Content uploaded by Angus Carnegie
Author content
All content in this area was uploaded by Angus Carnegie on Oct 16, 2014
Content may be subject to copyright.
Rapidly expanding host range for Puccinia psidii sensu lato
in Australia
Angus J. Carnegie &Jonathan R. Lidbetter
Received: 24 March 2011 /Accepted: 3 August 2011 /Published online: 26 August 2011
#Australasian Plant Pathology Society Inc. 2011
Abstract A rust affecting Myrtaceae was recently detected
in New South Wales, Australia. Based on urediniospore
morphology and host range, it was identified as Uredo
rangelii, a taxon regarded as a member of the eucalyptus/
guava rust (Puccinia psidii sensu lato) complex, although
confusion currently surrounds its taxonomy. The exotic rust
was given the common name of myrtle rust to distinguish it
from eucalyptus/guava rust. The more recent discovery of
teliospores in NSW that match those of P. psidii sensu
stricto indicates the rust in Australia is a strain (with
tonsured urediniospores) of P. psidii s.l. Outside Australia,
P. psidii has a wide host range within Myrtaceae, being
reported from 129 species in 33 genera, and is very
damaging in South and Central America–including in
eucalypt plantations in Brazil–the Caribbean and in Florida
and Hawaii. To ascertain the potential threat to forestry in
Australia posed by the introduced rust, we tested key
forestry species, as well as key known hosts of eucalyptus/
guava rust, in artificial inoculation experiments. We showed
that several species of Eucalyptus are susceptible (viz. E.
pilularis, E. cloeziana, E. agglomerata and E. grandis), as
is Melaleuca quinquenervia. Observations during testing
revealed a lengthened latent period (from inoculation until
pustule formation and eruption) of four to five weeks
during winter. Here we also report on observations on new
hosts from surveys in NSW under the emergency response
that followed the detection of the exotic rust, and surveys in
NSW and Queensland following the cessation of the
emergency response. In Australia, P. psidii s.l. has currently
been found on 107 host species in 30 genera during
surveys, including species in Angophora, Asteromyrtus,
Austromyrtus, Backhousia, Callistemon, Chamelaucium,
Choricarpia, Decaspermum, Eucalyptus, Eugenia, Gossia,
Lenwebbia, Leptospermum, Lophomyrtus, Melaleuca, Met-
rosideros, Myrtus, Pilidiostigma, Rhodamnia, Rhodomyr-
tus, Ristantia, Stockwellia, Syncarpia, Syzygium, Tristania,
Tristaniopsis, Ugni, Uromyrtus and Xanthostemon. Species
under cultivation (in nurseries and gardens) that are
severely affected include Gossia inophloia, Agonis flex-
uosa, Syzygium jambos and S. anisatum while species that
are severely damaged in native bushland include Rhodam-
nia rubescens, Rhodomyrtus psidioides,Choricarpia lep-
topetala and Melaleuca quinquenervia.
Keywords Biosecurity .Host testing .Surveillance .Exotic
rust
Introduction
In April 2010, an exotic rust of Myrtaceae was detected on
the Central Coast of New South Wales (NSW), Australia,
and identified as Uredo rangelii based on the presence of a
tonsure (smooth patch) on urediniospores (Carnegie et al.
2010). Uredo rangelii has been described as a taxon within
the Puccinia psidii sensu lato (eucalyptus/guava rust)
complex, due to its morphological similarities to P. psidii
sensu stricto (Simpson et al. 2006). To distinguish the
disease from eucalyptus/guava rust authorities managing
the incursion named it myrtle rust (Department of Agricul-
A. J. Carnegie (*)
Forest Biosecurity & Productivity Assessment,
NSW Department of Primary Industries, Forest Science Centre,
PO Box 100, Beecroft, NSW 2119, Australia
e-mail: angus.carnegie@industry.nsw.gov.au
J. R. Lidbetter
Forest and Rangelands Ecosystems,
NSW Department of Primary Industries, Forest Science Centre,
P.O. Box 100,
Beecroft 2119 NSW, Australia
Australasian Plant Pathol. (2012) 41:13–29
DOI 10.1007/s13313-011-0082-6
ture, Fisheries and Forestry 2010a), based on the host of the
type specimen for U. rangelii,Myrtus communis. During
the initial surveys of the incursion, U. rangelii was found
on Agonis flexuosa, Callistemon viminalis and Syncarpia
glomulifera in NSW (Carnegie et al. 2010), being previ-
ously known only from M. communis and Syzygium jambos
(Simpson et al. 2006).
There has been debate over the correct name of the
introduced rust in Australia, and several authors do not
regard the morphological features used by Simpson et al.
(2006) as sufficient to warrant retaining U. rangelii as a
separate species (Glen et al. 2007; Global Invasive Species
Network 2010; Ramsfield et al. 2010). Furthermore,
teliospores of the introduced rust have recently been
observed in Australia and Carnegie and Cooper (2011)
discuss the taxonomic implications of this. Briefly, Simpson
et al. (2006) described the uredinial state with tonsure as U.
rangelii, but this name has no precedent for a rust with
teliospores. Now that Puccinia-like teliospores have been
found, the introduced rust in Australia should be referred to
under a Puccinia name, and the only name available in this
genus is P. psidii s.l. It is believed that currently there is
only one of the numerous strains of P. psidii s.l. present in
Australia, and this has urediniospores with a tonsure
(Carnegie and Cooper 2011). The emergency response to
P. psidii s.l. in NSW has been summarised by Carnegie and
Cooper (2011).
Outside Australia, P. psidii s.l. has a wide host range,
being reported from 129 species from 33 genera within
Myrtaceae (Appendix I). It has been reported from the
majority of countries in South and Central America, and
from Florida, California and Hawaii in the United States,
and is considered a significant threat to Australia (Glen et
al. 2007; Grgurinovic et al. 2006; Office of the Chief Plant
Protection Officer 2007). Previous authors have conducted
host susceptibility tests for P. psidii s.l. outside Australia
with a range of myrtaceous species (e.g. Dianese et al.
1984,1986; Rayachhetry et al. 2001; Alfenas et al. 2003;
Tommerup et al. 2003; Zauza et al. 2010). Several studies
have determined conditions for spore germination and
infection (e.g. de Piza and Ribeiro 1988; Ruiz et al.
1989), and although there is some variation amongst
studies, it is generally agreed that optimum conditions are
15–25°C, high humidity or leaf wetness for up to 8 h, low
light or darkness, with infection only occurring on
immature foliage. Continued ambient temperatures and
high humidity are then generally required, with uredinial
pustules and sporulation observed within 10–12 days
(Marlatt and Kimbrough 1979; Rayachhetry et al. 1997;
Alfenas et al. 2003).
Due in part to the ambiguity between the historical host
range of ‘U. rangelii’and P. psidii s.l. (since they were only
separated recently [Simpson et al. 2006]), as well as the
taxonomic confusion between these taxa, the aim of this
study was to test a range of myrtaceous species for
susceptibility to the introduced rust to ascertain whether it
could be a threat to forestry in Australia. The work conducted
here was an interim study to provide quick answers during
the early period of the incursion on key questions on the host
range of this exotic myrtaceous rust and thus its potential
impact on the native environment and the forest industry.
