Pitch canker caused by Fusarium circinatum - A growing threat to pine plantations and forests worldwide

Abstract

Pitch canker, caused by the fungus Fusarium circinatum, is one of the most important pathogens of Pinus species. Sporadic outbreaks and epidemics caused by this fungus have been reported from numerous countries. Symptoms differ
depending on the host species, geographical region, climatic conditions and associated insects. Pitch canker represents a
significant threat to countries where non-native and susceptible Pinus spp. are grown intensively in plantations.Athorough understanding of the ecology and epidemiology of the causal agent is
an important prerequisite to managing this threat. The aim of this review is to summarise contemporary knowledge relating
to the pitch canker pathogen, with a particular focus on its threat to plantation forestry.

Full text

Pitch canker caused by Fusarium circinatum -- a growing threat
to pine plantations and forests worldwide
M. J. Wingfield
A
, A. Hammerbacher
A
, R. J. Ganley
C
, E. T. Steenkamp
A
, T. R. Gordon
D
,
B. D. Wingfield
B
and T. A. Coutinho
A,E
A
Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI),
University of Pretoria, Hillcrest 0002, South Africa.
B
Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria,
Hillcrest 0002, South Africa.
C
Scion, New Zealand Research Institute Ltd, Private Bag 3020, Rotorua 3046, New Zealand.
D
Department of Plant Pathology, University of California, Davis, CA 95616, USA.
E
Corresponding author. Email: teresa.coutinho@fabi.up.ac.za
Abstract. Pitch canker, caused by the fungus Fusarium circinatum, is one of the most important pathogens of Pinus
species. Sporadic outbreaks and epidemics caused by this fungus have been reported from numerous countries. Symptoms
differ depending on the host species, geographical region, climatic conditions and associated insects. Pitch canker represents
a significant threat to countries where non-native and susceptible Pinus spp. are grown intensively in plantations. A thorough
understanding of the ecology and epidemiology of the causal agent is an important prerequisite to managing this threat. The
aim of this review is to summarise contemporary knowledge relating to the pitch canker pathogen, with a particular focus on
its threat to plantation forestry.
Additional keywords: environmental influences, genetic diversity, host interactions, insect associations, symptoms,
taxonomy and identification.
Introduction
Pitch canker, caused by Fusarium circinatum (teleomorph =
Gibberella circinata) (Nirenberg and O’Donnell 1998), is a
destructive disease of pines in many parts of the world
(Hepting and Roth 1953; McCain et al. 1987; Muramoto and
Dwinell 1990; Santos and Tovar 1991; Viljoen et al. 1994;
Dwinell et al. 2001; Wingfield et al. 2002b; Landeras et al.
2005; Carlucci et al. 2007; Coutinho et al. 2007). The disease
is frequently associated with reduced yields and high levels of tree
mortality in certain areas, resulting in significant economic losses
(Dwinell etal.1985). Thesymptom mosttypically associatedwith
the pathogen is large resinous cankers on main trunks and lateral
branches of susceptiblepine species (Barnard andBlakeslee 1980;
Barrows-Broaddus and Dwinell 1985a), although other plant
parts such as roots, shoots, female flowers and mature cones,
seed and seedlings can also be affected (Barrows-Broaddus and
Dwinell 1985a; Barrows-Broaddus 1990; Correll et al. 1991;
Carey and Kelly 1994; Viljoen et al. 1994; Storer et al. 1998a).
Symptom expression and disease severity are strongly correlated
with host and prevailing biotic and abiotic conditions. The disease
is, therefore, quite dynamic and every outbreak in a particular
area usually has a unique case history. Here, we review the
fundamental aspects of the biology of the pathogen, its
interaction with the host, insects and the environment. Current
knowledge on how these factors contribute to pitch canker
outbreaks and epidemics, and the management thereof, are
considered, with particular reference to the threat the pathogen
poses to intensively managed plantations of non-native species.
Global importance of F. circinatum
In the south-eastern (SE) United States, the disease was first
recorded in 1946 (Hepting and Roth 1946) and is currently known
to occur from Florida to as far north as Virginia and westwards to
Texas (Dwinell et al. 1985; Ridley and Dick 2000). In these
regions, pitch canker occasionally causes epidemics (Blakeslee
et al. 1979; Dwinell et al. 1985), which may be associated with
abiotic stress (Lopez-Zamora et al. 2007). Usually, the disease
causes economic losses only in managed stands, such as seed
orchards and it is only rarely a problem in native pine stands
(Blakeslee et al. 1979).
The pitch canker fungus was first recorded in California in
1986 (McCain et al . 1987). The most severely affected area was in
Santa Cruz County, where F. circinatum caused branch dieback
in Pinus radiata, P. muricata, P. pinea and P. halepensis.
Initially, the disease appeared to be limited to landscape
plantings, but by 1992, it was found to occur in native
populations of P. radiata on the Monterey peninsula (Storer
et al. 1994). Pitch canker now occurs throughout the coastal
regions of California, from San Diego in the south, to Mendocino
County north of San Francisco (Gordon et al . 2001). Unlike the
CSIRO PUBLISHING
Invited Review
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disease distribution in the SE United States, pitch canker in
California appears to be confined to near-coastal regions, with
the exception of one site in the Sierra Nevada (Vogler et al. 2004).
The severity of the disease in California has been attributed to
favourable biotic and abiotic conditions for infection (Storer et al.
1999b; Gordon et al. 2001).
F. circinatum first appeared in South Africa in a single forestry
nursery in 1990, causing a root disease on P. patula seedlings and
cuttings (Viljoen et al. 1994). Since this initial outbreak,
F. circinatum has now spread to most pine-growing forestry
nurseries in South Africa, where it currently represents the most
important pathogen of Pinus spp. in the nurseries (Britz et al.
2005). More recently, pitch canker has been discovered in
established plantations of P. radiata in the Cape Peninsula
(Coutinho et al. 2007). The slow establishment of pitch canker
from the nurseries to plantations in South Africa is probably due to
a variety of different factors including climate, low initial levels of
airborne inoculum, absence of effective insect vectors and
wounding agents, and the lack of associations between native
biota and the plantation trees.
In 2002, the pitch canker pathogen was reported from Chile
where P. radiata nursery seedlings and clonal hedge plants were
affected (Wingfield et al. 2002b). Although symptoms typical of
pitch canker have been observed on older trees in plantations in
that country, those trees were probably planted from infected
nursery stock. There is no evidence that pitch canker has become
established as a plantation disease in Chile, but it seems likely this
will eventually occur, as it has in South Africa. The risk in Chile is
heightened by the fact that the highly susceptible P. radiata is
widely planted in that country.
Pitch canker also occurs in other parts of the world. Hepting
and Roth (1953) noted that the disease was abundant in Haiti on
P. occidentalis. In the late 1980s, pitch canker was reported to
cause trunk cankers and dieback of P. luchuensis on the islands of
Amamiooshima and Okinawa in Japan (Kobayashi and
Muramoto 1989). In Mexico, the disease is prevalent on
planted P. radiata and P. halepensis and in natural stands of
P. douglasiana, P. leicophylla, P. durangensis and other pine
species (Santos and Tovar 1991; Guerra-Santos 1999). In
northern Spain, F. circinatum has been reported as the causal
agent of a severe root disease of nursery seedlings of exotic
P. radiata and P. pinaster (Landeras et al. 2005; Pérez-Sierra
et al. 2007). Pitch canker symptoms were also reported on
P. radiata plantation trees. In Italy, pitch canker has recently
been reported on P. halepensis and P. pinea (Carlucci et al. 2007).
However, the extent of damage due to
F. circinatum throughout
this region and the rest of Europe is unclear, as is its presence in
native Pinus spp. in this region. Further spread of F. circinatum is
of great concern to many countries such as Australia and New
Zealand, where highly susceptible P. radiata is grown
extensively in plantations (Dick 1998).
Taxonomy and identification
In 1946, when the pitch canker pathogen was first described, it
was referred to as an undescribed species of Fusarium belonging
to the section Liseola (Hepting and Roth 1946). Three years later,
it was designated by Snyder et al. (1949) as F. lateritium f. sp. pini.
In the 1970s, the pitch canker pathogen was identified as
F. moniliforme var. subglutinans (section Liseola), based on
the abundant microconidia on sympodially branching
conidiophores and the absence of chlamydospores (Dwinell
and Phelps 1977; Kuhlman et al. 1978). The fungus was
then raised to species level in 1983 by Nelson et al. (1983) as
F. subglutinans. Later, it was concluded that there was
considerable justification for assigning strains of
F. subglutinans pathogenic to pines to a forma specialis, based
on differing restriction fragment length polymorphism (RFLP)
patterns of mitochondrial DNA and host specificity (Correll et al.
1992). The unique nature of the pitch canker fungus was also
supported by isozyme analysis (Huss et al. 1996) and random
amplified polymorphic DNA profiles (Viljoen et al. 1997a). The
pitch canker fungus was thus named F. subglutinans f. sp. pini.
Britz et al. (1999) introduced the biological species concept for
diagnosing isolates of the pitch canker pathogen by
demonstrating that it represents a discrete biological species or
mating population (designated mating population H) of Fusarium
section Liseola. Initially, the fungus was assigned to mating
population B within this section (Kuhlman 1982), but crosses
with B tester strains failed in later studies (Correll et al. 1992;
Viljoen et al. 1994). The sexual structures and ascospores
produced in the initial experiments were most probably due to
the homothallic nature of some of the B mating population strains,
as indicated by Britz et al. (1999). In their study, they showed
conclusively that the pitch canker pathogen is heterothallic
(Leslie 1995; Britz et al. 1999) and that mating is controlled
by a single locus (MAT) with two idiomorphs (MAT1-- 1 and
MAT1-- 2). Later, DNA sequences located at the MAT locus were
exploited to develop a PCR-based method to rapidly differentiate
fungal isolates of opposite mating type (Steenkamp et al. 2000).
This method, together with the discovery that reduced incubation
temperatures enhance female fertility of F. circinatum isolates
(Covert et al. 1999), greatly facilitated application of the
biological species concept for differentiating the pitch canker
pathogen from other fungi with similar morphology (e.g.
F. gutiforme, F. subglutinans mating population E and
F. sacchari).
Nirenberg and O’Donnell (1998) described the pine pitch
canker fungus as a member of the so-called Gibberella fujikuroi
complex, which roughly corresponds with the section Liseola of
Fusarium (O’Donnell et al. 1998). Based on morphology, they
named the asexual stage of the fungus F. circinatum and the
sexual stage Gibberella circinata (Nirenberg and O’Donnell
1998). Based on a limited number of isolates, the authors
differentiated F. circinatum from F. subglutinans sensu stricto
pathogenic to maize, by its polyphialides with more than
three openings (as opposed to fewer than three conidiogenous
openings in F. subglutinans), proliferating conidiophores (those
of F. subglutinans are strongly branched) and hyphal coils (absent
in F. subglutinans, but present in F. pseudocircinatum). A later
morphological study including a much larger collection of
isolates (Britz et al. 2002), phylogenetic analyses based on
histone H3 (Steenkamp et al. 1999), and b-tubulin and
translation elongation factor 1-a (O’Donnell et al. 1998;
O’Donnell et al. 2000) sequences, supported designation of
this pathogen as a distinct taxon in the G. fujikuroi complex.
Currently, two molecular methods are available for rapid and
reliable identifi
cation of F. circinatum. The first of these is based
320 Australasian Plant Pathology M. J. Wingfield et al.

