The Pitch Canker Epidemic in California - A. J. Storer and D. L. Wood - Urban Forest ...
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T. R. Gordon
University of California, Davis
A. J. Storer and D. L. Wood
University of California, Berkeley
The Pitch Canker Epidemic
in California
Native Monterey pine (Pinus radiata D. 1946 (23), where it remains a chronic troduction (7). Much greater diversity was
Don) forests are currently found at three problem in plantations and seed orchards found in a sample of the pathogen popula-
disjunct locations in coastal California and (13). At the time of its discovery in Cali- tion from Florida, which was selected to
on two islands off the coast of Mexico. The fornia, it was natural to suspect that F. represent the SE U.S., in part, because of
mainland forests comprise, in total, ap- circinatum was somehow transported to the generous assistance offered by G.
proximately 4,500 ha (11), whereas the two California from the SE U.S. A comparative Blakeslee at the University of Florida.
island populations are limited to 150 ha on study of the two regions revealed very This assessment of the California and
Cedros Island and fewer than 400 trees on limited diversity in the California popula- Florida populations was initially based on
Guadalupe Island (28). Collectively, these tion of the pitch canker pathogen, consis- vegetative compatibility among the col-
populations are significant ecological and tent with the view that it was a recent in- lected isolates (7). Isolates sharing com-
recreational resources, but they are also a
valuable repository of useful genetic traits
for improved varieties of Monterey pine,
which are widely used by the timber indus-
try. In California, Monterey pine is impor-
tant as a landscape tree, with an estimated
50 million standing trees as of 1985. Mon-
terey pines were especially popular for
plantings on freeway rights-of-way, where
they served as visual and sound barriers for
the adjacent properties. It was among such
trees that a dieback problem became ap-
parent in Santa Cruz County (Fig. 1) dur-
ing the mid-1980s.
In 1986, A. H. McCain, extension plant
pathologist at University of California
Berkeley, established that the affected trees
were suffering from pitch canker (30),
caused by Fusarium circinatum Nirenberg
& O’Donnell (=Fusarium subglutinans
(Wollenweb. & Reinking) Nelson, Tous-
soun, & Marasas f. sp. pini). Subsequent
surveys showed the disease to be wide-
spread in coastal Santa Cruz County, with
a clearly disjunct infestation being found
farther inland, in Alameda County (Fig. 1).
Curiously, the disease was also found in
Christmas tree farms in Los Angeles and
San Diego counties, more than 450 km to
the southeast (8).
Historical Development
of Pitch Canker in California
Pitch canker was first described in the
southeastern United States (SE U.S.) in
Fig. 1. Current distribution of pitch canker in California. The native populations of
Dr. Gordon’s address is: Department of Plant Monterey pine are within the heavily infested areas, which also include at least one
Pathology, University of California, Davis 95616; native stand of bishop pine (Monterey Peninsula). Outside of the native stands, most
E-mail: trgordon@ucdavis.edu of the pitch canker–affected trees are planted Monterey pines, but other pine species
are also affected to a lesser extent. Most of the isolated infestations are Christmas
Publication no. D-2001-0918-01F tree farms. The dotted lines enclose areas that approximate the locations of the Sierra
© 2001 The American Phytopathological Society Nevada and Cascade Range.
1128 Plant Disease / Vol. 85 No. 11
mon alleles at all loci that influence this California and initiated the epidemic that is suggests a close relationship between the
trait (typically eight or more) will be vege- currently in progress. two species, which may reflect a common
tatively (or somatically) compatible, and Since the discovery of pitch canker in origin, and in any case, provides further
are said to be associated with the same California, it has become apparent that this support to the view that the pitch canker
vegetative compatibility group (VCG). disease is also found in Mexico, where it pathogen has a long history in southern
Isolates that differ at one or more of these occurs in native forests as well as in plan- Mexico.
loci will be incompatible. Consequently, tations (21). Although recognized only If this interpretation is correct, the oc-
the number of distinct VCGs in a sample recently in Mexico, it is possible that pitch currence of pitch canker in the SE U.S.
provides one measure of diversity within canker has been of long residence there. must trace its origin, directly or indirectly,
the sampled population. Given that Mexico represents a center of to Mexico, although we have no data to
None of the isolates from Florida, or diversification of the pine genus (32,34), one document this connection. However, be-
elsewhere in the SE U.S., was vegetatively might even speculate that the pitch canker cause a clonal lineage is common to the
compatible with any isolates from Califor- pathosystem originated in this area. Consis- Florida and California populations, we
nia (7). Whereas this result did not support tent with this interpretation was the finding presume the SE U.S., rather than Mexico,
a SE U.S. origin for the isolate(s) that ini- that the Mexican population of F. circinatum was the proximate source of the infestation
tiated the California infestation, neither did had, by some measures, a higher level of now found in California. On the other
it militate strongly against this hypothesis. genetic diversity than populations in any of hand, there appears to be a more direct
A lack of vegetative compatibility be- the other regions examined (46). connection between the F. circinatum
tween isolates from different regions could Another hint of a Mexican origin for the populations in Mexico and South Africa
reflect inadequate sampling of one or both pitch canker pathogen comes from the (46), and we suspect that the disease may
populations. This would more likely apply recent discovery of interfertility between F. have reached South Africa as infested pine
to the Florida population of F. circinatum, circinatum (also referred to as G. fujikuroi seed from Mexico as proposed by Wing-
where 45 VCGs were identified among 117 mating population H [5]) and F. subgluti- field et al. (48).
