A global climatic risk assessment of pitch canker disease

Abstract

Pitch canker is a devastating disease of Pinus spp. and Pseudotsuga menziesii (Mirb.) Franco. The pathogen responsible for this disease, Fusarium circinatum Nirenberg & O'Donnell, has spread to many countries within the last three decades. The susceptibility of the widely planted commercial species Pinus radiata D.Don to this pathogen has been of concern to pine forest industries worldwide. Using the process-based distribution program CLIMEX, the global risk of pitch canker establishment was predicted based on a number of climatic variables. The predicted risk of pitch canker establishment by CLIMEX fit well with regions known to have the disease, such as the southeastern United States and Spain. Conversely, the model predicted that the climate in California was not optimal for pitch canker, which fits with the observed lower frequency of natural infections and the strong association with insects in this region. Likewise, Chile, which is known to have F. circinatum in the nurseries but not in the plantation forests, was also predicted to have marginal to suitable climatic conditions for pitch canker establishment. Regions of China, Brazil, Australia, and New Zealand were predicted to have optimal climate conditions for disease establishment. Thus, continued strict quarantine regulations are recommended to prevent the establishment and spread of this pathogen in these countries.

Full text

A global climatic risk assessment of pitch canker
disease
Rebecca J. Ganley, Michael S. Watt, Lucy Manning, and Eugenia Iturritxa
Abstract: Pitch canker is a devastating disease of Pinus spp. and Pseudotsuga menziesii (Mirb.) Franco. The pathogen re-
sponsible for this disease, Fusarium circinatum Nirenberg & O’Donnell, has spread to many countries within the last three
decades. The susceptibility of the widely planted commercial species Pinus radiata D.Don to this pathogen has been of
concern to pine forest industries worldwide. Using the process-based distribution program CLIMEX, the global risk of
pitch canker establishment was predicted based on a number of climatic variables. The predicted risk of pitch canker es-
tablishment by CLIMEX fit well with regions known to have the disease, such as the southeastern United States and
Spain. Conversely, the model predicted that the climate in California was not optimal for pitch canker, which fits with the
observed lower frequency of natural infections and the strong association with insects in this region. Likewise, Chile,
which is known to have F. circinatum in the nurseries but not in the plantation forests, was also predicted to have mar-
ginal to suitable climatic conditions for pitch canker establishment. Regions of China, Brazil, Australia, and New Zealand
were predicted to have optimal climate conditions for disease establishment. Thus, continued strict quarantine regulations
are recommended to prevent the establishment and spread of this pathogen in these countries.
Re
´sume
´:Le chancre re
´sineux est une maladie de
´vastatrice chez les espe
`ces de Pinus et Pseudotsuga menziesii (Mirb.)
Franco. L’agent pathoge
`ne responsable de cette maladie, Fusarium circinatum Nirenberg & O’Donnell, s’est propage
´dans
plusieurs pays au cours des trois dernie
`res de
´cennies. La susceptibilite
´de Pinus radiata D.Don, une espe
`ce commerciale
plante
´ea
`grande e
´chelle, a
`cet agent pathoge
`ne pre
´occupe les industries forestie
`res qui utilisent le pin partout dans le
monde. Gra
ˆce au programme de distribution CLIMEX, base
´sur les processus, le risque d’e
´tablissement du chancre re
´sin-
eux a
`l’e
´chelle du globe a e
´te
´pre
´dit a
`partir de plusieurs variables du climat. Le risque d’e
´tablissement du chancre re
´sin-
eux pre
´dit par CLIMEX correspond bien aux re
´gions ou
`la maladie est pre
´sente, telles que le sud-est des E
´tats-Unis et
l’Espagne. A
`l’inverse, le mode
`le pre
´dit que le climat de la Californie n’est pas optimal pour le chancre re
´sineux, ce qui
correspond a
`la faible fre
´quence des infections naturelles et a
`l’association e
´troite a
`des insectes observe
´es dans cette re
´-
gion. De la me
ˆme fac¸on, au Chili, ou
`F.circinatum est pre
´sent dans les pe
´pinie
`res mais pas dans les plantations, le mode
`le
pre
´dit que les conditions climatiques vont de marginales a
`propices. Le mode
`le pre
´dit que les conditions climatiques sont
optimales pour l’e
´tablissement de la maladie dans certaines re
´gions de la Chine, du Bre
´sil, de l’Australie et de la Nouvelle-
Ze
´lande. Par conse
´quent, des mesures strictes et permanentes de quarantaine sont recommande
´es pour pre
´venir l’e
´ta-
blissement et la propagation de cet agent pathoge
`ne dans ces pays.
