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© Australasian Plant Pathology Society 2003 10.1071/AP03043 0815-3191/03/030393
www.publish.csiro.au/journals/app Australasian Plant Pathology, 2003, 32, 393–402
CSIRO PUBLISHING
Variation in severity of target spot, caused by Aulographina eucalypti,
in a eucalypt species and provenance trial in Victoria
Angus J. CarnegieA,B,C and Philip J. KeaneA
ASchool of Botany, La Trobe University, Bundoora, Vic. 3068, Australia.
BCurrent address: Research & Development Division, State Forests of NSW, PO Box 100, Beecroft, NSW 2119,
Australia.
CCorresponding author; email: angusc@sf.nsw.gov.au
Abstract. Target spot caused by the fungus Aulographina eucalypti was assessed from spring 1990 to summer
1991 on 44 provenances of 14 Eucalyptus species to determine the variation in susceptibility to the pathogen. A
disease assessment scale for target spot was developed specifically for this study based on the development of
lesions caused by A. eucalypti and the proportion of leaf area affected. Significant variation was observed among
the 44 provenances in both spring and summer, with provenances from E. globulus (all provenances except Eden),
E. nitens, E. cypellocarpa, E. oreades, E. sieberi and E. viminalis scoring the highest for target spot. Provenances
from E. quadrangulata, E. saligna, E. botryoides and E. elata all scored low for target spot, as did E. globulus
provenance Eden. Variation within species for E. botryoides, E. globulus, E. nitens, E. saligna and E. viminalis was
also significant. In general, variation between provenances within species was much less than variation between
species. Severity of target spot on E. globulus (also assessed in winter 1990) increased from winter to spring and
again from spring to summer. The pathogen was recorded on all 14 species in the trial, including two new host
records. This paper also reports new host records from field collections by the first author over the past 12 years,
and from examination of herbarium specimens, adding 35 new host records for A. eucalypti and five new host
records for Australia.
AP03 043
Aulographina eucalypti
variation in
Eucalyptus
spp.A. J. Carnegie
et al.
Additional keywords: Eucalyptus, leaf pathogen, disease assessment scale, new host records.
Introduction
One of the most common and distinctive leaf diseases in
eucalypt forests and plantations in south-eastern Australia is
target spot caused by Aulographina eucalypti (anamorph:
Thyrinula eucalypti). The pathogen has been recorded on
over 40 species of Eucalyptus in Australia (Hansford 1954;
Marks et al. 1982; Wall and Keane 1984; Stone et al. 1998a;
Park et al. 2000) and, in native forests, is more common on
species in Eucalyptus subgenus Eucalyptus (Wall and Keane
1984). The classification of the genus Eucalyptus in this
paper follows Brooker (2000) and includes subgenus
Corymbia (formerly a genus, Hill and Johnson 1995),
subgenus Eucalyptus (formerly subgenus Monocalyptus,
Pryor and Johnson 1971) and subgenus Angophora (formerly
a genus, Pryor and Johnson 1971). Additional host species
have been reported overseas, mainly from plantations in
South Africa (Crous et al. 1989), but also from New Zealand
(Dick 1982), Brazil (Ferreira 1989, in Park et al. 2000), the
United Kingdom (Spooner 1981), Vietnam (Old and Yuan
1994), Chile (Wingfield et al. 1995) and Madagascar (Crous
and Swart 1995).
A. eucalypti has been described in detail previously (Wall
and Keane 1984). Leaf spots are roughly circular, 2–15 mm
in diameter, often raised and corky, and develop only part
way through the leaf lamina whether on the upper or lower
surface. Lesions develop very slowly, which allows time for
the formation of a cork cambium barrier, and are most
evident on older leaves. Small, black, pimple-like pycnidia
develop on the surface of lesions, followed by black,
elongate, often-branched pseudothecia, roughly in
concentric rings. The pathogen is also able to infect petioles,
small branches, fruits and smooth bark (Wall and Keane
1984), and severe infection of leaves and petioles can lead to
premature defoliation (Neumann and Marks 1976; Marks
et al. 1982).
Most reports of severe damage by A. eucalypti have been
from native forests. A. eucalypti was considered the major
causal agent amongst a complex of leaf pathogens that
394 Australasian Plant Pathology A. J. Carnegie et al.
reached epidemic levels and resulted in moderate to severe
defoliation of saplings and 120- to 180-year-old
E. denticulata (= E. nitens) on the Errinundra Plateau in East
Gippsland, Victoria, in 1974 (Neumann and Marks 1976).
Species of Alternaria, Harknesia and Mycosphaerella were
also associated with the defoliation. In 1973, defoliation and
death of several thousand hectares of mature E. obliqua
forest in several valleys in north-west Tasmania were
attributed mainly to A. eucalypti with Vermisporium
(= Seimatosporium) falcatum playing a minor role (Palzer
1978; Felton 1981). Target spot reached epidemic
proportions during 1993 in young E. regnans regrowth in
native forest in south-central Victoria (Stefanatos 1993).
Damage from target spot has generally been minor in
plantations. Localised outbreaks of infection caused by
A. eucalypti have been recorded from eucalypt plantations in
New South Wales (Gerrettson-Cornell and Dowden 1977;
Stone et al. 1998a, 1998b; Carnegie 2000; Carnegie and
Johnson 2004), New Zealand (Dick 1982), Chile (Wingfield
et al. 1995) and Madagascar (Crous and Swart 1995).
However, this pathogen has also been associated with severe
leaf spotting and defoliation on E. fastigata and
E. fraxinoides in South African plantations (Crous and
Wingfield 1991), and is considered of economic importance
due to its potential to cause extensive defoliation (Crous et
al. 1989).
This paper describes a disease assessment scale
developed for target spot on juvenile foliage and its use to
assess variation in susceptibility to the disease between 14
Eucalyptus species and 44 provenances in a 3-year-old trial
in south-eastern Australia.
