Global geographic distribution and host range of Dothistroma species: a comprehensive review

Rein Drenkhan; Nicola  La Porta

Dothistroma needle blight (DNB) is one of the most important diseases of pine. Although its notoriety stems from Southern Hemisphere epidemics in Pinus radiata plantations, the disease has increased in prevalence and severity in areas of the Northern Hemisphere, including Europe, during the last two decades. This increase has largely been attributed to expanded planting of susceptible hosts, anthropogenic dispersal of the causative pathogens and changes in climate conducive to disease development. The last comprehensive review of DNB was published in 2004, with updates on geographic distribution and host species in 2009. Importantly, the rec ognition that two species, Dothistroma septosporum and D. pini, cause DNB emerged only relatively recently in 2004. These two species are morphologically very similar, and DNA- based techniques are needed to distinguish between them. Consequently, many records of host species affected or geographic location of DNB prior to 2004 are inconclusive or even misleading. The objectives of this review were (i) to provide a new database in which detailed records of DNB from 62 countries are collated; (ii) to chart the current global distribution of D. septosporum and D. pini; (iii) to list all known host species and to consider their susceptibility globally; (iv) to collate the published results of provenance trials; and (v) to consider the effects of site factors on disease incidence and severity. The review shows that DNB occurs in 76 countries, with D. septosporum confirmed to occur in 44 and D. pini in 13. There are now 109 documented Pinaceae host taxa for Dothistroma species, spanning six genera (Abies, Cedrus, Larix, Picea, Pinus and Pseudotsuga), with Pinus being the dominant host genus, accounting for 95 host taxa. The relative susceptibilities of these hosts to Dothistroma species are reported, providing a resource to inform species choice in forest planting. Country records show that most DNB outbreaks in Europe occur on Pinus nigra and its subspecies. It is anticipated that the collaborative work described in this review will both underpin a broader global research strategy to manage DNB in the future and provide a model for the study of other forest pathogens.

Received: 6 December 2015 | Accepted: 16 May 2016 DOI: 10.1111/efp.12290 REVIEW ARTICLE Global geographic distribuion and host range of Dothistroma species: a comprehensive review R. Drenkhan1,* | V. Tomešová-Haataja2,* | S. Fraser3,* | R. E. Bradshaw4,* | P. Vahalík2,* | M. S. Mullet5,* | J. Marín-García6,7,* | L. S. Bulman8,* | M. J. Wingield9 | T. Kirisits10 | T. L. Cech11 | S. Schmitz12 | R. Baden5 | K. Tubby5 | A. Brown5 | M. Georgieva13 | A. Woods14 | R. Ahumada15 | L. Jankovský2 | I. M. Thomsen16 | K. Adamson1 | B. Marçais17 | M. Vuorinen18 | P. Tsopelas19 | A. Koltay20 | A. Halasz21 | N. La Porta22,23 | N. Anselmi24 | R. Kiesnere25 | S. Markovskaja26 | A. Kačergius27 | I. Papazova-Anakieva28 | M. Risteski28 | K. Soirovski28 | J. Lazarević29 | H. Solheim30 | P. Boroń31 | H. Bragança32 | D. Chira33 | D. L. Musolin34 | A. V. Selikhovkin34,35 | T. S. Bulgakov36 | N. Keča37 | D. Karadžić37 | V. Galovic38 | P. Pap38 | M. Markovic38 | L. Poljakovic Pajnik38 | V. Vasic38 | E. Ondrušková39 | B. Piškur40 | D. Sadiković40 | J. J. Diez6,7 | A. Solla41 | H. Millberg42 | J. Stenlid42 | A. Angst43 | V. Queloz43 | A. Lehijärvi44 | H. T. Doğmuş-Lehijärvi45 | F. Oskay46 | K. Davydenko47 | V. Meshkova47 | D. Craig48 | S. Woodward49 | I. Barnes9,* Insitute of Forestry and Rural Engineering, Estonian University of Life Sciences, Tartu, Estonia 1 Faculty of Forestry and Wood Technology, Mendel University, Brno, Czech Republic 2 Department of Plant and Soil Science, Forestry and Agricultural Biotechnology Insitute (FABI), University of Pretoria, Pretoria, South Africa 3 Bio-Protecion Research Centre, Insitute of Fundamental Sciences, Massey University, Palmerston North, New Zealand 4 Forest Research, Alice Holt Lodge, Farnham, Surrey, UK 5 Sustainable Forest Management Research Insitute, Unversity of Valladolid-INIA, Palencia, Spain 6 Department of Plant Producion and Forest, University of Valladolid (Palencia Campus), Palencia, Spain 7 Forest Protecion, Scion, Rotorua, New Zealand 8 9 Department of Geneics, FABI, University of Pretoria, Pretoria, South Africa Insitute of Forest Entomology, Forest Pathology and Forest Protecion (IFFF), Department of Forest and Soil Sciences, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, Austria 10 Federal Research and Training Centre for Forests, Department of Forest Protecion, Natural Hazards and Landscape (BFW), Vienna, Austria 11 Department of Life Sciences, Walloon Agricultural Research Centre, Gembloux, Belgium 12 Forest Research Insitute, Bulgarian Academy of Sciences, Soia, Bulgaria 13 Briish Columbia Ministry of Forests, Lands and Natural Resource Operaions, Smithers, BC, Canada 14 Bioforest SA, Concepción, Chile 15 Department of Geosciences and Natural Resource Management, Faculty of Science, University of Copenhagen, Frederiksberg, Denmark 16 NRA, Nancy Universit́, UMR 1136 Interacions Arbres Microorganismes, Champenoux, France 17 The Natural Resources Insitute Finland (Luke), Suonenjoki, Finland 18 19 Insitute of Mediterranean Forest Ecosystems, Athens, Greece Department of Forest Protecion, Hungarian Forest Research Insitute, Mátrafüred, Hungary 20 *Equally contribuing authors For. Path. 2016; 1–35 wileyonlinelibrary.com/efp © 2016 Blackwell Verlag GmbH | 1 | 2 Drenkhan et al. Naional Food Chain Safety Oice, Directorate of Plant Protecion, Soil Conservaion and Agri-environment, Plant Health and Molecular Biology Laboratory, Budapest, Hungary 21 IASMA Research and Innovaion Centre, Fondazione Edmund Mach, San Michele all’Adige, Trento, Italy 22 MOUNTFOR Project Centre, European Forest Insitute, Trento, Italy 23 Department for Innovaion in Biological Agrofood and Forest Systems (DiBAF), University of Tuscia, Viterbo, Italy 24 Latvian State Forest Research Insitute, Salaspils, Latvia 25 Laboratory of Mycology, Nature Research Centre, Vilnius, Lithuania 26 Vokė Branch of Lithuanian Research Centre for Agriculture and Forestry, Trakų Vokė, Lithuania 27 Faculty of Forestry, University ‘Ss Cyril and Methodius’ - Skopje, Skopje, Republic of Macedonia 28 29 Biotechnical Faculty, University of Montenegro, Podgorica, Montenegro Norwegian Insitute of Bioeconomy Research, Ås, Norway 30 Department of Forest Pathology, Mycology and Tree Physiology, University of Agriculture in Kraków, Kraków, Poland 31 Insituto Nacional de Invesigação Agrária e Veterinária, Oeiras, Portugal 32 Naional Insitute for Research and Development in Forestry ‘Marin Drăcea’, Closca, Romania 33 St. Petersburg State Forest Technical University, Saint Petersburg, Russia 34 St. Petersburg State University, Saint Petersburg, Russia 35 Southern Federal University, Rostov-on-Don, Russia 36 Faculty of Forestry-University of Belgrade, Belgrade, Serbia 37 Insitute of Lowland Forestry and Environment, University of Novi Sad, Novi Sad, Serbia 38 39 Slovak Academy of Science, Insitute of Forest Ecology Zvolen, Branch for Woody Plants Biology Nitra, Nitra, Slovak Republic Department of Forest Protecion, Slovenian Forestry Insitute, Ljubljana, Slovenia 40 Ingeniería Forestal y del Medio Natural, Universidad de Extremadura, Plasencia, Spain 41 Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden 42 Swiss Federal Research Insitute WSL, Birmensdorf, Swizerland 43 Faculty of Forestry, Bursa Technical University, Osmangazi, Bursa, Turkey 44 Faculty of Forestry, Süleyman Demirel University, Isparta, Turkey 45 Faculty of Forestry, Çankırı Karatekin University, Çankırı, Turkey 46 Ukrainian Research Insitute of Forestry & Forest Melioraion and Ukrainian State Forest Protecion Service, Kharkiv, Ukraine 47 Agri-Food and Biosciences Insitute, Belfast, UK 48 49 Insitute of Biological and Environmental Sciences, Department of Plant and Soil Science, University of Aberdeen, Aberdeen, UK Correspondence Rein Drenkhan, Insitute of Forestry and Rural Engineering, Estonian University of Life Sciences, Tartu, Estonia. Email: rein.drenkhan@emu.ee Summary Editor: M. Cleary Northern Hemisphere, including Europe, during the last two decades. This increase Dothistroma needle blight (DNB) is one of the most important diseases of pine. Although its notoriety stems from Southern Hemisphere epidemics in Pinus radiata plantaions, the disease has increased in prevalence and severity in areas of the has largely been atributed to expanded planing of suscepible hosts, anthropogenic dispersal of the causaive pathogens and changes in climate conducive to disease development. The last comprehensive review of DNB was published in 2004, with updates on geographic distribuion and host species in 2009. Importantly, the recogniion that two species, Dothistroma septosporum and D. pini, cause DNB emerged only relaively recently in 2004. These two species are morphologically very similar, and DNA-based techniques are needed to disinguish between them. Consequently, many records of host species afected or geographic locaion of DNB prior to 2004 are inconclusive or even misleading. The objecives of this review were (i) to provide a new database in which detailed records of DNB from 62 countries are collated; (ii) to chart the current global distribuion of D. septosporum and D. pini; (iii) to list all known host species and to consider their suscepibility globally; (iv) to collate | Drenkhan et al. 3 the published results of provenance trials; and (v) to consider the efects of site factors on disease incidence and severity. The review shows that DNB occurs in 76 countries, with D. septosporum conirmed to occur in 44 and D. pini in 13. There are now 109 documented Pinaceae host taxa for Dothistroma species, spanning six genera (Abies, Cedrus, Larix, Picea, Pinus and Pseudotsuga), with Pinus being the dominant host genus, accouning for 95 host taxa. The relaive suscepibiliies of these hosts to Dothistroma species are reported, providing a resource to inform species choice in forest planing. Country records show that most DNB outbreaks in Europe occur on Pinus nigra and its subspecies. It is anicipated that the collaboraive work described in this review will both underpin a broader global research strategy to manage DNB in the future and provide a model for the study of other forest pathogens. 1 | INTRODUCTION D. pini Hulbary, represening the lineage that was found in the USA ater the descripion of Hulbary (Hulbary, 1941), and D. septosporum Dothistroma needle blight (DNB) is one of the most damaging foliage (Dorogin) M. Morelet, represening the linage that included isolates diseases in natural pine stands and plantaions worldwide (Barnes, from many diferent parts of the world, including Europe. Following Crous, Wingield, & Wingield, 2004; Bulman, Ganley, & Dick, 2008; the “One fungus, one name” rule of fungal nomenclature, earlier sex- Jankovský, Bednářová, & Palovčíková, 2004; Karadžić, 1989a). The ual names for D. septosporum (Mycosphaerella pini and Scirrhia pini), are disease irst emerged as a serious problem in the 1950s and 1960s no longer valid (Crous, Hawksworth, & Wingield, 2015; Hawksworth, in plantaions of Pinus radiata in the Southern Hemisphere and on 2011). As it currently stands, DNB is caused by either one of two fun- a number of pine species in North America (Gibson, 1972, 1974). It gal species: D. pini Hulbary, designated with an epitype from Michigan, signiicantly curtailed large-scale pine planing of P. radiata in East the USA, and D. septosporum (Dorogin) M. Morelet, designated with a Africa (Gibson, 1974) and India (Bakshi & Singh, 1968) and conin- neotype from St. Petersburg, Russia (Barnes et al., 2016). ues to be a major constraint for pine plantaion forestry in New Zea- Dothistroma needle blight occurs in almost every country where land, Chile and other areas of the Southern Hemisphere (Ahumada, suscepible hosts are found, a range that includes climates from 2013; Bulman et al., 2013; Rodas, Wingield, Granados, & Barnes, tropical to subarcic (Wat et al., 2009). Although D. septosporum is 2016). Since the 1990s, DNB has increased in incidence and severity reported to have a worldwide distribuion, its exact distribuion based in the Northern Hemisphere, especially in Canada and, more recently, on reports validated using molecular methods has never been mapped. in some European countries (Barnes, Wingield, Carbone, Kirisits, & In contrast, D. pini appears to have a more limited geographic distri- Wingield, 2014; Bradshaw, 2004; Drenkhan, Hantula, Vuorinen, buion based on reports from north-central USA and Europe (Barnes, Jankovský, & Müller, 2013; Hanso & Drenkhan, 2008; Markovskaja Kirisits, Wingield, & Wingield, 2011; Barnes, Walla, Bergdahl, & & Treigienė, 2009; Millberg, Hopkins, Boberg, Davydenko, & Stenlid, Wingield, 2014; Barnes et al., 2004; Barnes, Kirisits et al., 2008; Ioos 2016; Müller, Hantula, & Vuorinen, 2009; Solheim & Vuorinen, 2011; et al., 2010; Piškur, Hauptman, & Jurc, 2013; Queloz, Wey, & Hold- Welsh, Lewis, & Woods, 2014). The rising incidence and severity of enrieder, 2014; Siziba et al., 2016). Similarly, although more than 82 DNB in the Northern Hemisphere has been linked to changing climaic pine species, as well as a growing number of non-pine species in the condiions, paricularly higher temperatures and changes in precipita- Pinaceae, have been recorded as hosts of Dothistroma species (Bed- ion paterns conducive for disease development (Hanso & Drenkhan, nářová, Palovčíková, & Jankovský, 2006; Drenkhan, Adamson, Jürimaa, 2013; Wat, Kriicos, Alcaraz, Brown, & Leriche, 2009; Welsh et al., & Hanso, 2014; Wat et al., 2009), the exact number of hosts afected 2014; Woods et al., 2016). by each of the pathogen species is unknown. There is no single body The causal agents of DNB are ascomycete fungi that have undergone a number of taxonomic name changes (Barnes et al., 2004, 2016). of literature that synthesizes all the current knowledge regarding the distribuion and host range of the two DNB pathogens. Up unil 2004, DNB was considered to be caused by one pathogen An ongoing problem for researchers dealing with DNB is that it is species with occasional variety designaions (Suton, 1980). It was not possible to know which species was being studied or referred to interchangeably referred to in the literature as either Dothistroma in some of the literature published prior to 2004, paricularly from the septospora (septosporum), Dothistroma pini, Mycosphaerella pini or Scir- Northern Hemisphere, where both species are now known to co-occur rhia pini. Taxonomic clarity was established when Barnes et al. (2004) in some regions. Furthermore, D. septosporum and D. pini produce showed that isolates causing DNB reside in two diferent phylogeneic similar symptoms on their hosts (Barnes et al., 2011) and it is almost lineages represening disinct species. The two species were named impossible to discriminate between the two pathogens based on 4 | Drenkhan et al. morphological characterisics (Anonymous, 2008; Barnes et al., 2004). DNA-based ideniicaion techniques, including direct sequencing 2 | The geographic range of DNB and its causal agents of gene regions such as the Internal Transcribed Spacer (ITS) region Dothistroma needle blight occurs across a wide range of climates (Barnes et al., 2016) therefore remain the only reliable opion for the (Wat et al., 2009) showing that the disease agents tolerate highly correct determinaion of species of Dothistroma (Barnes et al., 2011, variable climaic condiions (see secion 5). The last published synthesis 2016; Ioos et al., 2010). Ioos et al. (2010) developed convenional and of the distribuion of DNB was by Wat et