[Traduit par la Re
´daction]
Introduction
Pitch canker is a destructive disease of Pinus spp. and
Pseudotsuga menziesii (Mirb.) Franco (Wingfield et al.
2008). The pathogen responsible for this disease, Fusarium
circinatum Nirenberg & O’Donnell (teleomorph = Gibber-
ella circinata), has been recorded in numerous countries
worldwide, and the disease has caused serious problems in
both native and nonnative forests in many of these countries
(Ganley 2007; Wingfield et al. 2008). Based on the wide
distribution and high level of genetic diversity of the patho-
gen populations in these regions, the pathogen is believed to
have originated from Mexico and the southern region of
Florida in the United States (Gordon 2006; Wingfield et al.
2008). Although F. circinatum has a global distribution, the
establishment and severity of pitch canker in these countries
has been variable. This is attributed to differences in vector
and wound agents and climatic conditions.
Fusarium circinatum can be disseminated vertically
through infested seed or horizontally by spores vectored by
wind, rain, animals, insects, or soil. However, infection will
only occur when spores are associated with wounds or open-
ings on the tree; intact tissue is not susceptible to the fungus
(Gordon et al. 1998). In general, pitch canker has been asso-
ciated with wounds created by insects (Gordon et al. 2001),
weather-related injuries (hail or wind damage) (Kelley and
Williams 1982), and mechanical damage (branch removal
or cone harvesters) (Dwinell et al. 1985). The importance of
Received 4 January 2009. Accepted 10 August 2009. Published on the NRC Research Press Web site at cjfr.nrc.ca on 18 November
2009.
R.J. Ganley1and L. Manning. Scion, New Zealand Forest Research Institute, Private Bag 3020, Rotorua, New Zealand.
M.S. Watt. Scion, New Zealand Forest Research Institute, P.O. Box 29237, Christchurch, New Zealand.
E. Iturritxa. Neiker, Granja Modelo de Arkaute, P.O. Box 46, E-01080, Vitoria-Gasteiz, Spain.
1Corresponding author (e-mail: Rebecca.Ganley@scionresearch.com).
2246
Can. J. For. Res. 39: 2246–2256 (2009) doi:10.1139/X09-131 Published by NRC Research Press

specific vectors and wounding agents varies between loca-
tions that have pitch canker. For instance, the spread of
pitch canker in California is almost solely dependent on in-
sects. While infections do occur from weather-related inju-
ries, they occur so infrequently that they are considered
inconsequential (Gordon et al. 1998). Conversely, in the
southeastern United States the disease is mainly thought to
occur from weather and mechanical damage rather than
from insect damage (Dwinell et al. 1985).
The role of insect–host interactions versus nonnative
plantings of pine is also important. In California, nonnative,
susceptible Pinus spp. have considerably less infections in
the field than native Pinus radiata D.Don (Gordon et al.
1998). The low incidence of pitch canker on nonnative pines
is a function of fewer insects associated with the disease.
Thus, where nonnative Pinus species are planted, the impor-
tance of climate suitability is perhaps greater than insect
pests. Fusarium circinatum has been present in Chilean
nurseries since at least 2002; however, the disease has not
established in adjacent Pinus radiata plantations (Wingfield
et al. 2002b; Ganley 2007). The lack of field infection has
been attributed to fewer insects and unsuitable climatic con-
ditions. Similarly, F. circinatum has been present in South
African nurseries since the early 1990s (Viljoen et al.
1994), although it has only recently become established in
plantations (Coutinho et al. 2007).
The development of risk maps, which describe the poten-
tial distribution and probability of pitch canker establish-
ment, are likely to be useful to forest managers worldwide.