Methods
Description of trial
A trial was established in October 1988 by the Department of
Sustainability and Environment, Victoria, at Tostaree (37°47'S,
148°11'E), near Nowa Nowa, in south-eastern Victoria, Australia, to
test 44 provenances of 14 eucalypt species for their potential for use in
commercial plantations. The experimental design was a randomised
complete block with 25-tree plots and f ive replicates. Trees were spaced
3 m × 3 m on a square grid. Results for the incidence of Mycosphaerella
leaf diseases (caused by several species of Mycosphaerella) on the
juvenile foliage of 35 provenances of 13 species (Carnegie et al. 1998),
and the incidence and severity of Mycosphaerella leaf disease (both
M. cryptica and M. nubilosa, assessed together) on nine provenances of
E. globulus (Carnegie et al. 1994) have been reported previously.
Disease assessment scales
To develop a disease assessment scale (DAS) for target spot on
eucalypts, leaves with a range of damage caused by A. eucalypti were
collected from all 14 species in the trial (Table 1). These were placed
into four categories (trace, low, medium, high) based on the
development of leaf spots and the proportion of leaf area affected.
Representative leaves were then chosen from each category to illustrate
the scale of disease severity. As E. globulus was considered the most
important species in the trial (because of its potential for widespread
planting in southern Australia), the DAS was developed for target spot
on leaves of this species. Five categories of infection (severity) were
assessed: 0 = no infection; 1 = specks (ca. 2 mm in diameter); 2 =
specks plus spots (> 2 mm in diameter); 3 = specks plus spots, some
coalescing; and 4 = specks plus spots, many coalescing (Fig. 1).
Assessments of target spot
Severity of target spot was assessed using the above DAS. At each
assessment time, a branch at or near breast height in the juvenile crown
was chosen at random and the ten leaves at the tip of the branch were
assessed for severity of target spot. Where there were differences in
severity on the ten leaves the average severity was recorded. For
E. globulus, all 25 trees in each plot were assessed, whereas only the
first five trees in each plot were assessed for the remaining 13 species
and 35 provenances. The trial included provenances from the four
subspecies within E. globulus: subsp. bicostata, subsp. globulus, subsp.
maidenii and subsp. pseudoglobulus. E. globulus was more intensely
assessed because of its importance as a forestry species in south-easter n
Australia. This species was assessed in winter (August 1990), spring
(November 1990) and summer (February 1990), whereas the remaining
13 species were assessed in spring (November 1990) and summer
(February 1991) only.
Statistical analyses
All data were analysed using the GLM procedure of SAS (SAS
Institute Inc. 1992). Due to severe defoliation of the juvenile foliage in
summer, five of the E. nitens provenances and all but one of the
E. viminalis provenances could not be assessed in February. The
defoliation was attributed to Mycosphaerella leaf disease but shading of
lower leaves through canopy closure was also a factor (Carnegie et al.
1994, 1998) and possibly also defoliation due to target spot. For these
reasons, analyses of variance were carried out on spring scores to test
for variation among all 44 provenances. Analyses of variance were also
carried out on summer data for all species and provenances, except
E. nitens and E. viminalis, for which data for only one provenance each
was available due to severe defoliation. For those species with multiple
provenances (E. botryoides, E. globulus, E. nitens, E. saligna, E. sieberi
and E. viminalis), separate analyses of variance were carried out on
spring data to test for variation within species, and on summer data
except for E. nitens and E. viminalis. For E. globulus, analyses of
variance were carried out for winter, spring and summer data to test
provenance by season interaction. Transformations (arcsine and log)
did not improve homogeneity, and so raw scores were used in the
analyses.
New host records
Over the past 12 years, the first author has conducted numerous
surveys of eucalypt plantations, native forests and species trials in
Victoria, New South Wales, Tasmania, South Australia, Western
Australia and the Australian Capital Territory. Leaves collected during
these surveys were examined for leaf spot fungi. During May 2003, the
first author also examined specimens of A. eucalypti from herbariums
VPRI and DAR for new host records. Identification of A. eucalypti
from leaves was established by examination of symptoms under a
dissecting microscope, and squash mounts of mature pseudothecia
examined under a light microscope. A. eucalypti is a very distinctive
pathogen and is easily distinguished from other common leaf spot fungi
(e.g. Mycosphaerella spp.) based on leaf spot symptoms and ascospore
morphology. New host records identified from these studies are
reported here.
Results
A. eucalypti was recorded from all 14 Eucalyptus species
and 44 provenances in the trial (Appendix I). There were
Aulographina eucalypti variation in Eucalyptus spp. Australasian Plant Pathology 395
Table 1. Severity of target spot (on a scale of 0–4) on 44 provenances of 14 eucalypt species recorded at Tostaree in spring
and summer, showing Least Significant Differences for all provenances and for provenances within speciesA
Eucalyptus species Provenance Mean disease severity
Spring Summer
E. botryoides Meroo, NSW 0.32 0.76
E. botryoides Narooma, NSW 0.56 1.12
E. botryoides Nowa Nowa, Victoria 0.40 0.90
E. botryoides Orbost, Victoria 0.36 0.56
LSD for E. botryoides (0.36)A(0.24)
E. brookeriana Benwerrin, Victoria 0.42 1.56
E. cypellocarpa Mt Erica, Victoria 0.52 2.50
