Alien Stramenopilous Fungus-like Organisms (Oomycota) Diversity and Distribution in Lithuania

Abstract

This paper provides data on non-native fungus-like organisms (Oomycota, kingdom Stramenopila), their diversity, and distribution in Lithuania and is an addition to a previously published checklist of alien true fungi (Chytridiomycota, Ascomycota, and Basidiomycota; kingdom Fungi). All available published data were summarized, and the analysis showed that approximately 25% of recorded Lithuania stramenopilous fungus-like organism species are alien. The compiled list represented herein includes 54 species of alien terrestrial and aquatic stramenopilous fungus-like organisms (Oomycota). Most alien Oomycota are obligate pathogens of terrestrial plants. Aquatic organisms are represented by one alien dangerous crayfish pathogen, Aphanomyces astaci, which is currently noted as extinct in Lithuania. The taxonomy of the listed alien species of Oomycota has been revised, and the species names have been adjusted to reflect current nomenclature changes. The taxonomical and ecological analysis demonstrated the prevalence of terrestrial parasitic Peronosporales reported in Lithuania Oomycota and the highest diversity of alien species belonging to the Peronospora genus. The chronology of appearance, distribution within the country, and current status of these non-native organisms were assessed, and some of the most economically or ecologically important harmful invasive species were discussed.

1. Introduction

Among known alien and invasive organisms, fungi and oomycetes are poorly investigated groups, but at least 2% of them, approximately 2000 species, are invasive, easily spreading and adapting to new environment conditions [1,2,3]. Oomycetes, formerly classified as fungi, are fungus-like microorganisms belonging to one of the major eukaryotic clades, Stramenopiles, distinct from true fungi [4]. These organisms are widely distributed in various terrestrial, freshwater, and marine habitats [5,6]. The taxonomic rank of oomycetes varied from class to phylum and, along with diatoms, chromophytic algae, and other heterocontic protists, now are placed in the kingdom Stramenopila [4,7,8,9,10] (as Straminipila by Dick [5]), in Stramenopiles lineage of biflagellated “heterokont” organisms within the eukaryotic supergroup Stramenopiles–Alveolata–Rhizaria (SAR) [11,12,13,14,15]. Currently, the phylum Oomycota is separated into two major classes: most aquatic organisms belong to Saprolegniomycetes with two main orders—Leptomitales and Saprolegniales and most terrestrial species to Peronosporomycetes, with four main orders—Albuginales, Pythyales, Peronosporales, and Rhipidiales [5,16]. Phylogenetic studies have also confirmed the division of these fungus-like organisms (Oomycota) into four “crown” orders: Albuginales, Pythiales, Peronosporales, and Saprolegniales [12,15]. However, the taxonomical position and classification of these organisms remain uncertain till the present time, and most scientists still prefer to use the term “oomycetes”.

Evolutionarily stramenopilous fungus-like organisms (Oomycota) had their origins in the sea, and they could have appeared between the late Proterozoic and middle Paleozoic era (0.4 to 0.6 billion years ago) or even earlier, but the terrestrial branch is currently more specialized than the aquatic one [5,8,9,11,13,15,16]. Most of the early diverging marine members are simple holocarpic organisms that lack mycelial organization [6]. The fungal hyphal-like pattern of growth and the quiet complex oogamous sexual reproduction developed after their ancestor’s migration from the sea to freshwater and to land [9,10]. The traits characterizing representatives of Oomycota are mainly based on the features of their reproduction and composition of the cell wall; especially important is the presence of cellulose and other β-glucans in the cell wall [5,9,17]. Chitin or chitosaccharides, characteristic of true fungi, are absent or rarely found in the cell wall of Oomycota, only in some species such as Aphanomyces euteiches and Saprolegnia monoica [5]. Freshwater Saprolegniales and soilborne Pythiales are characterized by asexual reproduction via motile biflagellate zoospores and the production of sterols necessary for the induction of their sexual reproduction [5]. Terrestrial Albuginales and Peronosporales are characterized mainly by asexual reproduction via not motile conidia (except Phytophthora) and their inability to synthesize sterols. During the long-term evolutionary changes, these fungus-like organisms have adapted to a wide range of different lifestyles: saprotrophic, endophytic, facultative necrotrophic/hemibiotrophic/parasitic, or obligate biotrophic/parasitic and employing both sexual and asexual reproduction for propagation and survival [5,8,16]. The main criterion for an “alien species” is the occurrence or introduction into an area of a new, previously undiscovered species that is not native to the area [2]. Alien in Europe and in Lithuania, Albuginales and Peronosporales predominantly are highly specialized obligate plant pathogens, which cause white blister and downy mildew diseases [2,18]. Alien Phytophthora species are facultative pathogens that usually move with their hosts in latent or endophytic stages or with contaminated soil or water and are, therefore, particularly difficult to detect and prevent their introduction into new areas and to a new biogeographical region [19,20,21,22,23]. Different alien species need different periods for adaptation to new habitats and conditions. After adaptation, more aggressive and rapidly spreading alien species, especially Phytopthora spp., may move to other native hosts, change lifestyle, and cause disease outbreaks in native host populations [3,24]. Current increased socio-economic activity, movement and transportation of contaminated seeds or plant material, intensification of aquaculture, and climate change are factors increasing the risk for the emergence and spread of new alien stramenopilous fungus-like pathogens, which can lead to serious environmental or economic problems. In addition, the introduction of new haplotypes of pre-existing oomycetous pathogens from other countries or continents may provide an opportunity for future genetic recombination and hybridization of these pathogens, increasing the risk of the emergence and spread of more virulent strains or the emergence of a new species [25,26], as in the case of the potato late blight pathogen Phytophthora infestans [27,28,29] and alder trees pathogen—Phytophthora alni sensu lato species complex [30,31]. Data on the introduction and spread of alien species of Oomycota, the invasion of new terrestrial, and aquatic pathogens into new regions, the analysis of their ability to adapt and spread rapidly, and the elucidation of the vulnerability of native hosts are very important for the prevention and effective control of many harmful plant diseases, such as downy mildew, spotting, root rot and diseases of crayfish, or fish caused by water molds.