on PCR-RFLP of the histone H3 gene (Steenkamp et al. 1999),
which involves digestion of a specific portion of this gene with
restriction enzymes Cfo1 and Dde1. Following agarose gel
electrophoresis, a unique fingerprint is generated for the pitch
canker fungus. The other method is that of Schweigkofler et al.
(2004) who sequenced the rRNA intergenic spacer region in a
representative set of Fusarium isolates. From these data,
F. circinatum-specific PCR primers were designed, which
allow amplification of a 300 base pair fragment only in
reactions containing DNA obtained from the pitch canker
pathogen.
Genetic diversity of F. circinatum
F. circinatum reproduces both sexually and asexually. As with
other heterothallic pathogens, each of these cycles affects the
population structure differently. The asexual cycle results in
clonal propagation, whereas the sexual cycle results in
recombination leading to new genotypes (Leslie and Klein
1996; Britz et al. 1998). However, the outcome of sexual
interactions between F. circinatum isolates is not only
dependent on mating type compatibility as determined by the
MAT locus, but also by female fertility. Like many other
ascomycetes, isolates of the pitch canker fungus have clearly
defined male-- female roles, where only female fertile strains or so-
called ‘hermaphrodites’ are capable of producing sexual fruiting
structures upon fertilisation (Correll et al. 1992; Leslie 1995;
Leslie and Summerell 2006). Because male-only strains are
selected against during sexual recombination, populations
undergoing frequent cycles of sexual reproduction usually
have high numbers of female-fertile strains, while more male-
only strains are expected under conditions where asexual
reproduction predominates (Leslie and Klein 1996; Leslie and
Summerell 2006). Unfortunately, previous experiments to score
this trait in populations of F. circinatum were conducted at
suboptimal conditions, suggesting that conclusions drawn on
the reproductive mode and distribution of this phenomenon in
natural populations of the pathogen should be viewed
with caution (Britz et al. 1998, 2005; Covert et al. 1999).
Nevertheless, the pathogen can be expected to be more diverse
with limited male-only strains in its centre of origin and in regions
where it is well established than in areas where it has been recently
introduced. The population structure and the evolution of new
genotypes by outcrossing also have implications for disease
control using chemicals as well as for tree breeding for
resistance against the pathogen.
Most studies of genetic diversity in F. circinatum examined
distribution of mating type and vegetative compatibility groups
(VCGs). The loci in the fungal genome that control VCGs are
involved in determining the formation of somatic heterokaryons
between isolates of the same species (Leslie 1993). VCG assays in
sets of isolates representing the different populations of this
fungus revealed high VCG diversities in the SE United States
and Mexico (Correll et al. 1992; Gordon et al. 1996; Viljoen et al.
1997b; Wikler and Gordon 2000). Both mating types are also
present in these populations, indicating that they are well
established and may be reproducing sexually. However, many
VCGs in Florida were shown to be clonally related (Wikler and
Gordon 2000) and experimental evidence suggests that new
VCGs of
F. circinatum may arise spontaneously through
somatic mutations (Petersen and Gordon 2005). Thus, it is
possible that high levels of VCG diversity may be achieved in
the absence of sexual reproduction. Both mating types and
numerous VCGs of the pathogen have also been reported in
South Africa (Viljoen et al. 1997a, 1997b; Britz et al. 1998, 2005;
Wingfield et al. 2002a). Although these findings point towards an
established outcrossing population, the authors noted that the
observed diversity might also be due to a large and diverse
founder population of the pathogen.
Populationsof the pitchcankerpathogeninCaliforniaandJapan
are extremely low in VCG diversity. Since the fungus was first
reported in California, the population had been dominated by one
VCG andthe number of VCGs has only increased slightly (Gordon
et al. 1996). Although both mating types are present, comparison
of VCG diversity in progeny produced from laboratory crosses
of Californian isolates to that in field populations indicated that
sexual reproduction is rare or absent in the Californian population
of F. circinatum (Gordon et al.2006a). Similarly, the population in
Japan has very low VCG diversity, suggesting the fungus was
recently introduced into these regions with limited, if any,
outcrossing (Wikler and Gordon 2000).
More recently, the genotypic diversity of the pitch canker
pathogen has been determined using genomic polymorphic
markers. The two sets of markers that are currently available
have been developed using different strategies. Wikler and
Gordon (2000) used a genomic subtraction procedure that
involved enrichment of a genomic library of two isolates for
fragments unique to one of the isolates using a series of
DNA-- DNA hybridisations. Following this approach, they
developed eight polymorphic markers, four of which are
detectible by PCR and four that can be assayed with Southern
hybridisation (Wikler and Gordon 2000). Britz et al. (2002)
developed the second marker set, which is based on
polymorphic genomic sequences that are situated between
simple sequence repeats (SSRs). The set of nine polymorphic
markers are detectable by PCR.
The polymorphic marker set generated by genomic
subtraction was applied to a selection of F. circinatum isolates
from California, SE United States, South Africa, Mexico and
Japan, associated with known but different VCGs (Wikler and
Gordon 2000). The results indicated that the genetic diversity of
F. circinatum was highest in Mexico, suggesting that the
pathogen probably originated in this region. Furthermore,
despite being assigned to different VCGs, some isolates
representing different populations shared multilocus
genotypes. Specifically, populations in California, SE United
States and Japan were found to share common genotypes
(Wikler and Gordon 2000). Representatives of the South
African and Mexican populations of the fungus also shared a
genotype. However, no genotypes associated with United
States-- Japanese isolates were shared with the South
African-- Mexican isolates. Wikler and Gordon (2000)
concluded that pitch canker most likely spread from the SE
United States to California and the disease may have reached
Japan either directly from the SE United States or indirectly
through California. They further concluded that the South African
population of F. circinatum probably originated in Mexico,
supporting previous suggestions that the disease was brought
Pitch canker -- a threat to forests Australasian Plant Pathology 321