All Pinus spp. and Pseudotsuga menziesii are susceptible to
F. circinatum, although Pinus radiata is the most suscepti-
ble species (Hodge and Dvorak 2000; Gordon 2006). Since
Pinus radiata is the most widely grown plantation species
in the world (Wingfield et al. 2002a), the economic impact
of pitch canker could be substantial. Predicting the probabil-
ity of pitch canker becoming established in unaffected coun-
tries would be of considerable interest to biosecurity
agencies of both commercial and native pine forests. In re-
gions with established pitch canker, risk maps could assist
in the development of strategies to mitigate the impact of
the disease.
In this study, the process-based distribution model CLI-
MEX was used to predict the potential global distribution
and likelihood of pitch canker establishment in Pinus spp.
as a function of climate. CLIMEX has been successfully
used to project the potential distribution of other major dis-
eases, such as Dothistroma needle blight (Watt et al. 2009),
and rice blast disease (Lanoiselet et al. 2002). CLIMEX is
well suited for predicting disease distribution, as the climatic
parameters within the model are partitioned and can be used
to describe pathogen occurrence. As CLIMEX includes a
global meteorological database and process-based algo-
rithms, it can use distribution data or observed physiological
responses to project species distributions in novel climates
with more confidence than regression-based models
(Kriticos and Randall 2001).
Methods
The CLIMEX model
The analysis used CLIMEX version 3 for Windows
(Sutherst et al. 2007) to model the distribution of pitch can-
ker under current climatic conditions. CLIMEX integrates
the weekly responses of a population to climate into a series
of weekly and annual indices. For fungal diseases the CLI-
MEX annual growth index (GIA) describes the potential for
population growth of the host and fungus as a function of
soil moisture and temperature during favourable conditions.
Eight stress indices (cold, wet, hot, dry, cold–wet, cold–dry,
hot–wet, and hot–dry) were used to determine the probabil-
ity that the fungal population can survive unfavourable con-
ditions. Other conditions for growth, such as growing season
length in degree days (PDD), were used to limit the mod-
elled organism distribution (Table 1). The growth and stress
indices are calculated weekly and are combined into an
overall annual index of climatic suitability, the Ecoclimatic
Index (EI). The EI ranges from 0 for locations where the
species is not able to persist to 100 for locations that are op-
timal for the species. To attain an EI value of 100, it is nec-
essary for conditions to be optimal throughout an entire
year. In this study, EI was classified into marginal (EI = 1–
5), suitable (EI = 6–20), and optimal (EI > 20) categories for
pitch canker.
Disease and pathogen records
Depending on the data available, reported records of pitch
canker and (or) F. circinatum were compiled using individ-
ual point, county, state, and island locations for countries
known to have pitch canker. Disease and pathogen records
were obtained for the following countries: Chile (Wingfield
et al. 2002b), Japan (Muramoto et al. 1993), Mexico
(Guerra-Santos 1999; Britz et al. 2001), South Africa
(Viljoen et al. 1997; Britz et al. 2005; Hurley 2006;
Coutinho et al. 2007), Spain (Landeras et al. 2005; Pe
´rez-
Sierra et al. 2007; E. Iturrixta, Neiker, Granja Modelo de
Arkaute, unpublished data), and United States (Hepting
and Roth 1946; Schmidt and Underhill 1974; Claeson and
Smith 1977; Dwinell et al. 1977, 1985; Kelley and
Williams 1982; Kuhlman and Cade 1985; McCain et al.
1987; Huang and Kuhlman 1990; Correll et al. 1991;
Storer et al. 1994; Blakeslee et al. 1999; Carey et al.
2000, 2005; Wikler and Gordon 2000; Gordon et al. 2001;
Lopez et al. 2002; Enebak and Carey 2003; Vogler et al.
2004; Starkey et al. 2007; H.A. Pase, Texas Forest Service,
unpublished data). The disease and pathogen records ob-
tained were reported from a variety of different Pinus spp.
and Pseudotsuga menziesii.
For areas known to have pitch canker, positive pathogen
reports were used as positive disease records. Exceptions to
this were positive reports of F. circinatum from Chile
(Wingfield et al. 2002b, 2008), from the Sierra Nevada site
in the United States (Vogler et al. 2004), and from nursery
records in South Africa (Viljoen et al. 1997; Britz et al.
2005; Hurley 2006). For these locations, the positive
F. circinatum records were used as pathogen-only reports.
The Chilean and South African records used as pathogen-
only reports were from nurseries. For the Sierra Nevada
site, the pathogen was reported from a healthy tree, and
there was no evidence to suggest establishment of pitch can-
ker in the region (Vogler et al. 2004).