The main goal of this work was to summarize all available published data on alien stramenopilous fungus-like organisms (Oomycota) detected in Lithuania and to complete the previously published list of 142 species of alien true fungi (Chytridiomycetes, Ascomycetes and Basidiomycetes) found in Lithuania [32] with a new list of alien Oomycota. The specific aims were to evaluate the distribution and current status of listed alien species of Oomycota in our country, discuss the historical data on invasions of the most economically and ecologically important harmful pathogens, and assess the risk of new alien species emergence and adaptation.

2. Data Collection and Determination of the Current Status of Alien Species

Previously published literature data on Oomycota from Lithuania in different languages (Polish, Russian, Lithuanian and English) were used in this review to identify alien species, analyze their distribution and determine their current status in our country. In addition, Data from fungal collections of the BILAS herbarium of the State Scientific Research Institute Nature Research Centre (NRC, Vilnius) and WI herbarium of Vilnius University was used to review existing records on alien stramenopilous fungus-like organisms. After revision, only species with a confirmed and well-documented alien status in Europe [2,21,33,34,35] were included in the list. The names of species included in the checklist have been corrected in accordance with the changes in taxonomy and nomenclature adopted by Index Fungorum [36]. The currently used legitimate species names are accompanied by the most common synonyms mentioned in various publications.

The current status is based on the distribution of every alien (non-native) species of stramenopilous fungus-like organisms (Oomycota) and was determined following categories proposed for true fungi in the previously published paper [32]. Categories used in this review were the following: 1—established (the first record more than 15 years ago; currently common in various parts of the country), 2—spreading (the first record less than 15 years ago; currently, the number of localities increase), 3—unknown (one or few records; distribution is unknown or not investigated). Additional categories included the following: 4—extinct (naturally disappeared; currently not found) and 5—eradicated (when infected plans were destructed according to the quarantine requirements and pathogen was not detected more).

3. Alien Stramenopilous Fungus-like Organisms (Oomycota) Recorded in Lithuania

Our study considerably expands the previously published checklist of 142 species of alien true fungi [32]. The analysis showed that approximately 25% of more than 200 stramenopilous fungus-like organisms (Oomycota) recorded in Lithuania [18,37,38,39,40,41,42,43,44,45,46,47] can be considered alien, and its number currently reaches 54 species (Table 1).

3.1. Diversity and Distribution of Alien Oomycota

These non-native species are characterized by differences in distribution/current status and in functional capacity/lifestyle (Figure 1). Introduction vectors of most alien Oomycota species are unknown. About half of the species (26) from the list are noted as established and widely spread (Table 1). The first record of most of these species dates to more than 30 years, and currently, they are known from numerous localities around Lithuania. Some of them, such as Phytophthora infestans on Solanum, Albugo candida on various plants of Brassicaceae, Peronospora destructor on Allium, Plasmopara viticola on Vitis, and Pseudoperonospora cubensis on Cucumber can be regarded as invasive, causing considerable damage to the host plants [18]. One species, Phytophthora alni sensu lato, is indicated as spreading (it was recorded for the first time more than 15 years ago, but the number of localities has started to increase only during the last decades). The other species, Phytophthora ramorum, is noted as eradicated (after quarantine regulation), and Aphanomyces astaci was noted as extinct after 1979 (however, currently, its distribution is not investigated in Lithuania). The distribution and current status of the other 25 alien and cryptogenic species are indicated as “unknown” because they were not intensively investigated in Lithuania and were occasionally found once or only several times, and their introduction vectors are unknown (Table 1). Some of them, such as Peronospora sparsa on roses, P. fagopiri on buckwheat, P. ornithopi on serradella, and P. spinaciae on spinach, are sporadically occurring and not very common in Lithuania species [18]. Meantime, Hyaloperonospora camelinae (syn. Peronospora camelinae), P. corydalis-intermediae, P. digitalidis, P. kochiae, Plasmopara angustiterminalis are known as rare species [18].