into South Africa on contaminated seed collected in Mexico
(Britz et al. 2001).
The Britz et al. (2002) marker set was used to compare the
F. circinatum population isolated during the initial outbreak of the
disease in South Africa (Viljoen et al. 1994) to those of a
population collected more recently in 1996-- 98 (Britz et al.
2005). Analyses of the results revealed the presence of unique
alleles in the more recent population and an increase in allelic
diversity of the pathogen subsequent to the initial outbreak
(Britz et al. 2005), supporting the notion that the fungus is
well established and reproducing sexually in South Africa.
However, limited genetic differentiation between the initial
and recent populations was also reported, which is consistent
with the fact that the two populations of the fungus shared
a remarkable number of VCGs. Britz et al. (2005) concluded
that the observed genetic diversity is unlikely to be the result of
later additional introductions of the pathogen from external
sources, but rather that the occurrence of disease at multiple
South African pine nurseries reflected an expansion of the original
infestation.
Symptoms
F. circinatum can infect the vegetative and reproductive parts of
susceptible pine hosts of all ages. Shoots, branches, cones, seeds,
stems and exposed roots may all become infected. Infections by
the pathogen can also occur at any time of the year. However, the
specific symptoms expressed may vary from one pine host to
another and are dependent on the prevailing biotic and abiotic
conditions (Dwinell et al. 1985; Gordon 2006).
The fi rst symptoms of pitch canker are usually the wilting and
discolouration of needles, which eventually turn red and fall off,
resulting in branch dieback (Storer et al. 1995; Gordon et al.
2001). Dieback usually occurs from the tips of branches to the
infection sites (Fig. 1a, b), due to the obstruction of water flow by
girdling cankers that develop at the site of infection (Gordon et al.
2001). The tissues associated with these cankers are soaked with
resin and copious resin typically also bleeds from infection sites
(Fig. 1c, d). Because the fungus usually does not grow far
proximally from the infection site on branches, the pathogen is
unlikely to reach the tree bole and damage proximal to a canker is
minimal (Barrows-Broaddus and Dwinell 1983; Gordon et al.
2001). Infections can occur at any point along abranch (Fig. 1e, f ),
although succulent, current-year growth tends to be more
susceptible than woody tissue (Barrows-Broaddus and Dwinell
1983; Correll et al. 1991; Gordon et al. 2001).
Infections of reproductive structures with the pitch canker
fungus are associated with mortality of female flowers and mature
cones, and seed deterioration (Barrows-Broaddus 1990). Infected
cones may be misshapen and smaller than normal and can abort
before reaching maturity (Correll et al. 1991). F. circinatum may
even be present in cones from healthy branches where seeds are
only contaminated superficially with the pathogen (Storer et al.
1998a). F. circinatum may cause visible deterioration in infected
seed and can significantly reduce seedling emergence. However,
under certain conditions, infected seed that shows no apparent
symptoms can germinate and produce asymptomatic seedlings
from which the fungus can be isolated (Storer et al. 1998a). The
ability of the pathogen to infect and survive in or on the
reproductive organs of Pinus spp. greatly facilitates its spread
into new areas.
F. circinatum causes pre- and post-emergence damping-off of
seedlings (Fig. 2a), as well as mortality of established seedlings
(Viljoen et al. 1994). If pre-emergence damping-off occurs, seed
coats and coleoptiles of germinating seedlings are heavily
colonised by the pathogen (Viljoen et al. 1994). Storer et al.
(1998a) found that internal seed contamination by F. circinatum
causes higher rates of pre-emergence damping-off than
superficially contaminated seed. In the case of F. circinatum
associated post-emergence damping-off, root collars of seedlings
are girdled (Barnard and Blakeslee 1980). Mortality of
established seedlings tends to be lower than that of newly
germinated seedlings. The disease typically causes wilting of
the seedlings (Fig. 2b-- e) and roots are frequently underdeveloped
with discoloured lesions and necrosis of the cortex evident
(Viljoen et al. 1994). Seeds that germinate or seedlings
growing in infested soil can develop pitch canker associated
root rot or damping-off (Barnard and Blakeslee 1980; Viljoen
et al. 1994; Gordon et al. 2001). Seedling infections can also
remain undetected, since asymptomatic seedlings can harbour the
pathogen as an endophyte (Storer et al. 1998a).
Expression of pitch canker symptoms is almost always
associated with significant economic losses. In the nursery
setting, the pitch canker pathogen is associated with extensive
seedling mortality (Fig. 2f ), especially for susceptible species
such as P. radiata and P. patula. In planted and natural Pinus
stands, pitch canker is frequently associated with a reduction in
growth volume (Bethune and Hepting 1963; Arvanitis et al.
1984). This is largely attributable to loss of foliage due to
shoot dieback and water stress. Although individual branch
infections are unlikely to kill a tree, multiple infections can
cause extensive dieback in the canopy. Stem cankers are
usually indicative of an advanced diseased state where tree
girdling may result in large-scale tree mortality (Blakeslee and
Oak 1979). In addition to girdling stem cankers and crown
dieback, mortality can also, in some cases, be attributed to
secondary factors such as bark beetles (Storer et al. 2002b).
To date, infection of Pseudotsuga menziesii has been
characterised by twig dieback only, with swollen resinous
tissue apparent at the infection point on the twigs (Storer et al.
1994).
Host-- pathogen interactions
Trees that are considered susceptible to pitch canker include
57 species of Pinus (Hepting and Roth 1953; Muramoto et al.
1993; Storer et al. 1994, 1997; Clark and Gordon 1999;
Guerra-Santos 1999; Hodge and Dvorak 2000; Enebak and
Carey 2003; Enebak and Stanosz 2003) and Pseudotsuga
menziesii (Douglas-fir), the only recorded non-pine host
(Gordon et al. 2006b). Indications are that P. radiata could
be the most susceptible of all pine species (Hodge and Dvorak
2000; Gordon et al. 2001). A variety of other plant
species, including trees and herbaceous plants, have been
tested for susceptibility to F. circinatum, but all have been
found to be highly resistant (McCain et al. 1987; M. A. Dick
and J. A. Simpson, unpubl. data). Barrows-Broaddus and
Dwinell (1980) suggested that the pitch canker fungus
322 Australasian Plant Pathology M. J. Wingfield et al.