al. (2009) who docu- real-ime PCR methods for the rapid detecion of D. septosporum and mented the presence of the disease in 61 countries. Due to the D. pini, as well as Lecanosicta acicola (Thüm.) Syd., the brown spot problems associated with idenifying the species of Dothistroma involved, needle blight pathogen with which the DNB pathogens are oten con- the speciic distribuions of the two DNB pathogens were not dif- fused. These methods can be used to idenify species associated with fereniated. Results of collated publicaions and reports from 40 DNB outbreaks and also to validate species directly from herbarium countries in collaboraion with DIAROD (see Supporing Informaion) specimens or collecions linked to older literature (Fabre, Ioos, Piou, have provided the most comprehensive documented distribuion of & Marçais, 2012). DNB to date and, more speciically, the global distribuion of both The incidence and severity of DNB is strongly inluenced by both pathogens causing this disease. In compiling this review, we found environmental/climaic condiions (Peterson, 1973; Woods, Coates, that DNB occurs in 76 diferent countries (Table 1; Figs 1 and 2). & Hamann, 2005; Woods et al., 2016) and host suscepibility (Fraser, New country reports since Wat et al., (2009) include those from Woodward, & Brown, 2015; Ivory, 1968; Rodas et al., 2016). Mois- Belarus, Belgium, Estonia, Finland, Latvia, Lithuania, Netherlands, ture is a key environmental factor, as DNB outbreaks occur in areas or Norway, Russia (including Far East Russia), Sweden, Turkey, Bhutan, years with high levels of summer rainfall or frequent warm rain events Kazakhstan and Bolivia (see Table 1 for references). Although Nicaragua (Woods et al., 2005, 2016). Host species and provenance also afect and North Korea were reported to have DNB (Wat et al., 2009), DNB severity with several reports of both inter- and intraspeciic vari- we found no evidence or valid references to support these claims; aion in suscepibility to Dothistroma species (e.g. Cobb & Miller, 1968; however L. acicola (oten confused with Dothistroma species) was Fraser, Woodward et al., 2015; Ivory, 1968). The relaive suscepibil- reported as present in Nicaragua (Evans, 1984). In terms of species ity of host species and provenances oten varies across sites (Fraser distribuion, D. septosporum has a worldwide distribuion, having been Mullet, Woodward, & Brown, 2016; Wat et al., 2009). This variability conirmed using molecular methods in 44 countries across Europe, demonstrates the importance of the interacions between pathogen, Asia, the Americas, Africa and Oceania (Table 1; Fig. 2). In contrast, host and environment in deining DNB severity. Collaing informaion D. pini has a substanially restricted distribuion, having only been on these three factors, paricularly host suscepibility, will contribute detected in 13 countries on two coninents in the Northern Hemisphere: to the development of management guidelines for foresters. North America (in the USA) and Europe. The speed at which new reports of DNB have appeared over the An interacive map generated in this study, and available at htp:// last two decades, and the suggesion that increased incidence may arcgis.mendelu.cz/monitoring/, currently contains the geographic co- be related to changes in climate, pathogen virulence and/or anthro- ordinates of 3232 sampling or observaion records (as well as records pogenic movement of infected plant material is of great concern. for 37 countries and states where geographical co-ordinates are not Developing new tacics to manage and limit the impact of this globally known) and documents the presence of both species in 76 countries. important disease is clearly important. To accomplish this goal, it is These data are summarized in Table 1, Figs 1 and 2. Below we high- essenial to consolidate knowledge of the global distribuion of both light key trends in disease distribuion for each coninent, with a major D. septosporum and D. pini, their host ranges, as well as host suscep- focus on Europe. ibility and environmental factors that afect disease severity. Consequently, an important objecive of this review has been to collate so-called grey literature, together with more accessible literature, to provide a summary of the host and geographic distribuion of the DNB 2.1 | Europe Dothistroma needle blight has been recorded in 35 of 50 European pathogens. An important secondary goal is to highlight disease trends countries, with D. septosporum and D. pini conirmed, using molecular at both spaial and temporal scales. Although a global framework is methods, in 29 and 12 of these countries, respecively (Table 1; presented, the main focus is on highlighing recent trends in Europe, Fig. 2). The oldest record of DNB from Europe, and in fact in consistent with the goals and objecives of the DIAROD EU COST the world, comes from herbarium samples collected in Denmark Acion FP1102 (Determining Invasiveness And Risk Of Dothistroma, in 1880 (Munk, 1957). Inspecion of herbarium collecions from htp://www.cost.eu/COST_Acions/fps/Acions/FP1102?). France suggests that DNB has also been present in north-eastern A pracical and ongoing outcome of the work described here is a France since 1907 (Fabre et al., 2012). The irst descripion of new database with an interacive map including historical and updated the pathogen (as Cytosporina septospora Dorogin) causing DNB was monitoring informaion for DNB, available at htp://arcgis.mendelu.cz/ made from Pinus montana (a synonym of Pinus mugo) samples monitoring/. The map provides detailed informaion for the locaions collected in north-west Russia in 1910 (Doroguine, 1911), and where DNB has been reported and, where molecular conirmaion of symptoms of DNB were also present on herbarium samples of the pathogen is available, the species causing the disease is mapped. P. sylvestris collected by L. Kaznowski in 1914 in the Kiev region | Drenkhan et al. TABLE 1 5 The geographic distribuion of Dothistroma needle blight in diferent countries including the date the disease was irst recorded. Coninent/Country/ State Year DNB was irst recorded References Africa Ethiopia Kenya Malawi South Africa Swaziland Tanzania Uganda Zambia Zimbabwe 1972 1960 1961 1965 1967 1957 1964 1994 1943 Gibson (1972) Gibson et al. (1964) Bates (1962) Gibson (1972) Gibson (1972) Gibson et al. (1964) Gibson et al. (1964) Ivory (1994) Gibson et al. (1964) Asia Bhutan Brunei China India Japan Kazakhstan Nepal Pakistan Philippines Russian Far East South Korea Sri Lanka Turkey (Asian part) 2005 1972 1987 1968 1952 1992 1985 1986 1987 2014 1983 1987 2013 Barnes, Kirisits et al. (2008) Peregrine (1972) Ivory (1987) Bakshi and Singh (1968) Ito et al. (1975) Arapova (1992) Ivory (1990) Zakaullah and Abdul (1987) Ivory (1987) Barnes et al. (2016) Kim and Yi (1984) Ivory (1987) F. Oskay, unpubl. data Europe Austria Belarus 1960 2012 Belgium Bosnia-Herzegovina Bulgaria Croaia Czech Republic 2007 1988 1977 1963 2000 Denmark Estonia Finland France Georgia Germany Greece DS DP References * Barnes et al. (2004) * Barnes et al. (2004) * Barnes, Kirisits et al. (2008) * Barnes et al. (2016) * F. Oskay, unpubl. data Petrak (1961) V. Zviagintsev, unpubl. data * * * * * * 1880 2006 2007 1907 1965 1983 1969 EPPO (2008) Karadžić (1989a) Zlatanov (1977) Milatović (1976) Jankovský, Šindelková, and Palovčíková (2000) Munk (1957); Evans (1984) Hanso and Drenkhan (2008) Müller et al. (2009) Morelet (1968); Fabre et al. (2012) Shishkina and Tsanava (1966b) Buin and Richter (1983) Kailidis and Markalas (1981) Barnes et al. (2004) S. Markovskaja and A. Kačergius, unpubl. data Schmitz, Gischer, and Chandelier (2013) * * * * * * * Hungary 1990 Szabó (1997); Koltay (1997) * Italy Latvia 1976 2008 Magnani (1977) Drenkhan and Hanso (2009) * Lithuania 2002 Jovaišienė and Pavilionis (2005) * Macedonia Montenegro Netherlands Norway Poland Portugal 1980 1979 2007 2009 1990 1984 Portugal incl. Azores Romania 1979 1968 Papazov (1988) Karadžić (1986) EPPO (2007) Solheim and Vuorinen (2011) Kowalski and Jankowiak (1998) Neves, Moniz, De Azevedo, Ferreira, and Ferreira (1986) Fonseca (1980) Gremmen (1968) * * * * * * * * Tomšovský et al. (2013); Bergová and Kryštofová (2014); Barnes et al. (2016) Barnes et al. (2016) Hanso and Drenkhan (2008) Müller et al. (2009) Ioos et al. (2010) Barnes et al. (2004) Tsopelas, Barnes, Soulioi, and Wingield (2013) Barnes, Kirisits et al. (2008); Barnes et al. (2011) Drenkhan and Hanso (2009); Kiesnere (2014) A. Kačergius and S. Markovskaja, unpubl. data * * Lazarević, Davidenko, and Millberg (2015) Quaedvlieg et al. (2012) Solheim and Vuorinen (2011) Barnes et al. (2004) H. Bragança, unpubl. data H. Bragança, unpubl. data Barnes, Wingield et al. (2014); Barnes et al. (2016) (Coninues) 6 | Drenkhan et al. TABLE 1 (coninued ) Year DNB was irst recorded References DS DP References Russia 1910 Doroguine (1911) * * Serbia 1955 Krsić (1958); Karadžić (1986) * * Slovakia Slovenia Spain 1996 1971 1974 Kunca and Fofová (2000) Maček (1975) Fernández (1975) * * * * * Sweden Switzerland Turkey Ukraine 2007 1989 2013 1914 * * * * United Kingdom England Northern Ireland Scotland Wales Millberg et al. (2016) A. Angst, unpubl. data F. Oskay, unpubl. data Barnes et al. (2004); Barnes, Kirisits et al. (2008) Barnes, Kirisits et al. (2008); Musolin et al. (2014) Galovic et al. (2011, 2015); N. Keča, R. Drenkhan, H. Solheim, unpubl. data. Barnes et al. (2004) Piškur et al. (2013) Oriz de Urbina et al. (2015); Barnes et al. (2016) Millberg et al. (2016) Queloz et al. (2014) F. Oskay, unpubl. data Groenewald et al. (2007); Davydenko (2014) 1954 2014 1985 1958 Murray and Batko (1962) D. Craig, unpubl. data Briish Mycological Societya Brown and Webber (2008) * * * * Barnes et al. (2016) D. Craig, unpubl. data Barnes et al. (2016) M. S. Mullet, unpubl. data Oceania Australia New South Wales Queensland Tasmania Victoria New Zealand Papua New Guinea 1975 1980 1984 1979 1964 1997 Edwards and Walker (1978) Eldridge, Dowden, and Lind (1980) Podger (1984) Marks (1981) Gilmour (1965) EPPO (2015) * Barnes et al. (2004) * Prihaini et al. (2015) * Barnes et al. (2004) North America Canada Alberta Briish Columbia Manitoba Newfoundland Ontario Quebec Saskatchewan Jamaica Mexico 1999 1941 1966 2000 1991 2000 1966 1982 1979 Reid, Mathur, Basu, and Penner (1999) DAVFPe record 2077 Elliot, Laut, and Brandt (1967) Pister, Halik, and Bergdahl (2000) Myren (1991) Pister et al. (2000) Elliot et al. (1967) Evans (1984) Gibson (1979) * Barnes et al. (2004); Dale et al. (2011) * Barnes et al. (2016) 1982 1973 1967 Unknown Peterson (1982) Peterson (1973) Cobb and Miller (1968) Widely prevalent fungi of the United Statesb Widely prevalent fungi of the United Statesb Anonymous (1977) Ivory (1987) Evans (1984) Saccardo (1920); Peterson (1982) Peterson (1982) Hulbary (1941) Rogerson (1953); Peterson (1982) Peterson (1982) Peterson (1982) Peterson (1982) Nicholls and Hudler (1971) Peterson (1982) Thyr and Shaw (1964) Peterson (1967b) * Barnes et al. (2004) Coninent/Country/ State United States of America Alaska Arizona California Colorado Delaware Unknown Florida Hawaii Idaho Illinois Indiana Iowa Kansas Kentucky Maryland Michigan Minnesota Missouri Montana Nebraska 1975 1987 1917 1917 1973 1934 1951 1973 1973 1973 1971 1973 1914 1950 * * * Barnes, Walla et al. (2014) * * Barnes et al. (2004) Barnes et al. (2004) * Barnes, Walla et al. (2014) Barnes et al. (2004) * | Drenkhan et al. TABLE 1 7 (coninued ) Coninent/Country/ State Year DNB was irst recorded References DS DP References * Barnes, Walla et al. (2014) New Hampshire New Mexico 1988 2006 New York North Dakota Ohio Oklahoma Oregon Pennsylvania South Dakota Tennessee Texas Vermont Virginia Washington Wisconsin 1992 2010 1932 1934 1972 1982 2011 1989 1991 1994 1972 1973 1973 NAPISc Fairweather, McMillin, Rogers, Conclin, and Fitzgibbon (2006) NAPISc Barnes, Walla et al. (2014) Hulbary (1941) Hulbary (1941) Peterson and Harvey (1976) Peterson (1982) Barnes, Walla et al. (2014) NAPISc NAPISc Pister et al. (2000) Skelly (1972) Peterson (1981) Peterson (1981) 1980 1983 1981 Ford (1982); Evans (1984) Evans (1984) Evans (1984) * Groenewald et al. (2007) 1968 1995 1969 1965 2008 1982 1979 1967 Fresa (1968) Herb IMI 367865d Figueiredo and Namekata (1969) Dubin and Staley (1966) Rodas et al. (2016) Evans and Oleas (1983) Gibson (1979) Peterson (1969) * * * * Groenewald et al. (2007) Barnes et al. (2004) Rodas et al. (2016) Barnes et al. (2004) Central America Costa Rica Guatemala Honduras South America Argenina Bolivia Brazil Chile Colombia Ecuador Peru Uruguay Barnes et al. (2004) * * Barnes, Walla et al. (2014) *Indicates if the idenity of either pathogen, DS for Dothistroma septosporum, and DP for D. pini, was ideniied in the country using molecular methods. Briish Mycological Society. The Fungal Records Database of Britain and Ireland. htp://www.ieldmycology.net/FRDBI/FRDBIrecord.asp?intGBNum=7910. b Widely prevalent fungi of the United States. htp://www.prevalenfungi.org/subject.cfm?id=688. c NAPIS = Naional Agricultural Pest Informaion System, Purdue University. “Survey Status of Dothistroma needle blight - Dothistroma septosporum (All years).” Published: 06/02/2015. htp://pest.ceris.purdue.edu/map.php?code=FBAVDDX&year=allime. Accessed: 06/02/2015. d htp://www.herbimi.info/herbimi/specimen.htm?imi=367865. e DAVFP (Department of Agriculture, Victoria, Forest Pathology): Fernando, A.; Ring, F.; Lowe, D.; Callan, B., 1999: Informaion Report BC-X-385 “Index of plant pathogens, plant-associated microorganisms and forest fungi of Briish Columbia” htp://cfs.nrcan.gc.ca/herbarium/fungus/2071?lang=en_CA. a of Ukraine. Unfortunately, all the original herbarium material from start of a rapid increase in reports of the disease in the Balic countries Denmark and Russia has been lost, and molecular conirmaion of and Fennoscandia between 2006 and 2009 (Hanso & Drenkhan, 2008; the species causing the disease on the old herbarium specimens Millberg et al., 2016; Müller et al., 2009; Solheim & Vuorinen, 2011). from Ukraine has not been successful. It is therefore sill unknown The disease is now widespread and commonly encountered in these which of the two Dothistroma species was responsible for these countries (Drenkhan & Hanso, 2009; Markovskaja & Treigienė, 2009; early records of DNB in Europe. Millberg, 2015; Müller et al., 2009). Molecular ideniicaion of samples Ater the irst descripion of the DNB pathogen in 1911 (Doroguine, 1911), no new observaions of DNB were made in Europe unil 1954 collected from the abovemenioned countries in recent years has conirmed the presence of D. septosporum (Table 1). when the disease was found on P. nigra and Pinus ponderosa nursery The presence of D. pini in Europe spans an area from Spain to Rus- stock in England (Murray & Batko, 1962). In 1955, DNB was found on sia (Table 1; Fig. 2). The irst record of D. pini was based on isolates P. nigra in Serbia (Krsić, 1958). Between the 1960s and 1980s, reports collected in Ukraine (2004) and Russia (2006) on P. nigra subsp. pallasi- of DNB also came from several southern and central European coun- ana (Barnes, Kirisits et al., 2008). However, the oldest record of D. pini tries (Fig. 1; Table 1), but no serious damage was reported. It was only was on P. sylvestris herbarium material collected in France in 1907 and during the 1990s that the incidence and severity of DNB increased recently conirmed using real-ime PCR methods (Fabre et al., 2012). dramaically in several areas of Europe (Villebonne & Maugard, 1999; About half of the reports of DNB from France in recent years are associ- Brown & Webber, 2008; see also Supporing Informaion). A new record ated with D. pini, with the pathogen being mostly present in the south- of DNB in Lithuania in 2002 (Jovaišienė & Pavilionis, 2005) marked the ern part of the country (Fabre et al., 2012). Dothistroma septosporum 8 | Drenkhan et al. F I G U R E 1 The global distribution of Dothistroma needle blight (DNB) according to the date the disease was first recorded (see Table 1). DNB is confirmed based on literature and molecular methods, including 37 states and territories without geographical co-ordinates. The global emergence of the disease in time is shown in an additional interactive link “First record of DNB” on the monitoring map legend: http://arcgis. mendelu.cz/monitoring/ occurs in all countries of Europe where D. pini has been reported. In of the Dothistroma species on this coninent. The presence of the majority of these cases, both pathogens have been found in the D. septosporum has been conirmed in Bhutan (Barnes, Kirisits et al., same regions (Fig. 2, see interacive map) and can even co-occur on 2008) and Far East Russia (Barnes et al., 2016), but the causal the same needle (Barnes et al., 2011; Piškur et al., 2013). agent of DNB in the other Asian countries is unknown. Dothistroma To date, DNB has not been reported in iteen European countries. pini has never been reported in the region. These countries include Albania, Andorra, Armenia, Azerbaijan (partly The irst observaion of DNB in Asia was in 1952 from Japan (Ito, in Asia), Cyprus, Iceland, Republic of Ireland, Kosovo, Liechtenstein, Zinno, & Suto, 1975), where it was mostly found on exoic pine species Luxembourg, Malta, Republic of Moldova, Monaco, San Marino and in Honshu and Hokkaido. Ito et al. (1975) also found DNB on two naive Vaican City. Many of these countries are small, where the number of species, P. densilora and P. thunbergii, although serious damage was not suscepible species is low or the forest area is limited (e.g. Iceland has observed. The disease was subsequently reported in India on exoic P. radi- a forest area of only 0.3%). In other countries, however, where the for- ata, where it led to the abandonment of this species for forestry (Bakshi est area is larger (e.g. 43% in Liechtenstein and 28% in Albania) and & Singh, 1968). Later, DNB was reported in Brunei (Peregrine, 1972) and where conifer species grow naturally or are culivated (Karoles & Relve, on naive P. wallichiana in high alitude areas in Nepal (Ivory, 1990) (Fig. 2). 