Ganley et al. 2247
Published by NRC Research Press

CLIMEX model fitting
The climate dataset used within CLIMEX for the
parameter-fitting was a 0.5 degree of arc dataset generated
by Kriticos et al. (2006) from the 1961–1990 climate nor-
mals provided by the climate research unit (Mitchell et al.
2004). This dataset was used to infer the climatic require-
ments of the host and fungus from known occurrences of
pitch canker. To predict distribution elsewhere in the world,
the parameter values for the growth and stress functions in
CLIMEX were first fitted to the geographical distribution of
pitch canker in the United States. This area encompasses the
putative native range and exotic range of F. circinatum.
Phenological observations and relevant laboratory based bio-
logical information were also used to inform the selection of
relevant parameters in CLIMEX. The accuracy of the result-
ing model was tested against independent point observations
of the disease from Spain, Italy, Japan, and South Africa,
and from known disease occurrences on islands or at the
state level from Mexico, Japan, Haiti, and Spain. In Chile,
positive records of F. circinatum in infected nurseries, but
absence of pitch canker in adjacent plantations, were also
used to validate the model. In this case, model validation
was based on the unsuitability of climatic conditions in
Chile for pitch canker establishment.
Fitting CLIMEX parameters
Stress indices, which scale between 0 and infinity (0 = no
stress; ‡100 = lethal conditions), were initially adjusted so
that stresses largely constrained the fungal population from
expanding beyond its present observed distribution limits.
Several different values of cold stress and thermal accumu-
lation were tried to find values that best explained the ob-
served range boundaries. Growth indices, which scale
between 0 and 100 (0 = no growth, and 100 = perfect grow-
ing conditions year round) were adjusted iteratively so that
the projected climate suitability patterns most closely
matched the observed disease distributions. Where possible,
values for growth indices were based on available experi-
mental values.
Cold stress
Both the degree-day and cold stress temperature threshold
components were necessary to adequately describe the
known cool climate boundary to the northern limit of lati-
tude, approximately 378N from Arkansas in the east to Vir-
ginia in the west (Table 1).
Thermal accumulation
In addition to lethal cold temperatures, the distribution of
the pathogen was limited in cool environments, using ther-
mal accumulation, which is the annual integral of tempera-
ture and time required to complete the life cycle. A thermal
accumulation (PDD) of 1150 8C days was used to limit the
northern boundary of the disease to California on the west
coast of the USA (Table 1).
Dry stress
Because dry conditions are thought to limit disease estab-
lishment by drying the wound before a successful infection
can occur (Storer et al. 1997), a relatively high value of 0.3
for dry stress threshold (SMDS) was used with a stress accu-
mulation rate (HDS) of –0.005week–1 (Table 1). These val-
ues limited the potential distribution of the disease to the
narrow coastal strip where it has been found in California.
Table 1. Climatic values used for modelling the global distribution of pitch canker.
Index Parameter Valuea
Temperature DV0 = limiting low temperature 10 8C
DV1 = lower optimum temperature 18 8C
DV2 = upper optimum temperature 24 8C
DV3 = limiting high temperature 31 8C
Moisture SM0 = limiting low soil moisture 0.3
SM1 = lower optimum soil moisture 1
SM2 = upper optimum soil moisture 1.5
SM3 = limiting high soil moisture 2
Cold stress TTCS = temperature threshold 1 8C
THCS = stress accumulation rate –0.001week–1
DTCS = minimum degree-day cold stress threshold 15 8C days
DHCS = degree-day cold stress rate –0.00027week–1
Wet stress SMWS = wet stress threshold 2
HWS = wet stress accumulation rate 0.002week–1
Dry stress SMDS = dry stress threshold 0.3
HDS = dry stress accumulation rate –0.005week–1
Hot–wet stress TTHW = hot wet temperature threshold 30 8C
MTHW = hot wet soil moisture threshold 1.4
PHW = stress accumulation rate 0.003week–1
Hot–dry stress TTHD = hot dry temperature threshold 29 8C
MTHD = hot dry soil moisture threshold 0.3
PHD = stress accumulation rate 0.05week–1
Annual heat sum PDD = degree-day thresholdb1150 8C days
aValues without units are a dimensionless index of a 100 mm single bucket soil moisture profile.
bMinimum annual total number of degree-days above DV0 needed for population persistence.