may also be pathogenic to gladiolus corms, although this
was later refuted by Viljoen et al. (1995a), who showed
that the fungus on gladiolus was F. proliferatum. Thus,
the available evidence suggests that F. circinatum is
exclusively a pathogen of coniferous trees, and most
specifically Pinus spp.
(a)
(c)
(e)
(f )
(d )
(b)
Fig. 1. Pitch canker symptoms on mature pine trees: (a) plantation of infected trees showing dieback symptoms; (b) shoot tip dieback;
(c) resinous cankers on the main stem; (d) resinous cankers at the first branch whorl; (e) infected branch showing both external and internal
symptoms; and (f) infected branch showing the pitch soaking of the wood of an affected branch.
Pitch canker -- a threat to forests Australasian Plant Pathology 323

Although the host range of F. circinatum extends to most
Pinus spp., some appear to be resistant and quantitative
differences have been documented within species that are
susceptible (Rockwood et al. 1988; Viljoen et al. 1995b;
Hodge and Dvorak 2007). P. brutia and several other pine
species, especially those in the Pinus subspecies Pinaster,
appear to have relatively high levels of resistance to the
disease (Gordon et al. 1998b; Hodge and Dvorak 2000; Mead
2000). For some pines, such as P. lambertiana and P. jeffreyi ,
pathogenicity has been demonstrated in greenhouse experiments
(a)
(d )
(e)
(f )
(b)
(c)
Fig. 2. Symptoms caused by Fusarium circinatum in young pine seedlings: (a) damping-off of germinated Pinus patula seedlings; (b) wilted and dead
P. patula seedlings after natural infection; (c) inoculated pine seedlings showing dieback symptoms; (d) young P. radiata tree showing dieback of branch
tips; (e) branch showing dieback symptoms; and ( f ) discarded P. radiata seedlings infected with F. circinatum.
324 Australasian Plant Pathology M. J. Wingfield et al.

but has not been observed in the field (Storer et al. 1994).
However, studies of other pine species have shown that
greenhouse susceptibility levels are correlated with the
incidence of disease observed in the field. Thus, with sufficient
exposure to the pathogen, susceptible species might be expected
to display equivalent levels of disease in the field (Gordon et al.
1998a). Furthermore, species thought to be relatively resistant
frequently develop a high incidence of disease under the influence
of environmental stress and inoculum pressure (Blakeslee and
Rockwood 1999; Lopez-Zamora et al. 2007). Thus, the relative
resistance of different Pinus spp. is controlled by genetic as well
as environmental factors.
Genetic resistance to pitch canker has been demonstrated in all
pine species tested (Kelley and Williams 1982; Viljoen et al.
1995b; Hodge and Dvorak 2000) and within-species variation has
been reported for pines grown in the SE United States (Dwinell
and Barrows-Broaddus 1979; Bronson et al. 1992; Blakeslee
and Rockwood 1999), California (Storer et al. 1999a), and
Mexico and Central America (Hodge and Dvorak 2007). In
the case of P. radiata, Matheson et al. (2006) confirmed the
heritability of resistance to pitch canker in a study that included
material from breeding programs in Australia, Chile and New
Zealand. Similarly, Blakeslee and Rockwood (1999) found
variation in resistance to F. circinatum in breeding families of
P. elliottii and P. taeda. Families of P. elliottii and P. taeda in
which resistance persists in adverse environmental conditions
have been selected and are now used in operational plantations,
advanced breeding programs and in research on mechanisms of
resistance in the SE United States (Blakeslee and Rockwood
1999). The specific loci, alleles and gene regulation associated
with resistance traits against pitch canker in these pine
species are currently being investigated (Morse et al. 2004;
Kayihan et al. 2005).
In 1988, it became apparent that some P. radiata in California
were unaffected by pitch canker, despite their proximity to heavily
infected trees. Direct inoculations of these asymptomatic trees
showed that they supported a significantly slower rate of lesion
expansion than susceptible trees (Correll et al. 1991). Subsequent
studies showed that although most individuals of P. radiata are
susceptibleto pitchcanker (Storeret al. 2002b),a smallpercentage
of trees manifest resistance to the disease (Gordon et al. 1998b;
Storer
et al. 1999a). Although resistance can be detected in
greenhouse tests of relatively young trees (<2 years old),
resistance does not appear to be functional in emerging
seedlings (Aegerter and Gordon 2006). In addition to inherent
genetic resistance, systemic induced resistance (SIR) has been
reported to occur in P. radiata in California (Storer et al. 1999a;
Bonello et al. 2001a). This was the first report of SIR in coniferous
trees and the molecular and biochemical pathways stimulated by
this form of resistance are currently under investigation. Induced
resistance in P. radiata appears to be a critical component of
disease remission in areas where pitch canker was first observed in
California (Gordon 2006). Thus, SIR may help to minimise
damage to indigenous P. radiata pine forests and ensure the
continued vitality of this valuable natural resource.
Genetic resistance of pines to pitch canker is intrinsically
linked with pathogen virulence and the durability of resistance
may be affected by the ability of F. circinatum populations to
generate novel pathotypes. Variation in virulence of
F. circinatum populations has been detected (Barrows-
Broaddus and Dwinell 1979; Viljoen et al. 1995b; Gordon
et al. 2001) and the capacity to undergo sexual reproduction
may enhance prospects for the appearance of pathogen genotypes
capable of overcoming disease resistance. In South Africa,
Mexico and the SE United States, F. circinatum populations
are genetically diverse (Wikler and Gordon 2000; Britz et al.
2005), whereas in California and Japan there is no evidence that
sexual reproduction is occurring. Similarly, P. radiata genotypes
resistant to Californian strains of F. circinatum were susceptible
to strains from Florida, Mexico and South Africa (Gordon et al.
2001). Breeding for resistance to the pitch canker fungus will
prove effective only if a multi-faceted approach to resistance is
employed, which can meet the challenge of novel pathotypes that
might appear as a result of sexual recombination.
The genetic basis for F. circinatum virulence on Pinus spp. is
not well understood. A genetic linkage map for a hybrid cross
between F. circinatum and F. subglutinans was recently
constructed by De Vos et al. (2007). Although F
1
progeny for
this cross were avirulent on pine, backcross populations with
specificF
1
individuals and the parental F. circinatum strain
showed a wide range of virulence to pine (De Vos et al. 2007;
Friel et al. 2007). This map, therefore, represents an important
step towards clarifying the genetic basis for virulence in the pitch
canker fungus. Research currently focuses on utilising the
backcrossed populations to identify quantitative trait loci
associated with pathogenicity of F. circinatum to pine.
Biology and ecology
Various aspects of the biology and ecology of F. circinatum have
been investigated. However, in many cases these have been
limited to single tree species or geographical regions and
results have generally been extrapolated, despite relatively
little knowledge regarding variation between hosts and
countries. Biological parameters of F. circinatum that have
been studied include: inoculum dynamics, dispersal, infection,
colonisation, survival and sexual reproduction of the pathogen.
Inoculum of F. circinatum is available during all seasons of
the year, although in the SE United States and California, the
highest frequency of spores has been found to occur during the
autumn-- winter months (Kratka et al. 1979; Schweigkofler et al.
2004). Spores have also been found to survive longer during this
period than in spring-- summer (Blakeslee et al. 1978). In Florida,
sporodochia containing macroconidia occurred commonly on
infected branches in the upper crown of infected trees (Blakeslee
et al. 1978) and were commonly observed on dead needles
attached to infected shoots, where they possibly continue to
serve as an inoculum source in needle litter (Barrows-
Broaddus and Dwinell 1984). In California, airborne inoculum
of F. circinatum was detected in abundance throughout the year in
an area with a high incidence of pitch canker on P. radiata, but not
in areas where there was no evidence of the disease (Correll et al.
1991). On the central coast of California, where pitch canker is
known to be present, a bark wash survey revealed the presence of
spores on both symptomatic and asymptomatic trees (Adams
1989). The superficial infestations found on seeds in cones borne
on healthy trees are presumably due to deposition of airborne
spores (Storer et al. 1998a). Spores of the pitch canker fungus
Pitch canker -- a threat to forests Australasian Plant Pathology 325

