An Overview of Phytophthora Species on Woody Plants in Sweden and Other Nordic Countries

The genus Phytophthora, with 326 species in 12 phylogenetic clades currently known, includes many economically important pathogens of woody plants. Different Phytophthora species often possess a hemibiotrophic or necrotrophic lifestyle, have either a broad or narrow host range, can cause a variety of disease symptoms (root rot, damping-off, bleeding stem cankers, or blight of foliage), and occur in different growing environments (nurseries, urban and agricultural areas, or forests). Here, we summarize the available knowledge on the occurrence, host range, symptoms of damage, and aggressiveness of different Phytophthora species associated with woody plants in Nordic countries with a special emphasis on Sweden. We evaluate the potential risks of Phytophthora species to different woody plants in this geographical area and emphasize the increasing threats associated with continued introduction of invasive Phytophthora species.


Introduction
The genus Phytophthora, which includes fungus-like microorganisms, also known as water molds, belongs to the family Peronosporaceae and phylum Oomycota in the Stramenopila kingdom [1][2][3][4]. Initially, the classification of Phytophthora species was based on morphological characters (e.g., sporangia, homothallism, and configuration of antheridia), showing the presence of six groups [5]. However, homology and homoplasty among different Phytophthora species showed a high plasticity of the morphological features and their often inseparability [6][7][8][9]. Since the 2000s, the number of described Phytophthora species increased by over 180 species, which was primarily due to the use of novel molecular techniques, reaching a total of 326 species distributed in 12 phylogenetic clades [10]. Consequently, the taxonomy of the genus Phytophthora shifted from the morphology-based methods towards the development of molecular markers for multilocus phylogenies [11][12][13][14][15]. For example, phylogenies of Phytophthora species were constructed using an internal transcribed spacer (ITS) region [11], four nuclear and mitochondrial genes [16], or seven nuclear markers [17]. A more recent study advanced the Phytophthora phylogeny by including more than 180 species and by creating ancestral phylogeny reconstructions on the sporangial papillation [18]. These studies allow researchers to better understand the evolution of the genus Phytophthora and to link molecular phylogenies and individual morphological and physiological traits.
There are several techniques available to detect and identify Phytophthora species. A classical detection method is based on the cultivation of Phytophthora species on different nutrient media favoring the development of morphological features, which can be used in taxonomical classifications. Several molecular methods have also been developed to impeding the establishment of some Phytophthora species [102,103]. Additionally, the primacy of the Phytophthora species as causal agents of woody plant diseases might often be misinterpreted due to their specific lifecycles, which require specific detection methods, and the time of sampling, as inoculum levels often depend on the phase of the disease [3].
In this review, we summarize the available knowledge on Phytophthora species associated with woody plants in Sweden and other Nordic countries; the threat that they may pose in different environments; and their origin, host range, symptoms of damage, pathways of introduction, and geographic spread. Using this information, we evaluate the potential risks associated with Phytophthora species to different woody plants under Nordic conditions and demonstrate that their presence poses a potential threat for further spread within and between neighboring countries. We also would like to raise awareness about the risks associated with the continued introduction of invasive Phytophthora species via imported plant materials and other means. Despite the management strategies of forest pathogens in Nordic countries, disease control efforts can be hampered, owing to a lack of knowledge on how serious the threat by Phytophthora species may be to local woody plants in different environments.

Searching for Information
The occurrence of Phytophthora species in Sweden and in other Nordic countries and their current status was identified by searching both existing public databases and publications included in the Web of Science and Mendeley databases. All the databases were accessed between October 2022 and February 2023. We confined our searches to Phytophthora reports in the Web of Science and Mendeley using different combinations of keywords "Phytophthora", "Sweden", "Norway", "Denmark", "Finland", and "oomycetes". Grey literature was limited to published information about Phytophthora spp. in Sweden. The following public sources were used to extract country-level distribution data for Phytophthora species: Forest Phythophtoras of the World; IDphy: molecular and morphological identification of Phytophthora based on the types; Invasive Species Compendium CABI; EPPO Global Database; SLU Skogskada; identification of common Phytophthora species using a Lucid Key; Phytophthora Research Center. The SLU Artdatabanken (2021) was used to assess the risk of invasiveness of Phytophthora species in Sweden (https://doi.org/10.15468/j43wfc) (accessed on 24 February 2023).
Only Phytophthora species associated with woody plants in Sweden were considered, and results of this analysis are summarized in Table 1.