E. elata Narooma, NSW 0.20 0.20
E. fraxinoides Eden, NSW 0.69 1.52
E. globulus
ssp. maidenii Eden, New South Wales 0.38 1.10
ssp. pseudoglobulus Jeeralang, Victoria 1.52 1.94
ssp. globulus Judbury, Tasmania 1.52 2.60
ssp. globulus King Is., Tasmania 1.32 2.33
ssp. pseudoglobulus Kuark, Victoria 1.34 2.32
ssp. bicostata Mansfield, Victoria 1.48 2.44
ssp. globulus Otway National Park, Victoria 1.42 2.48
ssp. globulus St. Helens, Tasmania 1.86 3.10
ssp. globulus Wye River, Victoria 1.33 2.78
LSD for E. globulus (0.27) (0.48)
E. grandis Bulahdelah, NSW 0.36 1.54
E. grandis Coffs Harbour, NSW 0.80 1.60
E. nitens Mt Erica, Victoria 1.08 —
E. nitens Mt Kaye, Victoria 1.62 2.61
E. nitens Powelltown, Victoria 1.62 —
E. nitens Snobs Creek, Victoria 2.06 —
E. nitens Tallaganda, NSW 1.56 —
E. nitens Tooronga Plateau, Victoria 0.96 —
LSD for E. nitens (0.68) —
E. oreades Lithgow, NSW 0.68 2.28
E. quadrangulata Albion Park, NSW 0.59 1.28
E. saligna Batemans Bay, NSW 0.38 1.00
E. saligna Beaumont, NSW 0.64 0.86
E. saligna Coffs Harbour, NSW 0.20 1.03
E. saligna Glen Innes, NSW 0.18 1.27
LSD for E. saligna (0.93) (0.29)
E. sieberi Erica, Victoria 1.58 1.62
E. sieberi Nowa Nowa, Victoria 0.86 2.16
E. sieberi Nullica State Forest, NSW 0.76 1.66
E. sieberi Scamander, Tasmania 1.14 1.66
E. sieberi Yarram, Victoria 1.20 1.80
LSD for E. sieberi (1.07) (0.95)
E. smithii Mt Buck, Victoria 0.44 1.58
E. viminalis Big Badga, NSW 0.36 2.01
E. viminalis Bruthen, Victoria 1.06 —
E. viminalis Fingal, Tasmania 0.98 —
E. viminalis Nowa Nowa, Victoria 1.35 —
E. viminalis Silver Creek, Victoria 0.94 —
E. viminalis Templestowe, Victoria 0.60 —
E. viminalis Wye River, Victoria 0.78 —
LSD for E. viminalis (0.61) —
LSD between provenance means for all 0.71 0 .65
provenances analysed together (P < 0.05)
AFigures in parentheses are Least Significant Difference (P < 0.05) between provenance means for provenances within species,
analysed separately for each species. Where no LSD is shown, there were no signif icant differences between provenances.
396 Australasian Plant Pathology A. J. Carnegie et al.
significant differences (P < 0.05) in severity of target spot in
spring among the 44 provenances (Table 1). Provenances
within E. globulus (all but Eden, subsp. maidenii), E. nitens
(Mt Kaye, Powelltown, Snobs Creek and Tallaganda),
E. sieberi (Erica) and E. viminalis (Nowa Nowa) were
amongst the most severely affected by the disease.
Provenances within E. botryoides (Meroo, Nowa Nowa and
Orbost), E. brookeriana, E. elata, E. grandis (Bulahdelah)
and E. saligna (Coffs Harbour and Glen Innes) had the
lowest severities. One provenance from both E. globulus
(Eden) and E. viminalis (Big Badga) were also amongst the
least severely diseased.
For the majority of provenances, the severity of target spot
increased from spring to summer and there were also
significant differences (P < 0.05) among provenances in
summer (Table 1). Provenances within E. globulus (all but
Eden), E. nitens, E. sieberi (all provenances) and E. viminalis
were again amongst the most severely affected. Also,
provenances of E. cypellocarpa and E. oreades were
amongst the most severely affected in summer. The same
provenances within E. botryoides and E. elata scored the
lowest for disease in summer as in spring. Significant
changes in severity of target spot from spring to summer
were observed in E. viminalis, Big Badga (0.36 to 2.01),
E. saligna, Glen Innes (0.18 to 1.27), E. saligna, Coffs
Harbour (0.2 to 1.03), E. cypellocarpa (0.52 to 2.50),
E. grandis, Bulahdelah (0.36 to 1.54) and E. oreades (0.68 to
2.28). Disease severity in many provenances doubled from
spring to summer, with only E. elata staying constant over
both seasons. On E. globulus, disease severity increased
from winter to spring, and again from spring to summer, with
the highest severities on all provenances being recorded in
summer (Fig. 2).
Only E. globulus, E. nitens and E. viminalis showed
significant (P < 0.05) variation in disease among
provenances in spring, whereas in summer, E. botryoides, E.
globulus and E. saligna showed significant (P < 0.05)
variation in disease among provenances (Table 1). Within E.
globulus, which also showed provenance variation in winter,
Eden (subsp. maidenii) had significantly less disease than all
other provenances, with St Helens, Wye River, Otway
National Park and Judbury (all subsp. globulus) having the
most severe target spot (pooling means across seasons). For
E. globulus, provenances from Mansfield (subsp. bicostata)
had significantly lower disease than those from St Helens.
For E. nitens, Tooronga Plateau and Mt Erica had
significantly less disease in spring than Snobs Creek. For
E. viminalis, Big Badga and Templestowe provenances had
less disease in spring than Nowa Nowa. In summer,
E. botryoides provenance Orbost had significantly less
disease than Narooma and Nowa Nowa, and Meroo was
significantly lower than Narooma. Within E. saligna,
Beaumont had significantly less disease in summer than the
provenance from Glen Innes.
In the assessment of target spot in the present study,
A. eucalypti was isolated from two previously unrecorded
hosts (E. brookeriana and E. smithii), and from four hosts on
which the pathogen had not previously been reported in
Australia (E. elata, E. oreades, E. quadrangulata and
E. saligna). During a survey of a species and provenance
trial in Victoria in December 1993, A. eucalypti was isolated
from six hosts not previously recorded (E. badjensis,
E. bosistoana, E. cameronii, E. dendromorpha, E. dunnii and
E. melliodora), and a new host record for Australia
(E. muelleriana) (Appendix I). Surveys in commercial
plantations in NSW from 1996 to 2003 recorded A. eucalypti
Fig. 1. Disease assessment scale developed for severity of target spot
caused by Aulographina eucalypti on eucalypt leaves.