Here we also report new host records and observations from
surveys of the introduced rust in NSW and Queensland
reported on the NSW Department of Primary Industries
Biosecurity website (http://dpi.nsw.gov.au/biosecurity/plant/
myrtle-rust) and the Biosecurity Queensland website (http://
www.dpi.qld.gov.au/4790_19789.htm).
Methods
Test plants and inoculation
As the main aim of this study was to ascertain whether the
introduced rust could be a threat to forestry in Australia, the
species we selected were key commercial eucalypt species
in Australia: Eucalyptus agglomerata, E. cloeziana, E.
globulus, E. grandis, E. pilularis and Corymbia maculata
(Table 1). We were, however, restricted by availability of
suitable host material at short notice, so not all key species
were tested (e.g. E. dunnii, E. nitens, E. regnans, C.
citriodora subsp. variegata). Melaleuca quinquenervia was
also tested, as it is a known highly susceptible host of P.
psidii (Rayachhetry et al. 2001). Agonis flexuosa cv.
‘Afterdark’was used as a control, as it is highly susceptible
to the introduced rust in Australia (Carnegie et al. 2010).
Eucalypt seedlings were potted into 150 mm pots using
native potting mix and kept in a glass house until used, with
watering twice a day. A. flexuosa ‘Afterdark’plants were
sourced as either 150 mm pots or 200 mm pots. Two
200 mm pots of M. quinquenervia were also used. Plants to
be tested were selected to ensure they had fresh new growth
(immature leaves).
The eight species were tested in four experiments. Due to
biosecurity concerns, three experiments were conducted in
situ at IP1 (Infected Premises 1–the first property where P.
psidii s.l. was detected in Australia, on the Central Coast of
NSW) and the fourth in a Biological Safety Cabinet (Class
II) at the NSW DPI (forestry) laboratories at West Pennant
Hills, Sydney. For inoculation preparation, diseased A.
flexuosa ‘Afterdark’and/or S. glomulifera leaves and shoots,
with fresh uredinial pustules containing urediniospores, were
collected from IP1. In most cases, material was either
collected the same day as inoculations or a day or two
previously and kept in a fridge prior to inoculations.
Urediniospores were scraped from uredinial pustules using
14 A.J. Carnegie, J.R. Lidbetter
a clean scalpel such that they “dusted”onto immature leaves;
in some cases scraped urediniospores were gently wiped
onto immature leaves with the scalpel. In most cases, yellow
urediniospores could be seen on inoculated leaves either with
the naked eye or a 10× hand lens.
Experiment I
This experiment relied on natural infection from diseased
trees at IP1, and began in May 2010. Nine potted plants
each of E. agglomerata, E. cloeziana, E. grandis, E.
pilularis, C. maculata and A. flexuosa ‘Afterdark’were
placed under infected S. glomulifera and misted with water.
Although fungicide spraying had occurred at IP1 prior to
this experiment (as part of the emergency response), the
western side of the S. glomulifera had not been sprayed,
and so plants were located under diseased branches–with
freshly sporulating uredinial pustules present on leaves–on
the western side of trees. Test plants were moved after 48 h
into a shade house (due to an impending fungicide spray
operation), where they were misted twice-daily for 30 mins
in the morning and early evening. Plants were inspected
weekly for evidence of rust infection.
Experiment II
In this experiment we attempted to increase the chance of
infection by artificially inoculating plants with urediniospores
freshly collected from diseased S. glomulifera and by
maintainingleafwetnessforupto48h.Itwasagain
conducted at IP1, beginning in May 2010. Three potted
plants each of E. agglomerata, E. cloeziana, E. grandis, E.
pilularis, C. maculata and A. flexuosa ‘Afterdark’were
misted with water to ensure leaf wetness on immature leaves
and inoculated as described above. Inoculated plants were
then covered with clear plastic bags, which were misted with
water inside to increase humidity, and left outside. After 48 h,
most plants (and plastic bags) were still moist, and plants
were moved into a shade house, where they were misted
twice-daily for 30 mins in the morning and early evening.
Plants were inspected weekly for evidence of rust infection.
Experiment III
This was again performed at IP1, beginning in late May 2010.
A temporary inoculation chamber (1500 mm×1000 mm×
750 mm) was constructed out of black plastic and a wooden
frame and housed in a greenhouse located at IP1. Three plants
each of E. agglomerata, E. cloeziana, E. globulus, E. grandis,
E. pilularis, C. maculata, A. flexuosa ‘Afterdark’and a single
plant of M. quinquenervia were misted with water to ensure
leaf wetness on immature leaves and inoculated as above.
Plants were then placed inside the temporary inoculation
chamber, the walls of the chamber misted with water to
increase humidity, and the door sealed. Temperature within
the temporary inoculation chamber during this time ranged
from 7–25°C. This method allowed optimum temperatures
for infection (which only occur during the daytime in May in
this region) to be matched with darkness and leaf wetness.
After 72 h, most plants still had moist leaves and were moved
from the temporary inoculation chamber to a bench within
the greenhouse and misted for 5 s every hour. Plants were
inspected weekly for evidence of rust infection. Temperatures
within the greenhouse during early June ranged from 5–25°C
and in late June from 0–29°C.
Experiment IV
In this experiment, conducted in June 2010, we conducted
what we believe is a new method: using cuttings in
Table 1 Results of inoculation experiments (Experiments III & IV) with P. psidii sensu lato on a range of hosts
Species Provenance/Cultivar Inoculation Chamber at IP1
(Experiment III)
Cuttings in tissue culture jars
b
(Experiment IV)
Susceptible
Agonis flexuosa ‘Afterdark’3/3
a
2/3 +
Eucalyptus
agglomerata
Olney State Forest,
NSW
2/3 –+
E. cloeziana Gympie, Queensland 1/3 1/2 +
E. globulus unknown 0/3 0/2
E. grandis Bulahdelah, NSW 1/3 0/2 +
E. pilularis Newry State Forest,
NSW
1/3 –+
Corymbia maculata unknown 0/3 0/2
Melaleuca
quinquenervia
unknown 0/1 1/2 +
a
Number of plants observed with rust out of (/) total plants tested
b
Experiment using fresh inoculum
Rapidly expanding host range for Puccinia psidii sensu lato 15
polycarbonate (tissue culture) jars. Young shoots from
actively growing seedlings were cut and immediately
inserted into 1.5% or 2% water agar in 500 ml polycarbon-
ate jars (Fig. 1a–b). Six species were used for this
experiment: E. globulus, E. cloeziana, E. grandis, C.
maculata, M. quinquenervia and A. flexuosa ‘Afterdark’.
Initially we used “old”inoculum of P. psidii s.l. from both
A. flexuosa ‘Afterdark’and S. glomulifera leaves collected
a month or so previously from IP1 and air dried and stored
in herbarium envelopes. We then repeated the experiment
using “fresh”inoculum (actively sporulating pustules)
collected from potted plants of A. flexuosa ‘Afterdark’in
the greenhouse at IP1 and kept in a paper bag in the fridge
overnight. Viability of inoculum was tested by brushing
urediniospores onto 2% water agar in a Petri dish and
observing germination after 24 h.
