides and fungistatic chemicals in nurseries is decreasing disease incidences without eliminating the Phytophthora pathogens. This practice is masking the presence of the pathogens, which are surviving with enduring resting structures, resulting in plantings of visually healthy nursery stock that develop disease symptoms in subsequent years (Jung & Blaschke 2004, Brasier 2008, Pérez-Sierra & Jung 2013, Migliorini et al. 2015, Jung et al. 2016). In a critical review, Brasier (2008) underlined the need for a scientific revision of the international plant biosecurity protocols. The scientific community recommended replacing the list-based species-by-species regulation approach by a more efficient pathway regulation approach based on pathway risk analyses and combined with a strict quarantine system (Keller et al. 2007, Jung et al. 2016).

In natural ecosystems, there are a number of possible strategies to mitigate the impact of Phytophthora species. Phosphite (phosphoric acid) applications are the most common and most successful method for controling dieback of trees and forests resulting from extensive fine root losses caused by Phytophthora infections and slowing down disease spread (Shearer & Tippett 1989, Fernandez-Escobar et al. 1999, Pilbeam et al. 2000, Hardy et al. 2001, Tynan et al. 2001, Smith 2003, Shearer & Fairman 2007, Barrett & Rathbone 2018). Several early studies demonstrated that treatments with phosphite indirectly control Phytophthora diseases by acting on host physiology and on host-pathogen interactions (Fenn & Coffey 1984, Guest & Grant 1991), but the exact mode of action had long been a mystery. Recent studies have elucidated that phosphite induces systemic activity against Phytophthora spp. in plants mainly by priming plants for a rapid and intense response to infection via up-regulation of several defence-related genes in the jasmonate, salicylic acid, ethylene and auxin signalling pathways (Eshragi et al. 2011, 2014a, Dalio et al. 2014). However, it was suggested that phosphite-induced resistance to P. cinnamomi in susceptible Arabidopsis thaliana ecotypes and natural resistance of tolerant ecotypes may be triggered through different signaling pathways (Eshragi et al. 2014b). Generally, phosphite appears to be more effective for soilborne than for airborne Phytophthora diseases, although phosphite applications can significantly reduce canker size in tanoaks infected by P. ramorum (Garbelotto et al. 2009). The efficacy of the treatments is higher when plants are physiologically active (Pilbeam et al. 2000). Phosphite can be applied by injecting a water dilution directly into the trees (Fernandez-Escobar et al. 1999) or through foliar applications, with or without surfactants, although not all evergreen plants with waxy leaves absorb phosphite (Shearer & Fairman 2007). Application rates vary depending on the application mode, the host plants and the region (Hardy et al. 2001, Smith 2003, Shearer et al. 2006, Garbelotto et al. 2009). Overdosing commonly leads to phytotoxicity (Thao & Yamakawa 2009). Although phosphite applications can slow down disease spread and protect individual plants (Hardy et al. 2001), they cannot completely halt Phytophthora spread and disease progression in native vegetation (Shearer et al. 2004). Silvicultural and site-specific management measures, like soil amendments and reducing host plant density, have a proven effect in reducing disease incidence and/or slowing down further disease spread (Erwin & Ribeiro 1996, Pérez-Ramos et al. 2008). Thinning should be more intensive in those areas predicted to be more easily infested, such as areas downhill or downstream from outbreaks. If multiple plant species are present at an infested site, selective thinning of the best sporulation host will have the most significant impact on disease spread (Serrano et al. 2010, Fichtner et al. 2011). Containment and eradication of soilborne Phytophthora species from spot infestations in natural ecosystems can be achieved by a combination of robust treatments including host plant destruction with herbicides, application of selective fungicides, fumigation with strong biocides like metham-sodium, and mechanical root barriers (Dunstan et al. 2009). However, due to the lack of legal authorisations and for environmental reasons, such treatments are not realistic options for the control of Phytophthora diseases in natural areas of most countries.

On the long-term, increasing the genetic resistance of susceptible tree species against Phytophthora spp. seems to be the most promising sustainable management approach for stabilising declining natural ecosystems and reintroducing susceptible tree species at sites with high disease impact. The successful long-term resistance screening programme of C. lawsoniana concerning P. lateralis, can serve as a role model for other Phytophthora diseases (Hansen et al. 2000, 2011, Oh et al. 2006, Sniezko et al. 2006, 2011). Also for the pathosystems Castanea / P. cinnamomi and P. ×cambivora, A. glutinosa / P. ×alni, and E. marginata / P. cinnamomi the natural occurrence of genetic resistance has been demonstrated (Jung & Blaschke 2006, Robin et al. 2006, Miranda-Fontaíña et al. 2007, Costa et al. 2011, Santos et al. 2015, 2017a, b, Shearer et al. 2014, Chandelier et al. 2016).

Recently, the potential origin of several invasive Phytophthora species, including P. cinnamomi, P. lateralis, P. plurivora and P. ramorum, in Southeast Asia has been unravelled (Brasier et al. 2010, 2012, Huai et al. 2013, Jung et al. 2017a, c, T. Jung, C.M. Brasier, M. Horta Jung unpubl. data). Comparative phenotypic and molecular studies of the invasive and native populations of these pathogens will advance our understanding of their adaptation and evolution after introduction to new environments. In addition, future studies of the behaviour and ecological role of these pathogens and their interaction with the native vegetation in their centres of origin will help to elucidate the factors that shaped their outstanding invasiveness. This knowledge will help improving management concepts for the diseases these pathogens are causing. Moreover, tolerant or resistant species from tree genera affected by these pathogens in other continents may be found in the centres of origin which could be used in resistance screening programmes. Finally, natural antagonists which may be used as biological control agents in invasive situations, may be detected in the future.

Whether and how the projected future changes in temperature and precipitation patterns will affect the spread and activity of Phytophthora pathogens on the global and the regional scales remains unknown. However, using the CLIMEX model a significant increase in the activity of P. cinnamomi and the area suitable for this pathogen has been proposed (Brasier & Scott 1994, Brasier 1996, Burgess et al. 2017). Due to the known interaction between Phytophthora-caused fine root losses and droughts, and the multicyclic spread of Phytophthora zoospores and sporangia during persisting humid conditions, rising temperatures, in particular during winter, and increased summer droughts alternating with periods of unseasonal heavy rain, predicted by several models and extrapolations of climatic trends of the 20th century (Schönwiese et al. 1994, Rapp & Schönwiese 1995, Houghton et al. 1996, Watson et al. 1996, 1998, Pachauri & Reisinger 2007, Battles et al. 2008, Giannakopoulos et al. 2009, Ozturk et al. 2015), will most likely intensify root and collar rot incidences. This will further destabilise Phytophthora-infested natural ecosystems. Therefore, effective plant biosecurity protocols to prevent further introductions and spread of Phytophthora pathogens, management concepts and control measures to mitigate the impact of invasive Phytophthora diseases in natural ecosystems, and resistance screening programmes are urgently required.