In Sweden, six Phytophthora species (P. × alni, P. cactorum, P. cambivora, P. gonapodyides, P. plurivora, and P. quercina) were found to be associated with different types of damage on woody plants, and nine Phytophthora species (P. cinnamomi, P. citrophthora, P. cryptogea, P. ramorum, P. pini, P. pseudosyringae, P. rosacearum, P. syringae, and Elongisporangium undulatum) were detected on woody ornamentals. P. × alni, P. lacustris, P. plurivora, and P. megasperma were discovered in rivers/streams or other water sources. During the period of 1954 to 1958, a number of fungi that occurred at a high frequency on dying seedlings were isolated mainly from diseased seedlings from forest nurseries in central Sweden. Phytophthora cactorum was isolated from forest tree seedlings together with other pathogens Fusarium orthoceras, F. solani, F. culmorum, F. oxysporum, Pythium intermedium, and P. debaryanum. The first report about the detection of Phytophthora in Sweden was in 1961 [108]. The period between 1999 and 2006 was devoted to research on oak decline in Sweden, including studies on Phytophthora [110,118,120]. Since 2010, damage caused by Phytophthora has been discovered in recreational forests, parks, and urban settings around the Skåne county [109,121]. In 2012, quarantined species P. ramorum was reported several times on imported Rhododendron sp. [122], however, there are no reports of P. ramorum infecting trees in Sweden. More recently (2016-2018), extensive studies on Phytophthora were conducted across Sweden to evaluate the distribution, risk, and potential threat that new invasive Phytophthora species may pose to Swedish forests, cities, and landscapes [105,123]. Several Phytophthora species were also reported from Christmas tree plantations [113]. The occurrence of Phytophthora species on woody plants in Denmark, Finland, and Norway is shown in Table 2.
Symptoms: canker, collar rot, and dieback of alders Aggressiveness: Phytophthora disease of alder is now widespread in Europe in the riparian ecosystems where alder commonly grows. In Europe, surveys and modeling show that the risk of infection is higher in warmer, slow-moving waters, and in fine-textured soils, especially clay loams. Although the disease is usually observed along river systems, it has been found in sites far from riverbanks or other water courses, e.g., in orchard shelter belts and in new woodland plantings. This suggests that alder trees were already infected prior to planting [3]. P. × alni is an aggressive pathogen as, e.g., inoculations of mycelia culture on one-year-old seedlings of A. glutinosa and B. pendula showed the development of lesions in 89% and 67% of seedlings, respectively [124]. Finland Rhododendron sp. [137] a Previously Phytophthora uniformis; b Previously belonged to P. citricola complex.
Occurrence: In Sweden, the first report of the P. alni complex was from nurseries and alder-planted areas in the southwest in the 1990s [104]. In 2006 and 2010, it was discovered on A. incana at the Klarälven river in the city of Karlstad. A comprehensive study on the Phytophthora alni complex in Sweden was carried out between 2013 and 2018 to investigate the pathways of introduction and the spread of the two subspecies, alni and uniformis [103,138]. Both species were associated with Phytophthora bleeding cankers on 93% of declining A. glutinosa and some A. incana trees along the riverbanks, and within sampling plots connected to river swamps or ponds ( Figure 1a) [103,138]. It was considered that both P. alni subsp. alni and P. alni subsp. uniformis are invasive species that arrived in Sweden with plant material imported to forest nurseries, and that these species may further spread into natural ecosystems. P. alni subsp. uniformis was widespread throughout the country, whereas P. alni subsp. alni was only discovered in the southern and coastal part of Sweden [103,138]. P. alni subsp. alni is one of the most aggressive Phytophthora species [139], however, it is more sensitive to cold winters [140]. It was concluded that southern Sweden could be the northernmost distribution limit of P. × alni, however, there is a possible risk of its migration northwards due to climate change [138,141]. Due to the poor genetic potential of alder trees to resist P alni subsp. alni, alder decline is expected to increase in Sweden in the future [123]. In Finland, P. alni subsp. uniformis (identified as Phytophthora cf. uniformis) was found, for the first time, to cause dark stem lesions on A. glutinosa seedlings in 2015 [124]. In Denmark, P. alni subsp. uniformis (identified as Phytophthora uniformis) was isolated for the first time from symptomatic trees of A. glutinosa in 2016 [125]. Aggressiveness: P. cactorum is unequivocally a serious pathogen of a wide range of plant species. Despite its broad geographic distribution and host range, P. cactorum has similar symptomatology with other species of Phytophthora. Therefore, it is difficult to ascribe specific damage to P. cactorum and evaluate the extent of its damage to forest trees. There are several reports of noticeable "outbreaks" on Fagus and Betula [143], however, it appears that there is a considerable host specificity among strains of this pathogen. Swedish isolates of P. cactorum together with P. cambivora and P. plurivora were used for inoculation of common conifer and broadleaf tree species in Sweden (Pinus sylvestris, Picea abies, Larix × eurolepis, Betula pendula, Quercus robur, Fagus sylvatica, Populus trichocarpa, and Tilia cordata) to determine their relative susceptibility to root pathogens [144]. All the
Symptoms: root, collar, and crown rot on many species; brown-reddish stem lesions; slow decline or rapid dieback, depending on age and location of infections; root rot of nursery plants. For example, on woody plants, such as Malus domestica, P. cactorum is causing crown and root rot; on Betula spp., it causes stem lesions; and on rhododendron, it causes root rot and dieback symptoms [142].