Cuttings were first misted with sterilised water (with
Tween 20 added) to moisten actively growing leaves and
inoculated as above. Jars were sealed with parafilm and
placed into plastic zip-lock bags which were misted with
water then sealed (Fig. 1a–b). Due to limited inoculum,
only two cuttings of each species were inoculated, with
three cuttings of the A. flexuosa ‘Afterdark’inoculated. To
enhance biosecurity, inoculations were conducted in a
Biological Safety Cabinet (Class II) (Fig. 1b) at the Forest
Science Centre, NSW DPI, West Pennant Hills. Inoculated
cuttings were then left in the Biological Safety Cabinet,
with the glass covered to ensure darkness, for 24 h. The
temperature within the Biological Safety Cabinet over this
period ranged from 17–26°C, with the first 8 h being 21–
26°C. After 24 h, leaves on most cuttings were still moist.
The sealed jars (still within zip-lock bags) were then placed
on a laboratory bench in a secure room (i.e. restricted
access) with natural light and a temperature range of 14–
26°C. Cuttings were inspected regularly for presence of rust
pustules for two weeks.
Suspect positive samples from artificial inoculations
were sent to Dr Michael Priest at the NSW Plant Pathology
Herbarium (DAR) in Orange, NSW, for confirmation.
Positive samples are lodged at DAR.
Surveillance for P. psidii s.l. in NSW
Surveys for P. psidii s.l., as reported by Carnegie et al.
(2010)—on IPs, native forest within and surrounding IPs,
and of non-IP nurseries on the Central Coast–continued to
22 December 2010 (Carnegie and Cooper 2011). Surveil-
lance from April to mid-August 2010 was conducted
mainly by NSW DPI forest research staff, but from mid-
August onwards surveillance intensity increased signifi-
cantly (Carnegie and Cooper 2011) after the National
Management Group approved the Interim Response Plan
for Myrtle Rust (Department of Agriculture, Fisheries and
Forestry 2010b). The majority of myrtaceous species were
surveyed at each site visit, with multiple surveys on IPs and
high risk sites. Here we report on new host records or
significant findings from surveys to mid-August. We also
include new hosts records from surveys under the emer-
gency response in NSW, and ongoing surveys in both NSW
and Queensland since the emergency response was stood
down (Carnegie and Cooper 2011), which are reported on
http://dpi.nsw.gov.au/biosecurity/plant/myrtle-rust and
http://www.dpi.qld.gov.au/4790_19789.htm. Many of the
species on the NSW website have been recorded as a result
of reporting through general surveillance mechanisms,
including the biosecurity email and Exotic Plant Pest
hotline, which then enabled NSW DPI to validate the
report through the NSW Plant Health Diagnostic Service.
Voucher specimens of P. psidii s.l. on the majority of hosts
have been lodged at DAR.
Results
Experiment I & Experiment II
No evidence of infection (purpling or uredinial pustules)
was observed on any plant, including the A. flexuosa
‘Afterdark’, at one, two, three or four weeks, or at eight
weeks after inoculation. The fact that the A. flexuosa
‘Afterdark’was not infected, and that there was evidence of
a b
Fig. 1 a–bPolycarbonate jars
(tissue culture jars) with cuttings
placed in water agar and inocu-
lated with P. psidii sensu lato
within a Biological Safety
Cabinet (Experiment IV)
16 A.J. Carnegie, J.R. Lidbetter
infection on planted A. flexuosa cv. ‘Afterdark’at IP1
during this time (Carnegie, unpublished), indicates that
neither of these techniques worked, suggesting the optimum
conditions for infection were not obtained. All plant
material used in these two experiments was sprayed with
the fungicide Bayfidan
®
after 8 weeks and destroyed,
following biosecurity procedures.
Experiment III
After two weeks there was no evidence of infection on the
A. flexuosa ‘Afterdark’, but chlorotic to purple spots and
blotches were observed on leaves of one plant each of E.
pilularis and E. cloeziana. No rust pustules were associated
with this discolouration at this time. No change had
occurred after three weeks; but at four weeks, uredinial
pustules were observed on the three inoculated A. flexuosa
‘Afterdark’. There was still no evidence (using a 10× hand
lens) of uredinial pustules on the now purple spots and
blotches on the E. pilularis and E. cloeziana at four weeks.
Plants were not inspected in week five; but after six weeks
uredinial pustules were observed on the purple spots and
blotches of the E. pilularis (Fig. 2a–b) and E. cloeziana
(Fig. 2c). On both hosts sporulation was more prevalent on
the lower leaf surface. Also at six weeks, purple spots were
now observed on two plants of E. agglomerata and a single
plant of E. grandis, but there was no evidence (using a 10×
hand lens) of uredinial pustules on these plants.Later
examination under a dissecting then compound microscope
identified these spots as being associated with P. psidii s.l.
pustules and urediniospores, and rust on the A. flexuosa
‘Afterdark’,E. cloeziana and E. pilularis was confirmed as
P. psidii s.l. No other species inoculated showed any
evidence of infection (Table 1). Samples were collected
ba
c d
e f
Fig. 2 Symptoms of P. psidii
sensu lato on various hosts
following artificial inoculation
in Experiment III (a–c) and
Experiment IV (d–e). (a–b)
Eucalyptus pilularis, adaxial (a)
and abaxial (b) leaf surface; (c)
adaxial surface of E. cloeziana;
(d)Agonis flexuosa ‘Afterdark;
(e)E. cloeziana;
(f)Melaleuca quinquenervia
Rapidly expanding host range for Puccinia psidii sensu lato 17
from E. pilularis, E. cloeziana, E. agglomerata, E. grandis
and A. flexuosa ‘Afterdark’for confirmation, then all plants
were sprayed with Bayfidan
®
and then destroyed, following
biosecurity procedures.
Experiment IV
In most instances the cuttings remained healthy for the
duration of the experiment. However, some plants lost a
few leaves prematurely after 2 weeks, and some plants
became infected with fungi that were likely inhabiting
plants prior to cutting and placing in the tissue culture
jars. After 24 h on water agar, ~5% of urediniospores
from the “old”, air-dried inoculum had germinated,
while ~25% had germinated from the “fresh”inoculum.
No evidence of infection (purpling or uredinial pustules)
was observed after two weeks using the “old”inoculum.
However, using the “fresh”inoculum, uredinial pustules
were observed after two weeks on two of the three
cuttings of A. flexuosa ‘Afterdark’(Fig. 2d), one cutting
of E. cloeziana (Fig. 2e) and one of the M. quinquenervia
cuttings (Fig. 2f). No evidence of infection (purpling
or uredinial pustules) was observed on any other host
tested (Table 1). Rust pustules on A. flexuosa ‘Afterdark’,
E. cloeziana and M. quinquenervia were confirmed as
P. p s i d i i s.l.
Surveillance for P. psidii s.l. in NSW
Repeat surveys of IPs in July revealed three new hosts
for P. psidii s.l. in NSW (Table 2).On 19 July we
observed rust on Tristania neriifolia at IP2. Symptoms on
T. neriifolia included purple spots with old grey pustules
on mature leaves to freshly (golden yellow) sporulating
pustules on growing shoots (Fig. 3a). It is interesting to
note that we were still observing actively sporulating
pustules in mid-winter. Microscopic examination revealed
both urediniospores and teliospores within pustules.