2013), Dothistroma species are probably present, but have not yet been detected, most likely due to limited forest surveillance for this disease. This is probably also the case for the Republic of Ireland, where Pinus contorta is a commonly used forest plantaion species, given that DNB was observed in Northern Ireland in 2014 (D. Craig, unpublished data). 2.2 | Asia 2.3 | North America In North America, DNB has been reported from the USA, Canada, Mexico and Jamaica (Table 1; Fig. 1). DNB was recorded in Mexico in 1979 and in Jamaica in 1982 (Evans, 1984; Gibson, 1979), but the causal agents in these countries have not been determined. In the USA, the disease has been reported in 34 of the 50 states Dothistroma needle blight has been reported in 13 Asian countries (Table 1; Fig. 2). The earliest reports of DNB in the USA were (Table 1, Fig. 2); however, litle is known regarding the distribuion from P. ponderosa needles collected in 1914 from Montana (Thyr | Drenkhan et al. 9 F I G U R E 2 The geographic distribution of Dothistroma needle blight (DNB). Molecular methods were used to identify the causal agents of DNB: species are shown by different colours. Where this information was not available, the presence of DNB (identified using morphological methods) is shown (see map: http://arcgis.mendelu.cz/monitoring/) & Shaw, 1964) and from Idaho and Illinois in 1917 on P. ponderosa (Table 1; Fig. 1) and has caused extensive defoliaion and mortality (Evans, 1984; Saccardo, 1920). In the USA, D. septosporum has in P. contorta var. laifolia plantaions since the 1990s (Welsh et al., been conirmed only in the north-western states of Idaho, Montana 2009; Woods et al., 2005). The pathogen responsible for these dis- and Oregon (Barnes et al., 2004; Barnes, Walla et al., 2014) and ease epidemics in Briish Columbia was conirmed to be D. septospo- it has not emerged as a serious problem in these areas. In contrast, rum (Barnes et al., 2004; Dale, Lewis, & Murray, 2011). the irst molecular conirmaion of D. pini in 2004 was based on isolates obtained from Michigan, Nebraska and Minnesota, all afecting P. nigra subsp. nigra plantaions (Barnes et al., 2004). Subsequent 2.4 | Central America to these reports, D. pini has now been conirmed as present in Dothistroma needle blight has been documented in three Central six states (Barnes, Walla et al., 2014; Table 1), all of which are American countries (Table 1; Fig. 1). The irst record of DNB in located in north-central USA, where D. septosporum has never been Central America was from Costa Rica in 1980 on young plantaion detected. trees of P. caribaea (Evans, 1984; Ford, 1982). In Honduras, the The irst record of DNB in Canada was in 1963 from Vancouver disease was reported in 1981 on P. maximinoi (Evans, 1984) and Island (Parker & Collis, 1966). Surveys across Briish Columbia (BC) in Guatemala, in 1983 on several naive pine species, including between 1964 and 1966 showed that the disease was widely distrib- P. maximinoi, P. michoacana, P. oocarpa and P. tecunumanii (Evans, uted on P. contorta in the province (Parker & Collis, 1966). Reports in 1984). Only D. septosporum has been conirmed to occur in Central the Canadian Forest Insect and Disease Survey (FIDS) database sug- America, where it was isolated in Guatemala (Barnes et al., 2016; gest that DNB was present on P. contorta in north-west BC as early Groenewald et al., 2007). as 1941 and possibly as early as 1900 (DAVFP Collecions Database). Dendrochronological studies, however, indicate that DNB has been present in the northern temperate forests of Briish Columbia at least 2.5 | South America as early as 1831 (Welsh, Lewis, & Woods, 2009; Welsh et al., 2014). In South America, DNB has been recorded in eight of twelve coun- The disease has been recorded in seven of the 10 Canadian provinces tries, including Argenina, Bolivia, Brazil, Chile, Colombia, Ecuador, 10 | Drenkhan et al. Peru and Uruguay (Table 1; Fig. 1). The irst report of DNB was suggested that Dothistroma co-evolved with indigenous pine species, from Chile in 1965 where plantaions of suscepible P. radiata were such as P. caribaea, P. devoniana, P. maximinoi and P. tecunumanii infected (Dubin & Staley, 1966). The majority of the reports of in that region. In the Himalayas, Ivory (1994) discovered the patho- DNB in South America occurred in the 1960s, including those from gen in remote naive P. wallichiana stands, hundreds of miles from Uruguay (Peterson, 1969), Argenina (Fresa, 1968) and Brazil known outbreak areas and, therefore, postulated that Dothistroma (Figueiredo & Namekata, 1969; Groenewald et al., 2007). In Colombia, must be naive to this area. Gibson (1974) and Evans (1984) sug- the disease was irst observed in 2008 on P. tecunumanii, P. keysia gested that Dothistroma was also naive on pines in parts of Europe and P. oocarpa (Rodas et al., 2016). Only D. septosporum is known and North America. Consideraion of the early literature and her- to occur in South America, where it has been conirmed as present barium material shows that Dothistroma has been present on both in Brazil, Chile, Colombia and Ecuador (Barnes et al., 2004; Groenewald these coninents for over 100 years (see secion 2.1 and 2.3 above). et al., 2007; Rodas et al., 2016; see Table 1). An understanding of the origin as well as the occurrence and extent of sexual reproducion within the Dothistroma species can aid 2.6 | Africa in management of DNB. At the centre of origin, the host and pathogen may have co-evolved, resuling in less suscepible hosts and, overall, Dothistroma needle blight has been present on the African con- low levels of disease. Thus, this area may serve as a source of less sus- inent since at least the early 1940s, having been observed on cepible provenances or genotypes for future breeding programmes. P. radiata herbarium material collected in Zimbabwe in 1943 (Gibson, In areas where Dothistroma species are introduced, their reproducive Christensen, & Munga, 1964). The disease was subsequently recorded strategy governs how adapive they can be. Dothistroma species are in eight more of the 57 African countries, including Ethiopia, Kenya, heterothallic, where individuals carry a gene of either maing type Malawi, South Africa, Swaziland, Tanzania, Uganda and Zambia (MAT1-1-1 or MAT1-2 idiomorphs), and individuals of both maing (Table 1; Fig. 1). The DNB epidemic in East Africa led to the types are required for sexual reproducion to occur (Groenewald et al., abandonment of P. radiata plantaion forestry (Gibson, 1972). Among 2007). Sexual reproducion, and the associated geneic recombina- the above reports, the pathogen causing the disease has been ion, can give rise to haplotypes with novel gene combinaions, some conirmed in only two countries: D. septosporum is present in Kenya of which may increase virulence, overcome resistance mechanisms and South Africa (Barnes et al., 2004). In all other cases, the or be beter suited to new environments (McDonald & Linde, 2002; species responsible for the disease has not been conirmed, but McDonald, Mundt, & Zhan, 1999). In contrast, purely clonal reproduc- the distribuion and associaion with non-naive P. radiata suggests ion allows less opportunity for such adaptaion. that only D. septosporum is causing DNB in Africa. The possible origin of D. septosporum and D. pini can be inferred by studying their global populaion structures and sexual reproducion 2.7 | Oceania modes. Frequent sexual recombinaion events increase haplotypic diversity. It would thus be reasonable to assume that both haplotypic In Oceania, DNB has been found in New Zealand, Australia and and geneic diversity of the respecive populaions would be great- Papua New Guinea (Table 1; Fig. 1). In New Zealand, DNB was est at their centres of origin and that haplotypic diversity would be recorded for the irst ime in 1964 (Gilmour, 1965) on planted high due to frequent sexual recombinaion events (Allendorf & Lund- P. radiata and is now widespread throughout the country. In Australia, quist, 2003; Goodwin, Dunkle, & Zismann, 2001; McDonald et al., DNB was irst observed in 1975, also afecing P. radiata planta- 1999). Alternaively, muliple introducions of a number of diferent ions (Edwards & Walker, 1978). The disease in Australia seems haplotypes of a pathogen into an area could also increase the geneic to be limited to the Australian Capital Territory, New South Wales, diversity of the pathogen populaion to be similar to the diversity that Queensland, Tasmania and Victoria (Podger, 1984; Reddy, Puri, would be expected in naive populaions (Barnes, Wingield et al., Singh, & Pandey, 1976). In both these countries, only D. septo- 2014; Burgess, Wingield, & Wingield, 2001). sporum has been ideniied (Barnes et al., 2004; Prihaini, Glen, Recent populaion geneics research suggests that D. septosporum Wardlaw, & Mohammed, 2015). Nothing is known regarding the could be naive in Briish Columbia (Canada) and in some areas of Europe DNB agent in Papua New Guinea. (Barnes, Wingield et al., 2014; Dale et al., 2011; Drenkhan et al., 2013). The sexual state of the fungus (as Scirrhia pini) was irst formally described 3 | Origin, sexual reproducion and populaion structure of Dothistroma species by Funk and Parker (1966) from material in Briish Columbia. In Europe, Host speciic pathogens are more likely to be naive to areas in and illustrate the impact of sexual recombinaion on the populaion struc- which their hosts are naive (Gilbert, 2002). Before it was known ture of the pathogen in a number of areas (Dale et al., 2011; Drenkhan that two species cause DNB, Dothistroma was hypothesized to have et al., 2013; Mullet, Brown, & Barnes, 2015; Tomšovský et al., 2013). originated within either the cloud forests of Central America (Evans, Dothistroma septosporum populaions in Canada showed high gene and 1984) or in the Himalayas (Ivory, 1994). In Central America, Evans haplotypic diversity (Dale et al., 2011). Populaion studies on isolates from (1984) found both the asexual and sexual state of Dothistroma and Austria, Czech Republic, France, Hungary, Poland, Romania and Slovakia the sexual state has been recorded in 11 countries (Table 2). Tests for random maing on D. septosporum populaions support these observaions | Drenkhan et al. 11 T A B L E 2 Geographic distribuion of Dothistroma septosporum and D. pini maing types and sexual state in Northern and Southern Hemispheres. Locaion Dothistroma sp. Australia Canaberra Tumut D. septosporum D. septosporum Austria Gstaterboden, Gesäuse (Styria) Hollenstein/Ybbs (Lower Austria) Forest experimental garden “Knödelhüte” (Vienna) Raumberg (Styria) Thenneberg (Lower Austria) D. septosporum D. septosporum D. septosporum MAT1-1-1 * * MAT1-2 References * * Groenewald et al. (2007); Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) * * * Barnes, Wingield et al. (2014) Tomšovský et al. (2013); Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) * * D. septosporum * Barnes, Wingield et al. (2014) Groenewald et al. (2007); Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) Belarus Vitebsk D. septosporum * A. Kačergius and S. Markovskaja, unpubl. data Bhutan Lamey Goemba (Bumthang dzongkhag) Tangsibi (Bumthang dzongkhag) Ura (Bumthang dzongkhag) Yusipang (Thimphu dzongkhag) D. septosporum D. septosporum D. septosporum D. septosporum * * Brazil São Paulo Canadaa Bell Irving River, Briish Columbia (BC) Brown Bear Road, BC Bulkley Canyon, BC Evelyn Pasture, BC Goldstream River, BC Jonas Creek, BC Kinskutch Road, BC Kisgegas Canyon, BC Kuldo Creek, BC Miten Road, BC Mosque River, BC Motaze Lake and Squingula River, BC Nangeese Road, BC Nash Y, BC North Kuldo Road, BC Orendo, BC Sanyam River, BC Squingula River Mine, BC Sunday Lake, BC Chile Canteras, Bio Bio, VIII Region Dollinco, Valdivia, X Region Naguilan, Valdivia, X Region D. septosporum D. septosporum D. septosporum Wr. Neustadt (Lower Austria) D. septosporum D. septosporum * * * * * Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) D. septosporum * Groenewald et al. (2007) D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum * * * * * * * * * * * * * * * * * * * Funk and Parker (1966) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) * * * Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) * * * * * * * * * * * * * * * Costa Ricaa Evans (1984) a Croaia Milatović (1976) Czech Republica Chodská Lhota Borkovická Blata Bynina Havlíčkův Brod Jakule Jandovka Jarcová L. Jankovský and V. Tomešová-Haataja, unpubl. data Bergová and Kryštofová (2014) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) D. pini D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum * * * * * * * * * * (Coninues) 12 | Drenkhan et al. TABLE 2 (coninued) Locaion Jasenice Karolínka Koryčany Křiny Lanžhot Lidmilův mlýn Luhačovice Mezina u Bruntálu Mštenovice Nová Pec Nov́ Hrady – Sušidla Pernek Rožnov pod Radhoštěm Řícmanice Sádek u Poličky Soběslavská Blata Strhaře Sušidla Šance Tišnov Valašsḱ Klobouky Vídeň u Velḱho Meziříčí Zašová Zubří Dothistroma sp. MAT1-1-1 MAT1-2 D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum * * * * * * * * * * * * References * * * * * * * * * * * * * * * * Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Barnes, Wingield et al. (2014) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Barnes, Wingield et al. (2014) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) Tomšovský et al. (2013) * * Munk (1957) M. S. Mullet, unpubl. data. I. Barnes, unpubl. data * Barnes, Wingield et al. (2014) * * * * Denmarka Fredensborg Hørsholm D. septosporum D. septosporum Equador Cotopaxi D. septosporum Estonia