isolates examined (7). Thus, Florida iso- nans (G. fujikuroi mating population E) The ability of F. circinatum to survive in
lates associated with a VCG also found in isolated from teosinte (Zea mays subsp. and on pine seed is well known (1,37), and
California may have simply escaped detec- mexicana—the progenitor of corn) in Gua- seed seems a likely vehicle for the move-
tion due to insufficient sampling. Of temala and southern Mexico (12). F. sub- ment of pitch canker to California, perhaps
course, the high level of diversity found in glutinans was found to be intimately asso- originally to a seedling nursery. Such nurs-
Florida might indicate that this was an ciated with seed in teosinte and thus may eries supply seedlings to farms, where
outcrossing population. If so, a VCG be an endophyte, as this species is known Monterey pine is the preferred species for
would not necessarily have a consistent to be in corn. A successful cross, confirmed local production of Christmas trees; as
association with an individual strain or by demonstrating recombination of the noted above, pitch canker was documented
clonal lineage (27), and other methods alleles affecting vegetative compatibility, to occur in Southern California Christmas
would be required to evaluate the relation- has been documented with only one pair of tree farms soon after its discovery in the
ship between the two populations. isolates, with other combinations proving state. The affected trees, 2- to 3-year-old
The perception of the pitch canker to be infertile (12). Furthermore DNA Monterey pines, sustained infections at or
pathogen as an outcrossing species was sequences from conserved regions show below the soil line, which ultimately gir-
strengthened by findings from South Af- the isolates originating from teosinte dled the trunk and caused needles on the
rica, where the disease was discovered in clearly to be associated with mating popu- entire tree to become chlorotic and die
1990 (44). Field isolates of F. circinatum lation E, and not mating population H. (Fig. 2). Presumably, death of younger
(teleomorph = Gibberella circinata) in Thus we consider the cross to be a hybridi- seedlings occurred as well, but symptoms
South Africa were shown to be interfertile zation event between otherwise distinct at this growth stage are not distinctive and
and were confirmed to constitute a distinct biological species. Their ability to cross could easily have been dismissed as damp-
biological species (5). Thus it was reason-
able to suspect that a population long in
residence in Florida may engage in sexual
reproduction. However, closer scrutiny of
the Florida population using molecular
markers told a different story. In particular,
seven VCGs were shown to have identical
haplotypes based on eight polymorphic
molecular markers (46), suggesting that
novel VCGs may arise by mechanisms
other than recombination through outcross-
ing. This does not necessarily mean that
sexual reproduction is absent in the Florida
population, only that one need not invoke
this mechanism to explain the high level of
VCG diversity that has been observed
there.
As a practical matter, the fact that mo-
lecular haplotypes revealed far less diver-
sity than did VCGs made it more likely
that the former would detect genotypes
common to the two populations. In fact
this was the case, with identical molecular
haplotypes being found both in Florida and
California (46). This may indicate that a Fig. 2. A Monterey pine (arrow) with chlorotic needles, which are the typical symp-
clonally propagating lineage, well estab- toms of a pitch canker infection that has girdled the trunk of a tree near the soil line.
lished in the SE U.S., was introduced to Adjacent trees are healthy.
Plant Disease / November 2001 1129
ing-off caused by any of several resident VCGs within the state provides evidence to seedlings from a known infested site in Los
fungi. For that matter, to the uninitiated, suggest this is exactly what happened. Our Angeles County to a Christmas tree farm
symptoms on the older trees might resem- original assessment of the California popu- in Santa Barbara County (Fig. 1), where
ble root rot caused by Phytophthora spp. lation identified a total of five VCGs VCG C3 also was found.
Thus, the pitch canker problem may have statewide, based on 209 isolates collected It was not until a later survey was con-
remained cryptic for many years after the between 1987 and 1989 (7). One of these, ducted that we became aware of a much
pathogen was introduced to a seedling VCG C3, was found in a Christmas tree larger infestation north of Santa Barbara, in
nursery. farm in Los Angeles County and in an San Luis Obispo County, which included
The availability of infected but pre- isolated stand of planted Monterey pine in the native stand at Cambria (Fig. 1) (17).
symptomatic trees at a “choose and cut” Santa Barbara County (Fig. 1). This was Anecdotal evidence indicates that pitch
Christmas tree farm provided an ideal op- the only VCG represented in the collection canker, although not initially recognized as
portunity to move the pathogen to other of 15 isolates from the latter location. We such, was probably in San Luis Obispo
locations in California. The distribution of have since learned of past shipments of County at least as early as 1988. The
pathogen population throughout this region
was dominated by VCG C3 (17); the only
co-occurring VCG, C8, was recovered at a
low frequency and in a very limited area
(17).
Taken together, these facts are consistent
with the establishment of pitch canker in a
pine nursery and its subsequent dispersal
on infected but symptomless planting
stock. After its arrival in a new area, the
pathogen could have been further dissemi-
nated by insects colonizing the trees fol-
lowing their death, and possibly also as
wind-borne propagules (8). Once pitch
canker had killed large trees, their removal
and disposal (often as logs for firewood)
offered additional opportunities for the
pathogen to spread. As pitch canker has
become more widely established in Cali-
fornia, the multitude of inoculum sources
and means by which they can be moved
has probably greatly reduced the relative
importance of nursery stock and Christmas
trees as vehicles for dissemination of the
pathogen.
Fig. 3. Early symptoms of pitch canker on Monterey pine. The site of infection is indi- Dynamics of Disease
cated by the accumulation of resin (arrow), which may occur at branch whorls, A, or Development in California
between whorls, B, and by chlorotic needles close to the infection site. Eventually all
needles distal to the infection will become chlorotic and die. The fascicles typically Notwithstanding the problems caused by
abscise quickly, leaving a bare stem. pitch canker in the production of Monterey
pines as Christmas trees, by far the most
significant impact of the disease in Cali-
fornia has been the damage done to adoles-
cent and mature Monterey pines in land-
scape plantings and more recently in native
forests. Typically, the first symptom of
pitch canker on these larger trees is branch
dieback. This results from a lesion, usually
within one or two whorls of a branch tip
(Fig. 3), that girdles and kills the affected
branch distal to the point of infection (Fig.
4). In most cases, axial growth of the
pathogen does not extend very far proxi-
mally, and so does no further visible dam-
age to the tree. The disease intensifies
through repeated infections that can lead to
extensive dieback in the canopy (Fig. 5).
Infections may eventually include larger
diameter branches and the main stem
(trunk) of the tree; such infections are often
made conspicuous by extensive production
of resin (Fig. 6). In some cases, diseased
trees are severely weakened and may suffer
top kill due to girdling of the trunk and/or
attack by engraver beetles (Fig. 7); cankers
Fig. 4. A dead branch tip, in the canopy of a large tree, A, and at the top of a smaller lower on the trunk often result in death of
tree, B, resulting from a girdling lesion proximal to the symptomatic needles. the entire tree (15).