Aggressiveness: P. cactorum is unequivocally a serious pathogen of a wide range of plant species. Despite its broad geographic distribution and host range, P. cactorum has similar symptomatology with other species of Phytophthora. Therefore, it is difficult to ascribe specific damage to P. cactorum and evaluate the extent of its damage to forest trees. There are several reports of noticeable "outbreaks" on Fagus and Betula [143], however, it appears that there is a considerable host specificity among strains of this pathogen. Swedish isolates of P. cactorum together with P. cambivora and P. plurivora were used for inoculation of common conifer and broadleaf tree species in Sweden (Pinus sylvestris, Picea abies, Larix × eurolepis, Betula pendula, Quercus robur, Fagus sylvatica, Populus trichocarpa, and Tilia cordata) to determine their relative susceptibility to root pathogens [144]. All the tested Phytophthora species caused stem lesions of varying lengths on different host trees, except for species in the Pinaceae family, which had low susceptibility to the tested Phytophthora spp. Two-year-old bare-root seedlings of B. pendula, Q. robur, F. sylvatica, and P. sylvestris appeared to be susceptible to P. cactorum infection [144]. Inoculation trials in Finland using a Danish isolate, which was isolated from B. pendula in 2009, revealed that P. cactorum caused relatively small lesions on Rhododendron sp. and P. abies, moderate lesions on B. pendula, and no infections on Q. robur or P. sylvestris [129]. In an in vitro study using twomonth-old B. pendula, roots inoculated with P. cactorum often showed dark discolorations, loss of fine roots, and decreased branching [126], even though discolorations are not a specific symptom of Phytophthora infections [127]. The symptoms of the aboveground parts included reduced height growth, lower chlorophyll fluorescence, significantly longer dark or brown discolorations in the stems, and a higher proportion of brownish and wilting leaves [126]. Furthermore, inoculation trials on three-month-old B. pendula and A. glutinosa seedlings showed that P. cactorum was able to kill 40% of the B. pendula seedlings, but caused only small lesions on 40% of A. glutinosa seedlings [128]. However, in the inoculation trials, P. cactorum was found to cause low-to-moderate symptoms on Rhododendron sp. and P. abies, and no symptoms on P. sylvestris [129]. P. cactorum was also able to cause lesions on non-wounded B. pendula seedlings [145]. In stem inoculation trials, Orlikowski et al. [134] showed that A. glutinosa, B. pendula, and Prunus padus were highly susceptible to P. cactorum. Acer saccharinum, Corylus avellana, Q. robur, Rubus caesius, Sorbus aucuparia, and Tilia cordata were moderately susceptible, while Sambucus nigra and Sorbus aucuparia were not susceptible. Interestingly, P. cactorum can be detected in B. pendula seven years after outplanting, however, at this stage, the effect of stem lesions on seedling mortality or on the number of leader shoots is limited [146]. Bunyaviruses were shown to significantly reduce hyphal growth and the production of sporangia and their size, but not the pathogenicity of P. cactorum [147].
Occurrence: In Sweden, P. cactorum was first recognized as one of the root parasites causing damping-off disease in forest nurseries in 1961 [108]. Since the beginning of the 1990s, the oak population has been declining in Sweden [148], and in 2003, P. cactorum was found to be associated with oak decline in southern Sweden [110]. Later, P. cactorum was isolated from the diseased F. sylvatica in the city of Malmö and Stora Köpinge municipality in 2016 [109]. Recently, P. cactorum was detected on F. sylvatica and Q. robur in forest nurseries (close to the rivers Säveån, Kävlingeå, and Ätran) (composing 26.3% of all detected Phytophthora spp.), in urban F. sylvatica forests (near the river Lagan) (15%), and in natural forests affecting F. sylvatica (near the river Ronnebyån), A. alba, and P. abies (near the river Ätran) (30%) [105]. In Finland, P. cactorum was found for the first time in necrotic stem lesions of B. pendula seedlings in forest nurseries in 1991 [127] and in stem lesions of A. glutinosa seedlings in 1995 [128]. It was also detected on symptomatic Rhododendron sp. seedlings during surveys that were carried out between 2004 and 2010 [129]. Irrigation water used in Finnish forest nurseries was shown to be the possible source of P. cactorum inoculum [149]. The Finnish isolates of P. cactorum were shown to have a 17.5 • C optimal growth temperature [135], i.e., much lower than the 25−30 • C reported in other studies [150,151], and that these isolates survived −5 • C temperatures on agar medium for up to 14 days [135]. The observations above suggest that Nordic isolates of P. cactorum can be better adapted to local conditions and, in the future, may pose a threat to B. pendula seedlings in forest nurseries and reforestations.
Symptoms: canker, collar and root rot, bleeding cankers Aggressiveness: P. cambivora is an invasive pathogen that survives and spreads in different environments. Its ability to survive as a saprotroph in the soil and to produce oospores (resting structures) increases its invasiveness. It was described as a causal agent of ink disease on chestnut trees [152][153][154]. The infection causes root destruction, which leads to leaf chlorosis and wilting in the canopies. Depending on environmental conditions, the disease may lead to a quick or to a progressive dieback of infected trees [152,155]. Inoculation tests on Abies seedlings also showed the ability of P. cambivora to infect and cause characteristic canker symptoms [130].