The compiled list (Table 1) and cumulative graph of alien stramenopilous fungus-like organisms (Oomycota) recorded in Lithuania demonstrated that since the first records in 1830–1886, the number of newly recorded species and the cumulative number of records have been continuously increasing, and the higher increase of alien species records occurred in 1960–1980s and after 2000s (Figure 2).

These data undoubtedly reflect the periods of the highest mycological and phytopathological scientific activities in Lithuania [48] and are like those established in Lithuania for true fungi [32] and, overall, for alien fungi recorded in Europe [2,21,49]. The largest number of new alien species of true fungi in Lithuania was recorded in 1980–2000 [32]. In comparison with true fungi, in 1990–2024, the number of new finds of stramenopilous fungus-like organisms in Lithuania did not increase very much, which can be explained by a decrease in the intensity of taxonomic and ecological studies of this group of organisms in Lithuania. The exponential growth of the curve post-2000s is mainly associated with the increased impact of harmful oomycetes on forestry and the description of new Phytophthora species responsible for tree diseases [20,30,39,40,41,46,47].

Taxonomically, the vast majority of alien stramenopilous fungus-like organisms (Oomycota) established in Lithuania, about 94% (51 species of terrestrial plant pathogens) belong to the largest order Peronosporales, and only 6% of species belong to Albuginales and Saprolegniales (Figure 3).

Alien freshwater Saprolegniales recorded in Lithuania belongs to only one Aphanomyces genus and are represented by two species, waterborne crayfish pathogen Aphanomyces astaci [37,38] and soil-borne Aphanomyces eusteihes, which usually causes root rot of legumes but can also be spread by water [44]. The order Albuginales was represented by a single species, Albugo candida [18], a pathogen of terrestrial plants of the family Brassicaceae. The taxonomical analysis demonstrated high genetic diversity among the reported alien Peronosporales and the highest species diversity (28 species) of the genus Peronospora (Figure 4).

3.2. Terrestrial Alien Peronosporales Trophic Preferences, Spread Vectors, and Specificity to Hosts

Terrestrial alien Peronosporales (Basidiophora entospora, Bremia lactucae, Sclerophthora macrospora, all detected species of Hyaloperonospora, Peronospora, Plasmopara, and Pseudoperonospora genera) are obligate biotrophs/pathogens, which usually overwinters in seeds, leaf litter, soil, and are mainly spread by wind, rain, and contaminated living plant material or soil [18,50,51,52]. Most downy mildew pathogens of Peronospora, Plasmopara, and Hyaloperonospora genera recorded in Lithuania are highly host-specific (Table 1), often at the host genus/species level [18,50]. The importance of alien plant pathogenic species for agriculture is shown by their vide spectrum of host genera established in Lithuania: Allium, Brassica, Cucumis, Fagopyrum, Fragaria, Lactuca, Lycopersicon, Pastinaca, Pisum, Sisymbrium, Solanum, Spinacia, Trifolium, Triticum, Vicia, Vitis (Table 1).

Table 1. List of alien stramenopilous fungus-like organisms (Oomycota) recorded in Lithuania, their host/substrate, the year of first record/current status (based on distribution) and first published reference.