2248 Can. J. For. Res. Vol. 39, 2009
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Wet stress
The wet stresses were set to values that had little con-
straint on the disease distribution. The rationale for this is
that (i) host distribution exhibits little sensitivity to high
soil moisture in cool to warm environments (M.S. Watt,
Scion, New Zealand Forest Research Institute, unpublished
data) and (ii) there is an increase in F. circinatum spore fre-
quency, dispersal, and survival during the wettest months of
the year (Blakeslee et al. 1979). Following this rationale, the
wet stress threshold (SMWS) was set to a high value of 2
with a stress accumulation rate (HWS) of 0.002week–1
(Table 1).
Hot–dry stress
Hot–dry stress was used because these conditions are
likely to result in greater levels of water evaporation and
drying, which could dry wounds out preventing infection
from occurring (Storer et al. 1997). This stress was used to
constrain the distribution to the narrow coastal strip of Cali-
fornia (Table 1).
Hot–wet stress
Following previous research (Wharton and Kriticos 2004),
hot–wet stress was used to exclude the disease from areas
where the pine host would be out-competed by broad-leaved
tropical species. The hot–wet stress threshold (TTHW) was
set to 30 8C with the soil moisture above 1.4 and a stress
accumulation rate (PHW) of 0.003week–1 (Table 1). This
temperature reflects conditions that are favourable for
broad-leaved tropical plants (Fitzpatrick and Nix 1970).
Temperature index
A value of 10 8C was set as the minimum temperature for
development (DV0), as F. circinatum growth has been
shown to be suppressed below this temperature (McDonald
1994) (Table 1). The lower temperature for maximum
growth rates (DV1) was set to 18 8C, and the upper temper-
ature threshold for maximum growth rates (DV2) was set to
24 8C. This encompasses optimal temperatures for spore
germination and pathogen growth (Inman et al. 2008)
(Table 1). The maximum threshold for population growth
(DV3) was set to 31 8C (Table 1).
Moisture index
Since the incidence and severity of pitch canker tends to
be greater in regions subject to fog, high humidity, or heavy
rainfalls (Blakeslee et al. 1979; Wikler et al. 2003), indicat-
ing a necessity for moist conditions, a relatively high value
for the limiting soil moisture (SM0) of 0.30 was used
(Table 1). To reflect the preference of the pathogen for wet
Fig. 1. Ecoclimatic suitability for pitch canker establishment across the Caribbean and North and Central America. Dots () represent point
observations and thatching ( ) represents islands, counties, or states known to have pitch canker. The triangle (~) is a pathogen-only
report from the Sierra Nevada. Inset: Hawaii, in relation to North America.
Ganley et al. 2249
Published by NRC Research Press

conditions, the optimal soil moisture thresholds (SM1, SM2)
and the upper limiting soil moisture (SM3) were also set rel-
atively high at 1, 1.5, and 2, respectively (Table 1).
Results
Model fit
The modelled climatic suitability for pitch canker estab-
lishment fit the known occurrences within North America
well (Fig. 1). The model showed a high level of climate
suitability in the southeastern United States, with clear
northern and western boundaries, which fall within the
known disease occurrence in this region (Fig. 1). The only
other major region within the United States predicted to
have a climate that would allow the establishment of pitch
canker was the coastal region of California, where observa-
tions of the disease occurred in regions predicted to be mar-
ginal to suitable for the disease (Fig. 1).
Model validation
Validation of the model indicated that it fit the known oc-
currences of pitch canker. All known locations in the Bas-
que Country, Spain, had a climate predicted to be suitable
to optimal for pitch canker (Fig. 2 inset). Similarly, suitable
to optimal climate was predicted for the known presence of
the disease in Italy (Fig. 2), Japan (Fig. 3), and South Africa
(Fig. 4). At the state level, suitable climate was predicted in
parts of all affected states in Mexico (Fig. 1) and Spain
(Fig. 2). On islands where the disease has been recorded,
climate was predicted to be suitable to optimal in Haiti
(Fig. 1) and optimal in the southern Japanese Islands
Amami-O-shima, Okinawa, Miyako, and Iriomote (Fig. 3).