Occurrence: In Sweden, the first detection of P. cambivora was in association with oak health deterioration [110]. It was found together with P. cactorum in soil samples in one of ten surveyed forest stands. Later, P. cambivora was detected in soil samples collected near F. sylvatica trees with bleeding stem cankers in Bokskogen near the city of Malmö (Figure 1b) [109]. Nowadays, P. cambivora is present in nurseries, urban areas, and natural forests, and is mainly associated with F. sylvatica decline and bleeding cankers on the stems [105]. Inoculation of the stems showed that the Swedish isolate of P. cambivora is highly pathogenic to F. sylvatica, B. pendula, Tilia cordata, Q. robur, and Populus trichocarpa. P. trichocorpa is a non-native tree species in Sweden but it is important for biomass production. Therefore, the establishment of new P. trichocarpa plantations for energy should take place using clones more tolerant to Phytophthora infections [144]. In Norway, P. cambivora was detected for the first time on a 15-year-old Abies procera in 2004 [130]. The symptoms included cankers on the stems up to 1.5 m above the ground and dieback of the basal branches. There were 25% of trees that were already dead or dying. Infections of P. cambivora on F. sylvatica were observed for the first time in 2011, resulting in bleeding cankers [131]. The infected trees were in the areas of Larvik and Ås, which represent the northern limit of F. sylvatica distribution, showing that a northern location is not a limiting factor for the spread and infection by P. cambivora. The infected trees had a circumference between 40 and 310 cm, and the majority of the cankers were at the height of 0.1−2 m above the ground. Additional symptoms included crown dieback, chlorotic foliage, epicormic shoots, and cracked bark. The infection frequency in some areas around Larvik was up to 4.9% in 2012, but it was up to 9.2% in Ås in 2014 [131]. In addition to P. cambivora, P. plurivora and P. gonapodyides were detected in the water near the diseased trees in Larvik, and both species proved to be pathogenic on F. sylvativa. Today, P. cambivora can be considered an established species in different environments. To limit its spread, monitoring should take place in nurseries and on seedlings used for outplanting [81].
Symptoms: root rot, heart rot, wilt; causes ink disease of chestnut in conjunction with Phytophthora cambivora.
Aggressiveness: It is currently the most important Phytophthora pathogen of forest trees, and it is also destructive to woody ornamentals, especially rhododendrons and other Ericaceae, and orchard crops, including avocado. It is now widespread, owing to the international trade of plants, and continues to be destructive in the forests of Australia, Mediterranean countries, Mexico, and the SE United States, and is of increasing concern in the forests and wildlands of western North America. With the changing climate, P. cinnamomi is expected to expand its range and cause more damage, particularly in Europe and North America.
Occurrence: In Sweden, P. cinnamomi was detected in the rhizosphere soil of Rhododendron luteum 'Whitethroat' and Stewartia pseudocamellia growing in the same nursery, thereby representing the first record of this pathogen in a commercial stock of ornamental plants in the country [112].
Symptoms: root rot, stem necrosis, canker, fruit rot, twig blight, seedling blight Aggressiveness: P. citrophthora causes brown rot disease of citrus and is an economically important pathogen of citrus crops. It can also cause a dieback of rhododendron and other ornamental plants.
Occurrence: In Sweden, P. citrophthora was found in a nursery of Rhododendron catawbiense in 2018 [105]. In Norway, it was detected on Chamaecyparis lawsoniana [132].
Symptoms: damping-off, foot rot, stem rot, leaf rot, wilt. Aggressiveness: P. cryptogea is primarily a soil-borne plant pathogen in the temperate regions, but it also exists in nature (fresh water) as a saprotroph. It is most active at temperatures between 10 • C and 20 • C [55]. It is a serious plant pathogen in many countries, causing great damage to ornamentals produced in nurseries, greenhouses, and hydroponics. P. cryptogea is an aggressive soil-borne pathogen of fir species, which are produced as Christmas trees [156,157].
Occurrence: In Sweden, P. cryptogea was detected in soil samples associated with symptomatic F. sylvatica trees in a nursery (near the river Ätran) and in an urban forest (near the river Alsterån) [105]. It was also found in soil samples in Christmas tree plantations and, together with P. megasperma, demonstrated a high aggressiveness to P. abies and A. nordmanniana trees [113].
Symptoms: stem bleeding cankers, root rot Aggressiveness: P. gonapodyides is considered as a weak parasite with saprophytic abilities usually associated with aquatic environments, such as rivers, riparian areas, and wetlands [55]. However, some isolates of P. gonapodyides can be highly virulent [134,158]. Their aggressiveness appears to be stimulated by prolonged root flooding and cool soil conditions. P. gonapodyides can hinder seed germination and cause root rot and stem lesions in Q. robur and Q. ilex [159,160].
Occurrence: In Sweden, the first report of P. gonapodyides was in 2016, when the pathogen was isolated from characteristic bleeding cankers on F. sylvatica trees growing in Pildamms Park in the city of Malmö (Figure 1c) [114]. It was suggested that recent changes in local climatic conditions, such as high summer precipitation coupled with mild winter temperatures, could favor the multicyclic spread of P. gonapodyides via zoospores and/or that the increased average age of F. sylvatica stands contributed to their higher susceptibility [114]. P. gonapodyides was also reported in a nursery (Lagan area) in association with F. sylvatica seedlings [105]. In Denmark, P. gonapodyides was recovered from rainwater ponding in an old declining F. excelsior stand [134].