Name of Species	Host/Substrate	First Record and Current Status	Reference of First Record
Albugo candida (Pers. ex J.F. Gmel.) Roussel sensu lato species complex (A. candida × A. koreana × A. voglmayrii) (syn. Uredo candida (Pers. ex J.F. Gmel.) Pers.))	Various plants of Brassicaceae	1830 established	[53]
Aphanomyces astaci Schikora	Astacus astacus L. (crayfish)	1886 (after 1979 extinct) currently unknown	[37,38]
Aphanomyces eusteihes Drechsler	Plant debris in water	2005 unknown	[44]
Basidiophora entospora Roze & Cornu	Conyza	1964 Unknown	[50]
Bremia lactucae Regel	Various plants of Asteraceae	1926 established	[54]
Hyaloperonospora barbareae (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. Peronospora barbareae Gäum.)	Barbareae	1962 established	[55]
Hyaloperonospora berteroae (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. P. berteroae Gäum.)	Berteroa	1962 unknown	[55]
Hyaloperonospora camelinae (Gäum.) Göker, Voglmayr, Riethm., Weiss & Oberw. (syn. P. camelinae Gäum.)	Camelina	1937 established	[56]
Hyaloperonospora cochleariae (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. P. cochleariae Gäum.)	Armoracia	1927 established	[57]
Hyaloperonospora hesperidis (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. P. hesperidis Gäum.	Hesperis	1962 unknown	[55]
Hyaloperonospora iberidis (Gäum.) C. Salgado & J.A. Crouch (syn. P. iberidis Gäum.)	Iberis	1984 unknown	[50]
Hyaloperonospora parasitica (Pers.) Constant. (syn. P. erysimi Gäum.)	Erysimum	1962 established	[55]
Peronospora aestivalis Syd.	Medicago	1960 established	[58]
P. affinis Rossmann	Fumaria	1968 unknown	[50]
P. arborescens (Berk.) de Bary	Papaver	1928 established	[57]
P. buniadis Gäum.	Bunias	1962 unknown	[55]
P. chorale de Bary	Eustoma	1993 unknown	[18]
P. conglomerata Fuckel	Geranium	1962 unknown	[55]
P. corydalis-intermediae Gäum.	Corydalis	1984 unknown	[50]
P. destructor (Berk.) Casp. Ex Berk.	Allium	1928 established	[59]
P. digitalidis Gäum.	Digitalis	1962 unknown	[55]
P. erodii Fuckel	Erodium	1962 unknown	[55]
P. fagopyri Elenev	Fagopyrum	1984 established	[50]
P. grisea (Unger) Unger	Veronica	1960 established	[58]
Peronospora hyoscyami de Bary (syn.: P. tabacina D. B. Adam., P. nicotianae Speg.)	Nicotiana	1961 established	[55]
P. kochiae-scopariae Kochman & T. Majewski	Kochia	1984 unknown	[50]
P. lamii (A.Braun) Rabenh.	Lamium	1960 established	[56]
P. mathiolae Gäum.	Matthiola	1962 unknown	[55]
P. mayorii Gäum.	Vicia	1960 established	[58]
P. myosotidis de Bary	Myosotis	1962 established	[55]
P. obovata Bonord.	Spergula	1960 established	[56]
P. ornithopi Gäum.	Ornithopus	1984 Unknown	[50]
P. phyteumatis Fuckel	Phyteuma	1984 unknown	[50]
P. scleranthi Rabenh.	Scleranthus	1962 unknown	[55]
P. sisymbrii-officinalis Gäum.	Sisymbrium	1962 established	[55]
P. sparsa Berk.	Rosa	1984 established	[50]
P. spinaceae Laubert	Spinacia	1962 unknown	[55]
P. trifoliorum de Bary	Trifolium	1936 established	[60]
Peronospora viciae (Berk.) Casp. (syn. P. pisi (Syd.) Gäum.)	Pisum, Vicia	1927 established	[57]
P. violae de Bary	Viola	1928 established	[57]
Phytophthora alni Brasier & S.A. Kirk sensu lato species complex (P. × alni and P. uniformis)	Alnus	1999 spreading	[30,47]
Ph. cactorum (Leb. et Cohn) Schröt.	Rhododendron	2004 unknown	[41]
Ph. cinnamomi Rands	Pinus, Quercus	2000 unknown	[39]
Ph. fragariae Hickman	Fragaria	2000 unknown	[40]
Ph. infestans (Mont.) de Bary	Solanum, Lycopersicon, Petunia	1912 established	[61]
Ph. syringae (Kleb.) Kleb.	Syringa, Malus	1935 unknown	[62]
Ph. ramorum Werres, De Cock & Man	Rhododendron	2007 2019 eradicated	[63]
Plasmopara angustiterminalis Novot.	Xanthium	1984 unknown	[50]
Pl. pastinacae Săvul. & O. Săvul.	Pastinaca	1984 unknown	[50]
Pl. viticola (Berk. & M.A. Curtis) Berl. & De Toni	Vitis	1949 established	[58]
Pseudoperonospora cannabina (G.H. Otth)	Cannabis	1984 established	[50]
Pseudoperonospora cubensis (Berk. & M.A. Curtis) Rostovzev	Cucumis	1985 established	[64]
Pseudoperonospora humuli (Miyabe & Takah.) G.W. Wilson (syn. Peronoplasmopara humuli Miyabe & Takah)	Humulus	1927 established	[57]
Sclerophthora macrospora (Sacc.) Thirum., Shaw. et Naras	Triticum	1989 unknown	[65]

Table 1. List of alien stramenopilous fungus-like organisms (Oomycota) recorded in Lithuania, their host/substrate, the year of first record/current status (based on distribution) and first published reference.