Morphology of these teliospores matched the description
of P. psidii s.s. by Walker (1983). On 21 July a repeat
survey on IP1 identified two small spots typical of old P.
psidii s.l. infection (dark purple to brown spots with a
single grey blister-like pustule) on two plants of Lepto-
spermum rotundifolium (Fig. 3b).This species had been
surveyed on previous occasions at IP1, as well as other
hosts, including Kunzea spp., Melaleuca huegelii and
Regelia velutina. We also observed what appeared to be a
single old pustule on Beaufortia sparsa, but there was not
enough material to make a positive identification. On 26
July an extensive survey of approx. 10,000 plants at IP4,
covering all Myrtaceae at the nursery (including Callis-
temon spp., Syzygium spp. and Metrosideros spp.),
revealed a single spot on a single plant of Syzygium
‘Cascade’(S. wilsonii subsp. wilsonii × S. leuhmanii)that
was suspected as an old P. psidii s.l. pustule (Fig. 3c).
This was later confirmed, with teliospores identified
within the pustule. As above, plants of Syzygium
‘Cascade’had been inspected during previous surveys.
On 13 August a survey of a nursery not previously
surveyed, but in close proximity to IP3, identified P. psidii
s.l. on Metrosideros collina,Gossia (formerly Austro-
myrtus)inophloia ‘Aurora’and G. inophloia ‘Blushing
Beauty’, making this property IP6. On M. collina,
symptoms included purple flecks and spots with both
old and fresh pustules on leaves, as well as fresh pustules
on new shoots (Fig. 3d). On G. inophloia, which appears
to be a highly susceptible species, symptoms included
large old pustules interspersed within multiple small,
fresh pustules on expanded leaves, to severe and fresh
infection on expanding foliage (Fig. 3e). All collections
from surveys were confirmed as P. psidii s.l. and have
been lodged at DAR.
Surveys since mid-August have revealed many more
infected premises and added more than 95 hosts (Table 2);
this increasing host list was a trigger to stand down the
emergency response (Carnegie and Cooper 2011). These
surveys identified the first record of P. psidii s.l. on M.
quinquenervia,S. glomulifera and Eucalyptus species in the
native environment in Australia, previously identified only
in trees/plants under cultivation or in host testing. Initially,
the majority of new hosts for P. psidii s.l. in Australia were
identified from cultivated plants (in nurseries, gardens and
parks), but once the rust was found in bushland and began
to spread rapidly, many new host records were from
bushland.
Field surveys indicate that G. inophloia,A. flexuosa,
Syzygium jambos and S. anisatum are highly susceptible
cultivated species, while Rhodamnia rubescens (Fig. 3f–g),
Rhodomyrtus psidioides, Choricarpia leptopetala and Mela-
leuca quinquenervia are highly susceptible species in native
forests or bushland. Rhodamnia rubescens was the first
species known to have fruit infected by the rust (Fig. 3g,
inset), with G. inophloia and Rhodomyrtus psidioides also
recently found with infected fruit.
Here we also update the known hosts of P. psidii outside
Australia (Appendix I), based on published records, to
include 129 species in 33 genera within nine tribes. This
includes 87 species of Australian Myrtaceae.
Discussion
The work reported here, including surveys in NSW
carried out under the emergency response since mid-
August and ongoing surveys in both NSW and Queens-
land once the emergency response was stood down,
18 A.J. Carnegie, J.R. Lidbetter
Table 2 Current known hosts of Puccinia psidii sensu lato in Australia based on surveys in NSW
a
and Queensland
b
and host testing reported here.
Plant names according to Govaerts et al. (2011)
Tribe
c
Host
*
of Puccinia psidii s.l. in Australia
Xanthostemoneae
(3)
Xanthostemon chrysanthus (F.Muell.) Benth.
X. oppositifolius F.M.Bailey
X. youngii C.T.White & W.D.Francis
Melaleuceae (6) Callistemon pachyphyllus Cheel (Syn. Melaleuca pachyphylla (Cheel) Craven)
C. polandii F.M.Bailey (Syn. Melaleuca polandii (F.M.Bailey) Craven)
C. salignus (Sm.) Colv. ex Sweet
C. viminalis (Sol. ex Gaertn.) G.Don ex Loudon
C. viminalis xC. citrinus (Curtis) Skeels
Melaleuca alternifolia (Maiden & Betche) Cheel
M. decora (Salisb.) Britten
M. fluviatilis Barlow
M. leucadendra (L.) L.
M. linariifolia Sm.
M. nesophila F.Muell.
M. nodosa (Sol. ex Gaertn.) Sm.
M. quinquenervia (Cav.) S.T.Blake
M. saligna Schauer
M. sieberi Schauer
Kanieae (7) Ristantia waterhousei P.G.Wilson & J.T.Waterh.
Tristaniopsis laurina (Sm.) P.G.Wilson & J.T.Waterh. (Syn. Tristania laurina (Sm.) R.Br.)
Backhousieae (8) Backhousia angustifolia F.Muell.
B. citriodora F.Muell.
B. myrtifolia Hook. & Harv.
B. sciadophora F.Muell.
B. sp. ‘Prince Regent’
d
(W.O'Sullivan & D.Dureau WODD 42) WA Herbarium
Choricarpia leptopetala (F.Muell.) Domin
C. subargentea (C.T.White) L.A.S.Johnson
Metrosidereae (9) Metrosideros collina (J.R.Forst. & G.Forst.) A.Gray
M. excelsa Sol. ex Gaertn.
M. kermadecensis W.R.B.Oliv.
Tristanieae (10) Tristania neriifolia (Sieber ex Sims) R.Br.
Syzygieae (11) Syzygium anisatum (Vickery) Craven & Biffin (Syn. Backhousia anisata Vickery, Anetholea anisata (Vickery) P.G.
Wilson)
S. armstrongii (Benth.) B.Hyland
S. australe (J.C.Wendl. ex Link) B.Hyland
S. bamagense B.Hyland
S. canicortex B.Hyland
S. ‘Cascade’(S. wilsonii (F.Muell.) B.Hyland subsp. wilsonii × S. luehmannii (F.Muell.) L.A.S.Johnson)
S. claviflorum (Roxb.) Wall. ex A.M.Cowan & Cowan (Syn. Acmenosperma claviflorum (Roxb.) Kausel)
S. corynanthum (F.Muell.) L.A.S.Johnson
S. eucalyptoides (F.Muell.) B.Hyland
S. floribundum F.Muell. (Syn. Waterhousea floribunda (F.Muell.) B.Hyland)
S. hedraiophyllum (F.Muell.) Craven & Biffin (Syn. Waterhousea hedraiophylla (F.Muell.) B.Hyland)
S. hemilamprum (F.Muell.) Craven & Biffin (Syn, Acmena hemilampra (F.Muell.) Merr. & L.M.Perry)
S. jambos (L.) Alston
Syzygium luehmannii (F. Muell.) L.A.S.Johnson
S. maraca Craven & Biffin
S. moorei (F.Muell.) L.A.S.Johnson
Rapidly expanding host range for Puccinia psidii sensu lato 19
Table 2 (continued)
Tribe
c
Host
*
of Puccinia psidii s.l. in Australia
S. mulgraveanum (B.Hyland) Craven & Biffin (Syn. Waterhousea mulgraveana B.Hyland)
S. oleosum (F.Muell.) B.Hyland
S. paniculatum Gaertn.
S. pseudofastigiatum B.Hyland
S. rubrimolle B.Hyland
S. smithii (Poir.) Nied.
S. tierneyanum (F.Muell.) T.G.Hartley & L.M.Perry
S. xerampelinum B.Hyland
Myrteae (12) Austromyrtus dulcis (C.T.White) L.S.Sm.