Phytophthora inundata Clade 6a Key woody hosts: Aesculus hippocastanum, Olea sp., Salix sp., Vitis sp. Symptoms: root and collar rot of trees or shrubs in wet or flooded areas Aggressiveness: P. inundata is responsible for wilting and the root rot of olive trees [161]. It can also act as an opportunistic, albeit aggressive root pathogen. On A. nordmanniana, it caused poorly developed roots and brown to reddish discoloration under the bark at the stem base and downwards. The foliage exhibited drought symptoms, with leaves that were pale green, yellow, or brown [132].
Occurrence: There are no reports from Sweden. In Norway, P. inundata and P. megasperma were reported from Christmas tree plantations of A. nordmanniana and A. lasiocarpa in 2004, respectively [132]. Approx. 70% of A. nordmanniana and 25% of A. lasiocarpa were symptomatic. As the site was grassland for decades with no history of Christmas tree cultivation, it was suggested that the disease followed imported transplants [132].
Aggressiveness: It is primarily a root-rotting organism, causing the most serious losses on fruit and broadleaf trees. It appears to be restricted to more temperate regions of the world, however, its oospores can survive for up to 5 years, either free in the soil or in host tissue [162]. Prolonged wet conditions and heavy clay soils and soil impaction layers, which allow the maintenance of high soil water content, are often needed for the development of disease epidemics by P. megasperma [163].
Occurrence: In Sweden, P. megasperma was isolated from roots of a symptomatic P. abies seedling [113]. In Norway, P. megasperma was reported in association with A. lasiocarpa [132]. Both species P. cryptogea and P. megasperma may become problematic for Christmas tree and bough production, especially in saturated soils, which favor disease development.
Phytophthora pini Clade 2c Key woody hosts: Pinaceae Symptoms: root rot, canker Aggressiveness: There is only limited information about this species. It can cause root rot and rapid mortality of olive trees [164]. Inoculations of P. abies seedlings using both wound-mycelia and zoospore suspension showed that after seven days, P. pini caused 100% disease incidence and a high frequency of severe symptoms [135].
Occurrence: In Sweden, P. pini was reported in commercial nurseries (near rivers of Säveån and Mölndalsån) in association with R. catawbiense [105]. In Finland, it was also detected on Rhododendron sp. [129].
Symptoms: stem cankers, collar and root rot, dieback. P. plurivora can cause wilting and discoloration of current year shoots (on P. abies seedlings), bark necroses, fine root losses, and dieback on at least 45 woody host species [129,135].
Aggressiveness: P. plurivora is a highly aggressive plant pathogen, which has a worldwide distribution and a high diversity of hosts. P. plurivora is a hemibiotrophic organism that possesses the ability to infect living tissues and to continue its life cycle on dead tissues. In inoculation trials, P. plurivora was able to cause relatively large lesions or, in many cases, stem girdling on Rhododendron sp., B. pendula, A. incana, A. glutinosa, and P. abies, showing a high virulence on several woody plants and especially on P. abies as compared to other Phytophthora spp. tested [129]. The disease incidence on P. abies was also shown to be dependent on a particular isolate and inoculation method, as there were 83.3−100% disease incidence using wound inoculation with living mycelia and 0−77.8% using zoospores [135]. In P. abies shoot tissues, P. plurivora can grow both inter-and intracellularly, which is largely in the vascular tissues [135]. Pinus sylvestris and Q. robur showed no symptoms after four weeks of P. plurivora inoculation [129,137]; however, in other studies, this pathogen caused extensive bark lesions on Q. robur after a longer time [165]. In stem inoculation trials, Orlikowski et al. [134] showed that A. saccharinum, A. glutinosa, B. pendula, C. avellana, P. padus, R. caesius, and S. nigra were highly susceptible to P. plurivora, while Q. robur, S. aucuparia, and T. cordata were moderately susceptible. In addition to stem inoculations, soil infestation trials may also be needed to examine the susceptibility of fine roots of different tree species to P. plurivora and other Phytophthora spp. [129].
Occurrence: In Sweden, the earliest report of P. plurivora was from alder trees in Asslebyn (Bengtsfors locality) in Sept 2012 [105], even though the species was likely found during surveys near the city of Nyköping [103]. In 2016, P. plurivora was detected in soil samples and bleeding stem lesions of F. sylvatica in the city of Malmö (Figure 1c) [109]. It is one of the most abundantly detected Phytophthora species in natural forests and urban areas with declining and symptomatic F. sylvatica and Q. robur trees (Figure 1d) [105]. P. plurivora was also found to be highly virulent on F. sylvatica and Q. robur seedlings, causing large lesions, thus, it should be considered as a high-risk species to Swedish forests with a potential to severely destabilize the broadleaf forest ecosystems [114]. P. plurivora was also reported from Denmark and Norway as a disease agent of several deciduous tree species [125,133,166]. In Norway, P. plurivora was reported on F. sylvatica in a park in Oslo and in Ålesund [131]. Interestingly, the infection process for some F. sylvatica trees was rather fast and took only two years before the tree was dead. In Finland, surveys in 2005 on symptomatic Rhododendron sp. resulted in the detection of P. plurivora (originally identified as P. inflata) [129,137].