have been found in rainwater, in the air (Kuhlman et al. 1982),
and in spore traps beneath asymptomatic trees (Fraedrich and
Dwinell 1997).
Dispersal of F. circinatum spores occurs through wind, insect
vectors, water splash, soil and movement of infected plant
materials (Blakeslee et al. 1978, 1979; Dwinell and Barrows-
Broaddus 1978; Viljoen et al. 1994; Hoover et al. 1996; Fraedrich
and Dwinell 1997; Storer et al. 1998a; Wikler and Gordon 2000;
Gordon et al. 2001). In the SE United States, natural infection of
wounds by airborne spores has been found to be predominantly
associated with mechanical damage, caused by branch removal
and cone harvesters, and weather related injuries such as wounds
created from hail or wind damage to the trees (Dwinell and Phelps
1977; Dwinell and Barrows-Broaddus 1981; Kelley and Williams
1982; Dwinell et al. 1985). By contrast, the frequency of infection
of artificial or natural wounds in California is so low that this form
of infection is not considered important. In the field, natural
injuries have not been observed to be associated with pitch canker
infections and likewise, mechanical wounds, such as pruning, or
artificially wounded, non-inoculated branches either did not
become infected (Correll et al. 1991; Gordon et al. 1998a), or
sustained infections only at a very low rate (Sakamoto and
Gordon 2006). Instead, insects are considered to be the most
important agents of transmission of the fungus. It has been
speculated that if windblown or rain-splashed spores do access
natural or mechanical injuries, that the wound may dry out before
a successful infection can occur, as the type of wound created and
the age of the wound has been found to be significantly correlated
with successful colonisation. Specifically, infection frequencies
have been found to increase with fresh wounds compared with old
wounds, with the presence of a water droplet and by deeper
wounds (Barrows-Broaddus and Dwinell 1985a; Kuhlman 1987;
Sakamoto and Gordon 2006; Inman et al. 2008).
F. circinatum spores are capable of surviving in soil and wood
debris (Dwinell and Barrows-Broaddus 1978; Gordon et al. 2001).
Studieshave shownthatthepathogencansurvivefor over6 months
in wet soil, up to 1 year in dry soil (T. R. Gordon and B. J. Aegerter,
unpubl. data), and more than 3 years in soil under refrigeration
(Barrows-Broaddus and Kerr 1981). F. circinatum can be readily
isolated from the wood of infected trees and from slash piles near
infested sites. Studies on the survival of the fungus in wood chips
and branches in California found that it was still viable after 1 year
and it was recoverable at a low frequency from 3-year-old branches
(McNee et al.2002).F. circinatumcanbeisolatedfromneedlelitter
in pitch canker-infested stands of P. radiata (Aegerter and Gordon
2006) but the durability of inoculum in this substrate has not been
assessed. Likewise, the length of time that F. circinatum spores can
survive on insects is currently unknown.
Under certain conditions, the pitch canker fungus appears to be
able to enter an apparently endophytic state during which it does
not induce any symptoms in the host plant. In some cases, infected
seed can germinate and produce asymptomatic seedlings from
which the fungus can be isolated (Storer et al. 1998a). In Chile, it
is relatively common for such infected, asymptomatic seedlings
to be outplanted and, at some point, the fungus can switch from a
latent to an active form of infection. At present, it is unknown
whether all seedlings with latent infections would eventually
display pitch canker symptoms or what mechanisms governs this
change of behaviour.
F. circinatum has been observed to reproduce sexually
in vitro
on agar medium (Britz et al. 1999) and on surface sterilised host
tissue (Britz et al. 1999; Wikler et al. 2000). Nonetheless, sexual
fruiting structures or perithecia of this pathogen have never been
observed in the field. Yet, the results of genetic diversity studies
suggest that certain populations of the pathogen are reproducing
sexually, while others reproduce predominantly mitotically
(Wikler and Gordon 2000; Wikler et al. 2000; Britz et al.
2005; Gordon et al. 2006a). Scarcity of hermaphrodite strains
in the population would be expected to constrain the frequency of
recombination through outcrossing. Another contributing factor
may be a skewed distribution of mating type in the population,
thus reducing the probability of contact between isolates of
opposite mating type. Whereas both factors may be operative
in the California population of F. circinatum (Gordon et al. 1996;
Wikler et al. 2000), they seem less likely to limit outcrossing in
South Africa (Britz et al. 2005). Yet notwithstanding intensive
sampling, perithecia have never been observed in this area (Britz
et al. 2005), or anywhere else under natural conditions. One
possible explanation is that mating is favoured by low
temperatures (Covert et al. 1999), whereas disease outbreaks
occur during relatively warm periods. Thus, ambient conditions at
the time samples were taken may not have been conducive to
formation of perithecia (Britz et al. 2005). Also, the possibility
that F. circinatum completes its sexual cycle on some other host or
substrate cannot be discounted.
Environmental interactions
Several environmental factors are known to contribute to pitch
canker disease establishment and severity. Weather-related
injuries in the SE United States are known to provide infection
courts for F. circinatum (Dwinell and Barrows-Broaddus 1982)
and many of the outbreaks of pitch canker in this region have been
associated with hurricanes (Kelley and Williams 1982; Dwinell
et al. 1985). Nutrient levels can affect susceptibility to the pitch
canker pathogen. Specifically, high levels of nutrients, both in soil
and foliage, have been found to increase disease severity (Fisher
et al. 1981; Blakeslee et al. 1999; Lopez-Zamora et al. 2007).
The choice of planting site can have a pronounced effect on pitch
canker epidemiology. Susceptibility to pitch canker increases
during drought stress, waterlogging or shallow soils, especially
when trees are planted at high-stand densities (Dwinell
et al. 1985; Runion and Bruck 1986; Blakeslee and Rockwood
1999).
Air pollution can also play a role in development of disease.
High ambient ozone concentrations were found to enhance canker
development in susceptible trees, whereas in resistant trees, the
interaction of the pathogen and the air pollutant caused stunted
growth and decreased root mass (Carey and Kelly 1994). This
might, in part, help explain the predominance of pitch canker
incidence in California along highways and landscape plantings
(Correll et al. 1991). In the SE United States, air pollution from
chicken houses has been found to increase foliar nutrient levels,
thus increasing disease susceptibility (Lopez-Zamora et al. 2007).
Climatic conditions are thought to play a major role in disease
establishment and severity of pitch canker. Temperature is known
to influence growth, spore germination and infection of
susceptible hosts by F. circinatum. In culture, all tested isolates
326 Australasian Plant Pathology M. J. Wingfield et al.