Name of Species	Host/Substrate	First Record and Current Status	Reference of First Record
Albugo candida (Pers. ex J.F. Gmel.) Roussel sensu lato species complex (A. candida × A. koreana × A. voglmayrii) (syn. Uredo candida (Pers. ex J.F. Gmel.) Pers.))	Various plants of Brassicaceae	1830 established	[53]
Aphanomyces astaci Schikora	Astacus astacus L. (crayfish)	1886 (after 1979 extinct) currently unknown	[37,38]
Aphanomyces eusteihes Drechsler	Plant debris in water	2005 unknown	[44]
Basidiophora entospora Roze & Cornu	Conyza	1964 Unknown	[50]
Bremia lactucae Regel	Various plants of Asteraceae	1926 established	[54]
Hyaloperonospora barbareae (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. Peronospora barbareae Gäum.)	Barbareae	1962 established	[55]
Hyaloperonospora berteroae (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. P. berteroae Gäum.)	Berteroa	1962 unknown	[55]
Hyaloperonospora camelinae (Gäum.) Göker, Voglmayr, Riethm., Weiss & Oberw. (syn. P. camelinae Gäum.)	Camelina	1937 established	[56]
Hyaloperonospora cochleariae (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. P. cochleariae Gäum.)	Armoracia	1927 established	[57]
Hyaloperonospora hesperidis (Gäum.) Göker, Riethm., Voglmayr, Weiss & Oberw. (syn. P. hesperidis Gäum.	Hesperis	1962 unknown	[55]
Hyaloperonospora iberidis (Gäum.) C. Salgado & J.A. Crouch (syn. P. iberidis Gäum.)	Iberis	1984 unknown	[50]
Hyaloperonospora parasitica (Pers.) Constant. (syn. P. erysimi Gäum.)	Erysimum	1962 established	[55]
Peronospora aestivalis Syd.	Medicago	1960 established	[58]
P. affinis Rossmann	Fumaria	1968 unknown	[50]
P. arborescens (Berk.) de Bary	Papaver	1928 established	[57]
P. buniadis Gäum.	Bunias	1962 unknown	[55]
P. chorale de Bary	Eustoma	1993 unknown	[18]
P. conglomerata Fuckel	Geranium	1962 unknown	[55]
P. corydalis-intermediae Gäum.	Corydalis	1984 unknown	[50]
P. destructor (Berk.) Casp. Ex Berk.	Allium	1928 established	[59]
P. digitalidis Gäum.	Digitalis	1962 unknown	[55]
P. erodii Fuckel	Erodium	1962 unknown	[55]
P. fagopyri Elenev	Fagopyrum	1984 established	[50]
P. grisea (Unger) Unger	Veronica	1960 established	[58]
Peronospora hyoscyami de Bary (syn.: P. tabacina D. B. Adam., P. nicotianae Speg.)	Nicotiana	1961 established	[55]
P. kochiae-scopariae Kochman & T. Majewski	Kochia	1984 unknown	[50]
P. lamii (A.Braun) Rabenh.	Lamium	1960 established	[56]
P. mathiolae Gäum.	Matthiola	1962 unknown	[55]
P. mayorii Gäum.	Vicia	1960 established	[58]
P. myosotidis de Bary	Myosotis	1962 established	[55]
P. obovata Bonord.	Spergula	1960 established	[56]
P. ornithopi Gäum.	Ornithopus	1984 Unknown	[50]
P. phyteumatis Fuckel	Phyteuma	1984 unknown	[50]
P. scleranthi Rabenh.	Scleranthus	1962 unknown	[55]
P. sisymbrii-officinalis Gäum.	Sisymbrium	1962 established	[55]
P. sparsa Berk.	Rosa	1984 established	[50]
P. spinaceae Laubert	Spinacia	1962 unknown	[55]
P. trifoliorum de Bary	Trifolium	1936 established	[60]
Peronospora viciae (Berk.) Casp. (syn. P. pisi (Syd.) Gäum.)	Pisum, Vicia	1927 established	[57]
P. violae de Bary	Viola	1928 established	[57]
Phytophthora alni Brasier & S.A. Kirk sensu lato species complex (P. × alni and P. uniformis)	Alnus	1999 spreading	[30,47]
Ph. cactorum (Leb. et Cohn) Schröt.	Rhododendron	2004 unknown	[41]
Ph. cinnamomi Rands	Pinus, Quercus	2000 unknown	[39]
Ph. fragariae Hickman	Fragaria	2000 unknown	[40]
Ph. infestans (Mont.) de Bary	Solanum, Lycopersicon, Petunia	1912 established	[61]
Ph. syringae (Kleb.) Kleb.	Syringa, Malus	1935 unknown	[62]
Ph. ramorum Werres, De Cock & Man	Rhododendron	2007 2019 eradicated	[63]
Plasmopara angustiterminalis Novot.	Xanthium	1984 unknown	[50]
Pl. pastinacae Săvul. & O. Săvul.	Pastinaca	1984 unknown	[50]
Pl. viticola (Berk. & M.A. Curtis) Berl. & De Toni	Vitis	1949 established	[58]
Pseudoperonospora cannabina (G.H. Otth)	Cannabis	1984 established	[50]
Pseudoperonospora cubensis (Berk. & M.A. Curtis) Rostovzev	Cucumis	1985 established	[64]
Pseudoperonospora humuli (Miyabe & Takah.) G.W. Wilson (syn. Peronoplasmopara humuli Miyabe & Takah)	Humulus	1927 established	[57]
Sclerophthora macrospora (Sacc.) Thirum., Shaw. et Naras	Triticum	1989 unknown	[65]

3.3. Waterborne and Soilborne Alien Pathogens Trophic Preferences and Spread Vectors

The waterborne and soilborne representatives of alien Saprolegniales (Aphanomyces spp.) and species of Phytophthora genus (Peronosporales) are plant hemibiotrophs (except Aphanomyces astaci, which is obligate crayfish plague pathogen) and can develop as aquatic and riparian plant biotrophs-pathogens or saprotrophs [5,8,66]. The floating zoospores of Aphanomyces and Phytophthora are easily spread by running water. Streams and rivers, acting as vectors of infection, increase the risk of these pathogens spreading over long distances and represent corridors for the emergence of new invasive species that can be dangerous to various local vulnerable riparian plants and aquatic organisms [67,68,69,70,71].