Locations in Chile that were known to have F.circinatum
present in nurseries but no established pitch canker in the
field had an EI ranging from 0 to 11, which corresponded
to unsuitable to the lower range of suitable climate condi-
tions for this disease (Fig. 5).
Model projection
Projections show that the core range of the disease to be
humid subtropical and Mediterranean areas, with almost all
regions with these climate types predicted to be suitable for
pitch canker establishment. The disease is also predicted to
extend into warmer temperate climates, such as these found
in southwestern Europe and regions with tropical humid
rainforest and savanna climates.
Most of the Caribbean and all of Hawaii was predicted to
be suitable for pitch canker (Fig. 1). All countries within
Central America were predicted to have at least some re-
gions with optimal climate for pitch canker establishment
(Figs. 1 and 5). In South America, the model projected that
suitable to optimal conditions occur at high altitude in the
Andes from northern Colombia to northern Argentina
(Fig. 5). East of the Andes, the main region projected to be
favourable for pitch canker was a wide band on the east
coast from Rio de Janiero, Brazil, to northern Argentina
(Fig. 5).
The majority of continental Europe had climate conditions
not conducive to pitch canker (Fig. 2). The only exceptions
were regions near the Mediterranean Sea in southern Eu-
rope. Countries with regions of optimal climate for pitch
canker included Portugal, Spain, France, Italy, and Georgia
(Fig. 2).
In Asia, most suitable regions for disease were confined
to the southeast, with large tracts of land in southeastern
China being suitable to optimal for pitch canker establish-
ment (Fig. 3). Almost all of Laos and Vietnam were pre-
dicted to have areas optimal for pitch canker, as were large
Fig. 2. Ecoclimatic suitability for pitch canker establishment across the Mediterranean region in southern Europe. Dots () represent point
observations and thatching ( ) represents states known to have pitch canker. Inset: the northern region of the Basque Country, Spain.
2250 Can. J. For. Res. Vol. 39, 2009
Published by NRC Research Press

areas in Myanmar and north-east India. The vast majority of
islands within Malaysia, Indonesia and the Philippines were
also predicted to have areas optimal for pitch canker
(Fig. 3).
The majority of northern Africa had an unsuitable climate
(Fig. 4). Areas predicted to be optimal for pitch canker es-
tablishment were largely confined to Ethiopia, Madagascar,
and large land areas centred on the equator, extending from
the east to the west coast. Eastern regions, south of the
equator from Kenya to South Africa, were also predicted to
have climate conditions optimal for pitch canker (Fig. 4).
In mainland Australia, optimal regions were predicted to
cover a narrow strip of land along almost the entire eastern
coastline from northern Queensland to south Australia
(Fig. 6). Small areas with optimal climate were also pre-
dicted in western Australia and Tasmania. In New Zealand,
optimal areas were confined to coastal regions of the North
Island (Fig. 6). The southern and central regions of the
North Island and all of the South Island of New Zealand
were predicted to be unsuitable for pitch canker establish-
ment (Fig. 6).
Discussion
The CLIMEX model clearly shows the predicted core dis-
tribution of pitch canker to be in the Mediterranean and sub-
tropical regions, with the disease extending into warmer
temperate climates and tropical humid regions. Pitch canker
distribution did not favour cool temperatures and dry condi-
tions. As a result, the climatic range of the disease is consid-
erably narrower than that of host pine species from which it
is recovered. This disparity is most marked in cool temper-
ate, continental, and subarctic regions within Europe, Can-
ada, and Asia. In these regions, native pines occupy vast
tracts of land (Critchfield and Little 1966), which are un-
likely to be threatened by pitch canker under the current cli-
mate.
The potential distribution provides considerable insight
into the likelihood of disease outbreaks. It should be noted
that the model predicts regions that have climate conditions
conducive to the establishment of pitch canker but does not
predict the likely severity of this disease once established. It
would be expected that pitch canker would be more severe
in areas that have optimal climate ratings, as conditions that
favour disease establishment, such as warm temperatures
and high humidity, also favour disease buildup.
In addition to climatic conditions, the frequency and se-
verity of disease outbreaks can be influenced by nonclimatic
factors, such as insects, host resistance and availability, and
stand management (Dwinell et al. 1985; Blakeslee et al.