1130 Plant Disease / Vol. 85 No. 11
This sequence of events has been docu- (98%) eventually sustained at least one with various silvicultural practices, are
mented by monitoring the development of infection, with the remaining 2% of trees considered to be of primary importance as
pitch canker in plots of Monterey pine over being free of symptoms throughout the 4- infection courts (13).
a 4-year period (40). These plots were estab- year observation period (40). An additional In California, four species of twig bee-
lished in urban plantings of Monterey pine 7% never sustained more than two branch tles (Pityophthorus spp. (Coleoptera:Sco-
in 1992 and yielded a number of insights tip infections. The differential development lytidae)) have been shown to carry F. circi-
into the dynamics of pitch canker under of symptoms was probably a reflection of natum (9,25), and experimental evidence
California conditions. First, nearly all trees relative susceptibility to pitch canker. This documents the ability of P. setosus Black-
interpretation is supported by earlier find- man to transmit pitch canker to small
ings that disease-free trees in otherwise branches on Monterey pines (A. Storer and
heavily diseased stands showed a signifi- D. Wood, unpublished; T. Gordon and J.
cantly slower rate of lesion development Sakamoto, unpublished). Similar documen-
than the visibly susceptible trees, when tation has been obtained for the vectoring
inoculated artificially (8). Other studies activity of the cone beetle (Conophthorus
have more fully characterized resistance to radiatae Hopkins (Coleoptera:Scolytidae)),
pitch canker in Monterey pine and will be the deathwatch beetle (Ernobius punctula-
described below. tus (LeConte) (Coleoptera:Anobiidae))
Another important generality emerging (24,25), and the engraver beetle (Ips para-
from the urban plot studies was a tendency confusus Lanier (Coleoptera:Scolytidae))
for many trees in a stand to sustain a few (15). Two other Ips species are known to
infections before any of them became se- carry the pitch canker pathogen and most
verely diseased (40). This pattern was con- likely also serve as vectors. Engraver bee-
sistent with the hypothesized role of in- tles are presumed to be responsible for
sects as vectors that wound and thereby vectoring the pathogen to larger diameter
inoculate young branches more or less branches and tree trunks, as this is the type
randomly. Thus, when most trees are dis- of material in which they normally estab-
ease free, there is a greater probability that lish galleries. Finally, the spittlebug, Aph-
a newly infected branch will be on one of rophora canadensis Walley (Homop-
these trees, rather than on an already in- tera:Cercopidae), has been shown to act as
fected tree. As more trees in a stand be- a wounding agent capable of initiating
come diseased, the likelihood increases infections in internodal regions on succu-
that new infections will occur on trees that lent shoots during the late winter and early
already have at least one infection. spring (42). In aggregate, the above-cited
Fig. 5. A Monterey pine tree with exten- studies provide strong support for the view
Association of Insects that insect-mediated infections are a key
sive canopy dieback resulting from mul-
tiple branch tip infections. (Picture pro- with Pitch Canker Pathogen element in the pitch canker disease cycle in
vided by Jack Marshall, California De- The role of insects as wounding agents California (Fig. 8). Such infections could
partment of Forestry and Fire Protection) and vectors appears to be a critical feature be initiated by insect-borne inoculum, in
of the pitch canker pathosystem in Califor- which case the insect is truly a vector, or
nia, in contrast to the SE U.S., where in- by inoculum already present on the branch
sects are accorded a comparatively minor surface, with the insect serving as a
role in the epidemiology of pitch canker. In wounding agent. The relative importance
the SE U.S., wounds associated with wind, of these alternative modes of infection is
hail, and other weather-related events, and currently under study.
Fig. 6. Resin streaming on a Monterey
pine tree with infections on the main
stem (trunk) of the tree. Nearly all of the
visible resin is attributable to pitch can-
ker, but the small resin mass indicated
by the arrow is the result of colonization Fig. 7. Top-kill resulting from multiple pitch canker infections. Mass attack by en-
by pitch moth and is not diagnostic of graver beetles (Ips spp.) often contributes to this syndrome. (Picture provided by
pitch canker. Jack Marshall, California Department of Forestry and Fire Protection)
Plant Disease / November 2001 1131
Given that small branches are typically presumed to be important in the establish- A. Storer and D. Wood, unpublished) and the first to show symptoms of pitch canker, ment and early intensification of the dis- are likely applicable to three other twig Pityophthorus spp., which preferentially ease. Although Leach’s rules of proof (26) beetle species, in one key respect their colonize branches in this size class, are have been satisfied for P. setosus (25; hypothesized vectoring activity appears Fig. 8. Several of the insect-mediated infection pathways that collectively represent the principal means by which pitch canker in- fections are established on susceptible pines in California. The trees, shown in the center of the figure, represent the typical pro- gression of pitch canker symptoms. Tip dieback is most commonly associated with wounding caused by twig beetles or cone bee- tles, as represented on the right and left sides of the figure, respectively. Infections on the larger branches and the main stem of the tree are associated with wounding caused by engraver beetles (bottom center of figure). 1132 Plant Disease / Vol. 85 No. 11
inconsistent with their life histories as dry prior to their exposure to twig beetles. extrapolated to a similar level of mortality,
currently understood. A young adult twig Trees onto which twig beetles were re- it certainly constituted a disaster for land-
beetle emerging from a gallery is not leased developed infections, whereas trees owners who would not only suffer the
known to require feeding on healthy tissue sprayed with inoculum but not exposed to aesthetic and economic damage of losing
to achieve reproductive maturity, but in- insects did not (J. Sakamoto and T. mature landscape trees, but would also
stead immediately seeks a weakened Gordon, unpublished). Because inoculum bear the costs of removing hazardous trees.
branch in which to breed. Thus, beetles was already present on the branch, it was On the other hand, even if only 2% of the
emerging from a diseased branch may only necessary for the twig beetles to cre- host population proved to be resistant, it
carry the pathogen, but if they have no ate suitable wounds and not to act as vec- could allow for long-term management of
requirement to feed on a healthy branch, tors (i.e., to transport the inoculum). This the problem, provided the resistance proved
where is the opportunity to transmit the procedure was adopted because the insects to be heritable and durable. Consequently,
disease? used were obtained from pheromone-baited work was undertaken to document that
Contrast this with the life histories of traps, and only a low percentage of such resistance was a consistent attribute of
Scolytus scolytus Fabricus and S. multi- insects would be expected to carry F. circi- individual trees and not an artifact of the
striatus (Marsham) (Coleoptera:Scolytidae), natum (9). We have not confirmed that the circumstances under which these trees
which vector Dutch elm disease (16). behavior of P. setosus we observed under were growing.