ofF. circinatumgrewmost rapidlyat25

Cand progressivelymore
slowly at 20, 15 and 10

C, whereas spore germination occurred
mostrapidly at 20

Candwas slowestat10

C(Inman et al.2008).If
lower temperatures extend the time required for germination and
growth beyond the window of wound susceptibility a reduced
infection frequency is expected. This limiting effect of
temperature can explain the lower rate of infection resulting
from inoculations in winter as compared with those performed
during warmer spring months (Inman et al. 2008).
In addition to temperature, humidity may also influence the
establishment of pitch canker. Infections may not occur even
where temperatures are within the optimum range if sufficient
moisture is not available. These factors could help account for
differences in infections from injury-related wounds between the
SE United States compared with California; the high humidity
and temperature in the SE United States may be more conducive
to infection. In coastal California fog can occur throughout
the year, resulting in high humidity and condensation, both of
which favour infection. The frequency and duration of fog is
diminished at more inland locations and this correlates with a
significantly lower incidence and severity of disease (Wikler et al.
2003). Furthermore, experiments have documented a significant
effect of humidity on frequency of infection of insect-mediated
wounds (Sakamoto et al. 2007). However, disease intensity also
declines at more northerly latitudes, notwithstanding the regular
occurrence of fog, and this may be due to progressively lower
temperatures during periods when moisture is available.
Elsewhere, low humidity in parts of Chile and South Africa
where F. circinatum is present but pitch canker has not
developed, may be part of the reason why the disease has not
become established in these regions.
Insect associations
Insects can serve as wounding agents on trees or as vectors of
F. circinatum both in the SE United States (Blakeslee et al. 1978)
and in California (Gordon et al. 2001). When discussing different
insect-pathogen associations, it is necessary to differentiate
between insects indigenous to specific areas or specific pine
hosts compared with insects that are generalists for many
Pinus spp. or in an exotic setting. Likewise, it is necessary to
distinguish whether insects are involved in wounding of the host
or vectoring of F. circinatum to the wound site or both. The
association of insects with pitch canker varies from region to
region and is likely to refl ect complex interactions between the
host, insect wounding agents and/or vectors, and the
environment. It is, therefore, difficult to predict the influence
of insects, either native biota or introduced, host-coevolved
insect communities, in the establishment and spread of pitch
canker in forestry plantations located in exotic regions.
Insects indigenous to the SE United States
In the SE United States, pitch canker infections have
predominantly been found associated with injury-related
damage. It has been widely purported that insects are not a
significant factor in the spread of the disease. However, several
studies have shown an important association between insects and
the occurrence of pitch canker in various Pinus spp. (Hepting and
Roth 1953; Blakeslee et al. 1978, 1980; Blakeslee and Foltz 1981;
Runion and Bruck 1985). Application of the systemic insecticide,
carbofuran, resulted in a reduction of both insect shoot damage
and pitch canker infections, suggesting a direct relationship
between the two factors (Runion et al. 1993). Native insects of
the SE United States that have been implicated in the spread of
pitch canker include Pissodes nemorensis (deodar weevil),
Rhyacionia frustrana (Nantucket pine tip moth) and other
Rhyacionia spp., although, the frequency with which these
insects are involved in wounding and/or vectoring of the
pathogen is unclear. Specifically, F. circinatum has been
successfully isolated from shoots exhibiting damage from
Rhyacionia spp., as well as from larvae and pupae, suggesting
that these insects can vector the pathogen and may also be capable
of creating wounds sufficient for infection (Matthews 1962;
Runion and Bruck 1985). A positive correlation between
seedling terminals damaged by Rhyacionia spp. and the
incidence of pitch canker infections has also been reported
(Runion et al. 1993). Likewise, spores have also been isolated
from P. nemorensis in Florida and feeding wounds were found to
becorrelated withpitchcanker infectionsinplantations (Blakeslee
et al. 1978; Blakeslee and Foltz 1981). Greenhouse inoculations
using contaminated weevils have resulted in successful infections
of pine seedlings whereas trees with feeding wounds from
F. circinatum-free weevils remained disease free until
artificially inoculated (Blakeslee and Foltz 1981).
Several insects of secondary importance have been identified
as possible vectors of F. circinatum in the SE United States.
Wounds caused by Contarinia sp. (needle midge) are common on
pine in seed orchards and plantations and are often colonised by
the pitch canker pathogen (Dwinell et al. 1985). Cone and seed
feeding insects have also been identified, which may contribute
to pitch canker dissemination and infection. These include
Leptoglossus corculus, Tetrya bipunktulata (seedbugs),
Laspreyresia spp. (seed worms) and Megastionus atedius
(seed chalcids) (Dwinell et al. 1985). No association of the
pathogen with Ips spp. (bark beetles) has been demonstrated in
the SE United States (Blakeslee and Oak 1979).
Insects indigenous to California
The spread of pitch canker in California has been found to be
strongly correlated with native insects that feed on or are
associated with P. radiata. Numerous insects are capable of
creating wounds or carrying F. circinatum spores (Fox et al.
1991; Hoover et al. 1996; Storer et al. 1997; Gordon et al. 2001;
McNee et al. 2002) However, establishing the exact interaction
between the insects and pitch canker infections has been more
difficult. Conophthorus radiatae (Monterey pine cone beetles),
Pityophthorus spp. (twig beetles), and Ernobius punctulatus
(death-watch beetles), are known to be capable of vectoring
F. circinatum as well as creating wounds, through their
feeding activities, that can result in pitch canker infections
(Correll et al. 1991; Hoover et al. 1995, 1996; McNee et al.
2002). These insects predominantly feed in the crown of
P. radiata (Furniss and Carolin 1977; Ohmart 1979) and are
believed to initiate the majority of branch canker infections
observed. Repeated infestations by these insects can lead to
intensification of the disease and can severely weaken the tree.
E. punctulatus probe trees by excavating entrance tunnels that are
Pitch canker -- a threat to forests Australasian Plant Pathology 327