4. Historical Data on Invasions of Some Economically Important Pathogens into Lithuania

The first report on alien oomycetes in Lithuania appeared in the first part of the 19th century and was about the earliest known obligate biotrophic plant pathogen belonging to the order Albuginales, the causal agent of white blister rust disease Albugo candida.

4.1. The Oldest Obligate Plant Pathogen Albugo candida Sensu Lato

The cryptogenic pathogen Albugo candida sensu lato in Lithuania was found in 1830 by Jundzill and was reported as Uredo candida [53]. Many species previously identified based on morphology have now been found to be a complex of several cryptic species after genetic studies. The Albugo candida sensu lato represents a species complex that infects a wide range of Brassicaceae [72]. Currently, A. candida is widely spread in Lithuania on various plants of Arabis, Berteroa, Camelina, Capsella, Descurainia, Erysimum, Hesperis, Neslia, Roripa, Sisymbrium, and Thlaspi genera [18,50,73]. Recently, based on a polyphasic taxonomic approach, including morphological features of oospore wall ornamentation and various genetic inferences (analyses of ITS, LSU gene regions of rDNA, and cox2 gene region of mtDNA) in A. candida species complex were described three distinct species: A. candida, A. koreana, and A. voglmayrii [74,75,76]. Undoubtedly, Lithuanian collections of A. candida from the BILAS and VU herbariums also represent species complex and need an additional, more detailed taxonomical revision in the future.

4.2. The Crayfish Plague Pathogen Aphanomyces astaci

The introduction of the aquatic pathogen Aphanomyces astaci, the causative agent of the crayfish plague, to Lithuania took place at the end of the 19th century. This water mold first appeared in Europe in the mid-19th century and is currently known as a major causal agent responsible for the decline and massive mortalities of the native in European noble or broad-fingered crayfish (Astacus astacus) populations [37,38,77,78,79,80,81,82]. This rapidly expanding in the inner freshwater ecosystems crayfish plague pathogen usually does not invade in isolation but is dependent on co-invasion by its host. Initially, Aphanomyces astaci was introduced to Lithuania with its host—crayfish (Astacus leptodactylus) in 1886 and strongly reduced the population of native noble crayfish (Astacus astacus) in Duobžeris lake located in Rokiškis district [37]. Later, the spread of this crayfish parasite was especially facilitated by the introduction of the invasive North American crayfish species that serve as its reservoirs and vectors [78,80]. One of these hosts, the signal crayfish (Pacifastacus leniusculus), was introduced to Lithuania in about 1972 to supplement crayfish diversity and to increase fisheries of crayfish [83]. After its introduction, the crayfish plague epidemic have been recorded in many Lithuanian lakes up to 1979 [38,83]. During this period, native populations of noble crayfish Astacus astacus were practically destroyed in Lithuania, but after 1979, Aphanomyces astaci was not recorded and has been indicated as extinct [84]. The current status of Aphanomyces astaci is indicated as unknown because, nowadays, investigations on this crayfish pathogen are not conducted in Lithuania. However, in the 1990s, in Lithuanian, lakes and rivers appeared and began to spread the other invasive North American spiny-cheek crayfish Orconectes limosus, which is also known as the main host of Aphanomyces astaci [85,86,87]. Currently, the ongoing expansion of this spiny-cheek crayfish in Lithuania [88,89] undoubtedly increases the risk of reintroduction of new genetically distinct strains of Aphanomyces astaci and, as a result, increases the possibility of crayfish plague disease outbreak in Lithuania. Recent studies carried out in central Europe showed that the disease transmission risk may vary substantially between the different populations of native crayfish [90]. The absence of Aphanomyces astaci infection in some coexisting populations of the introduced spiny-cheek crayfish and the native noble crayfish confirmed the suggestion that the long-term coexistence of North American and European crayfish species probably resulted in pathogen virulence reduction in some local European freshwater ecosystems [90]. On the other hand, the immunity in the native noble crayfish populations has probably also increased, and that could have resulted in pathogen extinction. Currently, the crayfish aquarium trade may pose an additional risk of the crayfish plague disease reintroduction to the native water ecosystems. The health status of exotic crayfish kept in private aquaria is usually not monitored, and they can be infected by different, more aggressive, or new Aphanomyces astaci haplotypes [81,82], so control in aquaria is very important.

4.3. The Potato Blight Pathogen Phytophthora infestans and Grape Pathogen Plasmopara viticola

Among terrestrial crop pathogens, Phytophthora infestans is one of the most economically important, oldest, and best-investigated pathogens [27]. It infects Solanum, Lycopersicon, and Petunia plants. This Mexican/Andean species was introduced into Europe from North America in the middle of the 19th century, about 1843–1845 [91,92]. In Lithuania, this harmful and most devastating potato and tomato blight pathogen was recorded for the first time in 1912 [61] and, after that, widely spread across the country, causing epiphytoties and significant losses of potato and tomato yields every year [18,45,93,94,95,96]. The other most investigated in the world downy mildew pathogen, especially in the wine producing countries, the causal agent of grapevine downy mildew, Plasmopara viticola, is known in Europe since 1878, but in Lithuania appeared only in 1949 in Kaunas Botanical Garden. This North American species, after a presumably short adaptation period (less than 10 years), was found in 1955 in Vilnius Botanical Garden and afterward, year after year, showed an increasing tendency of spreading into new regions of Lithuania, affecting Vitis arisonica Engelm and Vitis vinifera L. [18,97]. However, P. viticola is not posing a significant threat to the Lithuanian economy, as there are no large grape plantations in the country.