A. tenuifolia (Sm.) Burret
Decaspermum humile (Sweet ex G.Don) A.J.Scott
Eugenia reinwardtiana (Blume) A.Cunn. ex DC.
Gossia acmenoides (F.Muell.) N.Snow & Guymer
G. bidwillii (Benth.) N.Snow & Guymer (Syn. Austromyrtus bidwillii (Benth.) Burret)
G. floribunda (A.J.Scott) N. Snow & Guymer
G. fragrantissima (F.Muell. Ex Benth.) N.Snow & Guymer
G. gonoclada (F.Muell. Ex Benth.) N.Snow & Guymer
G. hillii (Benth.) N.Snow & Guymer (Syn. Austromyrtus hillii (Benth.) Burret)
G. inophloia (J.F.Bailey & C.T.White) N.Snow & Guymer (Syn. Austromyrtus inophloia (J.F.Bailey & C.T.White) Burret)
G. macilwraithensis N.Snow & Guymer
G. punctata N.Snow & Guymer
Lenwebbia lasioclada (F.Muell.) N.Snow & Guymer
L. prominens N.Snow & Guymer
L. sp. ‘Blackall Range’
d
(P.R.Sharpe 5387) Qld Herbarium sensu Bean, A.R. Guymer, G.P. & Jessup, L.W. (2007)
Lophomyrtus bullata Burret
L. xralphii (Hook.f.) Burret
Myrtus communis L.
Pilidiostigma glabrum Burret
P. rhytispermum (F.Muell.) Burret
Rhodamnia angustifolia N.Snow & Guymer
R. arenaria N.Snow
R. argentea Benth.
R. costata A.J.Scott
R. dumicola Guymer & Jessup
R. glabrescens Guymer & Jessup
R. glauca Blume (Syn. R. spongiosa (F.M.Bailey) Domin)
R. maideniana C.T.White
R. pauciovulata Guymer
R. rubescens (Benth.) Miq.
R. sessiliflora Benth.
Rhodomyrtus macrocarpa Benth.
R. psidioides (G.Don) Benth.
R. tomentosa (Aiton) Hassk
R. trineura subsp. capensis Guymer
R. trineura var. canescens (C.T.White & W.D.Francis) A.J.Scott (Syn. R.canescens C.T.White)
Ugni molinae Turcz
Uromyrtus australis A.J.Scott
U. lamingtonensis N.Snow & Guymer
U. tenella N.Snow & Guymer
20 A.J. Carnegie, J.R. Lidbetter
expands the host range of P. psidii s.l. in Australia to
include 109 species (including host testing) and 30 genera
in 12 of the 17 tribes within Myrtaceae (Table 2), as well
as two hybrids. Seventy-eight species, four tribes and 16
genera are new records for the eucalyptus/guava rust
complex, culminating in a total for the eucalyptus/guava
rust complex worldwide of 207 host species. This rapidly
expanding host range is likely to increase with further
host testing underway at CSIRO in Canberra (L. Morin,
CSIRO, unpublished) and as the introduced rust spreads
further in Australia’s Myrtaceae-rich ecosystems. Similar
rapid host range expansion has been observed for P. psidii
as it established in other new areas, such as in Jamaica,
Florida and Hawaii (MacLachlan 1938; Rayachhetry et al.
2001; Leahy 2004; Loope 2010), but the incursion in
Australia has seen the fastest accumulation of hosts for
this rust. It is likely that the present strain of P. psidii s.l.
in Australia will eventually have a greater host range
within Australia than that reported for P. psidii outside
Australia because of Australia’s high Myrtaceae biodiver-
sity which has not previously been exposed to this rust.
Observations during field surveys in NSW under the
emergency response (to December 2010) indicated that
G. inophloia, A. flexuosa and S. jambos are highly
susceptible to P. psidii s.l. in nurseries or under cultivation,
while R. rubescens and C. leptopetala are highly suscep-
tible in the native environment. At present, most other
hosts are only lightly affected.However,thisislikelyto
change as P. psidii s.l. spreads and inoculum levels
increase as the rust encounters optimum conditions for
disease outbreaks. For example, severe infection has been
observed on Rhodomyrtus psidioides in native bush and of
S. anisatum in plantations on the north coast of NSW in
recent months (Carnegie and Cooper 2011). M. quinque-
nervia is being severely affected in northern NSW (P.
Entwistle, pers. comm.), as occurs in Florida (Rayachhetry et
al. 1997), and is likely to provide a conduit for the spread of
P. psidii s.l. due to the extensive distribution of this species.
Moderately to highly susceptible hosts such as R.
rubescens, M. quinquenervia, S. glomulifera, G. inophloia,
C. leptopetala and R. psidioides form a near contiguous
corridor along the east coast of Australia (Appendix II;
http://avh.rbg.vic.gov.au/avh/) which will assist the north-
ward and southward spread of P. psidii s.l. in Australia.
Climatic suitability for epidemic disease of the strain of P.
psidii s.l. in Australia is likely to be similar to that reported
Table 2 (continued)
Tribe
c
Host
*
of Puccinia psidii s.l. in Australia
Eucalypteae (13) Angophora floribunda (Sm.) Sweet
Eucalyptus agglomerata Maiden
E. cloeziana
e
F.Muell.
E. deanei Maiden
E. elata Dehnh.
E. grandis
e
W.Hill
E. pilularis Sm.
E. tindaliae Blakely
Stockwellia quadrifida D.J.Carr
Syncarpieae (14) Syncarpia glomulifera (Sm.) Nied.
Leptospermeae (16) Agonis flexuosa (Muhl.ex Willd.) Sweet
Asteromyrtus brassii (Byrnes) Craven
Leptospermum leuhmannii F.M.Bailey
L. petersonii F.M.Bailey
L. rotundifolium (Maiden & Betche) F.A.Rodway
Chamelaucieae (17) Chamelaucium uncinatum Schauer
a
NSW records from http://www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/hosts
b
Queensland records from http://www.dpi.qld.gov.au/4790_19789.htm
c
Tribes according to Wilson et al. (2005)
d
Species accepted by Australian Plant Census 2011 (http://www.chah.gov.au/chah/apc/index.html) but no formal species name published (verified
25/07/11)
e
Only from host testing (in NSW)
* See Table 3for synonym table
Rapidly expanding host range for Puccinia psidii sensu lato 21
for eucalyptus/guava rust, with high risk zones along the
east coast of Australia from southern NSW to far north
Queensland (Booth and Jovanovic, in Glen et al. 2007).