Aulographina eucalypti variation in Eucalyptus spp. Australasian Plant Pathology 397
on E. cloeziana (Carnegie 2000), E. haemastoma,
E. punctata, E. citriodora spp. variegata, and E. henryi, all
new host records (Appendix I). Examination of specimens in
herbariums DAR and VPRI revealed 22 hosts for
A. eucalypti not previously reported (E. transcontinentalis,
E. cyanophylla, E. leucoxylon, E. phaeotricha,
E. polyanthemos, E. pyrocarpa, E. triflora, E. urnigera,
E. tetraptera, E. grossa, E. stricklandii, E. kitsoniana,
E. gunnii, E. platypus, E. citriodora, E. ficifolia,
E. cordifolia, E. eremophila, E. lansdowneana, E. stricta,
E. robusta and E. torquata) (Appendix I). An updated host
list for A. eucalypti is provided in Appendix II.
Discussion
Target spot increased from winter to spring and again
from spring to summer in the trial at Tostaree, which is
consistent with other findings. Wall and Keane (1984)
followed the development of lesions of A. eucalypti on
tagged leaves of E. obliqua in Narbethong over 2 years.
Lesions on the majority of leaves increased in size from June
and August of one year to January and March the following
year. Stone et al. (1998a) reported that fungal damage
associated with A. eucalypti and other fungi increased from
February of one year to July the following year. Lesions
caused by A. eucalypti develop very slowly (Wall and Keane
1984) and so they are more evident on older leaves.
Epidemic development of A. eucalypti is limited in winter by
the availability of inoculum, which decreases at temperatures
below 15°C, and the lack of young, susceptible leaves (Wall
and Keane 1984) which start developing in spring.
A. eucalypti is also hindered by the lack of free moisture for
spore release and infection on hot, dry days in summer (Wall
and Keane 1984). Therefore, epidemic development of
A. eucalypti would be greatest in spring with the new leaf
flush of the host and spring rains, and would then decline as
the days become hot and dry during late summer and too cold
during winter. This pattern of disease development was
observed in the trial at Tostaree.
Wide variation in susceptibility to target spot was
observed both within, and between, species at Tostaree. In
general, variation between provenances within species was
much less than variation between species. As disease was
greatest in summer, ranking of provenances is best done with
summer scores. Due to wide variation within species, it was
not feasible to calculate species means for comparison of
target spot amongst the 14 species. However, in general, six
species had a high or relatively high ‘mean’ score for target
spot in summer. These were, in decreasing order of severity,
E. globulus (all provenances except Eden), E. nitens,
E. cypellocarpa, E. oreades, E. sieberi and E. viminalis, all
with ‘mean’ scores above 1.75 (species means of summer
scores). In contrast, E. quadrangulata, E. saligna,
E. botryoides and E. elata all had ‘mean’ scores below 1.30.
E. brookeriana, E. fraxinoides, E. grandis and E. smithii
were in the middle range with average scores in summer of
1.52 to 1.58. Crous and Wingfield (1991) reported that
A. eucalypti can cause extensive defoliation to E. fraxinoides
and E. fastigata in South Africa, but made no mention of
damage to E. nitens, which is widely planted there,
suggesting it is less susceptible to A. eucalypti. This contrasts
with our findings in which E. nitens was one of the most
susceptible species.
Intra-species variation for severity of target spot on
eucalypts has been reported previously. Significant variation
in severity of A. eucalypti was reported amongst provenances
of E. obliqua in a trial in Victoria (Parkin 1976). Variation
amongst provenances of E. regnans and E. laevopinea was
observed during assessments of fungal damage in trials in
0
0.5
1
1.5
2
2.5
3
3.5
Winter S
p
rin
g
Summer
Severity of target spot
Eden, NSW
Jeeralang, Victoria
Judbury, Tasmania
King Is., Tasmania
Kuark, Victoria
Mansfield, Victoria
Otway National Park,
Victoria
St Helens, Tasmania
Wye River, Victoria
Fig. 2. Severity of target spot on provenances of Eucalyptus globulus across three seasons at Tostaree. See
Table 1 for E. globulus subspecies.
398 Australasian Plant Pathology A. J. Carnegie et al.
NSW where A. eucalypti was the main pathogen on these
species (Stone et al. 1998a). Variation in severity of
Mycosphaerella leaf disease and target spot was observed in
a E. pilularis family trial in NSW (Carnegie and Johnson
2004). Significant variation was observed among
provenances within E. botryoides, E. globulus, E. nitens,
E. saligna and E. viminalis in the present study.
Variation in susceptibility of provenances to leaf spot
fungi has been attributed to the adaptation of the provenance
to the disease in their particular environment (Carnegie et al.
1994). Those provenances originating from areas where
disease is prevalent (such as in areas with a high summer
rainfall) may have undergone more intense selection for
resistance than those originating from areas with typically
dry summers, where disease may not be important and,
therefore, selection not as intense. When these latter
provenances are planted in areas where the disease is
common, they are likely to be severely damaged by the
disease. Although the results are variable, there is some
evidence for this phenomenon in the present study. For
E. globulus, St Helens and Judbury in Tasmania and
Mansfield in Victoria are areas that are typically too cold or
too dry for significant disease development. When planted at
Tostaree (an area with typically moist summers),
provenances from St Helens, Judbury and Mansfield
sustained high levels of target spot in the current study, and
also sustained severe Mycosphaerella leaf disease (Carnegie
et al. 1994). In contrast, provenances from Eden, NSW,
which is in an area in the same climatic region as Tostaree
and experiences typically moist summers, had low levels of
both target spot and Mycosphaerella leaf disease (Carnegie
et al. 1994) when planted at Tostaree.
Selective breeding of resistant or tolerant genotypes is an
important strategy for disease management in forestry. The
use of resistant genotypes in reducing the impact of foliar
pathogens has been widely discussed for eucalypts (Wilcox
1982a, 1982b; Purnell and Lundquist 1987; Carnegie et al.
1994, 1998; Dungey et al. 1997; Stone et al. 1998a; Carnegie
and Ades 2002; Carnegie and Johnson 2004). E. globulus
and E. nitens are the most important eucalypt species used in
short rotation plantations in southern Australia and in other
temperate regions of the world. Both target spot and
Mycosphaerella leaf disease are considered the most
important foliar diseases of these hosts in southern Australia.