4.4. The Most Harmful Phytophthora Invaders and Quarantine Species in Lithuania

Recently, three Phytophthora species, Ph. plurivora, Ph. alni, and Ph. cinnamomi, were included in the lists of the most harmful alien species or ‘worst’ invaders in Europe [98]. Two species from this list (Phytophthora alni and Phytophthora cinnamomi) have been found in Lithuania [39,47]. The cryptic alder pathogen Ph. alni is a causal agent of lethal root rot and collar disease of alder trees [31]. This species appeared for the first time in Europe in the United Kingdom in 1993 [30]; in Lithuania, it was detected in about 1999 [30] and is currently noted as spreading [46,47]. Recent taxonomical studies demonstrated that Ph. alni sensu lato represents a species complex composed of three distinct species: Ph. × alni, Ph. × multiformis and Ph. uniformis [31,71]. The parental species Ph. uniformis have possibly been introduced to Europe from North America, but future naturalization and hybridization with previously existing in Europe Ph. × multiformis led to the formation of extremely aggressive novel species Ph. × alni, which nowadays is widely spread in Europe [30,31,99]. Among riparian plants of streams, rivers and lakes, alder trees are highly vulnerable to Ph. alni species complex [71]. In Lithuania, two members of the Ph. alni sensu lato species complex, the novel species Ph. × alni and the oldest Ph. uniformis, are commonly found, infecting wet soil and alder trees growing mainly in moist riparian and alluvial forests [46,47]. The same tendency of Ph. alni sensu lato infection spread has been observed in Polish riparian ecosystems, where the decline of alder trees was commonly caused by Ph. × alni and by Ph. × multiformis [100]. At least 85 of the approximately 200 described Phytophthora species are currently known to have a predominantly saprotrophic aquatic lifestyle and may inhabit aquatic environments as litter decomposers or as potential opportunistic plant pathogens [24]. In Lithuania, Phytophthora spp. infection is commonly found on Alnus, Acer, Quercus, and Betula trees growing along the banks of water bodies in areas with excessive soil moisture and is considered a soilborne pathogen [70]. Phytophthora cinnamomi was discovered in our country around 2000, infecting Pinus and Quercus trees [39], but its distribution in Lithuania currently remains unknown. Notably, Ph. cinnamomi can also infect various fruit trees, nut trees, and other ornamental plants—about 5000 plant species in total [101]. The other species, Phytophthora cactorum, was found for the first time in 2004 in the Kaunas Botanical garden (Central Lithuania) and in the Šiauliai University Botanical garden (Northern Lithuania) in rhododendrons collections. Next year, in 2005, Ph. cactorum was detected on rhododendrons imported from Poland, demonstrating that infected planting material of ornamental plants imported from south-eastern European countries could be the vector of its spread [41]. This pathogen was known in Europe (Germany) from 1870 and has a very broad host range, about 250 plant species [66,102,103]. The large number of potential hosts in such generalist pathogens as Ph. cinnamomi and Ph. cactorum indicates a high risk of their jump on other hosts, successful adaptation and spread in Lithuania in the future.

The invasive quarantine species Ph. fragaria was detected in Lithuania in 2004 on strawberries, and according to the quarantine requirements, all infected plans were destroyed [40,104], but strawberries are widely grown in Lithuania in private gardens, and they are not controlled by phytosanitary inspectors; thus, real Ph. fragaria distribution is unknown. In 2007, the other invasive quarantine species, Ph. ramorum, was detected for the first time on Rhododendron catawbiense plants imported from Poland in the Marijampole region. After eradication until 2019, this pathogen was not detected, but in June 2019, Ph. ramorum was detected again on planted rhododendrons in the garden of the municipality of Dauparai-Kvietiniai, located in Klaipėda region [63]. Currently, these two quarantine pathogens, Ph. fragaria and Ph. ramorum, are under strict control, and the current status of Ph. ramorum in Lithuania is officially declared as ‘present, few occurrences, under eradication’. Meantime, Ph. fragaria is noted as present with restricted distribution in Lithuania [63,104].