Phytophthora pseudosyringae Clade 3a Key woody hosts: Quercus spp., Fagus sylvatica, Alnus glutinosa, Carpinus betulus Symptoms: root and collar rot, stem bleeding cankers Aggressiveness: It is an aggressive pathogen on several broadleaf tree species. Occurrence: In Sweden, P. pseudosyringae was reported causing basal cankers and dieback on horse chestnut in June 2014 in Sankt Jörgens Park in the city of Gothenburg [117].
Phytophthora quercina Clade 3b Key woody hosts: Quercus spp. Symptoms: rot of fine roots, overall oak decline Aggressiveness: P. quercina is often associated with other Phytophthora spp. [148], shows adaptation to different site conditions and soil pH, and has a high host specificity i.e., a high aggressiveness to different oak species [150,160]. P. quercina is also well-adapted to temporary dry conditions, possibly due to its particularly thick oospore walls [150]. Oaks with P. quercina or other Phytophthora spp. in their rhizosphere have ca. 50% higher probability of exhibiting severe aboveground disease symptoms than oaks without Phytophthora spp. [167]. Jönsson et al. [118] showed that Swedish isolates of P. quercina had the capacity to induce fine-root dieback of Q. robur seedlings growing in acid, N-rich but otherwise nutrient-poor forest soils (dominant in Sweden), as well as in high pH, nutrient-rich soils under the mesic water regime. Their aggressiveness, together with a high infection rate (all the seedlings were infected) showed a potential capacity of P. quercina to infect plants in acid forest soils [118]. In addition, the stress-induced susceptibility of the seedlings and/or increased aggressiveness of the pathogen in the forest soil could be factors accounting for differences of root dieback between soil types [118].
Occurrence: The decline of European oaks mainly occurs in trees older than 100 years, and in this process, trees may survive for a long time. It is only under exceptional circum-stances that oaks may die in large areas [160,168]. A similar decline of oaks (in particular, Q. robur) has occurred in Sweden during the recent decades [148]. The reason for this loss was unclear until the three different Phytophthora species were recovered from 11 out of 32 oak stands in the southernmost part of the country, with P. quercina being the most frequent species [110]. However, a weak association was found between the occurrence of P. quercina and the vitality of mature oak stands [169]. Thus, the decline of oaks in southern Sweden can probably be attributed to several different site-specific factors, such as infection by P. quercina or unusual weather events, which interact with a number of biotic and abiotic factors, leading to oak decline [170]. Later, Jönsson-Belyazio and Rosengren [171] summarized that P. quercina contributes to oak decline in southern Sweden. A conceptual model for the development of Phytophthora disease in Q. robur suggested that the link between the root damage caused by Phytophthora species and overall tree vitality is in the assimilation and allocation of carbon within the plants [120]. More recently, P. quercina was also found in both urban (Mölndalsån area) and natural forests (Säveån and Lyckebyån areas), but not in forest nurseries [105].
Symptoms: lethal stem cankers, shoot dieback, foliage blight Aggressiveness: P. ramorum is one of the most aggressive Phytophthora species. It is considered a highly invasive species due to its ability to spread, persist, and reproduce in new environments. The pathogen can infect plants in nurseries situated in close proximity to streams, later causing significant outbreaks on outplanted ornamentals. Spread events appear to be associated with either the movement of infected plant parts, normally from large wild infestations, or the introduction of infected plants, normally from infested ornamental nursery stock [172]. Infected nursery plants, such as Rhododendron, Camellia, and Viburnum, often contribute to long distance dispersal of the pathogen. Inoculation trials on stems showed that in addition to Rhododendron sp., P. ramorum caused necrotic lesions on A. glutinosa, A. incana, and B. pendula, while P. sylvestris and P. abies showed no disease symptoms [129,137], even though the pathogen might be able to infect individual P. abies needles [173]. Inoculation trials suggest that the damage can be substantial, as used isolates of P. ramorum were able to cause stem lesions in over 80% of B. pendula and over 30% of A. glutinosa seedlings [129].
Occurrence: In Sweden, the first report of P. ramorum was in 2002, which was found on 11 plants of Rhododendron sp. [174]. In 2017, it was detected on two plants of Rhododendron yakushimanum in a nursery in the municipality of Skurup. In 2018, P. ramorum was detected on four Rhododendron plants in a private garden in the municipality of Klippan. In Finland, P. ramorum was detected for the first time in 2004 [137]. It was found on marketed plants of Rhododendron spp., which were imported from other EU member states. The same year, P. ramorum was also discovered on Rhododendron sp. in a Finnish nursery, and detection was also successful in the following years, i.e., 2004−2010, except 2007, showing the persistent establishment of this pathogen despite the annual sanitation measures [129]. In Norway, P. ramorum was reported for the first time in 2002 [136]. It was isolated from symptomatic R. catawbiense in a nursery in Bergen. In the following years, the number of locations with P. ramorum has gradually increased (in 2004, there were 29 new locations, and in 2005, there were 43 locations), showing a broader distribution and/or rapid spread within the country. Apart from rhododendron, P. ramorum was also detected on Pieris japonica and Viburnum fragrans, and the latter was heavily infected. P. ramorum was most likely imported to Norway with symptomless plants and/or with plants that had mild symptoms, which are difficult to detect using random controls [136].