Fig. 3. Ecoclimatic suitability for pitch canker establishment across southeast Asia. Dots () represent point observations and thatching ( )
represents islands known to have pitch canker. Inset: the southern islands of Japan.
Ganley et al. 2251
Published by NRC Research Press

1999; Hodge and Dvorak 2000; Gordon et al. 2001). For in-
stance, insects could provide a more effective means of dis-
ease transmission in drier marginal to suitable climates than
could infection of wounds created by weather-related or me-
chanical damage. Similarly, the susceptibility of host pine
species is important. The CLIMEX model was fitted using
data obtained from different Pinus spp. of varying suscepti-
bility. Based on this model, pitch canker should be able to
establish on any susceptible pines present in areas predicted
to have optimal conditions for disease establishment,
although the frequency and severity of the disease is likely
to be influenced by host susceptibility and availability. It is
expected that more severe outbreaks of pitch canker will oc-
cur in more susceptible hosts, such as Pinus radiata, than in
more resistant species, such as Pinus pinea L.
Climate has a strong influence on pitch canker establish-
ment in the southeastern United States. Severe outbreaks of
pitch canker frequently occur after hurricanes and (or) in
years with high rainfall and humidity (Dwinell et al. 1985;
Starkey et al. 2007). The CLIMEX model showed clear
western and northern boundaries for pitch canker in the
southeastern United States, which largely conformed to the
recorded distribution and the subtropical climatic zone
within this region. Pitch canker has been recorded as far
west as Texas but does not extend far beyond this (Starkey
et al. 2007). This model shows that the western limit for the
disease here is attributable to excessive hot–dry stress, while
the northern limit for pitch canker is due to cold stress. The
western disease limit is also the limit for most Pinus spp. in
this region, so it may also reflect a lack of available host.
The absence of the disease north of Virginia (Dwinell et al.
1985) in susceptible pine species (Enebak and Stanosz 2003)
reinforces the importance of cold stress on the distribution in
this region.
The behaviour of pitch canker in California differs from
that which occurs in the southeastern United States and has
confused the understanding of the dynamics associated with
this disease. Unlike the southeastern United States, pitch
Fig. 4. Ecoclimatic suitability for pitch canker establishment across Africa. Dots () represent point observations and triangles (~) represent
pathogen-only reports from nurseries.
2252 Can. J. For. Res. Vol. 39, 2009
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canker infections in California are almost solely associated
with insects (Gordon et al. 2001). Natural infections can oc-
cur but are so infrequent that they are considered inconse-
quential (Gordon et al. 1998). However, pitch canker
infections have been found to progress significantly faster
in areas approximately 1.5 km from the coast. These regions
are more frequently covered in fog than other coastal areas
farther inland or within the central region of California
(Wikler et al. 2003). Fitting the observed pattern of disease
spread in this region, the CLIMEX model predicts that the
conditions in California are suitable closest to the coastline,
quickly progressing into marginal and then unsuitable condi-
Fig. 5. Ecoclimatic suitability for pitch canker establishment across South America. Triangles (~) represent pathogen-only reports from
nurseries.
Ganley et al. 2253
Published by NRC Research Press

tions (EI range = 0–13). No areas of optimal climate were
predicted. In view of this pattern, it is possible that the es-
tablishment of pitch canker in California is due to insects
causing deeper wounds. The increase in infection rate closer
to the coast indicates that even with insect involvement, ad-
ditional moisture expedites disease transmission. Further re-
search would be needed to verify this hypothesis and
determine the correlation between infection frequency and
wound type under a range of climatic conditions.
The distribution of pitch canker along the west coast of
the United States has clear boundaries to the north and east
(Gordon et al. 2001). The CLIMEX model showed that the
eastern limit for the disease is due to excessive hot–dry
stress, while the northern limit for pitch canker is from in-
sufficient thermal accumulation. The model also showed
small pockets of marginal climate in Oregon and Washing-
ton. The most eastern record of F. circinatum in this region
is from one location in the Sierra Nevada in a Pseudotsuga
menziesii seed orchard (Vogler et al. 2004). The pathogen
was found in one tree and appears to be an isolated infec-
tion, as pitch canker has not become established in this re-
gion (Vogler et al. 2004, Inman et al. 2008). In the Pacific
Northwest, pitch canker has never extended beyond Califor-
nia even though susceptible host species and known insect
wounding and (or) vectoring agents are present (Gordon et
al. 2001). Therefore, although insects may provide a means
of disease transmission in marginal climates, pitch canker
cannot establish in regions predicted to have unsuitable con-
ditions.
