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
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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
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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
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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
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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
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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
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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).
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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
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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.
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