These insects feed on the phloem in the controlled conditions also occurs in nature, The first step in the characterization of
axils of young shoots prior to seeking a but branches baited with a pheromone resistance to pitch canker was the devel-
weakened tree in which to breed. Thus, specific for P. setosus (10) did sustain very opment of an artificial inoculation proce-
where a beetle establishes a gallery in a small puncture wounds that were not seen dure that would provide a meaningful
diseased tree, the brood are likely to on the unbaited controls (A. Storer and D. measure of susceptibility. In the procedure
emerge carrying the pathogen, and they Wood, unpublished). These wounds may we adopted, an aqueous spore suspension
will then feed on healthy trees, to which have resulted from exploratory tasting by is deposited in a small wound made in a
the disease can be transmitted. Pityophtho- P. setosus. young branch. Sometime thereafter, typi-
rus spp., on the other hand, are not known If, as it appears, wounds created by cally 30 days in a greenhouse, the bark is
to feed on healthy branches, eliminating Pityophthorus spp. are very superficial, the pared away from the inoculation site and
the most obvious opportunity for transmis- fungus may require an external source of the length of the lesion is measured. We
sion of the pathogen to a healthy tree. moisture in order to establish an infection. used this method to screen vegetatively
Typically, twig beetles breed in branches In the experiments described above, where propagated clones of Monterey pine (19) as
that have died recently or that are shade- infections were associated with exposure to well as exotic pine species that constituted
suppressed and therefore less physiologi- P. setosus under controlled conditions, alternative landscape trees in some areas
cally active than younger branches higher trees were maintained at 100% relative (18).
in the canopy (9). However, suppressed humidity for 24 h following removal of the Based on lesion length at the site of in-
branches are rarely seen to develop symp- insects. Whether or not lower ambient oculation, a ranking of Monterey pine
toms of pitch canker. Rather it is young, humidity would allow infections to occur genotypes was shown to be consistent over
actively growing branches that become is currently under investigation. Possible time and to be independent of the location
infected (40), and these do not constitute implications of such environmental limita- where the experiment was conducted (19).
suitable breeding sites for Pityophthorus tions on the eventual distribution of pitch In addition, all the F. circinatum strains
spp.; hence the difficulty in explaining how canker in the western United States are known to occur in California were tested,
twig beetles could be vectoring the patho- discussed below. and they did not interact differentially with
gen to such branches. host genotypes (19). Statistically signifi-
To account for this anomaly, we hy- Differential Susceptibility to cant differences in virulence among Cali-
pothesized that twig beetles do not identify Pitch Canker in Monterey Pine fornia strains were observed, but these
suitable substrates prior to landing, using Pitch canker has long been known to differences were relatively small in magni-
either visual or olfactory cues. If so, then have a wide host range, and early work by tude. At a field site where pitch canker was
twig beetles may land on branches more or Hepting (22) showed that Monterey pine prevalent, trees judged to be resistant,
less randomly and thereafter engage in was among the species that were suscepti- based on artificial inoculations, remained
exploratory tasting and/or feeding in order ble, based on artificial inoculations. In- free of natural infections (19). As of 2001,
to gauge the suitability of a branch for deed, Monterey pine proved to be highly these putatively resistant trees had been
colonization. If the branch is physiologi- susceptible under field conditions, and this, disease-free for 8 years. A related study
cally active, exploration would probably be coupled with its popularity as a landscape confirmed the occurrence of resistant trees
limited to tasting and the beetle would tree, was an essential element in the devel- in a naturally regenerated native stand of
depart to continue its search, but wounding opment of the pitch canker epidemic in Monterey pine on the Monterey Peninsula
that resulted from tasting might be suffi- California. Dense and nearly continuous (36).
cient to inoculate the branch. plantings of Monterey pine provided a host These results suggested that resistant se-
Two lines of evidence support this view bridge from the initial infestations into lections could be used to reestablish land-
of twig beetle biology. First, experiments native stands of this species to the south, scape plantings of Monterey pines in areas
conducted in areas where twig beetle popu- on the Monterey Peninsula, and to the where pitch canker was a problem. In na-
lations were high showed they were not north at Año Nuevo (Fig. 1). The progres- tive forests, assuming heritability is suffi-
attracted to host volatiles produced by cut sion of the disease in these and other ciently high, resistance should increase
branches (3), suggesting that Pityophthorus coastal regions of the state thus appeared to over time through natural selection in the
spp. cannot use these chemicals as cues to be limited only by the availability of sus- presence of pitch canker. However, it is not
target weakened branches prior to landing. ceptible host trees. Data from our monitor- yet known to what extent genetic resis-
Second, experiments conducted under ing plots (discussed above) might suggest tance will be manifested in young seed-
controlled conditions confirmed that P. therefore that as few as 9% of standing lings. We do know that current-year succu-
setosus could induce wounding sufficient trees would survive and fewer still would lent growth tends to be more susceptible
to cause pitch canker infections on healthy escape damage entirely. Such a projection than woody tissue on the same tree, and
branches of Monterey pine. In these ex- now appears unduly pessimistic for reasons that, in some cases, juvenile tissue in
periments, branches were sprayed with an that will be detailed below. rooted cuttings sustains greater lesion de-
aqueous spore suspension and allowed to If initial estimates of susceptibility were velopment than the mature tree from which
Plant Disease / November 2001 1133it originated (T. Gordon, unpublished). the California population: VCG C4 (the Changes in the California population of
Thus it is possible a genotype capable of same as one of the parents) and VCG C1. F. circinatum could occur very quickly by
developing into a resistant tree would, at Thus if the California population were the introduction of strains from outside the
the seedling stage, succumb to pitch can- outcrossing, we would expect to find state. Limited samplings of the populations
ker. greater VCG diversity. One caveat to this in Florida, Mexico, and South Africa iden-
If genetic resistance is to contribute to conclusion is that some of the progeny tified isolates that were virulent on cloned
the management of pitch canker, it must were nearly avirulent, and thus might es- ramets of a Monterey pine genotype that
remain effective for an extended period of cape detection. was resistant to resident California strains
time. In a native forest, survival to repro- A separate line of evidence that is con- (T. Gordon and S. Kirkpatrick, unpub-
ductive age (10 to 15 years) might be suffi- sistent with clonality in the California lished). The opportunities to import F.