Studies of Mycosphaerella leaf disease on E. globulus and
E. nitens have reported significant provenance and family
variation within these species (Purnell and Lundquist 1987;
Carnegie et al. 1994, 1998; Dungey et al. 1997). The present
study showed that there was also wide variation in severity of
target spot within E. globulus and E. nitens. Phenotypic
correlations between severity of target spot and
Mycosphaerella leaf disease on E. globulus in the trial at
Tostaree were significant, more so for scores in summer (r =
0.52, P < 0.01) than in winter (r = 0.34, P < 0.05) (Carnegie
1991). Target spot was correlated only slightly with
Mycosphaerella leaf disease for E. pilularis in a trial in New
South Wales (Carnegie and Johnson 2004). In both these
trials (Carnegie 1991; Carnegie and Johnson 2004) trees
sustained more damage from Mycosphaerella leaf disease
than from target spot. Susceptibility to both Mycosphaerella
leaf disease and target spot has been shown to be low to
moderately heritable (Dungey et al. 1997; Carnegie and
Johnson 2004). Therefore, it could be feasible to select
provenances within E. globulus or E. nitens that have a low
susceptibility to both diseases. The present work on target
spot and that by others with Mycosphaerella leaf disease
indicate that breeding for resistance could be an effective
tool to reduce the impact of Mycosphaerella leaf disease and
target spot in Australian eucalypt plantations.
The current paper reports 35 new hosts for A. eucalypti,
and five host records not previously reported from Australia,
from field collections and herbarium specimens. Sankaran
et al. (1995) published a host list for A. eucalypti, derived
solely from published records, with 49 species of
Eucalyptus. The current work and other recent studies (Stone
et al. 1998a; Barber et al. 2003; M. Dick, personal
communication) bring the reported host range for
A. eucalypti to 90 species of Eucalyptus, in E. subg.
Eucalyptus, E. subg. Symphyomyrtus, E. subg. Corymbia,
E. subg. Eudesmia E. subg. Alveolata, E. subg. Idiogenes
and E. subg. Angophora (see Appendix II). Heather (1971)
and Burdon and Chilvers (1974) reported that A. eucalypti is
more common on species in E. subg. Eucalyptus in native
forests. However, the current study and numerous others
(e.g. Marks et al. 1982; Dick 1982; Wall and Keane 1984;
Crous et al. 1989; Stone et al. 1998a) have revealed a much
wider host range for the pathogen, especially from
plantations. These reveal that A. eucalypti has many hosts in
both E. subg. Eucalyptus and E. subg. Symphyomyrtus.
Few eucalypt leaf spot pathogens have such a wide host
range. M. cryptica, considered one of the most important leaf
spot fungi in Australia, has a reported host range of over 50
eucalypt species in both E. subg. Symphyomyrtus and
E. subg. Eucalyptus, but not in E. subg. Corymbia. Other leaf
fungi with wide host ranges include Phaeophleospora
epicoccoides (Park et al. 2000) and several species of
Cylindrocladium (Brown and Ferreira 2000). Of these,
A. eucalypti and M. cryptica are considered the most
damaging in eucalypt plantations in Australia.
Acknowledgments
Peter Ades assisted with statistical analyses; Ian Smith
and Paul Clements helped with data collection; the
Department of Sustainability and Environment gave
permission to assess their field trials; La Trobe University
provided support during this research; and herbariums VPRI
and DAR provided loans of specimens and received our
collections for accession. For this we are most grateful.
Aulographina eucalypti variation in Eucalyptus spp. Australasian Plant Pathology 399
References
Barber PA, Smith IW, Keane PJ (2003) Foliar diseases of Eucalyptus
spp. grown for ornamental cut foliage. Australasian Plant
Pa th ol og y 32, 109–111.
Brooker MIH (2000) A new classification of the genus Eucalyptus
L’Her. (Myrtaceae). Australian Systematic Botany 13, 79–148.
Brown BN, Ferreira FA (2000) Diseases during propagation of
eucalypts. In ‘Diseases and pathogens of eucalypts’. (Eds PJ Keane,
GA Kile, FD Podger, BN Brown) pp. 119–151. (CSIRO Publishing:
Melbourne)
Burdon JJ, Chilvers GA (1974) Fungal and insect parasites contributing
to niche differentiation in mixed stands of eucalypt saplings.
Australian Journal of Botany 22, 103–114.
Carnegie AJ (1991) ‘The susceptibility of certain Eucalyptus species
and provenances to infection by Mycosphaerella spp. and other leaf
parasites.’ Honours Thesis, School of Botany, La Trobe University,
Australia.
Carnegie AJ (2000) State and company overviews of eucalypt
plantation estates and pest problems — New South Wales. In
‘Proceedings of a workshop on managing pests of eucalypt
plantations’. 10–11 February 2000, Department of Forestry, ANU,
Canberra. (Eds H Elliot, C McArthur, R Floyd, D de Little)
pp. 15–25. (CRC for Sustainable Production Forestry)
Carnegie AJ, Ades PK (2003) Mycosphaerella leaf disease reduces
growth of plantation-grown Eucalyptus globulus. Australian
Fo re st r y 66, 113–119.
Carnegie AJ, Ades PK, Keane PJ, Smith IW (1998) Mycosphaerella
diseases of juvenile foliage in a eucalypt species and provenance
trial in Victoria, Australia. Australian Forestry 61, 190–194.
Carnegie AJ, Johnson IA (2004) Variation among families of blackbutt
(Eucalyptus pilularis) in early growth and susceptibility to damage
from leaf spot fungi. Canadian Journal of Forest Research (in
press).
Carnegie AJ, Keane PJ (1994) Further Mycosphaerella species
associated with leaf diseases of Eucalyptus. Mycological Research
98, 413–418.
Carnegie AJ, Keane PJ, Ades PK, Smith IW (1994) Provenance
variation in Eucalyptus globulus in susceptibility to Mycosphaerella
leaf disease. Canadian Journal of Forest Research 24, 1751–1757.
Crous PW, Knox-Davies PS, Wingfield MJ (1989) A summary of
fungal leaf pathogens of Eucalyptus and the diseases they cause in
South Africa. South African Forestry Journal 149, 9–16.