Kautsi Konguta D. septosporum D. septosporum * * * * R. Drenkhan, unpubl. data R. Drenkhan, unpubl. data Finland Pyhtää Suonenjoki Ähtäri D. septosporum D. septosporum D. septosporum * * * * Tomšovský et al. (2013) Tomšovský et al. (2013); R. Drenkhan, unbubl. data Tomšovský et al. (2013) Francea Bois du Meinguen, Bretagne Forêt Domaniale du Cranou, Bretagne Forêt Domaniale du Huelgoat, Bretagne Forêt Domaniale du Mesnil, Bretagne La Fert́-Imbault La Feuilĺe Meurthe-et-Moselle Neung-sur_Beuvron Sainte-Brigite Selles-Saint-Denis Souesmes Villefranche-sur-Cher D. septosporum D. septosporum D. septosporum D. septosporum D. pini D. septosporum D. septosporum D. pini D. septosporum D. pini D. pini D. pini * * * * * * * * * * * * * * * * * * * * * * * Georgiaa Morelet (1967) Mullet et al. (2015) Mullet et al. (2015) Mullet et al. (2015) Mullet et al. (2015) Siziba et al. (2016); I. Barnes, unpubl. data Mullet et al. (2015) Groenewald et al. (2007) I. Barnes, unpubl. data Mullet et al. (2015) I. Barnes, unpubl. data Siziba et al. (2016); I. Barnes, unpubl. data I. Barnes, unpubl. data Shishkina and Tsanava (1966b) a Germany Bavarian Alps D. septosporum Greece Lagada D. septosporum * * Buin and Richter (1983) Groenewald et al. (2007) * Tsopelas et al. (2013) * Evans (1984) Groenewald et al. (2007) a Guatemala Sierra de Chuacús Hondurasa D. septosporum Evans (1984) | Drenkhan et al. TABLE 2 (coninued) Locaion Dothistroma sp. MAT1-1-1 MAT1-2 References Hungary Csabrendek Csabrendek Diszel Diszel Sopron D. septosporum D. pini D. septosporum D. pini D. septosporum * * * * * * Barnes et al. (2011) Barnes et al. (2011) Barnes, Wingield et al. (2014) Barnes et al. (2011) Barnes, Wingield et al. (2014) Jamaica 13 * * a Evans (1984) Kenyaa Napkoi D. septosporum * * Ivory (1972) Barnes, Wingield et al. (2014) Latvia Kegums Skujas D. septosporum D. septosporum * * * * Kiesnere (2014) R. Drenkhan, unpubl. data * A. Kačergius and S. Markovskaja, unpubl. data A. Kačergius and S. Markovskaja, unpubl. data A. Kačergius and S. Markovskaja, unpubl. data * * * A. Kačergius and S. Markovskaja, unpubl. data A. Kačergius and S. Markovskaja, unpubl. data A. Kačergius and S. Markovskaja, unpubl. data * * * * * * * * * * * Groenewald et al. (2007) Groenewald et al. (2007) Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) Groenewald et al. (2007); Barnes, Wingield et al. (2014) Barnes, Wingield et al. (2014) Groenewald et al. (2007) Barnes, Wingield et al. (2014) Groenewald et al. (2007) Groenewald et al. (2007) Groenewald et al. (2007) * * Tomšovský et al. (2013) H. Solheim and R. Drenkhan, unpubl. data Lithuania Marijampolė, Ąžuolų Būda Prienai Šalčininkai, Rūdninkai, Jašiūnai, Baltoji Volė Trakai, Aukštadvaris Varėna, Čepkeliai Vilnius, Kairėnai, Lake Gulbinas D. septosporum D. septosporum D. septosporum * * * D. septosporum D. septosporum D. septosporum * New Zealand Bay of Plenty Golden Downs Hokonui Forest Kaharoa Nursery, Rotorua Kaingaroa Forest Karioi Kinleith Lake Okareka, Rotorua Mt. Maunganui Tongariro West Coast South Island D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum Norway Rundhaug Hedmark, Engerdal, Semmings D. septosporum D. septosporum Polanda Brynek (Świerklaniec Forest District) Bzowo (Dąbrowa Forest District) Czernichów Dębowiec (Prudnik Forest District) Domiarki (Miechow Forest District) D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum Kamyk (Krzeszowice Forest District) Leśnice (Lębork Forest District) Łysa Polana Pększyn (Oborniki Śląskie Forest District) Połomia (Świerklanice Forest District) Prusice (Oborniki Śląskie Forest District) Strzeszewo (Lębork Forest district) Strzybnica (Świerklanice Forest District) Tarnowskie Góry Trybsz Wisła Wróblew Wrocław Zawiercie (Siewierz Forest District) D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum * * * * * * * * * * * * * * * * * * Portugala * * * * * * * * * * * * Kowalski and Jankowiak (1998) Boroń, Lenart-Boroń, and Mullet (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Groenewald et al. (2007); Barnes, Wingield et al. (2014); Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Boroń et al. (2016) Fonseca (1998) a Romania Valea Putnei * * * * * D. septosporum * Gremmen (1968) Barnes, Wingield et al. (2014) (Coninues) 14 | TABLE 2 Drenkhan et al. (coninued) Locaion Dothistroma sp. MAT1-1-1 MAT1-2 References Russia Kamenskiy district (Rostov Region) Krasnosulinskiy district (Rostov Region) Karelia, Ruskeala (north-west Russia) St. Petersburg Tarasovskiy district (Rostov Region) D. pini D. pini D. septosporum D. septosporum D. pini * * * * * Barnes et al. (2011) Barnes et al. (2011) R. Drenkhan, unpubl. data I. Barnes and R. Drenkhan, unpubl. data Barnes et al. (2011) Serbiaa Pasuljanske livade D. septosporum * * Karadžić (1986) N. Keča and R. Drenkhan, unpubl. data Slovakia Strážovsḱ vrchy D. septosporum Slovenia Dutovlje Hruševica Ljubljana Panovec Pivka Pivka Podčetrtek Podčetrtek Pokljuka Radenci Radenci Ribčev Laz Rimš Stara Fužina Škocjan Škocjan Trenta Volčji Potok * * Barnes, Wingield et al. (2014) D. pini D. pini D. septosporum D. pini D. septosporum D. pini D. septosporum D. pini D. septosporum D. septosporum D. pini D. septosporum D. septosporum D. septosporum D. septosporum D. pini D. septosporum D. septosporum * * * * * * * * * * * * * * I. Barnes, unpubl. data I. Barnes, unpubl. data Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) B. Piškur, unpubl. data Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) Piškur et al. (2013) B. Piškur, unpubl. data Siziba et al. (2016); B. Piškur, unpubl. data B. Piškur, unpubl. data Piškur et al. (2013) * South Africa Haenertsburg (Tzaneen) Hogsback D. septosporum D. septosporum * * * * Groenewald et al. (2007); Barnes, Wingield et al. (2014) Groenewald et al. (2007); Barnes, Wingield et al. (2014) Switzerlanda Egga Walensee D. septosporum D. pini * * * * R. Engesser, unpubl. data R. Engesser and V. Queloz, unpubl. data Queloz et al. (2014) * * * * * * * * * * * Tanzaniaa Gibson (1972) Turkey Western Burdur province D. septosporum * * M. S. Mullet and F. Oskay, unpubl. data Ukraine Hola Prystan D. pini * * Mykolaiv Kinburn Peninsula D. pini * * Nova Zburivka Tsjurupinsk Kharkiv D. pini D. pini D. septosporum * * * * * * Siziba et al. (2016); I. Barnes and R. Drenkhan, unpubl. data Siziba et al. (2016); I. Barnes and R. Drenkhan, unpubl. data I. Barnes and R. Drenkhan, unpubl. data Groenewald et al. (2007); Barnes et al. (2011) R. Drenkhan, unpubl. data D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum * * * * * * * United Kingdom England - Forest Districts Central England East England Forest of Dean New Forest North England South East England South England West England West Midlands Yorkshire * * * * * * * * * * M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data Groenewald et al. (2007) Groenewald et al. (2007) M. S. Mullet, unpubl. data Groenewald et al. (2007) M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data Groenewald et al. (2007) M. S. Mullet, unpubl. data | Drenkhan et al. TABLE 2 15 (coninued) Locaion Scotland - Forest Districts Cowal & Trossachs Dumfries & Borders Galloway Inverness, Ross & Skye Lochaber Moray & Aberdeenshire North Highland Scoish Lowlands Tay West Argyll Wales United States of Americaa Alaskaa Californiaa Idaho, Lochsa Historical Ranger Staion Indiana, Shelby County Michigan, Massaukee County, Riverside Township Michigan, Montcalm County, Crystal Township Michigan, Montcalm County, Evergreen Township Minnesota (Central) Montana, Missoula Lola Naional Forest Nebraska, Lincoln North Dakota, Cass County North Dakota, Pembina County Oregon, Bandona South Dakota, Brookings County Zimbabwea Dothistroma sp. MAT1-1-1 MAT1-2 References D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum D. septosporum * * * * * * * * * * * * * * * * * * * * * * M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data Peterson and Harvey (1976) Peterson (1982); Barnes et al. (2016) Cobb and Miller (1968) Barnes, Wingield et al. (2014) Barnes, Walla et al. (2014) Groenewald et al. (2007); I. Barnes, unpubl. data D. septosporum D. septosporum D. pini D. pini * * * * D. pini * * Groenewald et al. (2007) D. pini * * Groenewald et al. (2007); I. Barnes, unpubl. data D. pini D. septosporum D. pini D. pini D. pini D. septosporum D. pini * * * * * * * * Groenewald et al. (2007) Barnes, Wingield et al. (2014) Groenewald et al. (2007) Barnes, Walla et al. (2014) Barnes, Walla et al. (2014) Peterson and Harvey (1976); Groenewald et al. (2007) Barnes, Walla et al. (2014) Gibson (1972) *Indicates the idenity of Dothistroma septosporum and D. pini maing types. Areas where the sexual state has been reported. a also showed high levels of geneic diversity as well as gene low, indicaive et al., 2014; Goodwin, Cohen, & Fry, 1994; Taylor, Jacobson, & Fisher, of naive populaions (Barnes, Wingield et al., 2014; Mullet et al., 2015; 1999). For example, the New Zealand populaion has been clonal for Tomšovský et al., 2013). In addiion, populaion studies on D. septosporum more than 60 years (Barnes, Wingield et al., 2014; Groenewald et al., from Estonia and Finland showed that these pathogen populaions are 2007; Hirst, Richardson, Carson, & Bradshaw, 1999). These highly geneically diverse and thus most likely naive and not originaing from clonal populaions of D. septosporum present possible strategies for recent introducions from central Europe (Drenkhan et al., 2013). control by avoiding the introducion of the opposite maing type or In the Southern Hemisphere, D. septosporum is known to be an new, more virulent haplotypes (Barnes, Wingield et al., 2014). invasive and alien species, as the naive ranges of its hosts are almost In Asia, only one small populaion of D. septosporum from Bhutan enirely in the Northern Hemisphere. The sexual state has been has been analysed (Barnes, Wingield et al., 2014). Preliminary inves- reported from only three African countries (Table 2). Populaion geneic igaions using microsatellite markers (Barnes, Corinas, Wingield, & studies in South Africa and Kenya have shown that both maing types Wingield, 2008) showed that this populaion in Bhutan was genet- of D. septosporum are present in these countries, consistent with the ically diverse and disinct from other populaions studied outside observaion of the sexual state in Kenya and the moderate levels of Asia, suggesing that the pathogen could be indigenous to this area geneic diversity in these populaions (Barnes, Wingield et al., 2014). (Barnes, Wingield et al., 2014). Although the sexual state of the fun- The results are consistent with the long history of pine culivaion in gus has been reported from six countries in North and Central America these areas, where muliple introducions of the pathogen could have (Table 2), populaion studies in these areas have not been conducted occurred due to trade of plant material and the establishment of non- and remain an important gap in our knowledge regarding the popula- naive pine plantaions for commercial purposes (Gibson, 1972). ion geneics of the DNB pathogens on a global scale. In contrast to Africa, only MAT1-2 strains have been found in The sexual state of D. pini has never been described, despite Oceania and South America and the homogeneity of D. septosporum the presence of both maing types reported in the USA and Europe populaions is likely the consequence of more recent human-mediated (France, Slovenia, Switzerland and Ukraine) and in the same sam- introducions of the pathogen into these areas (Barnes, Wingield pling area (Table 2). It is, however, important to note that some of 16 | Drenkhan et al. the early observaions of the sexual state of D. septosporum were Montana (Taylor & Walla, 1999), where molecular methods have within the geographic range of D. pini (e.g. in France; Morelet, 1967) confirmed only the presence of D. septosporum to date (Barnes, and these indings could have been the sexual state of this species. Wingfield et al., 2014). There is evidence to suggest that recent introducions of the pathogen might have occurred in certain geographic areas, as only the MAT1-2 idiomorph, for example, has been ideniied in a populaion from Hungary (Table 2). 4.1 | Newly recorded hosts Informaion regarding the 20 newly reported hosts of Dothistroma Microsatellite markers have recently been developed for D. pini species is presented in Table 4. There are two factors that could (Siziba et al., 2016) making it possible to study the populaion diver- explain the recent growth in the number of recorded hosts from sity of this pathogen in all areas reported. Preliminary studies show 89 to 109. One possibility is that the pathogens are undergoing that D. pini is clonal in Pivka, Slovenia and geneically diverse in an expansion of their host ranges. A more likely situaion, however, La Fert́-Imbault, France (Siziba et al., 2016). No other populaion is an increased awareness of the disease in Europe and other geneic studies have been conducted on D. pini and it is currently not areas, partly resuling from the DIAROD COST Acion, leading to possible to consider the origin of this pathogen. A global populaion a deeper study of literature in both English and local languages. study of both pathogens, especially from areas of their hypothesized There has also been a recent increase in surveys and monitoring naive origins, would provide more informaion regarding the pos- for the pathogens in forests, plantaions, botanical gardens, arboreta sible origin of Dothistroma species. There is currently an on-going and parks. Three observaions support this view. Firstly, six of the project related to one of the objecives of the DIAROD Working 20 “newly reported” hosts were recorded before 2008, but were Group 1 (dealing with the DNB pathogens) that will address these either overlooked by Wat et al., (2009) or were published in less- knowledge gaps. accessible local language journals. Of these hosts, three experienced severe DNB damage (Table 4; Cobb & Libby, 1968; Peterson, 1984; 4 | HOST RANGES OF THE DOTHISTROMA PATHOGENS Shishkina & Tsanava, 1966a,b), demonstraing the importance of re-visiing older literature when considering pathogen host ranges. Secondly, the low DNB severity reported on many of the 14 host taxa recorded ater 2008 suggests that Dothistroma species on these All reported hosts of Dothistroma species belong to the Pinaceae, hosts may have been overlooked in the past. Finally, several of and the vast majority of these are in the genus Pinus (Table 3). the newly reported hosts are subspecies, or varieies of three spe- Pinus species are oten dominant members of naive forest veg- cies already ranked as highly suscepible to infecion by Dothistroma etaion across the Northern Hemisphere (Richardson et al., 2007). species (Pinus bruia, P. contorta and P. nigra). It is thus possible They are also commonly grown commercially throughout both that Dothistroma species have been observed on these taxa before, the Northern and Southern Hemispheres to produce imber, pulp but that the host subspecies/variety was not reported. and other wood products, as well as seed and resin (Richardson Since 2008, Dothistroma species have been observed on fourteen et al., 2007). In a previous review of the hosts of Dothistroma new hosts (Table 4). Dothistroma septosporum was conirmed on 13 of species, Wat et al. (2009) listed 89 host taxa (species, subspe- these host species using molecular methods and it likely also occurs cies, varieies and hybrids). These included 82 Pinus taxa, as on Pinus parvilora in Latvia and Lithuania, given the locaions of these well as Larix decidua, ive Picea species and Pseudotsuga menziesii. reports (Kiesnere, 2014; S. Markovskaja & A. Kačergius, unpublished Wat et al. (2009) did not difereniate the host ranges of the data). Only one of the newly recorded hosts, P. nigra subsp. pallasiana, two Dothistroma species. In this review, we have atempted to is a conirmed host of D. pini (Barnes, Kirisits et al., 2008). Rather than accomplish this task, but it was not always possible and in D. septosporum truly having a broader host range than D. pini, the reason several cases we can refer only to Dothistroma species in for the predominance of new D. septosporum host reports could be that general. most of these records come from areas, such as the UK and the Balic Surveys forming part of the DIAROD project have shown that countries, where only D. septosporum is known to occur. All of these new there are now 109 known host taxa for Dothistroma species, 95 of host reports come from Europe, probably partly due to increased inter- which are within the genus Pinus (Table 3). The known host range est in Dothistroma species emerging from the DIAROD COST Acion of D. septosporum includes 52 taxa in six genera (Abies, Cedrus, and the extensive network of arboreta found in this region. However, Larix, Picea, Pinus and Pseudostuga), 42 of which are in the genus the climaic suitability of northern Europe is also known to be increasing Pinus. In contrast, the known host range of D. pini consists of only for Dothistroma species (Woods et al., 2016), which may have contrib- 12 Pinus taxa, 11 of which are also hosts of D. septosporum. For the uted to the observed increase in DNB incidence and severity and a pos- remaining 56 host taxa the Dothistroma species observed has not sible true host expansion. Severe DNB symptoms have been observed been confirmed with molecular methods. The one host species for on only two of these newly recorded hosts. The extensive damage which only D. pini has been confirmed is Pinus albicaulis (Barnes, caused by D. pini in P. nigra subsp. pallasiana plantaions in the Ukraine Walla et al., 2014). It is likely that P. albicaulis is also a host of and southwest Russia (Barnes, Kirisits et al., 2008) shows that even D. septosporum, because DNB has been reported on this host in newly recorded hosts of Dothistroma species can be badly afected by The hosts of Dothistroma needle blight pathogens and their suscepibility to the disease. Suscepibility/Host speciesa, b, c, d Highly suscepible Pinus atenuata Lemmon Pinus × atenuradiata Stockw. et Righter Pinus bruia Ten. Pinus bruia Ten. var. pityusa (Steven) Nahal$ Pinus canariensis C. Sm.