cient to sustain the species, but to be useful population of F. circinatum is a lack of circinatum on various forms of host mate-
as landscape trees, resistant Monterey variation within VCGs. Eight polymorphic rial are many. Recent examples include
pines must survive for longer periods of molecular markers showed identical haplo- seed of longleaf pine from South Carolina
time and sustain few enough infections to types for all isolates associated with the used to establish a nursery planting in San
retain their aesthetic value. The durability same VCG (46). If isolates sharing the Luis Obispo County, and pine needles from
of genetic resistance will be strongly influ- same VC genotype were products of recent Georgia, brought in for use as a mulch in a
enced by the pathogen population. Varia- recombination, they would be associated new housing development in the Sierra
tion that affects virulence could result from with different genetic backgrounds. In this Nevada (Fig. 1). F. circinatum was recov-
mutation, recombination due to outcross- case it would be extremely unlikely that ered from one of 50 longleaf pine seed
ing, or introduction of exotic strains. If a isolates associated with the same VCG tested, and this isolate was not vegetatively
major gene contributes to host resistance, would be identical with respect to eight compatible with resident California strains
its effect might be negated by a single other markers. On the other hand, this is (T. Gordon and S. Kirkpatrick, unpub-
mutation in the pathogen. On the other exactly the pattern one would expect if all lished). Likewise, an isolate of F. circi-
hand, if resistance is determined by multi- the isolates in question were clonally re- natum obtained from the imported pine
ple genes, then any given mutation in the lated. needles was not associated with any of the
pathogen might affect resistance only in- Obviously it remains possible that re- VCGs known to occur in California. In
crementally. Of course sexual reproduction combination has occurred and that sam- neither case did the importation violate any
could greatly accelerate the rate at which pling has simply failed to detect recombi- state regulations, so there is little prospect
more virulent genetic combinations are nant progeny. It is also possible that for preventing similar occurrences in the
generated. reproduction is entirely clonal, but only future.
because of limited overlap in the distribu-
Potential for the Pathogen to tions of the opposite mating types of F. Induced Resistance
Overcome Genetic Resistance circinatum (47). Presumably this is an and Disease Remission
As already indicated, F. circinatum is artifact of the manner in which the initial The relative abundance of resistant and
capable of producing a sexual stage introductions were made, and over time susceptible Monterey pines in native for-
(teleomorph = Gibberella circinata, = G. continued movement of isolates by various ests will provide an indication of the extent
fujikuroi mating population H). The fungus means will lead to more general distribu- to which this species will ultimately be
is heterothallic, and both mating types are tions of both mating types. This may in- affected by the pitch canker epidemic in
found in the California population (47). crease the prospects for mating under field California. However, we now know that
However, as yet there is no evidence to conditions in the future. initial measures of resistance to pitch can-
indicate that anything other than clonal Although we cannot forecast the likeli- ker are not entirely predictive of the dam-
propagation has occurred in nature. From a hood of outcrossing under natural condi- age individual trees will sustain from the
sample of over 900 isolates, collected over tions, we can anticipate, to some extent, disease. In particular, it has become appar-
a period of 14 years, only nine VCGs have how progeny of sexual reproduction might ent that susceptibility is not necessarily a
been identified (7,17; T. Gordon and S. differ from the parental types with respect static characteristic of a tree, but that it can
Kirkpatrick, unpublished); three of the nine to virulence. In a laboratory cross of Cali- change over time. The first clues to this
VCGs are unified by weak compatibility fornia strains, the progeny showed a wide phenomenon were progressive declines in
among some of their constituent isolates range of variation in virulence (T. Gordon lesion lengths on trees that were inoculated
and might equally well be regarded as a and S. Kirkpatrick, unpublished). Nearly four times over a 2-year period (19), or
single heterogeneous VCG (46). So, by all were intermediate relative to the two three times over a 1-year period (36).
this measure, diversity in the California parental strains, and none was significantly These changes were suggestive of systemic
population is low. more virulent than the most virulent of the induced resistance (SIR).
Although a low level of VCG diversity two parents. To test the hypothesis that exposure to
would be consistent with clonal propaga- Our tests do not preclude the possibility the pathogen could enhance host resistance
tion, it could also be explained by a limited that more virulent genotypes might result to a subsequent infection, we used trees
potential to generate different VC geno- from a cross that occurs in nature. One way established as clones from rooted cuttings
types. For example, if the two mating types to evaluate the potential for such crosses to and tested them under controlled environ-
differed at only three of the loci affecting affect virulence over time is to characterize ment conditions. This allowed us to com-
vegetative compatibility, recombination the heritability of virulence and the poten- pare identical genotypes in a common
could generate at most eight different com- tial for directional selection to increase the environment and thereby document a sig-
binations (2n, where n = 3). By this logic, a mean virulence of the prevalent isolates. nificant effect of prior inoculation on the
low level of allelic diversity at VC loci Such studies are currently in progress and lesion length that resulted from a subse-
could beget limited VCG diversity in the may provide an indication of how the pitch quent challenge with the pathogen (2). This
population. However, this is not the case in canker pathogen will evolve over time. appears to be the first confirmed case of
the California population, as 30 VCGs Although increases in virulence within the SIR in a coniferous tree.
were identified among 152 progeny of a population could have negative conse- Whereas the phenomenon of induced re-
single cross between wild type strains (T. quences for susceptible hosts, if such sistance is interesting in and of itself, it
Gordon and S. Kirkpatrick, unpublished). changes are gradual, they might be offset was not immediately clear that it had any
Only two VCGs identified among the to some extent by selection for enhanced significant implications for the course of
progeny were known to occur naturally in resistance in the host population. the pitch canker epidemic in California.
1134 Plant Disease / Vol. 85 No. 11After all, thousands of infected trees had do not know how many of these may have infections are evident as well on some of
already died, so to the extent that their expressed remission had they been retained those species found in proximity to the
resistance was altered along the way, it did in the landscape. existing infestations. Noteworthy in this
not prevent their ultimate demise. This The observed disease remission may be respect are coastal stands of the other
picture changed dramatically when the due to SIR, such as we have documented in closed cone pines, knobcone pine (P. at-
urban plots that were originally established Monterey pine under experimental condi- tenuata) and bishop pine (P. muricata),
in 1992, and monitored through 1996 (40), tions (2). However, it is also possible the many of which now have a high incidence
were reevaluated in 1999. activity of insect vectors in these areas had of infection (A. Storer, T. Gordon, and D.