Crous PW, Swart WJ (1995) Folicolous fungi of Eucalyptus spp. from
eastern Madagascar: implications for South Africa. South African
Fo re st r y 172, 1–5.
Crous PW, Wingfield MJ (1991) Eucalyptus leaf pathogens in South
Africa: a national perspective. In ‘Proceedings of the IUFRO
symposium for intensive forestry. The role of eucalypts’. Durban,
South Africa. (Ed APG Schonau) pp. 749–759.
Dick M (1982) Leaf-inhabiting fungi of eucalypts in New Zealand. New
Zealand Journal of Forestry Science 12, 525–537.
Dungey HS, Potts BM, Carnegie AJ, Ades PK (1997) Mycosphaerella
leaf diseases: genetic variation in damage to Eucalyptus nitens,
E. globulus and their F1 hybrid. Canadian Journal of Forest
Research 27, 750–759.
Felton K (1981) Eucalyptus diebacks in Tasmania. In ‘Eucalyptus
dieback in forests and woodlands’. (Eds KM Old, GA Kile, CP
Ohmart) pp. 51–54. (CSIRO Publishing: Melbourne)
Gerrettson-Cornell L, Dowden HGM (1977) Soil and leaf fungi in a
eucalypt plantation at Olney State Forest, New South Wales.
Australasian Plant Pathology Society Newsletter 6, 24–25.
Hansford GC (1954) Australian fungi. II. New species and revisions.
Proceedings of the Linnean Society of New South Wales 79, 97–141.
Heather WA (1971) Diseases in native forests. The Forestry Log 4,
25–27.
Hill KD, Johnson LAS (1995) Systematic studies in the eucalypts. 7. A
revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea
6, 173–505.
Marks GC, Fuhrer BA, Walters NEM (1982) ‘Tree diseases in Victoria.’
Forests Commission Victoria Handbook No. 1, Forests
Commission, Victoria
Neumann FG, Marks GC (1976) A synopsis of important pests and
diseases in Australian forests and forest nurseries. Australian
Fo re st r y 39, 83–102.
Old KM, Yuan ZQ (1994) ‘Foliar and stem diseases of Eucalyptus in
Vietnam and Thailand’. CSIRO Division of Forestry and ACIAR,
Australia (internal report), Canberra.
Palzer C (1978) Defoliation and death in Eucalyptus obliqua forest.
Australian Forest Research Newsletter 5, 171.
Park RF, Keane PJ, Wingfield MJ, Crous PW (2000). Fungal diseases
of eucalypt foliage. In ‘Diseases and pathogens of eucalypts’. (Eds
PJ Keane, GA Kile, FD Podger, BN Brown) pp. 153–239. (CSIRO
Publishing: Melbourne)
Parkin AM (1976) ‘The study of some aspects of leaf spots of
Eucalyptus regnans F.Muell. and Eucalyptus obliqua L’Herit.’
Honours Thesis, School of Botany, La Trobe University, Australia.
Pryor LD, Johnson LAS (1971) ‘A classification of the eucalypts.’
(Australian National University Press: Canberra)
Purnell RC, Lindquist JE (1986) Provenance variation of Eucalyptus
nitens on the Eastern Traansvaal Highveld in South Africa. South
African Forestry Journal 138, 23–31.
Sankaran KC, Sutton BC, Minter D (1995) ‘A checklist of fungi
recorded from Eucalyptus.’ Mycological Papers 170
(Commonwealth Mycological Institute: Kew)
SAS Institute Inc. (1992) ‘SAS Technical report P-229, SAS/STAT
software: changes and enhancements. Release 6.09.’ (SAS Institute
Inc.: Cary, NC)
Spooner BM (1981) New records and species of British microfungi.
Transactions of the British Mycological Society 76, 265–301.
Stefanatos A (1993) ‘A study of the severity of leaf parasites of
Eucalyptus globulus in a progeny trial and E. regnans in a
silvicultural systems trial.’ Honours Thesis, School of Botany, La
Trobe University, Australia.
Stone C, Simpson JA, Eldridge RH (1998a) Insect and fungal damage
to young Eucalypt plantings in northern New South Wales.
Australian Forestry 61, 7–20.
Stone C, Simpson JA, Gittens R (1998b) Differential impact of insect
herbivores and their fungal pathogens on the Eucalyptus subgenera
Symphyomyrtus and Monocalyptus and the genus Corymbia.
Australian Journal of Botany 46, 723–734.
Wall E, Keane PJ (1984) Leaf spot of Eucalyptus caused by
Aulographina eucalypti. Transactions of the British Mycological
Society 82, 257–273.
Wilcox MD (1982a) Preliminary selection of suitable provenances of
Eucalyptus regnans for New Zealand. New Zealand Journal of
Forestry Science 12, 468–479.
Wilcox MD (1982b) Selection of genetically superior Eucalyptus
regnans using family tests. New Zealand Journal of Forestry
Science 12, 480–493.
Wingfield MJ, Crous PW, Peredo HL (1995) A preliminary, annotated
list of foliar pathogens of Eucalyptus spp. in Chile. South African
Forestry Journal 173, 53–57.
Received 30 October 2003, accepted 10 April 2003
400 Australasian Plant Pathology A. J. Carnegie et al.
Appendix I. Herbarium specimens
Aulographina eucalypti (Cooke & Massee) Arx & Müller [anamorph: Thyrinula eucalypti (Cooke & Massee) H.J. Swart] on E. botryoides,
Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22873a); on E. brookeriana, Tostaree, Nowa Nowa, East Gippsland,
Vic., Feb. 1991, A.J. Carnegie (VPRI 22874a); on E. cypellocarpa, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI
22875a); on E. elata, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22876a); on E. fraxinoides, Tostaree, Nowa
Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22877a); on E. globulus, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J.