‡ Pinus caribaea Morelet var. bahamensis (Griseb.) W.H. Barret et Golfari Pinus caribaea Morelet var. caribaea Pinus caribaea Morelet var. hondurensis (Śńcl.) W.H. Barret et Golfari Pinus cembroides Zucc. Pinus contorta Douglas ex Loudon‡ Pinus contorta Douglas ex Loudon var. laifolia (Engelm.) Critchf. Pinus engelmannii Carrière Pinus halepensis Mill.‡ Pinus jefreyi Balf.‡ Pinus kesiya Royle. ex Gordon Pinus mugo Turra‡ Common English names References for host suscepibility datae DSf Knobcone pine, narrowcone pine Knobcone pine x Monterey pine Calabrian pine, Turkish pine, East Mediterranean pine, Bruia pine Pitsundian pine Canary pine, Canary Islands pine Bahamas pine, Caicos pine, Caribbean pine Caribbean pine, Nicaragua pine, pitch pine Honduras pine, Caribbean pine Gilmour (1967b); Gibson (1979) Gilmour (1967b); Gibson (1979) Ivory (1968); Gibson (1979) * I. Barnes and M. S. Mullet, unpubl. data * Tsopelas et al. (2013) * I. Barnes, unpubl. data Mexican nut pine, pinyon pine Lodgepole pine, Tamarack pine, shore pine Lodgepole pine Ivory (1968); Gibson (1979) Gibson (1979) * Barnes et al. (2004) Woods et al. (2005) * Barnes et al. (2004) Apache pine Aleppo pine Jefrey pine, Jefrey’s pine Khasia pine, Khasi pine, Benguet pine Mountain pine, dwarf mountain pine * * * * M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data Rodas et al. (2016) Barnes et al. (2004, 2011) Shishkina and Tsanava (1966a,b) Gilmour (1967b); Ivory (1968) Wat et al. (2009) DPf References for molecular ideniicaion Drenkhan et al. TABLE 3 Wat et al. (2009) Ford (1982) Pinus muricata D. Don.‡ Bishop pine Pinus nigra J.F. Arnold Black pine Pinus nigra J.F. Arnold subsp. nigra‡ Austrian pine Pinus nigra J.F. Arnold subsp. laricio (Poir.) Maire Pinus nigra J.F. Arnold subsp. pallasiana (Lamb.) Holmboe$ Pinus oocarpa Schiede ex Schltdl.‡ Pinus pinaster Aiton‡ Corsican pine Ivory (1968); Gibson (1979) Ivory (1968); Gibson (1979) Gilmour (1967b); Bulman et al. (2004) Rodas et al. (2016) Drenkhan et al. (2013); P. Boroń, unpubl. data Gilmour and Noorderhaven (1969); Gibson (1979); Fraser, Woodward et al. (2015) Gibson (1979); Jankovský, Bednářová et al., (2004) Geo-database (htp://arcgis.mendelu.cz/ monitoring/) Gilmour (1967b) Crimean pine * Barnes et al. (2004) * Barnes et al. (2004) * * Barnes et al. (2004); Fabre et al. (2012) * * Fabre et al. (2012) Barnes, Kirisits et al. (2008) * * Egg-cone pine Mariime pine Rodas et al. (2016) Gilmour and Noorderhaven (1969) * * * Barnes, Kirisits et al. (2008); M. S. Mullet, unpubl. data Rodas et al. (2016) M. S. Mullet, unpubl. data; D́partement de la Sant́ des Forêts databaseh Pinus pinea L.‡ Pinus ponderosa Douglas ex C. Lawson‡ Umbrella pine, stone pine Western yellow pine, ponderosa pine * * Barnes et al. (2004); Barnes, Walla et al. (2014) Pinus ponderosa Douglas ex C. Lawson var. ponderosa$ Pinus radiata D. Don Paciic ponderosa pine, ponderosa pine, western yellow pine, bull pine Monterey pine, radiata pine Ivory (1968), Gibson (1979) Gilmour and Noorderhaven (1969); Fraser, Woodward et al. (2015) Peterson (1984) * * Barnes et al. (2004); Piou and Ioos (2014) (Coninues) Ivory (1968); Gilmour and Noorderhaven (1969); Gibson (1979) 17 * | * (coninued) Pinus radiata D. Don var. binata (Engelm.) Lemmon Pinus radiata D. Don radiata$ Pinus sabineana Douglas ex D. Don‡ (syn. Pinus sabiniana) Pinus sylvestris L.‡ Pinus thunbergii Parl. Pinus tecunumanii Low Elevaion Eguiluz & J. P. Perry Moderately suscepible Pinus bungeana Zucc. ex Endl. Pinus canariensis C. Sm.‡ Pinus caribaea Morelet Pinus clausa (Chapm. ex Engelm.) Sarg. Pinus coulteri D. Don‡ Pinus cubensis Griseb. Pinus densilora Siebold & Zucc. Pinus echinata Mill. Pinus ellioii Engelm.‡ Common English names References for host suscepibility datae Guadalupe Island pine, Cedros Island pine Cobb and Libby (1968) Monterey pine, Cambria pine, radiata pine Ghost pine, grey pine, California foothill pine, digger pine, bull pine Scots pine Japanese black pine Schwerdfeger’s pine Cobb and Libby (1968) Ivory (1968) Lacebark pine Canary pine, Canary Islands pine Caribbean pine Sand pine, Florida spruce pine Coulter pine, big-cone pine Cuban pine Japanese red pine Shortleaf pine Slash pine Gibson (1979) Gibson (1979) Rodas et al. (2016) DSf * * Barnes et al. (2004); Fabre et al. (2012) * Rodas et al. (2016) * I. Barnes, unpubl. data * Barnes et al. (2004) * M. S. Mullet, unpubl. data * M. S. Mullet, unpubl. data Slash pine South Florida slash pine Limber pine, Rocky Mountain white pine Gibson (1979); Taylor and Walla (1999) * Pinus jefreyi Balf.‡ Pinus kesiya Royle. ex Gordon kesiya Pinus lamberiana Douglas Pinus massoniana Lamb. Pinus monicola Douglas ex D. Don‡ Pinus mugo Turra‡ Pinus mugo Turra subsp. mugo (Scop.) Pinus muricata D. Don‡ Pinus nigra J.F. Arnold subsp. nigra‡ Jefrey pine, Jefrey’s pine Khasia pine, Khasi pine, Benguet pine Sugar pine Masson’s pine, Chinese red pine Western white pine Mountain pine, dwarf mountain pine Swiss mountain pine Bishop pine Austrian pine * * Pinus occidentalis Sw. Pinus palustris Mill. Pinus pinaster Aiton‡ Hispaniolan pine Longleaf pine, Florida pine Mariime pine Gibson (1979) Ivory (1968) Gadgil (1984) Ivory (1968); Gibson (1979) Gibson (1979) Gibson (1979) Gibson (1979) Ivory (1968); Bulman et al. (2004) Fabre et al. (2012); Fraser, Woodward et al. (2015) Ivory (1968); Gibson (1979) Ivory (1968); Gibson (1979) Ivory (1968); Gibson (1979) Pinus ponderosa Douglas ex C. Lawson‡ Pinus ponderosa Douglas ex C. Lawson subsp. scopulorum (Engelm.) E. Murray Pinus pungens Lamb. Ponderosa pine Rocky Mountain yellow pine Ivory (1968) Peterson (1984) Table Mountain pine, prickly pine, hickory pine Red pine, Norway pine Gibson (1979) * Barnes, Walla et al. (2014); Barnes, Wingield et al. (2014) M. S. Mullet, unpubl. data Rodas et al. (2016) * * Barnes et al. (2004, 2011) * * * Barnes et al. (2004) Barnes et al. (2004); Fabre et al. (2012) * * M. S. Mullet, unpubl. data; D́partement de la Sant́ des Forêts databaseh Drenkhan et al. Pinus ellioii Engelm. var. ellioii$ Pinus ellioii Engelm. var. densa Litle & Dorman Pinus lexilis E. James Gibson (1979) References for molecular ideniicaion M. S. Mullet, unpubl. data * Gibson (1979) Gadgil (1984); Bulman et al. (2004) Gibson (1979) Ivory (1968); Karadžić (2004) Gibson (1979) Ivory (1968); Gibson (1979) Gibson (1979) Ivory (1968); Gibson (1979) Gilmour and Noorderhaven (1969); Gibson (1979) Ivory (1968) Ivory (1968) Pinus resinosa Aiton DPf | Suscepibility/Host speciesa, b, c, d 18 TABLE 3 (coninued) Suscepibility/Host speciesa, b, c, d Common English names References for host suscepibility datae Ivory (1968); Gibson (1979) Gibson (1979) Pinus strobus L.‡ Long-leaved Indian pine, chir pine Southwestern white pine, southern limber pine Eastern white pine, Weymouth pine Pinus taeda L.‡ Pinus roxburghii Sarg. Pinus strobiformis Englem. Slightly suscepible Abies alba Mill.$ Abies concolor (Gord. et Glend.) Lindl.$ Cedrus atlanica (Endl.) Manei ex Carrière var. glauca$ Cedrus deodara (Lamb.) G. Don. $g Cedrus libani A.Rich. subsp. libani. $g Larix decidua Mill. DPf References for molecular ideniicaion * D́partement de la Sant́ des Forêts databaseg Loblolly pine Gilmour and Noorderhaven (1969); Gibson (1979) Ivory (1968); Gibson (1979) European silver ir, silver ir White ir Blue Atlas cedar Drenkhan et al. (2014) Drenkhan et al. (2014) Mullet and Fraser (2015) * * * Drenkhan et al. (2014) Drenkhan et al. (2014) Mullet and Fraser (2015) Deodar cedar, Himalayan cedar Lebanon cedar, cedar of Lebanon European larch Mullet and Fraser (2015) Mullet and Fraser (2015) Basset (1969); Bulman et al. (2004); Kirisits, Halmschlager, Hintsteiner, Barnes, and Cech (2013) Lang and Karadžić (1987); Bednářová et al. (2006) Karadžić (1994); Bulman et al. (2004) Jankovský, Palovčíková et al. (2004) Bednářová et al. (2006) Bulman et al. (2004) Jankovský, Bednářová et al. (2004) Gilmour and Noorderhaven (1969) Kirisits and Cech (2006, 2007) * * * Mullet and Fraser (2015) Mullet and Fraser (2015) I. Barnes, M. Hintsteiner, T. L. Cech and T. Kirisits, unpubl. data * Tomšovský et al. (2013) * * M. S. Mullet, unpubl. data I. Barnes, unpubl. data Picea abies (L.) H. Karst. Norway spruce Picea omorika (Pančić) Purk. Picea pungens Engelm. Picea shrenkiana Fisch. & C.A. Mey. Picea sitchensis (Bong.) Carrière Pinus aristata Engelm. Pinus ayacahuite Ehrenb. ex Schltdl. Pinus cembra L. Serbian spruce Blue spruce, Colorado spruce Schrenk spruce Sitka spruce Colorado bristlecone pine, hickory pine Mexican white pine Arolla pine, Swiss stone pine Pinus contorta Douglas ex Loudon‡ Pinus coulteri D. Don‡ Pinus devoniana Lindl. Lodgepole pine, Tamarack pine, shore pine Coulter pine, big-cone pine Michoacan pine Pinus ellioii Engelm.‡ Pinus halepensis Mill.‡ Pinus hartwegii Lindl. Slash pine Aleppo pine Hartweg’s pine Pinus heldreichii H. Christ Pinus koraiensis Siebold & Zucc. Pinus maximinoi H.E. Moore Pinus merkusii Jungh. & de Vriese Pinus montezumae Lamb. Heldreich’s pine, Bosnian pine Korean pine Thin-leaf pine Merkurs’s pine Montezuma pine, rough-branched Mexican pine Western white pine Mountain pine Bulman et al. (2004); Fraser, Woodward et al. (2015) Bulman et al. (2004) Gilmour and Noorderhaven (1969); Gibson (1979); Bulman et al. (2004) Bulman et al. (2004) Fabre et al. (2012) Gilmour and Noorderhaven (1969); Gibson (1979) Bednářová et al. (2006) Lang and Karadžić (1987) Rodas et al. (2016) Gibson (1979) Gilmour and Noorderhaven (1969); Ivory (1968) Bulman et al. (2004) Fabre et al. (2012) * Barnes, Walla et al. (2014); Barnes, Wingield et al. (2014) Barnes et al. (2004) * Barnes et al. (2004) * * M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data * Rodas et al. (2016) * Tomšovský et al. (2013) * * | Pinus monicola Douglas ex D. Don‡ Pinus mugo Turra subsp. uncinata (Ramond ex D. C.) Domin. DSf Drenkhan et al. TABLE 3 19 (Coninues) 20 | TABLE 3 (coninued) Common English names References for host suscepibility datae DSf DPf References for molecular ideniicaion Pinus nigra J.F. Arnold subsp. nigra‡ Pinus oocarpa Schiede ex Schltdl.‡ Pinus patula Schiede ex Schltdl. & Cham. Pinus peuce Griseb. Austrian pine Egg-cone pine Jelecote pine, Mexican weeping pine Balkan pine, Macedonian pine * * * * * Barnes et al. (2004); Fabre et al. (2012) Rodas et al. (2016) I. Barnes, unpubl. data Barnes et al. (2004) Pinus pinaster Aiton‡ Mariime pine Gadgil (1984); Bulman et al. (2004) Ivory (1968) Gilmour (1967b) T. Kirisits, S. Markovskaja, R. Drenkhan, unpubl. data Fabre et al. (2012) * * M. S. Mullet, unpubl. data, D́partement de la Sant́ des Forêts databaseh Pinus pinea L.‡ Pinus pseudostrobus Lindl. Umbrella pine, stone pine False Weymouth pine Pinus rigida Mill. Pinus sabineana Douglas ex D. Don‡ (syn. Pinus sabiniana) Pinus seroina Michx. Pinus sibirica Du Tour Pinus strobus L.‡ Pitch pine, hard pine Ghost pine, grey pine, California foothill pine, digger pine, bull pine Pond pine, marsh pine Siberian stone pine, Siberian pine Eastern white pine, Weymouth pine Pinus strobus L. var. chiapensis (Marińz) Andresen Pinus sylvestris L.‡ Chiapas white pine Scots pine Pinus tabuliformis Carrière Pinus taeda L.‡ Chinese red pine Loblolly pine Pinus torreyana Parry ex Carrière Pinus wallichiana A.B. Jacks. Pseudotsuga menziesii (Mirb.) Franco Torrey pine, Soledad pine, Del Mar pine Himalayan white pine Douglas ir Suscepibility/Host speciesa, b, c, d Bulman et al. (2004) Jankovský, Bednářová et al., 2004 Bulman et al. (2004); D́partement de la Sant́ des Forêts databaseh Ivory (1968) Lang and Karadžić (1987); Bulman et al. (2004); Fabre et al. (2012); Fraser, Woodward et al. (2015) Lang and Karadžić (1987) Bulman et al. (2004); D́partement de la Sant́ des Forêts databaseh Ivory (1968) Ivory (1990); Wat et al. (2009) Dubin and Walper (1967); Bulman et al. (2004) Atlas cedar Balsam ir Whitebark pine Cooper’s pine Petrescu (1976) Kiesnere (2014) Taylor and Walla (1999) Browne (1968) Jack pine, black pine Iranian pine Lodgepole pine x jack pine Jankovský, Bednářová et al. (2004) Soylu, Kurt, and Soylu (2001) Parker and Collis (1966); Funk and Parker (1966) * M. S. Mullet, unpubl. data * D́partement de la Sant́ des Forêts databaseh * * M. S. Mullet, unpubl. data Barnes, Corinas et al. (2008) Tomšovský et al. (2013) * * * * * * Barnes et al. (2004); Fabre et al. (2012) * Kiesnere (2014) Barnes, Walla et al. (2014) M. S. Mullet, unpubl. data Drenkhan et al. Unknown suscepibility Cedrus atlanica (Endl.) Manei ex Carrière$ Abies balsamea (L.) Mill.$ Pinus albicaulis Engelm. Pinus arizonica Engelm. var. cooperi (C. E. Blanco) Farjon Pinus banksiana Lamb. Pinus bruia Ten. var. eldarica (Medw.) Silba$ Pinus contorta Douglas ex Loudon x Pinus banksiana Lamb.e D́partement de la Sant́ des Forêts databaseh Gilmour and Noorderhaven (1969); Ivory (1968) Bednářová et al. (2006) Bulman et al. (2004) Drenkhan et al. TABLE 3 (coninued) Suscepibility/Host speciesa, b, c, d Pinus contorta Douglas ex Loudon var. contorta Pinus contorta Douglas ex Loudon var. murrayana (Balf.) Engelm.$ Pinus echinata Mill. × Pinus taeda L. Pinus gerardiana Wall. ex D. Don$ Pinus monophyllaTorr. & Fŕm$ Pinus mugo subsp. rotundata (Link) Janchen & Neumayer Pinus nigra J.F. Arnold subsp. dalmaica (Vis.) Franco$ Pinus nigra J.F. Arnold subsp. salzmannii (Dunal) Franco$ Pinus parvilora Siebold & Zucc.