The original motivation for revisiting decreased, and therefore that new infec- Wood, unpublished observations). Both
the urban plots was to assess the amount of tions were not being initiated on disease- species have much more extensive native
tree removal that had occurred during the 7 free trees. Empirical measures of tree sus- ranges than Monterey pine, and although
years since the plots were established. ceptibilities and levels of insect activity are bishop pine is restricted to the coast, knob-
During the course of the data collection, it needed to establish the relative importance cone pine is also found farther inland, in
became clear that in areas considered to of these factors. Whatever the explanation, the Sierra Nevada (29).
have severe pitch canker in 1992, some the remission phenomenon argues for a Other pine species known to be suscep-
trees that had high levels of infection in conservative approach to tree removal. tible, based on greenhouse tests, are rare or
1992 were free of disease symptoms in Consequently, our recommendations have absent in the coastal forests where pitch
1999 (A. Storer, D. Wood, and T. Gordon been modified to the effect that diseased canker is found, so it has not been possible
unpublished). Old branch tip infections had trees should not be removed until deemed to accurately gauge their relative suscepti-
broken from many of these trees, and sub- necessary based on other criteria, such as bility to natural infections (Table 1). This
tending lateral branches continued to grow. safety or aesthetic considerations, to allow includes ponderosa pine (P. ponderosa),
Thus, branch stubs with growth of laterals for the possibility that trees may go into gray pine (P. sabiniana), and shore pine (P.
around them were characteristic of an in- remission. Thus the cost of tree removal contorta subsp. contorta). Studies of other
fection that had become inactive. and replacement may at least be delayed, if pine species indicate that greenhouse tests
The highest levels of apparent disease not avoided entirely. Of course, we do not are highly predictive of disease incidence
remission were recorded at New Brighton yet know how persistent the remission in the field (18), suggesting that once the
State Beach (Santa Cruz County), where effect will prove to be. abovementioned native pines receive suffi-
pitch canker was discovered in 1986; 30% cient exposure to the pathogen, they will
of the trees remaining in our monitoring Ecological Limitations suffer the effects of pitch canker to the
plot had indications of disease remission, on Pitch Canker in California extent that Monterey pine and others have.
or 17% of the original population in this The epidemic of pitch canker in Califor- If this proves to be the case, the distribu-
plot. In areas where pitch canker became nia demonstrates that the environment in tion of gray pine, which rings the Central
established more recently, smaller percent- central and southern coastal California is Valley of California (20), will offer an
ages of trees showed signs of remission (A. generally conducive to disease develop- ideal infection pathway from the coastal
Storer, D. Wood, and T. Gordon, unpub- ment. Within this area, most of the damage forests to the Sierra Nevada and southern
lished). The proportion of trees capable of to date has been associated with Monterey Cascade Range (Fig. 1), where extensive
expressing disease remission may be pine, but many other native California coniferous forests are found. In a similar
higher than our data suggest because many species are at least as susceptible, based on fashion, shore pine and bishop pine could
trees were removed prior to their death. We greenhouse inoculations (Table 1). Natural facilitate expansion of the pitch canker
Table 1. Susceptibility of pines grown in California to pitch canker, caused by Fusarium circinatum
Susceptibilitya
Species Common name Statusb Greenhouse Field Reference
Pinus attenuata Knobcone pine Native S S 6, 17
P. canariensis Canary Island pine Exotic R R 18
P. contorta subsp. contorta Shore pine Native S S 6, 17
P. coulteri Coulter pine Native S S- 6
P. halepensis Aleppo pine Exotic S S 18
P. jeffreyi Jeffrey pine Native S N 6
P. lambertiana Sugar pine Native S N 30
P. muricata Bishop pine Native S S 6,17
P. pinea Italian stone pine Exotic R R 18
P. ponderosa Ponderosa pine Native S S- 6, 17
P. radiata Monterey pine Native S S 18, 19, 40
P. sabiniana Gray pine Native S S- 6, 17
P. thunbergiana Japanese black pine Exotic R N 18
P. torreyana Torrey pine Native NT S- 17
a Greenhouse tests of susceptibility are based on the results of artificial inoculations; the procedure described in the text was used for all species
except sugar pine, for which a different inoculation method was used (30). Species are rated as susceptible (S) if they sustained definite lesions
at the site of inoculation, or resistant (R) if there was little or no lesion development; NT indicates a species that has not been tested. Field sus-
ceptibility is based on observations of natural infections. Species are rated as susceptible (S) if numerous trees are known to be infected and/or
some trees have sustained severe damage from pitch canker (e.g., multiple branch infections leading to extensive dieback in the canopy). Species
that have frequently been observed in otherwise infested areas and for which few or no trees are known to have sustained natural infections and
none have been severely damaged by pitch canker are rated resistant (R); the level of resistance differs within this group. For species rated S-,
one or more infected trees have been observed, but the number of observations is too limited to provide a meaningful estimate of their relative
susceptibility. For a species rated N, no infected trees have been observed, but the occurrence of this species in proximity to natural inoculum is
too infrequent to conclude that the lack of disease is indicative of resistance.
b Native species are found in native forests but may also be grown for timber in plantations (e.g., ponderosa pine) or as landscape trees (e.g., Mon-
terey pine); the exotic species are planted in various parts of the state.