Wind and anthropogenic movement (e.g. via nursery and
garden plants) are likely to be the greatest dispersers of
myrtle rust, however, nectar-feeding fauna, such as bats and
birds, could also act as vectors, especially in those host
plants that are likely to have myrtle rust high in the crown,
such as M. quinquenervia. Experience with poplar rust
(Melampsora medusa)—which spread from greater-Sydney
north to Queensland and south to Victoria within 14 weeks
of detection (Walker et al. 1974)—provide some indication
of how rapidly rusts can spread with suitable hosts and
climatic conditions.
Experiments in situ at IP1 revealed that during the
colder winter months on the Central Coast of NSW the
period from inoculation to sporulation (latent period)
lengthened significantly. Under optimum conditions for P.
psidii (15–25°C, de Piza and Ribeiro 1988;Ruizetal.
1989) infection occurs within two weeks, from inoculation
to sporulation (Marlatt and Kimbrough 1979; Rayachhetry
et al. 1997; Alfenas et al. 2003). Likewise, we observed
infection within two weeks in Experiment IV in the
laboratory, where temperatures were within the optimum
range. However, in Experiment III (in situ at IP1), where
temperatures were much colder, the infection period was
four weeks on A. flexuosa ‘Afterdark’and five weeks on
the Eucalyptus spp. Similar observations have been made
for chrysanthemum white rust (P. h o r i a n a ), which has an
infection period of approx. one week under optimum
conditions but up to eight weeks under sub-optimum
conditions (Zandvoort et al. 1968). This has implications
for myrtle rust surveillance and domestic quarantine, as
the time from infection to observation of symptoms is
significantly greater during cooler temperatures. We
observed moderate disease on T. neriifolia and G.
inophloia during winter. This indicates that these hosts
are likely to be severely impacted during optimum
conditions for infection, which are expected from spring
to autumn. Severe infection on hosts such as S. jambos, R.
rubescens, R. psidioides and S. anisatum in NSW
(Carnegie and Cooper 2011) illustrates the potential
impact of P. p s i d i i s.l. under optimum conditions in
Australia.
To the best of our knowledge this is the first time
cuttings in polycarbonate jars have been used for
inoculation experiments with a member of the eucalyp-
tus/guava rust complex. With optimum conditions
providing infection (uredinial pustules) within two
weeks, this method is a useful addition to current
artificial inoculation methods to identify susceptible
hosts. This technique was very useful during the
emergency response, enabling host testing to be con-
ducted under quarantine conditions to provide quick
answers to questions on host range and thus potential
impact of the incursion. We did, however, encounter
some problems, including fungal contamination on
plants and some premature leaf senescence. Enhancing
plant/cutting hygiene (i.e. ensuring plants are free from
disease) as well as dipping plants/cuttings in a
decontaminant (e.g. dilute chlorine), would reduce
fungal contamination problems. This technique has
recently been used to test the susceptibility of endan-
gered plant species to P. psidii s.l. in Australia, where
seed or seedlings were not available (L. Morin, CSIRO,
unpublished).
Authorities managing the incursion have recently
concluded that P. p s i d i i s.l. is now no longer technically
feasible to eradicate, due mainly to the widespread
distribution in native forests on the Central Coast of
NSW and the expanding host range (Department of
Agriculture, Fisheries and Forestry 2010c; Carnegie and
Cooper 2011). As such, a National Transition to Manage-
ment Strategy has been developed that includes actions to
“slow the spread”, community awareness and engagement,
as well as research on taxonomy, epidemiology, host
testing and ecological impacts (Department of Agriculture,
Fisheries and Forestry 2011). One of the main aims of the
morphological and molecular research to clarify the
taxonomy of P. psidii s.l. in Australia is to ensure there
are robust characters to distinguish the strain of P. psidii
Table 3 Synonym table
Synonym Currently accepted name
Acmena hemilampra Syzygium hemilamprum
Acmenosperma claviflorum Syzygium claviflorum
Anetholea anisata Syzygium anisatum
Austromyrtus bidwillii Gossia bidwillii
Austromyrtus hillii Gossia hillii
Austromyrtus inophloia Gossia inophloia
Backhousia anisata Syzygium anisatum
Melaleuca pachyphylla Callistemon pachyphyllus
Melaleuca polandii Callistemon polandii
Rhodamnia spongiosa Rhodamnia glauca
Tristania laurina Tristaniopsis laurina
Waterhousea floribunda Syzygium floribundum
Waterhousea hedraiophylla Syzygium hedraiophyllum
Waterhousea mulgraveana Syzygium mulgraveanum
22 A.J. Carnegie, J.R. Lidbetter
s.l. in Australia from other strains within the eucalyptus/
guava rust complex not present in Australia. It is
important for Australia to continue to keep quarantine
restrictions in place to reduce the chance of other strains
entering and becoming established. Similarly, Hawaiian
authorities have recommended regulating imports to
reduce the threat to Hawaiian flora from additional
strains of P. psidii (State of California Department of Food
Fig. 3 Symptoms of P. psidii
sensu lato on various hosts
observed during surveys in
nurseries (a–e) or native forest
(f–g). aTristania neriifolia; b
Leptospermum rotundifolium;
cSyzygium ‘Cascade’;dMetro-
sideros collina; eGossia
inophloia; f–gRhodamnia
rubescens; (g inset) fruit of R.
rubescens
Rapidly expanding host range for Puccinia psidii sensu lato 23
and Agriculture 2007; Loope and La Rosa 2008; Loope
2010).
The full ecological and commercial impact of P. psidii
s.l. in Australia is not yet known at this early stage.
However, observation of severe damage to R. rubescens, R.
psidioides, S. anisatum and M. quinquenervia give some
guide to its potential impact. Experiences in Florida and
Hawaii, where native and introduced Myrtaceae have been
devastated by eucalyptus/guava rust (Rayachhetry et al.
1997; Leahy 2004; Uchida and Loope 2009; Loope 2010),
and the impact on the all-spice and eucalypt industries in
Jamaica and Brazil (MacLachlan 1938; Furtado and Marino
2003) are a sobering indication of what might occur in
Australia.
Acknowledgements The host testing work was funded by Forest
and Wood Products Australia Ltd. (Project No: PRC179-0910) and
Forests NSW. We thank the owners of IP1 for the use of their
greenhouse and cooperation during the in situ experiments, Michael
Priest for diagnostics and Kerrie Sims for assistance with microscope
photography. Staff from various agencies in Australia involved in the
emergency response, as well as ongoing surveys, especially from
NSW DPI and Biosecurity Queensland/DEEDI, are also thanked. We
also thank Peter Wilson for advice on nomenclature of species in
Myrtaceae, Morag Glen and Acelino Alfenas for sourcing some
references, and Fabiano Ximenes for translation of Portuguese
literature.
Appendix I. Species of Myrtaceae reported to show
some susceptibility to Puccinia psidii outside Australia
from field observations and host testing. Plant names
according to Govaerts et al. (2011)
Tribe
a
Species
*
Heteropyxideae
(2)
Heteropyxis natalensis Harv. (Alfenas et al. 2005)
Callistemon citrinus (Sims) Sweet (Tommerup et
al. 2003;Leahy2004), C. pachyphyllus (Curtis)
Skeels (Zauza et al. 2010), C. speciosus (Sims)
Sweet (Viégas 1945)(asC. glaucus (DC.)