Carnegie (VPRI 22878a); on E. grandis, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22879a); on E. nitens,
Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22880a); on E. oreades, Tostaree, Nowa Nowa, East Gippsland, Vic.,
Feb. 1991, A.J. Carnegie (VPRI 22881a); on E. quadrangulata, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI
22882a); on E. saligna, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22883a); on E. sieberi, Tostaree, Nowa Nowa,
East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22884a); on E. smithii, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie
(VPRI 22885a); on E. viminalis, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22886a); on E. fastigata, Darlimurla,
South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24891a); on E. muelleriana, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie
(VPRI 24893a); on E. dendromorpha, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24889a); on E. melliodora, Darlimurla,
South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24892a); on E. cameronii, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie
(VPRI 24888a); on E. dunnii, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24890a); on E. badjensis, Darlimurla, South
Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24886a); on E. bosistoana, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI
24887a); on E. citriodora spp. variegata, Cavanaugh Plantation, Camira Creek, NSW, 17 Jan. 2002, A.J. Carnegie (DAR 76087); on E. cloeziana,
Inglebar Plantation, Jackadgery, NSW, 14 March 2002, A.J. Carnegie (DAR 76088); on E. punctata, University of Western Sydney, Richmond,
NSW, 15 Feb. 2002, A.J. Carnegie (DAR 76089); on E. haemastoma, University of Western Sydney, Richmond, NSW, 15 Feb. 2002, A.J. Carnegie
(DAR 76090); on E. henryi, Inglebar Plantation, Jackadgery, NSW, 17 March 2002, A.J. Carnegie (DAR 76091); on E. transcontinentalis,
Camberwell, Vic., 6 Nov. 1985, I.G. Pascoe (VPRI 12999a); on E. citridora, Mt. Gambier, S.A., Jan 1984, E. Wall, (VPRI 13237a); on E.
cyanophylla, Canberra, ACT, 9 Feb. 1982, E. Wall, (VPRI 13244a); on E. leucoxylon, Mt. Gambier, South Australia, Jan. 1984, E. Wall (VPRI
13278a); on E. phaeotricha, Mt. Gambier, South Australia, Jan. 1984, E. Wall (VPRI 13310a); on E. polyanthemos, Nowa Nowa, Vic., 1983, R.
Park (VPRI 13315a); on E. pyrocarpa, Mt. Gambier, South Australia, Jan. 1984, E. Wall (VPRI 13316a); on E. triflora, Canberra, ACT, 9 Feb.
1982, E. Wall (VPRI 13330a); on E. urnigera, Mt. Wellington, Tas., 1983, R. Park (VPRI 13335a); on E. ficifolia, Hill End, Vic., 8 Feb. 1986, I.G.
Pascoe (VPRI 13365a); on E. rupicola, Montrose, Vic., 13 Feb 1986, I.G. Pascoe (VPRI 13474a); on E. tetraptera, Cheltenham, Vic., 1 July 1986,
B.C. Sutton & I.G. Pascoe (VPRI 14039a); on E. grossa, Balwyn, Vic., 12 Aug 1986, I.G. Pascoe & B.C Sutton (VPRI 14182a); on E. stricklandii,
Balwyn, Vic., 12 Aug 1986, B.C. Sutton & I.G. Pascoe (VPRI 14184a); on E. stricklandii, The Basin, Vic., 1 Mar 2000, B. Henderson (VPRI
22326a); on E. kitsoniana, The Basin, Vic., 25 Oct 2000, B. Henderson (VPRI 22567a); on E. gunnii, Silvan South, Vic., 20 Nov 2000, B. Rowe
(VPRI 22641a); on E. platypus, Balwyn, Vic., 25 Jan 2002, V. Beilharz (VPRI 24927b); on E. cordifolia, Dural, NSW, 4 July 1964, L. Fraser (DAR
13952a); on E. eremophila, Bayview, NSW, 27 Oct. 1976, J. Walker (DAR 28265a); on E. lansdowneana, Helensburgh, NSW, 2 May 1982, P. Kable
(DAR 42078a); on E. robusta, Baulkham Hills, NSW, 2 Sep. 1984, J. Walker (DAR 50116a); on E. stricta, Mount Werong, NSW, April 1962, W.
Stahl (DAR 7088a); on E. torquata, Onooma, NSW, 12 Aug. 1976, W. Stahl (DAR 29600a).
Appendix II. Recorded hosts of Aulographina eucalypti
Eucalyptus species Eucalyptus subgenus Country Reference(s)
(Brooker 2000)A
E. agglomerata Eucalyptus Australia Gerrettson-Cornell and
Dowden (1977)
E. amplifolia Symphyomyrtus Australia Stone et al. (1998a)
E. andrewsii Eucalyptus South Africa Crous et al. (1989)
E. approximans Eucalyptus Australia Wall and Keane (1984)
E. badjensis Symphyomyrtus Australia B
E. baxteri Eucalyptus Australia Wall and Keane (1984)
E. bosistoana Symphyomyrtus Australia B
E. botryoides Symphyomyrtus Australia Marks et al. (1982), B
New Zealand M. Dick pers. comm.C
E. bridgesiana Symphyomyrtus Australia Wall and Keane (1984)
E. brookeriana Symphyomyrtus Australia B
E. caesia Symphyomyrtus Australia Wall and Keane (1984)
E. camaldulensis Symphyomyrtus Australia Wall and Keane (1984)
Vietnam Old and Yuan (1994)
E. cameronii Eucalyptus Australia B
E. citriodora Corymbia Australia B
E. citriodora spp. variegata Corymbia Australia B
E. cladocalyx Symphyomyrtus Australia Wall and Keane (1984)
E. cloeziana Idiogenes Australia Carnegie 2000, B
E. coccifera Eucalyptus UK Spooner (1981)
Aulographina eucalypti variation in Eucalyptus spp. Australasian Plant Pathology 401
Appendix II. (Continued)
Eucalyptus species Eucalyptus subgenus Country Reference(s)
(Brooker 2000)A
E. consideniana Eucalyptus Australia Wall and Keane (1984)
E. cordata Symphyomyrtus Australia Barber et al. (2003)
E. cordifolia Angophora Australia B
E. cosmophylla Symphyomyrtus Australia Hansford (1954)
E. costata Angophora Australia Wall and Keane (1984)
E. cyanophylla Symphyomyrtus Australia B
E. cypellocarpa Symphyomyrtus Australia Marks et al. (1982), B
E. dalrympleana Symphyomyrtus Australia Wall and Keane (1984)
South Africa Crous et al. (1989)
E. delegatensis Eucalyptus Australia Marks et al. (1982)
New Zealand Dick (1982)
South Africa Crous et al. (1989)
E. dendromorpha Eucalyptus Australia B
New Zealand M. Dick pers. comm.