Plant Disease / November 2001 1135infestation northward along the California of disease increase over a 3-year period Altered Interactions coast and into Oregon. Also relevant in this (45). It is noteworthy that this “coastal Resulting from Pitch Canker regard is Douglas-fir (Pseudotsuga menzi- effect” is apparent over a relatively short What we know about pitch canker as a esii), the only species outside the pine distance, as many of the inland plots are pathogen in native forests is limited to genus that has been shown to be suscepti- little more than 1 km from the coast. Al- what we have learned from its fairly recent ble to pitch canker (38); Douglas-fir is though the basis for the effect is not development in Monterey pine stands. widely distributed on the north coast and in known, it is consistent with an influence of Already it appears that the impact of pitch the Sierra Nevada. The extent to which this fog and the associated condensation, which canker goes far beyond the direct effects species will be affected by pitch canker is occurs with greater frequency and duration on susceptible trees. Although there are unclear, but evidence available to date near the coast, relative to more inland loca- likely to be many as yet unrecognized ef- suggests that Douglas-fir is only moder- tions. If this is the basis of the differential fects on animal and plant communities ately susceptible to pitch canker (6); more effect we have observed, it may portend a associated with Monterey pine, here we extensive testing is required to confirm this. significant environmental limitation on the will consider only the insects associated The availability of a suitable host is nec- establishment of pitch canker in drier areas with the pitch canker pathogen, for which essary but may not be sufficient for a dis- farther inland. we have some evidence as to how they ease to be manifest. In the case of pitch On a regional scale, a coastal effect have been affected. canker, as it occurs in the western United might also be inferred from the distribution Insects that function as primary decom- States, insect vectors (or wounding agents) of pitch canker in California (Fig. 1). Of posers in Monterey pine forests, such as also are important. However, based on course, this could be the result of greater twig beetles and deathwatch beetles, were published host records (4), it appears this development in areas where the pathogen once benign associates of Monterey pine will not impose a limitation to the infection was first introduced, but the longer the but are now injurious because they vector of most native California pine species, present distribution remains in place, the the pitch canker pathogen. Hence their because many insects known to vector more compelling the argument it offers for impact on Monterey pine has been altered pitch canker are reported from multiple an environmental limitation on pitch can- from a neutral to a negative one. A similar pine hosts (38). Furthermore, many less ker. Experimental studies now underway story pertains for the cone beetle, which obvious pathways involving parasites, should provide a more complete picture of reduces reproduction by damaging seeds predators, and other gallery associates of the extent to which atmospheric moisture but generally does not cause branch tip the known vectors may also serve to move affects the infection process mediated by mortality distal to the cone whorl. When F. circinatum between host species (9). twig beetles. However, such limitations pitch canker is present, however, the nega- Thus, one might conclude that pitch canker may not apply to other vectors, such as the tive impact of these insects is increased will eventually affect native pines through- cone beetle, which can incite infections in because they vector the pathogen into cone out the extensive inland pine forests of the process of colonizing first- and second- whorls and thereby cause mortality of the California and perhaps Oregon, Washing- year cones (25). Because the cone beetle branch tip distal to the colonized cone. ton, and Canada as well. Whether or not has the potential to carry the fungus deeply Furthermore, in the absence of pitch can- the disease progresses to this extent may into the cone, infection may occur in the ker, cone beetle activity did not signifi- depend on how environmental conditions absence of free moisture on the cone sur- cantly enhance the quantity of breeding affect disease establishment. Two factors face. If so, the prospects for expansion of substrate for twig beetles. In the presence that seem likely to be important in this the pitch canker infestation to more inland of pitch canker, however, both the cone respect are: the effect of atmospheric mois- locations may be strongly influenced by beetle-colonized cone and the branch tip ture on the infection process, and the tem- the distribution of the cone beetle, which is distal to the infected cone whorl are ren- perature range for growth of the pathogen. not yet well characterized. dered suitable for colonization by twig As noted above, wounding by twig bee- The ultimate geographic limits for pitch beetles (25). Hence the effect of cone bee- tles, which appears to be an important canker in western North America may also tle activity on twig beetles has been altered mechanism by which infections are estab- be affected by temperature requirements from neutral to positive (39). lished on young branches, is relatively su- for growth of the pathogen. In particular, Ordinarily, twig beetles do not weaken perficial. This reflects the fact that physio- 9°C appears to be near the lower limit for trees, because they rarely colonize branches logically active branches are not suitable for fungal growth in culture (31). A similar that were not already shade suppressed. colonization by twig beetles, and hence the limitation on infection was observed on However, where they are acting as vectors of wounding they cause presumably results trees under growth chamber conditions the pitch canker pathogen, twig beetles (and only from limited bark penetration. As a (31). This lower limit for growth and infec- cone beetles) help to weaken trees. This result, the infection court is unlikely to be tion should make it increasingly difficult benefits engraver beetles (Ips spp.), which deep enough to reach an adequate supply of for the pathogen to become established as preferentially attack such predisposed hosts water. For this reason, the pathogen may it moves to more northerly latitudes and to (14,38). Undoubtedly the population sizes of depend on external sources of moisture to higher elevations. In the eastern United many of these insect species have increased establish an infection. Although we have yet States, pitch canker has not been reported in the presence of the pitch canker pathogen, to experimentally confirm a requirement for north of Virginia (13). and work is underway to quantify the mag- high ambient humidity, evidence from field Even if these potential environmental nitude of these changes and of the altered studies suggests that such a limitation may limitations on the disease are borne out, interactions among insects and between be operative under natural conditions. extensive inland-forested areas in Califor- insects and their host trees. In 1996, we established plots in native nia would offer suitable conditions for Monterey pine forests on the Monterey pitch canker during some parts of the year. Prospects for Management Peninsula. The principal objective of this For example, prevailing weather in the As is generally the case with diseases of study was to test for an effect of landscape foothills of the Sierra Nevada would be trees, we are without realistic therapeutic type on disease development. However, the permissive during parts of the spring and options for dealing with pitch canker. Fun- distribution of plots allowed us to subdi- fall in most years. Consequently, introduc- gicides with activity against the pathogen vide them into two geographic categories: tion of the pathogen to these locations, as are available, so, in principle, trees could coastal and inland. The results documented could occur through movement of fire- be protected from infection. Such chemical a significant effect of geography, with wood, seed, soil, or infected trees, might controls might be exploited under nursery coastal plots having a higher mean disease well allow pitch canker to become estab- conditions to prevent seedling disease severity than inland plots and a greater rate lished. caused by F. circinatum, but for larger 1136 Plant Disease / Vol. 85 No. 11
trees, maintaining a sufficiently high con- follow, with the attendant problems of trees have been identified and propagated
centration of the active ingredient on all disposal. To the extent that this material is vegetatively, there is as yet no commercial
susceptible surfaces would be problematic, kept within already infested areas, oppor- source for this material. Local efforts are
even if cost were not a consideration. Simi- tunities for movement of the pathogen to underway to select and propagate resistant
lar constraints would apply to insecticidal new areas can be minimized. However, the cuttings from parent trees of appropriate
treatments for control of insect vectors. volume of material often exceeds the ca- local origin, and this may ultimately be
Furthermore, because the insects involved pacity for local utilization, so procedures sufficient to meet the demand. However,
are all native associates of California coni- that can reduce or eliminate the pathogen because the long-term durability of genetic
fers that contribute to the decomposition of and its vectors from branches and logs are resistance can never be guaranteed, we
wood, any large-scale effort to reduce their being explored. In particular, chipping of recommend deployment of pitch canker
numbers would be difficult to justify. branches has been shown to greatly reduce resistant Monterey pines only where land
The early phases of pitch canker devel- the size of resident insect populations (W. managers conclude that the value of retain-
opment are characterized by branch tip McNee, D. Wood, A. Storer, and T. ing this species exceeds the risk that their
infections, which can be pruned out to Gordon, unpublished). However, pathogen trees may eventually be damaged by pitch
effectively eliminate the disease, at least survival is not greatly diminished by this canker.