The marginally suitable climatic conditions (EI range =
0–11) predicted by CLIMEX coupled with a low frequency
of suitable insects may account for the absence of pitch can-
ker in plantations in Chile. Fusarium circinatum has been
present in 14 nurseries across the central region of Chile
since at least 2002 (Wingfield et al. 2002b). The pathogen
has caused problems within these nurseries but has never
spread to adjacent Pinus radiata plantations, even when in-
fected seedlings have been outplanted (Ganley 2007). In
nurseries, disease outbreaks are thought to occur from conta-
minated soil rather than from airborne spores. The lack of
subsequent infection in exotic Pinus radiata plantations has
been attributed to a lack of pine-associated insects. While it
has always been assumed that the climate would be optimal
for establishment of pitch canker, the CLIMEX model
shows marginal to suitable regions along the coast of central
Chile that encompass some of the infected nurseries. No re-
gions were shown to have optimal conditions. In view of
this, it would be expected that climatic conditions along the
central coastal region of Chile would limit the spread of
pitch canker, as has occurred in California. The likelihood
of pitch canker establishing in Chile is predicted to be low.
Interestingly, the moist southern pine-growing regions of
Chile, which were thought to be high risk regions for pitch
canker, were shown to be unsuitable.
Fig. 6. Ecoclimatic suitability for pitch canker establishment across Australia and New Zealand.
2254 Can. J. For. Res. Vol. 39, 2009
Published by NRC Research Press

The slow spread of pitch canker throughout the pine-
growing regions of South Africa is more difficult to explain.
Fusarium circinatum has been present in nurseries in South
Africa since the 1990s (Viljoen et al. 1994), yet pitch canker
has only recently been reported in pine plantations
(Coutinho et al. 2007). Similar to Chile, infections in the
nurseries in South Africa are thought to occur from contami-
nated soil, and there is a lack of associated insect species
present for the nonnative Pinus radiata and Pinus patula
Schiede ex Schltdl. & Cham. The projected distribution of
pitch canker in this region would suggest that pine forests
near the infected nurseries would be at high risk. The pres-
ence of pitch canker in the plantations (Coutinho et al.
2007) shows that South Africa’s climate is suitable for pitch
canker. Based on this model, it is expected that pitch canker
will spread in areas with optimal conditions, assuming avail-
able susceptible hosts, adequate levels of inoculum, trans-
mission between regions, and the creation of suitable
wounds during optimal times.
The establishment of pitch canker is predicted to be opti-
mal in parts of Spain, France, and Portugal, and marginal to
suitable for other regions within southern Europe and the
Mediterranean. The suitability of the northern region of the
Basque Country (EI range = 12–27) fits with the known
range of the pathogen in this region, and likewise, with dis-
ease reports of the pathogen in the adjacent provinces of Ga-
licia, Cantabria, and Asturias (Landeras et al. 2005; Pe
´rez-
Sierra et al. 2007). Pitch canker has not been reported in
Portugal, and in France, F. circinatum has been reported to
be eradicated (European and Mediterranean Plant Protection
Organization 2004). However, given the predicted suitability
of climate in parts of these countries and proximity to the
pathogen, plantations and native stands of pine should be
regularly monitored for this disease.
The CLIMEX model predicted some of the highest sus-
ceptibilities to pitch canker establishment for regions in
China, Brazil, Australia, and New Zealand. This should be
of concern for pine-growing industries in these countries. In
nonnative pine plantations, pitch canker would be expected
to establish in regions with optimal climate conditions
should F. circinatum be introduced. Continued strict quaran-
tine and monitoring of the disease is recommended to pre-
vent introductions of the pathogen to these countries.
Acknowledgements
We thank H.A. Pase for providing county locations of
pitch canker in Texas. This work was funded by the Forest
Biosecurity Research Council, the National Centre for Ad-
vanced Bio-Protection Technologies, and the Foundation for
Research Science & Technology.
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