E. diversicolor Symphyomyrtus New Zealand M. Dick pers. comm.
E. dives Eucalyptus Australia Burdon and Chilvers (1964)
E. dunnii Symphyomyrtus Australia B
E. elata Eucalyptus South Africa Crous et al. (1989)
Australia B
E. eremophila Symphyomyrtus Australia B
E. fastigata Eucalyptus New Zealand Dick (1982)
South Africa Crous and Wingfield (1991)
Australia Stone et al. (1998a)
E. ficifolia Corymbia Australia B
New Zealand M. Dick pers. comm.
E. fraxinoides Eucalyptus New Zealand Dick (1982)
South Africa Crous and Wingfield (1991)
Australia Stone et al. (1998a), B
E. globoidea Eucalyptus Australia Marks et al. (1982)
South Africa Crous et al. (1989)
E. globulus Symphyomyrtus Australia Marks et al. (1982), B
(includes 4 subsp.) USA Wall and Keane (1984)
South Africa Crous et al. (1989)
Chile Wingfield et al. (1995)
E. grandis Symphyomyrtus Australia Wall and Keane (1984), B
New Zealand M. Dick pers. comm.
E. gregsoniana Eucalyptus Australia Wall and Keane (1984)
E. grossa Symphyomyrtus Australia B
E. gunnii Symphyomyrtus Australia B
E. haemastoma Eucalyptus Australia B
E. henryi Corymbia Australia B
E. johnstonii Symphyomyrtus Australia Wall and Keane (1984)
E. kitsoniana Symphyomyrtus Australia B
E. laevopinea Eucalyptus Australia Stone et al. (1998a)
E. lansdowneana Symphyomyrtus Australia B
E. lehmannii Symphyomyrtus Australia Wall and Keane (1984)
E. leucoxylon Symphyomyrtus Australia B
E. macarthurii Symphyomyrtus South Africa Crous et al. (1989)
E. macrorrhyncha Eucalyptus Australia Wall and Keane (1984)
E. maculata Corymbia Australia Marks et al. (1982)
E. marginata Eucalyptus Australia Hansford (1954)
E. melliodora Symphyomyrtus Australia B
E. microcorys Alveolata Australia Marks et al. (1982)
E. moluccana Symphyomyrtus South Africa Crous et al. (1989)
E. muelleriana Eucalyptus South Africa Crous et al. (1989)
Australia B
New Zealand M. Dick pers. comm.
402 Australasian Plant Pathology A. J. Carnegie et al.
http://www.publish.csiro.au/journals/app
Appendix II. (Continued)
Eucalyptus species Eucalyptus subgenus Country Reference(s)
(Brooker 2000)A
E. nitens Symphyomyrtus Australia Marks et al. (1982), B
New Zealand Dick (1982)
South Africa Crous et al. (1989)
E. nitidia Eucalyptus Australia Wall and Keane (1984)
E. obliqua Eucalyptus Australia Marks et al. (1982)
South Africa Crous et al. (1989)
New Zealand M. Dick pers. comm.
E. oreades Eucalyptus South Africa Crous et al. (1989)
Australia B
E. pauciflora Eucalyptus Australia Burdon and Chilvers (1964)
New Zealand M. Dick pers. comm.
E. perriniana Symphyomyrtus Australia Wall and Keane (1984)
E. phaeotricha Eucalyptus Australia B
E. pilularis Eucalyptus Australia Marks et al. (1982)
South Africa Crous et al. (1989)
New Zealand M. Dick pers. comm.
E. platypus Symphyomyrtus Australia B
E. polyanthemos Symphyomyrtus Australia B
E. punctata Symphyomyrtus Australia B
E. pyrocarpa Eucalyptus Australia B
E. quadrangulata Symphyomyrtus South Africa Crous et al. (1989)
Australia B
E. radiata Eucalyptus Australia Burdon and Chilvers (1964)
E. regnans Eucalyptus Australia Marks et al. (1982)
New Zealand Dick (1982)
South Africa Crous et al. (1989)
E. resinifera Symphyomyrtus Australia Marks et al. (1982)
South Africa Crous et al. (1989)
E. robusta Symphyomyrtus Australia B
New Zealand M. Dick pers. comm.
E. saligna Symphyomyrtus USA Wall and Keane (1984)
South Africa Crous et al. (1989)
Australia B
New Zealand M. Dick pers. comm.
E. sieberi Eucalyptus Australia Marks et al. (1982), B
E. smithii Symphyomyrtus Australia B
E. stellulata Eucalyptus Australia Wall and Keane (1984)
E. stricklandii Symphyomyrtus Australia B
E. stricta Eucalyptus Australia B
E. tenuiramis Eucalyptus New Zealand M. Dick pers. comm.
E. tetragona Eudesmia Australia Wall and Keane (1984)
E. tetraptera Symphyomyrtus Australia B
E. torquata Symphyomyrtus Australia B
E. transcontinentalis Symphyomyrtus Australia B
E. triflora Eucalyptus Australia B
E. urnigera Symphyomyrtus Australia B
E. viminalis Symphyomyrtus Australia Marks et al. (1982), B
New Zealand M. Dick pers. comm.
E. woodwardii Symphyomyrtus Australia Wall and Keane (1984)
A
The classification of genus Eucalyptus here follows Brooker (2000), and includes subgenus Corymbia
(formerly a genus, Hill and Johnson 1995), subgenus Eucalyptus (formerly subgenus Monocalyptus, Pryor and
Johnson 1971) and subgenus Angophora (formerly a genus, Pryor and Johnson 1971).
BRecorded in present study.
CDr Margaret Dick, Forest Research, New Zealand.