abandoned if resin flow is prolonged and abundant. It has thus
been suggested that this ‘tasting’ phenomenon may enhance
transmission of the disease by the beetles to apparently healthy
trees (Fox et al. 1990; Bonello et al. 2001b). Several Ips spp. are
also known to carry F. circinatum and are responsible for causing
infections on large branches or the main bole, as this is where they
establish galleries (Fox et al. 1991). Ips spp. are attracted to
stressed trees thus, they are more likely to be involved in killing
already weakened trees and spreading the disease to adjacent
trees, rather than initiating infections in uninfected, healthy stands
(Furniss and Carolin 1977; Fox et al. 1990, 1991; Storer et al.
2002a). Bark beetles can cohabitate with F. circinatum and in this
way it appears that a new association has developed between these
insects and the pathogen (Fox et al. 1990; Storer et al. 2002a).
A substantial body of work supports a key role for twig beetles
(Pityophthorus spp.) in the establishment and intensification of
pitch canker in P. radiata. These insects are well known as
colonisers of dead and declining branches. Their association
with pitch canker was supported by a high rate of recovery
from symptomatic branches, with most of the emerging beetles
carrying propagules of the pitch canker pathogen (McNee et al.
2002). However, the life history of Pityophthorus spp. seemed
inconsistent with a role in disease transmission because emerging
adults immediately seek weakened host material in which to
breed. Consequently, there was not an obvious opportunity for
them to visit a healthy branch and thereby establish an infection.
This contrasts with a well known vector of Dutch elm disease,
Scolytus multistriatus, which feeds on healthy trees before
establishing a gallery in a declining (and possibly diseased)
tree (Webber 1984).
In the case of pitch canker, twig beetles appear to meet the
requirements for vectoring in a more subtle manner, reflecting
limitations on their ability to locate a substrate in which to breed.
Field experiments conducted by Bonello et al. (2001b) showed
that Pityophthorus spp. could not identify branches that were
suitable for colonisation, before landing. This suggests that
Pityophthorus spp. will, by chance, occasionally land on
healthy branches and thereafter may ‘ taste’ them to assess
their acceptability. To determine if this activity might result in
wounds that could serve as infection courts, trees to which spores
had been applied were exposed to twig beetles (P. setosus) that
were allowed to move freely over the surface of the trees.
Subsequent examination revealed a high frequency of pitch
canker infections on trees explored by P. setosus, whereas
control trees not visited by insects had no infections
(Sakamoto et al. 2007). Similar results were obtained using
P. carmeli (Sakamoto et al. 2007). In aggregate, these results
indicate that two common twig beetle species are capable of
transporting the fungus and creating infection courts on healthy
branches. That this actually occurs under natural conditions is
supported by field studies showing that trees baited with
pheromones attractive to Pityophthorus spp. sustained
significantly higher infection rates than control trees, which
were not baited (Storer et al. 2004).
Several other insects have been identified that potentially have
a role in vectoring or creating infection courts. Spores of
F. circinatum have been isolated from a variety of insects that
are not known to feed on pines such as flies, wasps and beetles
(Correll et al. 1991). The importance of these insects in the
epidemiology of the disease is unknown although they may
visit wounds on trees and incidentally transmit the pathogen.
Conversely, Aphrophora canadensis (spittlebug) has been
implicated as a wounding agent for pitch canker infections but
infections may be caused by spores deposited from the air that get
trapped in the spittle masses, rather than by spores transported to
the infection court by A. canadensis (Storer et al. 1998b).
Insects with a wide host range may provide a means for
expansion of an infestation to include new hosts. Thus,
Pityophthorus spp. may have contributed to the high incidence
of pitch canker on bishop pine (P. muricata), where this species
co-occurs with P. radiata (Erbilgin et al. 2005). However, some
Pityophthorus spp. are associated with both P. radiata and
Pseudotsuga menziesii (Douglas-fir), but limited susceptibility
to pitch canker in the latter species makes the consequences of
this connection less obvious (Erbilgin et al. 2005; Gordon et al.
2006b).
Insects associated with Pinus spp. in South Africa, Chile
and Spain
In South Africa, fungus gnats (Bradysia difformis) were
suspected to vector F. circinatum in pine nurseries. However,
Hurley et al. (2007a) showed that although these insects are
present in nurseries, they do not play a significant role in
transmitting diseases to pine seedlings. The exact role of the
larvae of these insects in facilitating wounding and thus
transmission of the pitch canker fungus still has to be ascertained.
In the Tokai plantation, in the Western Cape Province, where
the first outbreak of pitch canker was reported on adult trees, trees
showing typical symptoms were heavily infested with the weevil,
Pissodes nemorensis (Coutinho et al
. 2007). This insect has
previously been shown to be associated with F. circinatum in
the SE United States where it creates wounds that may become
infected by airborne spores of the fungus (Blakeslee et al. 1978).
An association between this fungus and insect had been
previously predicted (Gebeyehu and Wingfield 2003), but the
nature of this association is poorly understood and requires further
investigation.
In Spain, Romón et al. (2007) determined the association
between several insects and the pitch canker fungus. They
isolated F. circinatum spores from the root weevil Brachyderes
incanus, as well as several of the bark beetles species. They also
showed that the anti-aggregation pheromone verbenone could
potentially be used as part of an integrated pest management
strategy for controlling pitch canker as it significantly
reduces aggregation of Pityophthorus pubescens and Ips
sexdentatus, both of which frequently harbour F. circinatum.
However, aggregation of other insects carrying F. circinatum
in Spain at significant frequencies (e.g. Brachyderes incanus,
Hylurgops palliatus, Hypothenemus eruditus, Hylastes
attenuatus and Orthotomicus erosus) were not affected.
Heavy levels of F. circinatum are found in most P. radiata
nurseries in Chile, where the fungus infects both seedlings and
clonal hedge plants (Wingfield et al. 2002b). Infections are also
found on the roots and root collars of young trees, in the first year
after establishment. Where roots of these trees have been infested
by the scolytine bark beetle Hylastes ater, F. circinatum has
occasionally been isolated from damage associated with this
328 Australasian Plant Pathology M. J. Wingfield et al.

insect (M. J. Wingfield, unpubl. data). The pine shoot moth,
Ryocionia bouliana, an insect known to be associated with
F. circinatum in the United States (Matthews 1962; Runion
and Bruck 1985) causes serious damage to P. radiata in
Chilean plantations. While the insect and pathogen have not
been found in association in Chile, this could develop in the
future and lead to the appearance of pitch canker on adult trees.
Control
Cultural control
At present there is no absolute means of controlling pitch canker
in nurseries and forest plantations. An integrated management
approach can, however, reduce the economic impact of the
disease. Integrated management can include adequate
quarantine measures, appropriate nursery and silvicultural
management, and genetic selection for clones of species that
are less susceptible to the pitch canker pathogen.
Quarantine measures should be in place to exclude the fungus
from areas that are currently free of pitch canker and to prevent the
establishment of new strains of F. circinatum in areas where the
pathogen is already present. In New Zealand, stringent
regulations have been established to limit importation of plant
material including a complete restriction on the importation of
conifer seed or live plant tissue from countries known to have
pitch canker. These measures can be effective in excluding
F. circinatum propagules from New Zealand, but great
concern exists about the accidental introduction of the fungus
via wood products such as packaging material and contaminated
insects and plant material harboured in second-hand vehicles,
used logging equipment or in camping equipment (Dick 1998;
Gadgil et al. 2003).
Little research has been conducted on the control of
F. circinatum in pine seedling nurseries. The most important
means to prevent new infections in nurseries is the use of disease-
free seed. However, where a pathogen is already established in a
nursery, sound nursery practices and the highest levels of hygiene
are of great importance in preventing disease outbreaks. The use
of pathogen-free irrigation water, sterile growth media and
containers as well as roguing diseased plants can reduce the
population size of the pathogen within a nursery. The control of
vectors and wounding agents is also economically feasible in
nurseries (Hurley et al. 2007a, 2007b).
In pine plantations and seed orchards it can be possible, in
some instances, to avoid or reduce the impact of disease outbreaks
with appropriate silvicultural practices. Environmental stress
increases the susceptibility of Pinus spp. to the pitch canker
pathogen. Planting sites, therefore, should be suited for pine
production, planting density should not be inordinately high,
trees should be thinned to appropriate stocking levels, and the site
should have adequate drainage to avoid waterlogging (Blakeslee
et al. 1982; Runion and Bruck 1986; Blakeslee et al. 1999).
California’s protracted drought from 1987 to 1992 is believed to
have contributed to the Californian pitch canker epidemic,
especially since high mortality stands were situated on soils
with poor water holding capacity (Owen and Adams 2001).
Heavy levels of fertilisation also increase the susceptibility of
pines to pitch canker (Fisher et al. 1981; Fraedrich and Witcher
1982; Blakeslee et al. 1999) and nutrient supplementation should,
therefore, be carefully managed. Severe outbreaks of pitch canker
have also been associated with high levels of nitrogen emissions
from air-conditioned chicken houses (Lopez-Zamora et al. 2007).
Although first reported in Florida, a similar phenomenon has been
observed in many other south-eastern states and it is believed that
outbreaks of pitch canker will become more prevalent as nitrogen
loads increase (Meeker et al. 2005). Because F. circinatum is a
wound-infecting pathogen, wounding of trees should be avoided
during cone harvesting and other forest management practices
(Dwinell et al. 1985). Branch tip cankers have been pruned out of
landscape trees in California, but this practice has not been
successful in slowing the progress of the disease or in
increasing the lifespan of a tree (Gordon et al. 2001).
Long-term management of pitch canker of Pinus spp. grown in
plantations can only be achieved by planting resistant selections
or species in conjunction with appropriate silvicultural
management practices. Strong genetic heritability has been
observed in several SE United States pines (Rockwood et al.
1988; Kayihan et al
. 2005) and a wide variation in resistance has
been observed in native P. radiata forests (Gordon et al. 2001).
Therefore, it is feasible to develop resistant planting stock, which
can be used for commercial forestry and for replanting of native
forests. Planting of resistant Pinus spp. can be considered as an
alternative to improving the existing planting stock, which is
currently utilised by commercial forestry (Wingfield et al. 2002a).
In this regard, prior screening of Pinus spp. and families can be
used to reduce the likelihood of disease in plantations (Hodge and
Dvorak 2000; Matheson et al. 2006; Roux et al. 2007).
In addition to inherent genetic resistance, evidence of induced
resistance has been reported in stands of P. radiata in California
(Gordon 2006). Repeated inoculation of trees and seedlings has
resulted in reduced lesion expansion both in greenhouse trials and
in the field (Storer et al. 1999a; Bonello et al. 2001a) and this may
provide opportunities to enhance the resistance of planting stock
in the future. The long-term applicability of induced resistance to
disease management in plantation forestry is, however, unknown
and it deserves further study. Key issues to be explored include:
(1) the duration of elevated resistance following an induction
event, (2) the specificity-generality of induced resistance, and
(3) potential decreases in productivity resulting from differential
allocations of carbon to defence rather than growth.
Chemical and biological control
A variety of control methods have been investigated for
preventing or reducing the effects of pitch canker in pines.
Thiabendazole is a systemic and residual fungicide that has
been tested in various concentrations in vitro and in vivo with
varying results. Initial studies showed that this fungicide limited
growth of F. circinatum and that it prevented pitch canker
symptom expression (Runion and Bruck 1988a, 1988b),
although, the reduction in disease incidence observed was not
considered sufficient to warrant its use (Runion et al. 1993). The
application of thiabendazole in paint on pruning wounds has been
found to prevent artificial infection of F. circinatum. However, it
has been reported that relatively high levels of resistance to
benomyl, a thiabendazole derivative, exist in populations of
the G. fujikuroi species complex (Yan and Dickman 1993),
making the use of thiabendazole and its derivatives
Pitch canker -- a threat to forests Australasian Plant Pathology 329