temporarily. Of course new infections can procedure, so exposure of the chips to In native stands, management of pitch
occur, and this is especially likely where elevated temperatures, as by tarping or canker can best be achieved through prac-
many diseased trees are present. Conse- composting, is recommended. Recent stud- tices that promote natural regeneration of
quently, removal of infected branches is ies using infested wood chips showed that the forest. Fire results in plentiful
unlikely to alter the course of disease, and temperatures as low as 50°C can quickly regeneration and would also have the
this expectation is supported by results eliminate the pathogen if the material re- benefit of eliminating inoculum associated
from several rounds of eradicative prun- mains wet (T. Gordon and S. Kirkpatrick, with the litter layer and the soil surface.
ing in Monterey pine stands that were unpublished). However, the proximity of human
relatively distant from other diseased Logs cut from diseased trees could serve habitations and other safety considerations
trees (T. Gordon and M. Schultz, unpub- to disseminate the pathogen, and although will make fire impractical in many areas.
lished). they could be rendered pathogen-free The ability of Monterey pine to colonize
At approximately 6-month intervals, all through heat treatments or fumigation (33), openings in the forest canopy will ensure
infected branches were removed from trees the costs are prohibitive. For this reason, regeneration in areas where gaps are
in selected stands in Santa Cruz and Mon- we have conducted preliminary tests of created by any of various means, including
terey counties. At one location, 57 symp- fungicides registered for sap stain control, pitch canker–induced mortality (41). Under
tomatic branches were removed in the some of which show the potential to reduce these circumstances, selection in the
initial round of pruning in a stand com- or eliminate the pathogen on the surface of presence of pitch canker should ultimately
prised of 51 mature trees. Totals of 101, logs, whether debarked or intact. The use increase the frequency of resistant trees in
69, 370, and 588 diseased branches were of such treatments would be entirely the population.
identified and removed 7, 14, 22, and 43 voluntary, however, as no laws are in place Monterey pines are relatively short-
months later, respectively. At the beginning to require them. lived, and many native stands are consid-
of the study, only four trees in the stand Identifying suitable replacement trees in ered senescent due to the preponderance of
had symptoms of pitch canker, but by the pitch canker–affected areas is not a prob- trees near the end of their natural life span.
final pruning date, 48 of the 51 trees were lem in most situations. Only pines are at Thus, the process of regeneration will be
diseased. Similar results were obtained at risk of severe disease, and even within the critical to maintaining a Monterey pine
three other locations. Although it is possi- pine genus, several species are known to forest, irrespective of pitch canker (41).
ble the development of pitch canker would sustain little or no damage from pitch can- Consequently, it may not be necessary to
have been more rapid in the absence of the ker (Table 1). This includes Japanese black treat pitch canker–affected stands any dif-
pruning efforts, this approach was clearly pine (P. thunbergiana), Italian stone pine ferently than those that are free of disease.
not effective in eliminating the disease or (P. pinea), and Canary Island pine (P. ca- However, if natural regeneration is insuffi-
even in reducing its incidence or severity. nariensis), all of which are popular land- cient, more direct intervention might be
Moreover, given that the pruning opera- scape trees in Mediterranean climates (18). required.
tions required a lift truck and a crew of However, the abovementioned pines would Where natural regeneration fails, re-
skilled tree climbers, the costs involved not necessarily be considered acceptable planting might be required to retain a Mon-
would probably preclude the application of replacements for Monterey pine in com- terey pine forest at that location. If herita-
such measures in most situations, even if munities that are within or adjacent to bility of resistance to pitch canker proves
there were reasonable prospects for suc- native stands of this species. to be high, broadcasting seed from nearby
cess. However, where pruning restores the Two of the native populations of Mon- resistant trees might be an acceptable
aesthetic value of a tree and therefore al- terey pine (Cambria and Monterey) are means of obtaining a stand and increasing
lows it to be retained in the landscape, adjacent to extensive residential and com- the frequency of resistance to pitch canker.
costs might be repaid if the tree recovers mercial developments. At many of the If this approach is not successful, seedlings
and the expense of removal and replace- forest–urban interfaces, native trees have prescreened for resistance could be trans-
ment is thereby avoided. been retained and/or Monterey pines have planted into the forest. Alternatively, vege-
Given the limited options for dealing been planted in an attempt to maintain a tatively propagated cuttings could be used.
with diseased trees, management of pitch semblance of the native plant community The latter method has the appeal of allow-
canker must focus on efforts to minimize throughout the developed area; such areas ing for rapid production of planting stock
future damage. For landscape trees, this have been referred to as “urban (or urban- but naturally raises concerns about exten-
includes: (i) minimizing dissemination of ized) forests.” Replanting with species sive deployment of any single genotype.
the pathogen through proper handling of other than Monterey pine would be incon- Until more is known about the genetic
infected materials, and (ii) replacing dis- sistent with this objective, although it basis for resistance, the best way to address
eased trees with nonsusceptible species or would be desirable from the standpoint of this issue is to propagate from as many
resistant selections. disease management. Genetically resistant different parental trees as practicable.
Where pitch canker becomes established Monterey pines would be an obvious Whatever approach is adopted, reforesta-
in Monterey pines or other highly suscep- choice under these circumstances. How- tion efforts will need to be carefully con-
tible species, tree removal may eventually ever, although many pitch canker–resistant sidered in terms of genetic conservation, in
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