$ Common English names References for host suscepibility datae DSf Shore pine, beach pine Peterson and Harvey (1976) * Tamarack pine, Sierra lodgepole pine M. S. Mullet, unpubl. data * Barnes, Wingield et al. (2014); Fraser, Woodward et al. (2015) M. S. Mullet, unpubl. data Shortleaf pine × loblolly pine Parker and Collis (1966); Funk and Parker (1966) M. S. Mullet, unpubl. data V. Queloz, unpubl. data * * M. S. Mullet, unpubl. data V. Queloz, unpubl. data Chilgoza pine Single leaf pinyon pine, one-leaved nut pine Bog pine DPf References for molecular ideniicaion Bednářová et al. (2006) Dalmaian black pine J. Lazarevic, unpubl. data * J. Lazarevic, unpubl. data Pyreneean pine, Atlas Mountains black pine Japanese white pine M. S. Mullet, unpubl. data * M. S. Mullet, unpubl. data * Kiesnere (2014) Pinus pumila (Pall.) Regel$ Siberian dwarf pine, dwarf Siberian pine, dwarf stone pine, Japanese stone pine, creeping pine Pinus sylvestris L. var. mongolica Litv. Mongolican Scots pine, Mongolian pine, Hailar pine Kiesnere (2014); S. Markovskaja and A. Kačergius, unpubl. data Kiesnere (2014); S. Markovskaja and A. Kačergius, unpubl. data Li et al. (1998) a Host taxonomy is based on Farjon (2001). Host species that have been rated diferently by various authors and are therefore in more than one category are marked with a “‡.” c “New” host species not recorded by Wat et al. (2009) are marked with a “$.” d Two unconirmed possible new host records from the Paciic Forestry Centre’s Forest Pathology Herbarium (Canada) were excluded from Table 3. The report on already included the same as P. contorta x banksiana Pinus contorta var. murrayana x P. banksiana (syn. P. murrayana x banksiana) (DAVFP 16702) is likely in the Table. The report on Abies lasiocarpa (Hooker) Nutall (DAVFP 21525) was never conirmed (B. Callan, pers. Comm.). e For species with unknown suscepibility the reference for the host report is given. f Where molecular methods have been used to idenify the Dothistroma species causing DNB, this informaion is also included and indicated with a “*” (DS, D. septosporum; DP, D. pini). g DNB has only been observed on ariicially inoculated Cedrus libani subsp. libani and Cedrus deodara. h D́partement de la Sant́ des Forêts database: htp://agriculture.gouv.fr/departement-de-la-sante-des-forets. b | 21 22 | TABLE 4 Newly reported hosts of Dothistroma species. Host Dothistroma species Recorded before 2008 Cedrus atlanica Unknown Pinus bruia var. Unknown eldarica Pinus bruia var. Unknown pityusa Pinus ellioii var. D. septosporuma ellioii P. ellioii var. Unknown ellioii Pinus ponderosa D. pinia var. ponderosa Pinus radiata var. D. septosporuma radiata Recorded ater 2008 Abies alba D. septosporum Suscepibility Notes/source Reference Unknown Unknown Petrescu (1976) Soylu et al. (2001) Moderate Recorded in Romania. DNB only found in plantaions of this variety that had been severely damaged by other pathogens in Turkey. DNB caused severe damage and even mortality in young stands in wet and warm regions of western Georgia. Slightly atacked under moderate and high disease hazard in Kenyan arboreta. Unknown Recorded in Japan. Ito et al. (1975) High Greater suscepibility than the inland form P. ponderosa var. scopulorum in central USA. Peterson (1984) High Greater suscepibility than P. radiata var. binata in California. Cobb and Libby (1968) Slight Dothistroma septosporum conirmed molecularly from mature trees growing with infected exoic pines and Pseudotsuga menziesii in northern Latvia. Severity was slight, with symptoms conined to the lower canopy. Dothistroma septosporum was found on trees growing close to an infected Pinus cembra stand in the Naional Botanic Garden in Latvia. Severity was slight, with symptoms conined to the lower branches Dothistroma septosporum isolated from mature trees growing in an arboretum near an infected Pinus sylvestris stand in south east Estonia. Incidence and severity was low. Needles with symptoms were conined to the lower canopy. Dothistroma septosporum isolated from a mature tree growing near a heavily infected Pinus jeferyi in an arboretum in Scotland. Symptom severity was only slight. Conidiomata developed ater ariicial inoculaion with a D. septosporum isolate from C. atlanica var. glauca. Conidiomata developed ater ariicial inoculaion with a D. septosporum isolate from C. atlanica var. glauca. Dothistroma septosporum isolated and conirmed using molecular methods. The tree was growing in the southeast of England. Drenkhan et al. (2014) Unknown Abies balsamea D. septosporum Unknown Abies concolor D. septosporum Slight Cedrus atlanica var. glauca Cedrus deodara D. septosporum Slight D. septosporum Slight Cedrus libani subsp. libani Pinus contorta subsp. murrayana Pinus gerardiana D. septosporum Slight D. septosporum Unknown D. septosporum Unknown Pinus monophylla D. septosporum Unknown Ivory (1968) Kiesnere (2014) Drenkhan et al. (2014) Mullet and Fraser (2015) Mullet and Fraser (2015) Mullet and Fraser (2015) M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data V. Queloz, unpubl. data Drenkhan et al. Dothistroma septosporum isolated and conirmed using molecular methods. The tree was growing in the naional pinetum (an arboretum specializing in Pinus sp.) in the southeast of England. Previously classiied as “immune” in Kenya by Ivory (1968). Two trees growing in diferent locaions were severely afected in Switzerland. Only one-needled pine species. Second pinyon pine (subsecion Cembroides) species to be recorded as a host of Dothistroma species ater P. cembroides. Shishkina and Tsanava (1966a,b) | Drenkhan et al. 23 Queloz, unpublished data). Pinus monophylla, the sole one-needle pine species, is only the second pinyon pine (subsecion Cembroides) species to be recorded as a host of Dothistroma ater P. cembroides, a species Kiesnere (2014) ranked as being highly suscepible by Ivory (1968). 4.2 | Suscepibility rankings of hosts of Dothistroma species Suscepibility rankings of hosts are listed in Table 3. Because conDothistroma species not conirmed using molecular techniques, but DNB was probably caused by the noted Dothistroma species, given the locaion of the report. a Unknown Dothistroma septosporum found on this species growing c. 100 m from infected P. sylvestris in the Naional Botanic Garden in Latvia. Severity was moderate. Symptoms mostly found in the lower canopy, but also observed at greater heights. fusion remains over which Dothistroma species is being referred D. septosporum Unknown D. septosporuma Unknown D. septosporum two P. monophylla trees growing in diferent locaions in Switzerland (V. Pinus pumila Kiesnere (2014); S. Markovskaja and A. Kačergius, unpubl. data M. S. Mullet, unpubl. data M. S. Mullet, unpubl. data Dothistroma septosporum isolated and conirmed using molecular methods. The trees were growing in the southeast of England and were moderately afected by DNB. Dothistroma septosporum isolated and conirmed using molecular methods. The tree was growing in the southeast of England. Disease severity was slight on trees growing in arboreta, botanic gardens and parks in Latvia and Lithuania. Unknown D. septosporum Barnes, Kirisits et al. (2008) Severe epidemics reported in plantaions in Ukraine and in regions of southwest Russia. High D. pini J. Lazarevic, unpubl. data Seed stand in Montenegro. Notes/source Suscepibility Unknown D. septosporum Dothistroma species Host (coninued) TABLE 4 Pinus nigra subsp. dalmaica Pinus nigra subsp. pallasiana P. nigra subsp. pallasiana Pinus nigra subsp. salzmanii Pinus parvilora Reference DNB. Severe damage caused by D. septosporum was also observed on to in work either carried out prior to 2004 or in areas where both pathogens occur, we have not atempted to separate host suscepibility based on Dothistroma species. Wat et al. (2009) listed 16 hosts as highly suscepible, 22 as moderately suscepible and 26 as slightly suscepible to atack by Dothistroma species. Thirteen species had unknown suscepibility, and the remaining 12 were classiied diferently by various authors. We have rated 20 of the host species as highly suscepible, 20 as moderately suscepible and 33 as slightly suscepible to Dothistroma species. Eighteen species have unknown suscepibility and 18 were classiied diferently by various authors (Table 3). These suscepibility rankings were based on results from both ield observaions and experimental trials reported in both peer-reviewed and “grey” literature. The majority of these rankings were based on surveys of naturally infected trees in arboreta, ield trials and mixed or single species stands (Cobb & Miller, 1968; Gibson et al., 1964; Ivory, 1968; Muir & Cobb, 2005; Peterson, 1967a), but others emerged from experimental trials with limited numbers of species (Cobb & Libby, 1968; Fraser, Woodward et al., 2015; Gibson et al., 1964; Rodas et al., 2016). The suscepibility rankings of some species, for example P. torreyana (Ivory, 1968), are based on small numbers of individuals growing in arboreta and should thus be considered as “preliminary” and requiring further conirmaion. 4.2.1 | Modiicaions to suscepibility rankings of hosts of Dothistroma species Recent research has elucidated the suscepibility of several hosts for which this informaion was previously unknown. These species include P. maximinoi and P. tecunumanii, the relaive suscepibiliies of which were invesigated by Rodas et al. (2016) ater the emergence of a serious D. septosporum epidemic in Colombia. These authors found that P. maximinoi was only slightly suscepible to D. septosporum, while P. tecunumanii showed intraspeciic variaion in suscepibility; the low elevaion provenance was highly suscepible, whereas the high elevaion provenance remained symptom free. Following surveys in Europe, P. peuce is now considered as slightly suscepible, as it is only known as a host of D. septosporum in four European countries (Austria, Estonia, Lithuania and Montenegro) and appears to be less suscepible than some other exoics in Estonia (see Country notes, Supporing Informaion). 24 | Pinus mugo subsp. uncinata has also been placed in the slightly Drenkhan et al. from France, where both Dothistroma species occur (Fabre et al., suscepible category based on data from French forest disease 2012; D́partement de la Sant́ des Forêts database). Further support surveys (Fabre et al., 2012). Similarly, P. cembra is now classiied for the reposiioning of the suscepibility ranking of P. pinea comes as slightly suscepible, due to the frequent observaion of symptoms from south-western Turkey where a small P. pinea plantaion had no of DNB on this species in some parts of its natural range in the DNB symptoms, despite being surrounded by P. bruia stands heavily Austrian Alps (Kirisits & Cech, 2007; see also Supporing Informaion). infected by D. septosporum (F. Oskay, unpublished data). Pinus pinas- The suscepibility ranking for several other hosts has also been ter, previously ranked as moderately suscepible to D. septosporum by updated. Cobb and Libby (1968) reported that P. radiata var. binata Ivory (1968), is now placed in all suscepibility categories. This host was less suscepible than P. radiata var. radiata, and Wat et al. (2009) was found to have similar levels of suscepibility to D. septosporum as therefore placed the former variety in the moderately suscepible cate- several highly suscepible Pinus species in New Zealand (Gilmour & gory. However, Cobb and Libby (1968) also reported that P. radiata var. Noorderhaven, 1969). In France, however, where more than a million binata was more suscepible than P. muricata, a moderately to highly hectares of P. pinaster are present, this host has been reported to be suscepible host and accordingly, this variety of P. radiata has now only slightly suscepible to Dothistroma species (Fabre et al., 2012). been moved to the highly suscepible category. Rodas et al. (2016) found that P. kesiya and P. oocarpa were highly suscepible to D. septosporum in Colombia. This report was in contrast to earlier reports of moderate suscepibility for P. kesiya var. kesiya and slight suscepibility 4.2.2 | Analysis of geo-database data and country notes for P. oocarpa to D. septosporum in Kenya (Ivory, 1968). Pinus mugo, Analysis of the geo-database data and inspecion of the country ranked as moderately suscepible by Gibson (1979), is now also ranked notes (see Supporing Informaion) enabled analysis of the relaive as highly suscepible to Dothistroma species (see secion 4.2.2). Pinus suscepibility of the three most common European pine species, nigra subsp. nigra was previously described as slightly suscepible to P. mugo, P. nigra and P. sylvestris. In addiion to being important what was probably D. septosporum in New Zealand (Bulman, Gadgil, components of naive forests, P. nigra and P. sylvestris are important Kershaw, & Ray, 2004; Gadgil, 1984), but is now also ranked as mod- species in plantaion forestry, while P. mugo is widely used as an erately suscepible to this pathogen (Fraser, Woodward et al., 2015) ornamental tree. The country notes indicated that most DNB out- and highly suscepible following analysis of the geo-database data (see breaks in Europe (involving either D. pini or D. septosporum) are secion 4.2.2). Both P. halepensis and P. pinea, which were both previ- on P. nigra (and its subspecies) and that this host appears to be ously described as highly suscepible to D. septosporum when grow- more suscepible than P. sylvestris to Dothistroma species. This ing in East Africa (Ivory, 1968), have also been placed in the slightly was true for many countries, including Austria, Britain (Fig. 3), suscepible category following analysis of forest disease survey data Bulgaria, Czech Republic, Estonia, Hungary, Lithuania, Poland, Serbia, F I G U R E 3 Pinus nigra subsp. laricio showing severe Dothistroma needle blight (DNB) symptoms (centre and right of picture) growing adjacent to green Pinus sylvestris trees showing little or no apparent DNB symptoms (left of picture) in the south of England (Photo Credit: M.S. Mullett) | Drenkhan et al. 25 and moderately suscepible categories. The placement of P. nigra subsp. nigra in these other suscepibility categories is based on comparisons of this subspecies with P. nigra subsp. laricio and other species, which have produced contrasing results. Surveys in New Zealand and in France, where P. nigra subsp. laricio and P. nigra subsp. nigra are widely planted, suggest that P. nigra subsp. nigra is less suscepible to Dothistroma species (B. Marcais & L. Bulman, unpublished data). Fraser, Woodward et al. (2015) found P. nigra subsp. nigra to have moderate suscepibility to D. septosporum in experiments in Britain. The suscepibility of two other P. nigra subspecies, P. nigra subsp. dalmaica and P. nigra subsp. salzmannii to either Dothistroma species is unknown. F I G U R E 4 Dothistroma needle blight (DNB) severity on the three most common host species in Europe (Pinus mugo, P. nigra and P. sylvestris). The data obtained from geo-database see the Supporting Information. The disease severity index was calculated by multiplying the mean percentage of crown damaged and percentage of trees affected in the stand. Different letters above bars indicate significantly different means (Generalized Welch procedure 0.2 trimmed means, p = 0.05, procedures of statistical analyses are presented in the Supporting Information). Note: pine species with less than 30 records were excluded from the analysis Slovakia and Ukraine. The greater suscepibility of P. nigra compared to P. sylvestris is also clear from the analysis of the disease severity index derived from the geo-database data (Fig. 4). Previous reports also suggested greater suscepibility of P. nigra compared to P. sylvestris, with the later species showing litle or no DNB symptoms, even when planted adjacent to or mixed with severely afected P. nigra (Lang & Karadžić, 1987; Peterson, 1967a). Data obtained from the geo-database indicate that DNB severity levels on P. mugo are signiicantly greater than those on P. sylvestris