problematic. Likewise, the use of such chemicals is strongly
discouraged in many countries and they are unlikely to provide
solutions for nursery infestations.
Various biological control strategies have been evaluated for
the control of the pitch canker fungus involving antagonistic fungi
or bacteria. Dumroese et al. (1988) noted the benefits of
Trichoderma spp. on the seed coats of conifer seed to control
seedling diseases caused by Fusarium spp. However, later studies
have found Trichoderma spp. to be ineffective against
F. circinatum (Mitchell et al. 2004). Barrows-Broaddus and
Kerr (1981) found that several Arthrobacter spp. (common
soilborne bacteria) that were recovered during isolations of
F. circinatum were effective at inhibiting the pitch canker
pathogen in culture. The ability of these bacteria to influence
disease progress on P. elliottii was subsequently investigated.
Although several of the Arthrobacter isolates were able to reduce
the number of F. circinatum conidia present at the wound site in
comparison to the control, none were effective at reducing canker
size or preventing infection by F. circinatum (Barrows-Broaddus
and Dwinell 1985b).
Seed is a potential source of inoculum and a vehicle for
dispersal of the pitch canker fungus. Levels of contamination
of seed can be tested by embryo dissection, crushing seeds on
Fusarium selective medium (Nelson et al. 1983) or crushing
seeds on blotting paper and subsequently examining them for
fungal growth (Anderson 1986). On potentially contaminated
seed, several seed treatments have been tested for the control of
F. circinatum seedling disease. Runion and Bruck (1988a) found
that thiabendazole suspended in 10% dimethyl sulfoxide was an
effective seed treatment for the control of the pitch canker fungus.
Treating seed before stratification with sodium hypochloride,
after stratification with sodium peroxide or ethanol, or after
stratification in hot water significantly reduced seedborne
Fusarium spp. (Dumroese et al. 1988). In contrast, Storer
et al. (1998a) found that sodium hypochloride was ineffective
in reducing F. circinatum contamination of P. radiata seed due to
high levels of internal seed contamination by the pathogen.
Dwinell and Fraedrich (1999) found that internal seed
contamination by F. circinatum could be reduced by soaking
P. radiata seed for 15 min in a 30% hydrogen peroxide solution.
Hydrogen peroxide can penetrate the seedcoat, thereby scarifying
the seed, which increases the germination rate. However, due to
the endophytic nature of F. circinatum in seeds, no absolute
means of controlling the fungus has been found (Storer et al.
1998a).
Summary
Since its initial discovery in 1946, pitch canker has become one of
the most important diseases of pines in the world. There is little
doubt that the disease seriously threatens plantation forestry
worldwide, especially where there is a strong reliance on
highly susceptible species such as
P. radiata and P. patula.
The appearance of F. circinatum in plantations in Spain and
South Africa, along with its presence in nurseries in Chile,
substantially enhances this threat.
Pitch canker is a varied and complex disease of Pinus spp. Our
understanding of the susceptibility of pine species and the
epidemiology of this pathogen has improved over the past few
decades. However, despite a substantial increase in the
knowledge of pitch canker and its causal agent, there are many
questions that remain to be answered. Although pitch canker is
established in many countries on a variety of hosts, predicting
how this fungus will behave in a plantation situation is difficult.
For instance, the reason why the pathogen has remained restricted
to nurseries in South Africa for at least one and a half decades is an
enigma. Whether it will remain restricted to nurseries in Chile is
likewise unknown and it is a cause for considerable concern. It is
possible that the absence of certain insects has influenced this
situation, although in both these countries insects similar to those
associated with the disease in various parts of the United States are
present. Furthermore, the disease can occur on large trees in the
absence of insect damage. This would suggest a strong
environmental effect also contributes to disease development.
It is possible that the drier climate in South Africa and northern
Chile, where F. circinatum is present, may not be conducive for
disease establishment or spread.
The recent appearance of F. circinatum and pitch canker in a
variety of new areas worldwide is of great concern to both
plantation forestry as well as the protection of native stands of
Pinus. Efforts to exclude this pathogen have thus far not been very
effective, despite knowledge on how it is disseminated and the
strict quarantine measures that have been applied to prevent its
introduction into new areas. In many cases, swift and stringent
eradication of the fungus could certainly have prevented both the
establishment and spread of this disease in new regions.
While new outbreaks of pitch canker in various parts of the
world are of concern, there are also positive signs regarding this
disease. Reports of success in lowering or maintaining the level of
pitch canker through management of pine plantations in the SE
United States and the apparent remission of pitch canker in
California are encouraging. However, it is unknown whether
these control methods would be effective in intensively managed
monocultures of Pinus spp. such as those found in many southern
hemisphere countries. Problems in controlling this devastating
pine disease and the associated economic losses to the forestry
sector highlight the importance of promoting an understanding of
the ecology and epidemiology of the pathogen. Pitch canker is
clearly a pine disease of growing global importance and every
effort must be made to manage this threat to pine forest
ecosystems and plantations worldwide.
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