Phytophthora Symptoms: twig blight, fruit rot, root and collar rot, stem canker, wilt, leaf spot, and shoot dieback of lilac Aggressiveness: P. syringae is known to infect nursery plants, particularly apple and pear trees. It infects plants through wounded areas and is most pathogenic during cold and wet weather conditions.
Occurrence: In Sweden, P. syringae was found in the soil in the vicinity of horse chestnut growing in Pildamms Park in the city of Malmö [109]. It was also detected in a nursery (near Kävlingeå) and in urban forests (near the Nyköpingsån river) in association with R. catawbiense [105].

Phytophthora Species Detected in the Water and Soil in Sweden
Two species, P. alni subsp. alni and P. alni subsp. uniformis, were found in the Säveån and Mölndalsån rivers near Gothenburg in 1996 and 1998 [104]. Systematic sampling of the Phytophthora species was performed in 16 rivers in southern Sweden in 2013 using inspection of active bleeding cankers on alder trees along the rivers [103]. P. alni subsp. multiformis was detected in 7 rivers and P. alni subsp. uniformis was in 13 rivers, while P. plurivora was isolated from alders growing along three rivers [103]. Phytophthora cryptogea, P. gonapodyides, P. lacustris, P. megasperma, P. plurivora, P. taxon paludosa, and an unknown Phytophthora species were isolated from waterways and soil samples in Christmas tree plantations in southern Sweden [113]. Recently, P. scandivavica, a new waterborne species, was isolated from the riverbank soil in the Kiruna area in northern Sweden [175].

Concerns Regarding Phytophthora Pathogens on Woody Plants
Over the last 60 years and since the calamity of P. cinnamomi in Western Australia and Victoria in the 1960s, incidences of Phytophthora diseases have exponentially increased globally [3,176,177]. In Nordic countries, the majority of Phytophthora detections took place after the 2000s, highlighting the importance of these destructive pathogens, and providing critically needed information on their occurrence, spread, and possible impact in different environments. However, the concerns remain that new Phytophthora species may arrive and establish itself, which should be tackled by harmonizing both phytosanitary regulations/processes and exchanging information between EU countries [178][179][180][181][182]. Most of the Phytophthora species detected in Nordic countries are exotic invasive pathogens, often introduced through the 'plants-for-planting' pathway. Global change poses a risk for the spread and establishment of these Phytophthora species in natural ecosystems, which may subsequently result in the decline of local forest tree species [89,183,184]. To reduce such damage in Nordic countries, targeted efforts and knowledge are needed to monitor new and manage existing Phytophthora species of woody plants.
Assessing the potential risks of Phytophthora spp. to woody plants (Table 3) is a highly complex task that is further complicated by the ability of different Phytophthora species to cause multiple infections on different hosts and to produce hybrids, which might be more virulent than their progenitors under specific conditions, thereby facilitating adaptation of these Phytophthora species to different environments [55,[185][186][187]. Due to their multicycling nature and a strong dependence on free water in the soil, Phytophthora species can also predispose woody plants to other abiotic and biotic factors by primarily colonizing fine roots and weakening their hosts [55]. For disease management, it is important to understand which Phytophthora species can be pathogenic and cause disease in a particular host. The presence of aggressive Phytophthora species in Sweden and other Nordic countries (e.g., P. × alni, P. cactorum, P. cambivora, P. gonapodyides, P. plurivora, or P. quercina) means that these should be considered as a serious threat to woody plants in urban and forest ecosystems (Table 3). In Sweden, more than half of the territory is covered by forests, which are mainly composed of coniferous tree species; however, due to a mild climate, broadleaved tree stands dominate in the southern part of the country. In these stands, F. sylvatica, Quercus sp., F. excelsior, B. pendula, U. glabra, and A. glutinosa are the dominant and ecologically most important tree species that are planted both for forestry purposes and as ornamentals in urban and landscape settings. These tree species are also increasingly planted to promote both biodiversity and sustainable land use and enhance the resilience of local forests to climate change [188]. However, there is a rising concern regarding increasing damage caused by Phytophthora species on broadleaved tree species, especially F. sylvatica, A. hippocastanum, A. glutinosa, A. incana, and Q. robur [105,109,115,117]. This represents a new challenge to broadleaved forestry, as, according to the Swedish Forestry Act [189], selected valuable broadleaved tree species must be used for the regeneration of broadleaved forests. Climate change should also be considered, as it can escalate Phytophthora damage by altering the susceptibility of woody hosts and modifying the development of Phytophthora pathogens [190][191][192]. For example, damage caused by P. × alni, P. cinnamomi, P. ramorum, P. pseudosyringae, or P. plurivora are considered to increase due to climate change [191]. Warmer winters may not only increase the activity of P. × alni, but may also lead to a northern expansion of its range [141], while warmer summers and droughts are likely to favor Phytophthora species adapted to higher temperatures [191]. In Sweden, climate change modelling predicts an increase of the annual temperature between 3 • C and 7 • C, and the increase of local precipitation up to 40% [193]. Similarly, 3 • C to 5 • C higher winter and summer temperatures, and up to a 25% longer annual rainfall period are expected in the future in southern Sweden [194]. The Swedish Meteorological and Hydrological Institute (SMHI) has already recorded droughts during the summer of 2018 and high temperatures during the summer of 2022, including a temperature record of 37.2 • C on 21 July 2022, which was the highest temperature in Sweden since 29 July 1947 [195]. These climatic changes may have a substantial effect on the activity and spread of Phytophthora species in the future.