and not diferent to those on P. nigra (Fig. 4). Both D. pini and D. septosporum have been found on P. mugo, and this pine species was frequently recorded as a host in the country notes. In Switzerland, where it is widely planted in parks and gardens, P. mugo is the most common host. In the Czech Republic and Slovakia, P. mugo was the second most common host ater P. nigra. Ornamental P. mugo has also been recorded as a common host in several countries, including Austria, Estonia, Finland, Hungary and Lithuania, with severe damage caused by D. septosporum in both Estonia and Lithuania. In both Poland and Slovakia, damage caused by D. septosporum was observed on ornamental P. mugo, but not on P. mugo growing in natural/naive stands. In Switzerland and France, Dothistroma species have been observed in naive stands of P. mugo subsp. uncinata. Country notes (see Supporing Informaion) from Romania, Slovenia and Ukraine also list P. mugo as a host of Dothistroma species. Analysis of the geo-database data allowed for an invesigaion of the relaive suscepibility of two P. nigra subspecies, P. nigra subsp. nigra and P. nigra subsp. pallasiana. Combined data for DNB caused by both Dothistroma species suggested that there were no signiicant diferences in disease severity between these two subspecies across diferent countries (FWe = 0.22, p = 0.62). For this reason, P. nigra subsp. nigra was included in the highly suscepible category, as well as in the slightly 4.2.3 | Species with variable suscepibility rankings The suscepibility ranking of 18 hosts varied between reports. The suscepibility for most of these species did not vary considerably, spanning either slight to moderate (e.g. Pinus coulteri) or moderate to high suscepibility (e.g. P. mugo). However, six species (P. contorta, P. halepensis, P. oocarpa, P. pinea, P. sabineana and P. sylvestris) have been categorized as both slightly and highly suscepible to Dothistroma species. For example, Ivory (1968) reported that Pinus oocarpa growing in arboreta in Kenya was slightly suscepible, but this host has recently been seriously afected by D. septosporum in Colombia (Rodas et al., 2016). For P. sylvestris, the majority of authors have reported lower disease incidence and severity compared to other pines and have suggested that it is only slightly suscepible to these pathogens (Fraser, Woodward et al., 2015; Gilmour, 1967a,b; Karadžić, 1989b; Lang & Karadžić, 1987; Peterson, 1967a). In contrast, Millberg et al. (2016) found that P. sylvestris seedlings were more suscepible to D. septosporum than P. contorta seedlings in Sweden. Consistent with the fact that Gibson (1979) ranked P. sylvestris as highly suscepible, DNB-induced mortality on this host was observed in a Christmas tree plantaion in Virginia, the USA (Skelly, 1972) and on natural regeneraion in Norway (H. Solheim, unpublished data). Pinus contorta has been rated as slightly suscepible to D. septosporum by some authors (Bulman et al., 2004; Fraser, Woodward et al., 2015), but as highly suscepible (Gibson, 1979) and prone to mortality due to D. septosporum infecion in several areas by others (Graham & Heute, 2014; Parker & Collis, 1966; Woods et al., 2005). There are several possible explanaions for the inconsistency in host suscepibility rankings between reports, which centre on diferent aspects of the disease triangle. These include between-provenance variaion in suscepibility (Table 5), an interacion between environmental condiions and relaive host suscepibility, variaion in the relaive virulence of Dothistroma species, haplotypes or populaions on diferent host species (although this is yet to be demonstrated), variaion in the relaive suscepibility of a species at diferent ages, differences in the interpretaion of suscepibility categories by diferent assessors and the comparison of diferent sets of host species by different authors. Of these possible explanaions, between-provenance variaion in suscepibility to Dothistroma species has received the most atenion and will subsequently be discussed here. 26 | TABLE 5 Between-provenance variaion in host suscepibility to Dothistroma species. Hosta Dothistroma species Notes Reference D. septosporum East Africa No clear trend with provenance alitude. Ivory (1968) Pinus contorta D. septosporumb New Zealand Gilmour and Noorderhaven (1969) D. septosporum UK Provenance trial. Lower alitude provenances less suscepible. Some coastal provenances very resistant. Disease surveys of plantaions. Coastal origins are less suscepible than interior origins. Alaskan origins seem to be the least suscepible. Pinus ellioii D. septosporumb East Africa No details given. Gibson (1972) Pinus monicola D. septosporumb Briish Columbia, Canada Provenance trials. Interior provenances were more suscepible than coastal BC provenances. Hunt, Roke, Cleary, Carlson, and Berger (2011) Pinus muricata D. septosporumb California Mixed planing. Northern provenance less suscepible. Muir and Cobb (2005) A. Brown (unpubl. data) Australia Provenance trials. Northern provenances less suscepible. Ades, Simpson, Eldridge, and Eldridge (1992) Pinus nigra D. pinib Nebraska Provenance trials. Seed from the Tara Plateau, Montenegro, had low suscepibility. Seed sourced from eastern Austria had moderate suscepibility. Other provenances had high or variable suscepibility. Peterson and Read (1971) Pinus ponderosa D. septosporumb Australia Provenance trial. Arizona less suscepible than mariime provenances. Eldridge et al. (1980) Great Plains, USA Provenance trials. Southern Rockies, New Mexico, Arizona and one Nebraskan provenances less suscepible than others. Peterson (1984) Pinus radiata D. septosporumb California Cobb and Libby (1968) D. septosporumb California D. septosporumb New Zealand D. septosporumb Australia Natural infecion experiments. Island provenances less suscepible than Monterey provenances. Natural infecion experiments. Guadalupe Island less suscepible than Monterey, Año Nuevo and New Zealand provenances. Provenance trials. Monterey, Año Nuevo and New Zealand less suscepible than island and Cambria provenances. Provenance trials. Monterey and Año Nuevo less suscepible than Cambria provenances. D. septosporum UK Ariicial inoculaion and natural infecion experiments. Scoish populaions varied in suscepibility. Relaive suscepibility varied between years and sites. Fraser, Brown et al. (2015); Fraser et al. (2016) D. septosporum UK Natural infecion experiments. Some Scoish provenances more suscepible than some coninental European provenances. Fraser, Woodward et al. (2015) D. septosporum Estonia Provenance trial. Needle disease severity (including DNB) greater on northern Finland than southern Finland and Estonia provenances. R. Drenkhan, unpubl. data D. septosporum Colombia Provenance trial. Suscepibility was greater on low elevaion (c. 100% incidence and c. 40% severity) than on high elevaion (0% incidence) provenances. Rodas et al. (2016) D. septosporum Pinus sylvestris Pinus tecunumanii a Locaion Pinus caribaea b D. pini b b Power and Dodd (1984) Burdon and Bannister (1973) Ades and Simpson (1991) Drenkhan et al. Except for P. tecunumanii, all these hosts have been placed in more than one suscepibility category (when subspecies and varieies are included). Dothistroma species not conirmed using molecular techniques, but DNB was probably caused by the noted Dothistroma species, given the locaion of the report. b | Drenkhan et al. There is some support for the role of between-provenance vari- 27 Collecively, these indings show that, although important, aion in suscepibility, as it has been reported for ten Pinus species between-provenance variaion in suscepibility to Dothistroma spe- (Table 5), including half of the 18 species that are placed in more cies may not fully explain the diferent suscepibility rankings reported than one suscepibility category (when subspecies and varieies are by various authors. Furthermore, although it may be due to lack of included). Two widespread species, P. contorta and P. sylvestris, which research in this area, between-provenance variaion has not been have been classiied as both highly and slightly suscepible, provide reported for the four other host species (P. halepensis, P. oocarpa, prime examples of the possible efect of between-provenance varia- P. pinea and P. sabineana) that were ranked as both highly and slightly ion. Pinus contorta comprises three varieies, all of which are known suscepible, or for P. pinaster which has been placed in all suscepibility hosts of D. septosporum. The most widespread variety, P. contorta categories. Litle is currently known about the efect of environment var. laifolia, has been classiied as highly suscepible to D. septos- or pathogen variaion on the relaive suscepibility of Dothistroma porum following a widespread and highly damaging epidemic on this species hosts, which remain alternaive explanaions for the observed variety in Briish Columbia (Woods et al., 2005). The two other vari- variaion. eies, P. contorta var. contorta and P. contorta var. murrayana, have unknown suscepibility to D. septosporum. Results from early work in New Zealand suggested that P. contorta provenances varied signiicantly in DNB symptom expression (Gilmour & Noorderhaven, 1969) and, similarly, surveys in the UK indicated that provenances varied 5 | IMPACT OF THE ENVIRONMENT, OTHER FUNGAL SPECIES AND ANTHROPOGENIC FACTORS ON DNB signiicantly in suscepibility to D. septosporum. However, recent ariicial inoculaion and natural infecion experiments in the UK, including provenances of both P. contorta var. contorta and P. contorta var. laifolia, revealed no evidence for variaions in suscepibility 5.1 | Environmental impacts on the distribuion of DNB agents and DNB severity in diferent habitats (Fraser, Woodward et al., 2015). Moreover, DNB-induced mortality Understanding the impact of abioic factors can facilitate an under- on P. contorta var. contorta was observed recently in Alaska (Graham standing of the recent increase in incidence and severity of DNB. & Heute, 2014), further suggesing that variaion in suscepibility Abioic factors such as temperature (Peterson, 1973), precipitaion ranking may be caused by other factors besides varietal diferences (Cobb & Miller, 1968; Gibson, Christensen, & Dedan, 1967; Murray and that suscepibility may be strongly dependent on the area where & Batko, 1962; Woods et al., 2016), light (Gibson et al., 1964), trees are planted. topography and tree density (Marks & Hepworth, 1986), can all Recent research has also shown intraspeciic variaion in sus- inluence disease development and are covered in other reviews cepibility to D. septosporum within P. sylvestris. Ariicial inoculaion in this issue (Bulman et al., 2016; Woods et al., 2016). Of these experiments suggested that naive Scoish populaions of P. syl- abioic factors, moisture is the most important. Severe outbreaks vestris varied in suscepibility to D. septosporum (Fraser, Brown, & have been observed in years and locaions with high rainfall and Woodward, 2015). Subsequent natural infecion experiments with humidity (Bulman et al., 2013; Fabre et al., 2012; Murray & Batko, the same populaions also showed between-populaion variaion 1962; Peterson, 1973; Rodas et al., 2016; Rogerson, 1953; Woods in suscepibility, but relaive suscepibility varied between years et al., 2005). Conversely, DNB outbreaks do not occur in drier and sites, suggesing local adaptaion in either the P. sylvestris or years or dry regions, as observed in many countries in Europe D. septosporum populaions (Fraser et al., 2016). Surveys in a P. syl- (Murray & Batko, 1962; Fraser et al., 2016; Supporing Informaion). vestris trial in Estonia, which included provenances from Estonia The inluence of climate on disease development can serve to and Finland, demonstrated that needle disease severity (including mask the presence of Dothistroma species in regions that are marginal DNB caused by D. septosporum) was greatest on northern Finland or unsuitable for disease development (Hanso & Drenkhan, 2013). provenances (R. Drenkhan, unpublished. data). Field experiments This observaion could explain the apparent incongruity in northern in Scotland with P. sylvestris provenances from across Europe indi- Europe, where D. septosporum has been known for over 100 years in cated that some Scoish provenances might be more suscepible to Denmark and Russia, but has only recently been recorded in Balic and D. septosporum than some coninental provenances, although these Fennoscandia countries. The warmer and weter weather experienced diferences were not always signiicant (Fraser, Woodward et al., during the last two decades in northern Europe may have contributed 2015). Although this work showed that P. sylvestris provenances to increased disease severity and, combined with greater efort spent from across Europe vary in suscepibility to D. septosporum, it also looking for DNB over that ime, may have resulted in the recent dis- demonstrated that all P. sylvestris provenances were less suscepible covery of the disease in this part of Europe (Hanso & Drenkhan, 2008; than the highly suscepible P. muricata and P. ponderosa. This inding Müller et al., 2009; Solheim & Vuorinen, 2011). This is despite the like- suggests that the placement of P. sylvestris in the highly suscepible lihood that Dothistroma was already present in these areas for a long category may be erroneous or caused by factors other than prove- period of ime. nance diferences, although examinaion of the suscepibility of a There are several regions in the world where the climate is pre- wider range of P. sylvestris provenances is needed before this can be dicted to be suitable for the development of the disease and where conclusively proven. suscepible hosts occur, but where DNB has not yet been recorded 28 | Drenkhan et al. (Wat et al., 2009). Such regions are found in all coninents, especially Asia (Figs 1 and 2). It is not known whether Dothistroma species occur in these areas and remain undetected or whether these areas are truly free of Dothistroma species (see secion 2.2). The former is more likely given the recent observaion of D. septosporum in areas, such as Turkey and the Far East Russia, that were predicted to be suitable by Wat et al. (2009), but were not previously recorded as having DNB. Preliminary populaion geneic analyses show that a populaion of D. septosporum from Turkey includes both maing types and has a high haplotypic diversity (M. S. Mullet & F. Oskay, unpublished data). This suggests that the pathogen has been in Turkey, unnoiced, for some ime. This may also be the case for the Far East Russia (Fig. 2) where D. septosporum was irst recorded in 2014 (Barnes et al., 2016). The impact of climaic condiions on DNB incidence and severity underpins the importance of understanding the efect of climate change on the suitability of diferent areas for infecion by Dothistroma species. Under climate change projecions, the suitable area for Dothistroma species is set to decrease by 11–22% over the next 70 years (Wat, Ganley, Kriicos, & Manning, 2011). However, the predicted decrease in the suitable area for Dothistroma species was mainly seen in areas of F I G U R E 5 Severity of Dothistroma needle blight in different habitats. The data obtained from geo-database see Supporting Information. The disease severity index was calculated by multiplying the mean percentage of crown damaged and percentage of trees affected in the stand. Different letters above bars indicate significantly different means (Generalized Welch procedure 0.2 trimmed means, p = 0.05, procedures of statistical analyses are presented in the Supporting Information). Note: types of habitats with less than 30 records were excluded from the analysis the Southern Hemisphere without pine plantaions (Wat et al., 2011). The severity of DNB is predicted to increase in the Northern Hemisphere in areas with substanial natural woodlands and plantaion forests, including Fennoscandia, eastern Russia and western Canada (Wat et al., 2011). As this review has shown, this trend is already being witnessed. Although demonstraing causal relaionships between climate change and biological phenomena is diicult, Woods et al. (2005) did ind a clear mechanisic relaionship between a climate trend (increased summer precipitaion) and DNB severity in western Canada, one of the areas where Wat et al. (2009) predicted DNB severity to increase with climate change. However, it must also be stressed that several other bioic, abioic and anthropogenic factors, such as an increase in host use (Woods 2003) or the introducion of more virulent pathogen haplotypes, may also be important drivers of DNB epidemics. 