Sweet, OCCPO 2007), C. viminalis (Sol. ex
Gaertn.)G.DonexLoudon(Rayachhetryetal.
2001)
Eremaea asterocarpa Hnatiuk (Old et al. 2004;
OCCPO 2007), E. pauciflora (Endl.) Druce (Old
et al. 2004; OCCPO 2007)
Melaleuceae
(6)
Melaleuca alternifolia (Maiden & Betche) Cheel
(Tommerup et al. 2003), M. cajuputi Powell
(Tommerup et al. 2003), M. decora (Salisb.)
Britten (Rayachhetry et al. 2001),M.
hypericifolia Sm. (Old et al. 2004; OCCPO
Tribe
a
Species
*
2007), M. leucadendra (L.) L. (Zauza et al. 2010)
(as M. leucodendron (L.) L., Viégas 1961 in
Furtado and Marino 2003), M. nesophila F.Muell.
(Zauza et al. 2010), M. quinquenervia (Cav.) S.T.
Blake (Rayachhetry et al. 1997)
Regelia ciliata Schauer (Zauza et al. 2010)
Metrosidereae
(9)
Metrosideros collina (J.R.Forst & G.Forst) A.Gray
(Loope 2010), M. excelsa Sol. ex Gaertn. (Loope
2010), M. kermadecensis W.R.B.Oliv. (Loope
2010), M.polymorpha Gaudich. (Killgore and
Heu 2007)
Syzygieae (11) Syzygium alatoramulum B.Hyland (Zauza et al.
2010), S. australe (J.C. Wendl. ex Link) B.
Hyland (Zauza et al. 2010), S. cumini (L.)
Skeels (Junghans et al. 2003)(asEugenia
jambolana L., Hennen et al. 2005), S. fibrosum
(F.M.Bailey) T.G.Hartley & L.M.Perry (Zauza et
al. 2010), S. grande (Wight) Walp. (as Eugenia
grandis Wight, Rangel 1916;Hennenetal.
2005),S.jambos(L.) Alston (as Eugenia
jambos L., MacLachlan 1938), S. luehmannii (F.
Muell.) L.A.S.Johnson (Zauza et al. 2010), S.
malaccense (L.) Merr. & L.M.Perry (as Eugenia
malaccensis L. (MacLachlan 1938), S.
paniculatum Gaertn. (Leahy 2004), S.
samarangense (Blume) Merr. & L.M.Perry
(Zambino and Nolan 2011), S. sandwicense (A.
Gray) Müll. Stuttg. (Loope 2010), S. smithii
(Poir.) Nied. (as Acmena smithii Poir.) (Zauza et
al. 2010)
Myrteae (12) Acca sellowiana (O.Berg.) Burret (as Feijoa
sellowiana (O.Berg.) O.Berg., in Blum and
Dianese 2001)
Archirhodomyrtus beckleri (F.Muell.) A.J.Scott
(Zauza et al. 2010)
Calycorectes pohlianus (O.Berg) Kiaersk. (as
Eugenia cambucae
b
Mattos [Syn. Schizocalyx
pohlianus O.Berg], Hennen et al. 2005)
Campomanesia guaviroba (DC.) Kiaersk. (as
Abbevillea maschalanthe (DC) O.Berg, Rangel
1916; Hennen et al. 2005)
Decaspermum humile (Sweet ex G.Don.) A.J.Scott
(Zauza et al. 2010)
Eugenia brachythrix Urb. (Dale 1955), E.
brasiliensis Lam. (Hennen et al. 2005) (as E.
dombeyi Skeels, Junghans et al. 2003), E.
candolleana DC. (as E. christovana Kiaersk.,
Rangel 1916; Simpson et al. 2006), E. foetida
Pers. (Leahy 2003), E. involucrata DC. (as
Phyllocalyx involucratus (DC.) O.Berg,
Lindquist 1960 in Hennen et al. 2005), E.
kanakana N.Snow (as Monimiastrum globosum
J.Gueho & A.J.Scott, Loope 2010), E.
koolauensis O.Deg. (Killgore and Heu 2007),
E. pyriformis Cambess. (as Eugenia uvalha
Cambess., Viégas 1945; Laundon and Waterson
1965), E. pitanga (O.Berg) Nied. (as
24 A.J. Carnegie, J.R. Lidbetter
Tribe
a
Species
*
Stenocalyx pitanga O.Berg, Carvalho et al.
2007), E. reinwardtiana (Blume) A.Cunn. ex
DC. (Rayachhetry et al. 2001), E. stipitata
McVaugh (as araçá-boi, Junqueira et al. 2001),
E. uniflora L. (Rangel 1916; Junghans et al.
2003)
Myrcia splendens (Sw.) DC. (as M. acuminata
b
(Kunth) DC., Carvalho et al. 2007), M.
stenocarpa Krug & Urb. (Baker and Dale
1948), M. xylopioides (Kunth) DC. (Buriticá
and Pardo-Cardona 1996 in Simpson et al.
2006)
Myrcianthes fragrans (Sw.) McVaugh (Rayachhetry
et al. 2001), M. pungens (O.Berg) D.Legrand
(Leahy 2004)(asEugenia pungens O.Berg,
Hennen et al. 2005)
Myrrhinium atropurpureum Schott (Pérez et al.
2010)
Myrtus communis L. (Leahy 2004)
Pilidiostigma glabrum Burret (Zauza et al. 2010),
P. tropicum L.S.Sm. (Zauza et al. 2010)
Pimenta dioica (L.) Merr. (as Pimenta officinalis
Lindl., MacLachlan 1938), P. racemosa var.
racemosa (Mill.) J.W.Moore (as Pimenta acris
(SW.) Kostel., MacLachlan 1938)
Plinia cauliflora (Mart.) Kausel (as Myrciaria
jaboticaba (Vell.) O.Berg, Laundon and Waterson
1965)(asMyrcia jaboticaba (Vell.) Baill.,
Hennen et al. 2005)(asMyrciaria cauliflora (Mart.)
O.Berg, Rayachhetry et al. 2001), P. edulis (Vell.)
Sobral (as Eugenia edulis Vell., Rangel 1916)(as
Marlieria edulis Nied., Hennen et al 2005)
Psidium cattleianum Afzel. ex Sabine (as
araçazeiro, Junqueira et al. 2001), P. grandifolium
Mart. ex DC. (as Psidium incanescens Mart. ex
DC., Hennen et al. 2005), P. guajava L. (as
Psidium pomiferum L., Winter 1884), P.
guineense Sw. (Viégas 1961 in Simpson et al.
2006)
Rhodamnia rubescens Benth. (Zauza et al. 2010)
Rhodomyrtus psidioides (G.Don) Benth. (Zauza et
al. 2010), R. tomentosa (Aiton) Hassk. (Loope
2010)
Eucalypteae
(13)
Angophora costata (Gaertn.) Hochr. Ex Britten
(Tommerup et al. 2003)
Corymbia citriodora (Hook.) K.D.Hill & L.A.S.
Johnson (as Eucalyptus citriodora Hook., Joffily
1944; Dianese et al. 1984), C. grandifolia (R.Br.
ex Benth.) K.D.Hill & L.A.S.Johnson (as E.
grandiflora
b
, Hennen et al. 2005), C. gummifera
(Gaertn.) K.D.Hill & L.A.S.Johnson (Zauza et al.