5. Adaptation and Spreading Ability of Alien Plant Pathogenic Oomycota

Various alien stramenopilous fungus-like (Oomycota) organisms detected in Lithuania demonstrated different adaptations and spreading abilities to new environmental conditions. All aquatic and soil-inhabiting Phytophthora species are known as rapidly spreading generalists, but terrestrial specialized plant pathogenic Peronospora species are characterized by different adaptation and distribution abilities [24]. The ability of unspecialized and specialized generalist pathogens to become successful invaders is likely due to their ability to infect a wide range of new hosts under suitable environmental conditions and spread over long distances [3]. The emergence and prevalence of specialized plant pathogens also depend on the aggressiveness of the pathogen, as well as on the vulnerability and distribution of its hosts [2]. It is evident that current climate change affects both plants and their pathogens and that environmental disturbances, severe episodes of drought and heat, severe storms, and floods increase stress levels in plants. All of these factors can alter the rate of adaptation of new pathogens, contributing to the emergence of new diseases [105].

To the group of rapidly spreading in Lithuania invasive pathogens, in addition to abovementioned Albugo candida, Phytophthora infestans and Plasmopara viticola, also belong to Pseudoperonospora humuli, the causal agent of hop and hemp downy mildew. This hop pathogen was described in Japan initially as Peronoplasmopara humuli at the beginning of the 20th century [106]. In Europe, Ps. humuli appeared around 1920 [107], and soon in 1927 was found in Lithuania [57]. Then, within a few decades, Ps. humuli spread widely on Humulus lupulus L. throughout the country [18,50]. The other, closely related to Ps. humuli, harmful and rapidly spreading cucumber pathogen Pseudoperonospora cubensis was introduced to Europe from Central America (Cuba) in about 1971; in Lithuania, it appeared in 1985, and in the same year, it spread extremely rapidly across the country, causing epiphytoty on Cucumis sativus L. cultivated in greenhouses and in open soil [18,64]. Starting from 1984, Ps. cubensis has become the most economically important invasive pathogen on various Cucurbitaceae plants in Central Europe—cucumbers, melons, squashes, gourds, and watermelons [108,109,110,111,112]. Ps. cubensis also can infect Cannabaceae and Balsaminaceae plants [75,113]. The genetic studies indicated that the pathogen’s ability to hybridize is one of the most important drivers of invasions and that current epidemics of cucurbits are caused not by a single race but evidently by a recently appeared new subspecies or hyper-virulent hybrids of Ps. cubensis, characterized by a high degree of adaptability and ecological plasticity [114,115].

The rapidly spreading species also belongs to pea downy mildew Peronospora viciae (syn. P. pisi) and onion downy mildew P. destructor. Both pathogens appeared in Lithuania in the first part of the 20th century [57,59] and soon became widely spread over the country. During rainy summers, these pathogens demonstrated very rapid spread, causing serious outbreaks of epiphytotic diseases [50,51,52,64]. The onion downy mildew pathogen P. destructor was recorded on eight Allium species in Lithuania, but A. cepa L. is among the most damaged onion species, which during epidemics could become infected up to 80–100% [18,52]. About the same time, in 1926, the most harmful oomycete pathogen of lettuce was Bremia lactucae [54], which also rapidly spread and soon became very common in Lithuania [18].

Many species of Peronospora and Hyaloperonospora genera, such as P. aestivalis, P. arborescens, P. grisea, P. hyoscyami, P. farinose, P. lamii, P. trifoliorum, and P. violae, as well as H. barbareae, H. berteroae, H. camelinae, H. parasitica, and H. hesperidis, appeared about the middle of the 20th century, but it took more time (several decades) for its adaptation, naturalization, and distribution across the territory of Lithuania [18]. Some species of Peronosporales had been introduced in the end of 20th century: Peronospora chlorae, P. corydalis-intermediae, P. fagopyr, P. ornithopi, P. phyteumatis, P. sparsa, Plasmopara angustiterminalis, Pl. pastinacae Pseudoperonospora cannabina, and Sclerophthora macrospora [18,50,64,65], but in most cases they were not widely spread (Table 1). Notably, Peronospora sparsa and P. fagopiri are sporadically occurring species in different districts of Lithuania [18]. Current investigations of downy mildew in Lithuania are very fragmentary, dealing with some economically important agricultural plants, such as onions, potatoes, tomatoes, grapes, and alfalfa, which are cultivated in our country [45,51,95,96,97,116,117].

6. Conclusions

This study showed a rather large number of alien fungus-like (Oomycota) pathogens registered in Lithuania and revealed their negative impact on native terrestrial and aquatic ecosystems, agriculture, forestry, and aquaculture. The great adaptability and efficient dispersal are the main drivers of the new oomycetous pathogen’s successful invasions. Early detection and continuous control of the emergence and spread of alien Oomycota, as well as immediate eradication of new and especially quarantine species, are very important tasks aimed at preventing and reducing the negative impact of these pests on plant health and productivity of native ecosystems. Among detected alien stramenopilous fungus-like organisms, Albugo, Bremia, Pseudoperonospora and especially Phytophthora species are the most harmful and rapidly spreading plant pathogens, causing significant economic losses in agriculture and silviculture. The crayfish plague pathogen Aphanomyces astaci requires additional attention, as there is a high probability of reintroduction of its new haplotypes to Lithuania and to other European countries, together with new invasive crayfish species. Not only alien but all oomycetous pathogens require strict control aiming to prevent outbreaks of latent and emerging infectious diseases (EIDs).