5.2 | DNB severity in diferent habitats and other fungi associated with Dothistroma species The introducion of highly suscepible hosts in plantaion forestry or monocultures can alter fungal behaviour and increase disease severity (Evans, 1984). With data obtained from entries in the geo-database and informaion based on country notes, analysis of the impact of stand type on DNB severity and the associaion of DNB with other diseases were measured. Signiicant diferences in the damage caused by DNB were conirmed in diferent habitats (N = 372, FWe = 51.4, p < 0.001). Speciically, forests originaing from natural regeneraion showed lower levels of damage than Other needle inhabiing fungi are oten overlooked or go unreported during DNB surveys, and litle is therefore known regarding the impact of other fungi on Dothistroma species and afected trees. Data collected in the geo-database, however, revealed diferences in the frequency of other fungal species associated with DNB, at both tree and stand level. In paricular, at the tree level the foliar fungi mainly associated with DNB were Lophodermium pinastri, Lophodermium sediiosum, Cyclaneusma spp., Diplodia sapinea, Coleosporium spp. and Neocatenulostroma spp. (Fig. 6a). A similar patern was found at the stand level, where L. pinastri was the most frequent fungus reported, followed by D. sapinea, Cyclaneusma spp., L. sediiosum, Coleosporium spp., Neocatenulostroma spp., Pestaloiopsis funerea, Heterobasidion annosum and Epicoccum nigrum (Fig. 6b). These fungi were, in most cases, ideniied based on visual symptoms and morphology (mainly fruiing bodies) and not necessarily conirmed using molecular diagnosics. Other needle fungi frequently occur together with Dothistroma species, on the same host and oten on the same needle (Jurc, 2007; Jurc & Jurc, 2010). These fungi oten overgrow each other, making it diicult to disinguish between species. In some cases, DNB damage is exacerbated by other pathogens, for example losses caused by Dothistroma species increased when Armillaria spp. and Diplodia sapinea were also causing disease on the same host (Karadžić, 1989b; Shaw & Toes, 1977). As a result, damage to forest stands is oten the result of a complex of pathogens, rather than being due to a single paricular pathogen. ariicial plantaions or sowings, urban trees and arboreta (Fig. 5). Many country also notes reported that trees were infected by Dothistroma species in plantaions, gardens and arboreta, but less frequently in naturally regenerated woodlands. However, there was no diference in damage caused by DNB between pure and mixed stands (N = 875, FWe = 0.56, p = 0.46). 5.3 | Impact of anthropogenic factors on DNB One of the main factors contribuing to the increase in biological invasions by plant pathogens is an expansion in internaional travel and trade (Liebhold, Macdonald, Bergdahl, & Mastro, 1995). | Drenkhan et al. 29 (a) (b) F I G U R E 6 Frequency of other fungi associated with Dothistroma needle blight (DNB) at the tree level (a) and the stand level (b) . The data obtained from geo-database see Supporting Information Globalizaion has increased the rate of anthropogenic introducions infected nursery stock consituted the iniial inoculum source for of plant pathogens to new regions mainly through the trade of DNB outbreaks. Furthermore, idenical haplotypes and a lack of infected plant material (Sanini et al., 2013). Further trade and geneic diversity of D. septosporum in Chile and Ecuador supports movement of plant material within regions can contribute to the the hypothesis that D. septosporum may have been introduced into local spread of these damaging agents. The most likely pathway Ecuador from Chile on live plants (Barnes, Wingield et al., 2014). for Dothistroma species is the movement of infected plants, espe- Similarly, in the Czech Republic, DNB was irst reported in 1999 cially as infected plants can appear symptomless for months before on nursery stock of Pinus nigra and P. mugo imported from Hungary, symptom development occurs (Ganley, Hargreaves, & Donaldson, and was subsequently found in forest stands (Jankovský, Palovčíková 2015; Millberg et al., 2016). The increase in the trade of live et al., 2004; Jankovský, Bednářová et al., 2004). In Australia and plants is, therefore, a likely contribuing factor to the observed New Zealand, spread of D. septosporum has also been atributed increase in the incidence and impact of DNB. Supporing this view, to the movement of infected plants (Brown & Wylie, 1991; Bulman Evans and Oleas (1983) suggested that the isolated occurrence of et al., 2013). the Dothistroma pathogen in nurseries, and in widely dispersed Another important trend afecing the range expansion or move- and recently established smallholdings in Ecuador, indicated that ment of invasive pathogens is the increased planing of suscepible 30 | Drenkhan et al. host plants in suitable climates for the pathogen (Wat et al., 2009). regularly be added and updated as this informaion becomes avail- The expansion of DNB in the Southern Hemisphere relects the able. In paricular, it is hoped that the inclusion of more sample anthropogenic history of the introducion and establishment of P. radi- informaion from poorly studied regions, such as Asia, will provide ata plantaion forestry (Barnes, Wingield et al., 2014). In western beter knowledge of the distribuion of DNB worldwide. Canada, recent increases in DNB incidence and severity were linked An enhanced understanding of the distribuion of the two causal to the increase in the planing of suscepible P. contorta var. laifolia species, D. septosporum and D. pini, is beginning to emerge due to (Woods, 2003). While in the UK, the recent DNB outbreak followed an the more widespread use of molecular ideniicaion tools required increase in the planing of highly suscepible P. nigra subsp. laricio over to disinguish between them. DIAROD training courses in molecular P. sylvestris. Likewise, in the rest of Europe, new disease reports of DNB diagnosics enabled many European forest pathologists to determine in several countries involved P. nigra or its subspecies (see Supporing which of the two Dothistroma species are present in their country. Informaion), the most common introduced two-needle pine species in Dothistroma septosporum was already known to have a worldwide dis- central Europe (Novotný, Modlinger, Pešková, & Čáp, 2012). The high tribuion and to be responsible for some recent epidemics in Europe DNB severity index of this host (Fig. 4), and the high suscepibility of and Canada. What became apparent from the work outlined in this this pine species observed in diferent countries (Table 3), suggests review is that D. pini is more prevalent in Europe than previously that the introducion of P. nigra and its subspecies has likely contrib- thought, with 12 country reports for this species. In the USA, the uted to the increase in incidence and severity of DNB in Europe. It is geographic ranges of D. pini and D. septosporum appear disinct from not known to what extent, if any, the known cases of non-pine hosts one another according to current records. These results suggest that (various species in the genera Abies, Cedrus, Larix, Picea, Pseudotsuga; we are only just staring to understand the distribuion of D. pini. It see Table 3) contribute to movement of the Dothistroma species. is realisic to anicipate that even broader adopion of the molecular The 2011 IUFRO meeing addressed the important topic of anthropogenic transfers of forest pathogens and published the diagnosic tools will show a clearer picture of the ranges of the two species of Dothistroma. Montesclaros Declaraion (htp://www.iufro.org/science/divisions/ The origins or centres of diversity of D. septosporum and D. pini division-7/70000/publicaions/montesclaros-declaraion). This doc- are sill unknown and require further invesigaion. There is clearly ument highlighted the increased risks of internaional trade of plant a great need to acively expand eforts to collect cultures of these material to forest health worldwide and, while recognizing that it is fungi, paricularly from poorly studied areas. In addiion, broader use impossible to completely stop trade of biological materials (including, of molecular tools such as microsatellite markers on local and global e.g. wooden packaging material and wood chips), declared that path- DNB populaions, especially from regions such as the Americas and ways with a high phytosanitary risk, and low overall economic impor- Asia is needed and will help to test hypotheses about origins and to tance, should be closed to avoid the spread of pathogens, such as develop models of migraion of the two pathogens. This informaion Dothistroma species, to new areas. Although this review demonstrates will also be important to implement targeted eforts to limit the spread that Dothistroma species are already widespread, introduced control of Dothistroma species and to prevent the introducion of new strains mechanisms on the trade of live plants should sill be considered to of either species into countries that currently have limited geneic stop the introducion of diferent Dothistroma species or haplotypes diversity of these pathogens. that may lead to greater DNB incidence and severity in the future. There are now 109 documented host taxa for both Dothistroma pathogens. Of these, 95 are Pinus species while the remainder are 6 | CONCLUSIONS AND FUTURE PROSPECTS from ive other genera in the Pinaceae. The host ranges of the Dothistroma pathogens appear to be increasing, as there have been 14 newly reported hosts (species or subspecies) since 2008, as well as the six that had only been reported in “grey” or local language liter- Collaion of informaion from a wide range of sources has provided ature before this date. Of special note are two newly reported hosts the most comprehensive documentaion of the global range of DNB on which severe levels of DNB have been observed; P. nigra subsp. made to date. An unprecedented level of informaion about DNB pallasiana in the Ukraine and southwest Russia (Barnes, Kirisits et al., was compiled using mainstream, “grey” and local language literature, 2008), and P. monophylla in Switzerland (V. Queloz, unpublished along with re-assessment of herbarium specimens, individual country data). Increased awareness of DNB, along with more widespread dis- reports and results from new disease surveys iniiated as part of ease surveys, clearly accounted for some of these new host records. the DIAROD COST Acion. DNB is now reported in 76 countries However, expansion of host ranges by the pathogens, anthropogenic of the world of which 35 are in Europe. The geo-database (htp:// transfer of Dothistroma species, or efects of changing climate on host arcgis.mendelu.cz/monitoring/) established to house these data, along suscepibility may also play a role. with the country reports available in the Supporing Informaion, In this review, the rankings of host suscepibility were updated and record a depth of local knowledge about DNB, such as hosts and various factors that inluence suscepibility were ideniied. Based on pathogens involved, and disease trends and impacts over ime. It results from both ield observaions and experimental trials reported in is envisioned that this database will remain acive and that any both peer-reviewed and “grey” literature, relaive suscepibility rank- new informaion regarding DNB and its associated pathogens will ings of DNB hosts were comprehensively assessed and updated from Drenkhan et al. previous summaries. Most DNB outbreaks in Europe have occurred on P. nigra and its subspecies, and in general, this host appears to be more suscepible than the widely distributed P. sylvestris. The host range and host suscepibility informaion presented in this review is anicipated to be of immense pracical importance to foresters and landscape managers when planning which species to plant in DNBprone regions. Inconsistent rankings, atributed to 18 of the hosts by diferent authors, may be accounted for by a range of bioic factors such as host provenance and geneics, host age and pathogen haplotype or abioic factors (planing site, climate). These inconsistencies highlight that further research is needed to determine the inluence of bioic and abioic factors before accurate predicions can be made about how a speciic host will perform at a paricular locaion. The host–pathogen interacions are an unexplored area of study in Dothistroma research. Informaion about the true host range of each of the Dothistroma species is far from complete. This is partly due to the lack of knowledge of pathogen species idenity for many of the hosts. It is also partly due to the limited knowledge we have of the global distribuion of D. pini, despite the new reports of this species in Europe, cited above. Other unanswered quesions include how much variaion there is in virulence and environmental preferences between D. pini and D. septosporum, and also between isolates of each of these species. Finally, the inluence of both inter- and intraspeciic variaion of the pathogen on suscepibility of diferent host species needs to be a focus of future work, so that this important bioic factor can be taken into account when planning forest planing. The collaboraive work described here presents a model that answers the recent call of the president of the Internaional Union of Forest Research Organizaions (IUFRO) for a global, rather than singlecountry, strategy to manage forest pests and diseases (Wingield, Brockerhof, Wingield, & Slippers, 2015). This type of global collaboraive research is “vitally important and urgently needed” (Wingield et al., 2015) and the work of the DIAROD COST Acion described in this review provides a plaform on which these further studies can be built. AC KNOWLE DG E MENTS This study was parially supported by the EU COST Acion FP1102 DIAROD (Determining Invasiveness and Risk of Dothistroma, http://www.cost.eu/COST_Actions/fps/Actions/FP1102?), Norwegian Financial Mechanism 2009–2014 under the project EMP162 and the Insituional Research Funding IUT21-04. We would like to thank Angus Carnegie, Jim Walla and Tod Ramsield for providing informaion regarding DNB in Australia, the USA and Canada, respecively, and four anonymous reviewers for valuable correcions and suggesions for the manuscript. REFERENCES DAVFP Collecions Database. Retrieved from htp://cfs.nrcan.gc.ca/herbarium/fungus/2071?lang=en_CA (Accessed on 10.03.2016) Ades, P. K., & Simpson, J. A. (1991). Variaion in suscepibility to dothistroma needle blight among provenances of Pinus radiata var. radiata. Silvae Geneica, 40, 6–13. | 31 Ades, P. K., Simpson, J. A., Eldridge, K. G., & Eldridge, R. H. (1992). 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Global geographic distribution and host range of Dothistroma species: a comprehensive review

Global geographic distribution and host range of Dothistroma species: a comprehensive review

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