Another concern is related to the 'never-ending story' about the presence of Phytophthora species in the nurseries. In Sweden, the early reports of Phytophthora causing damage to woody plants came from nurseries [108]. The richness of the Phytophthora species detected in nurseries, anthropogenic forests, or urban greeneries is higher than in natural forests, demonstrating the potential introduction of these pathogens with infected nursery plants [89,93,109,138]. Indeed, nurseries, commercial ones in particular, are well-known to be an important pathway of introduction of invasive pathogens globally, including Phytophthora species in Europe [78,89,[196][197][198]. Despite chemical treatments, which usually do not cure the disease, infected nursery plants often arrive visually symptomless, passing unnoticed through phytosanitary controls, thereby acting as 'pathogen reservoirs' and assuring the unintentional distribution of Phytophthora species [89,[199][200][201]. The detection of P. ramorum on ornamental woody plants in several Nordic countries (Finland, Norway, and Sweden; Tables 1 and 2) is one of the examples of accidental introduction of Phytophthora pathogens to new areas [136]. The detection of P. cinnamomi, which is one of the most aggressive invasive plant pathogens, on imported plant material in Sweden highlights the importance of surveillance activities for the early detection of Phytophthora pathogens and the provision of relevant knowledge for plant growers.
In Nordic countries, there is also a concern about the increasing risk of Phytophthora damage to Christmas tree plantations. Denmark is one of the largest exporters of Christmas trees to many European countries, including Sweden (6%) and Norway (3%) [202]. Although there are no reports about Phytophthora in Christmas trees plantations in Denmark, reports from Norway [132] and Sweden [113,115] show that Phytophthora may become a threat to Christmas tree production in the future. Indeed, Phytophthora species were introduced with imported Christmas tree seedlings to Norway, repeatedly showing the risk of possible future problems, including hybridization, in local forest nurseries and/or Christmas tree plantations [203].

Management of Phytophthora Diseases
One of the best approaches to Phytophthora management is the prevention of its introduction and establishment. Once Phytophthora spp. have been introduced, they will remain for many years due to the longevity of their resting propagules. However, the presence of Phytophthora infection does not necessarily mean that the tree will die, as some trees may successfully prevent continued growth of the pathogen around the trunk, at least for some time [204]. Nevertheless, management measures are often recommended to limit Phytophthora infections and the spread of these pathogens.
Some general management guidelines include restricting the deposition of organic waste in the vicinity of areas (forests, parks, or city plantations) sensitive to Phytophthora infestations and on infested sites eliminating human, animal, and vehicle movement; estab-lishing routines for the thorough cleaning of machines and equipment used in management operations; harvesting dead/infected woody plants when the ground is frozen, which also helps to prevent soil compaction by used machines; prohibiting the use of materials (e.g., woodchips) from diseased woody plants in nature; improving root aeration by draining wet and especially flooded areas; and, if possible, adding organic mulch on top of the roots of woody plants [131,204,205]. The use of chemical fungicides and/or biological control products is another important management measure in highly managed environments, such as nurseries. For the establishment of new plantations, it is essential to use healthy nursery stock that has been thoroughly examined for the presence of Phytophthora. The replacement of susceptible woody plant species by those that are more tolerant to Phytophthora infections and are well-adapted to environmental conditions of a specific planting site can be another management measure. For example, to reduce the incidences of Phytophthora spp. in Christmas tree plantations, it is recommended to plant spruce instead of fir [206]. Invasive pests, such as Arion vulgaris, which may be vectors for the transmission of Phytophthora spp. to woody plants, should also be controlled [207].

Conclusions
Since the first report on Phytophthora species on woody plants in Sweden, the number of detected Phytophthora species and the number of disease incidences has sharply increased both in Sweden and in other Nordic countries. The introduction of new Phytophthora species with imported plants and/or by other means, recent changes in local climatic conditions, and the availability of new detection methods appears to be among the major reasons for this increase. Field observations and inoculation trials demonstrate that some of the detected Phytophthora species can be aggressive pathogens, posing a high risk to several woody plants in Nordic countries. To prevent and/or reduce damages, targeted efforts and knowledge are needed to monitor new and manage existing Phytophthora species of woody plants.
Author Contributions: All authors contributed equally to this work. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.