2010), C. intermedia (F.Muell. ex R.T.Baker) K.
D.Hill & L.A.S.Johnson (Zauza et al. 2010), C.
maculata (Hook.) K.D.Hill & L.A.S.Johnson (as
E. maculata Hook., Dianese et al. 1984), C.
torelliana (F.Muell.) K.D.Hill & L.A.S.Johnson
Tribe
a
Species
*
(as E. torelliana F.Muell., Ferreira 1983; LaRosa
and Hauff 2007)
Eucalyptus acmenoides Schauer (Zauza et al.
2010), E. agglomerata Maiden (Old et al. 2002;
OCCPO 2007), E. alba Reinw. ex Blume
(Zauza et al. 2010), E. amplifolia Naudin
(Kawanishi et al. 2009), E. andrewsii Maiden
(as E. montivaga A.R.Bean, Old et al. 2004,
incorrectly assigned; OCCPO 2007), E.
benthamii Maiden & Cambage (Auer et al.
2010; Vieira et al. 2011), E. botryoides Sm.
(Aparecido 2004), E. brassiana S.T.Blake
(Tommerup et al. 2003), E. camaldulensis
Dehnh. (Dianese et al. 1984), E. cloeziana F.
Muell. (Dianese et al. 1984), E. deglupta
Blume(Zauzaetal.2010), E. diversicolor F.
Muell. (Zauza et al. 2010), E. dunnii Maiden
(Zauza et al. 2010), E. elata Dehnh. (Zauza et
al. 2010), E. globulus Labill. (Alfenas et al.
2003), E. grandis W.Hill (Dianese et al. 1984),
E. guilfoylei Maiden (Zauza et al. 2010), E.
melanophloia F.Muell. (Zauza et al. 2010), E.
microcorys F.Muell. (Dianese et al. 1984), E.
moluccana Wall ex Roxb. (Zauza et al. 2010),
E. nigra F.Muell. ex R.T.Baker (as E.
phoetricha
b
[= E.phaeotricha Blakely &
McKie], Hennen et al. 2005), E. nitens (H.
Deane & Maiden) Maiden (Zauza et al. 2010),
E. obliqua ĽHér. (Zauza et al. 2010), E.
paniculata Sm. (Dianese et al. 1984), E. pellita
F.Muell. (Dianese et al. 1984), E. pilularis Sm.
(Ferreira 1983; Zauza et al. 2010), E. propinqua H.
Deane & Maiden, E. punctata A.Cunn. ex DC.
(Dianese et al. 1984), E. pyrocarpa L.A.S.Johnson
& Blaxell (Dianese et al. 1984),E.regnansF.
Muell. (Zauza et al. 2010), E. resinifera Sm.
(Zauza et al. 2010), E. robusta Sm. (Ferreira 1983;
Zauza et al. 2010), E. rubiginosa Brooker (Old et
al. 2004; OCCPO 2007),E.rudisEndl.
(Kawanishi et al. 2009), E. saligna Sm. (Dianese
et al. 1984),E.sciasL.A.S.Johnson & K.D.Hill.
(Zauza et al. 2010), E. sieberi L.A.S.Johnson (Old
et al. 2004;OCCPO2007), E. smithii F.Mue ll. ex
R.T.Baker (LaRosa and Hauff 2007), E.
tereticornis Sm. (Ferreira 1983; Zauza et al. 2010),
E. tetrodonta F.Muell. (Old et al. 2004; OCCPO
2007), E. tindaliae Blakely (Old et al. 2004;
OCCPO 2007), E. urophylla S.T.Blake (Dianese et
al. 1984), E. viminalis Labill. (Alfenas et al. 2003)
Syncarpieae
(14)
Syncarpia glomulifera (Sm.) Nied. (Tommerup et
al. 2003), S. hillii F.M.Bailey (Zauza et al.
2010)
Leptospermeae
(16)
Kunzea baxteri (Klotzsch) Schauer (Tommerup et
al. 2003), K. ericoides (A.Rich.) Joy Thomps.
(Old et al. 2004; OCCPO 2007), K. recurva
Schauer (Old et al. 2004)
Pericalymma ellipticum (Endl.) Schauer (Zauza et
al. 2010)
Rapidly expanding host range for Puccinia psidii sensu lato 25
Tribe
a
Species
*
Chamelaucieae
(17)
Astartea fascicularis (Labill.) A.Cunn. ex DC.
(Old et al. 2004; OCCPO 2007), A. heteranthera
C.A.Gardner (Zauza et al. 2010)
Chamelaucium uncinatum Schauer (Loope 2010)
Hypocalymma robustum (Endl.) Lindl. (Zauza et
al. 2010)
Thryptomene australis Endl. (Old et al. 2004;
OCCPO 2007)
a
Tribes according to Wilson et al. 2005
b
Citing authors uncertain of host identification
*
Synonym table:
Names used by cited author,
or commonly used
synonyms
Currently accepted name
Abbevillea maschalantha (DC)
O.Berg
Campomanesia guaviroba
(DC.) Kiaersk.
Acmena smithii Poir. Syzygium smithii (Poir.) Nied.
Callistemon glaucus (DC.)
Sweet
Callistemon speciosus
(Sims) Sweet
Eucalyptus citriodora Hook. Corymbia citriodora (Hook.) K.D.
Hill & L.A.S.Johnson
Eucalyptus grandiflora Corymbia grandifolia (R.Br. ex
Benth.) K.D.Hill & L.A.S.
Johnson
Eucalyptus maculata Hook. Corymbia maculata (Hook.) K.D.
Hill & L.A.S.Johnson
Eucalyptus phaeotricha
Blakely & McKie
Eucalyptus nigra F.Muell. ex R.T.
Baker
Eucalyptus torelliana F.Muell. Corymbia torelliana (F.Muell.) K.
D.Hill & L.A.S.Johnson
Eugenia brasiliensis Lam. Eugenia dombeyi Skeels
Eugenia cambucae Mattos Calycorectes pohlianus (O.Berg)
Kiaersk.
Eugenia christovana Kiaersk. Eugenia candolleana DC.
Eugenia dombeyi Skeels Eugenia brasiliensis Lam.
Eugenia edulis Vell. Plinia edulis (Vell.)
Sobral
Eugenia grandis Wight Syzygium grande
(Wight)
Eugenia jambolana L. Syzygium cumini
(L.) Skeels
Eugenia jambos L. Syzygium jambos
(L.) Alston
Eugenia malaccensis L. Syzygium malaccense (L.)
Merr. & L.M.Perry
Eugenia pungens O.Berg Myrcianthes pungens
(O.Berg)
Eugenia uvalha Cambess. Eugenia pyriformis
Cambess.
Feijoa sellowiana (O.Berg)
O.Berg
Acca sellowiana (O.Berg)
Burret
Melaleuca leucodendron
(L.) L.
Melaleuca leucadendra
(L.) L.
Monimiastrum globosum J.
Gueho & A.J.Scott
Eugenia kanakana N.Snow
Stenocalyx pitanga O.Berg Eugenia pitanga (O.Berg)
Nied.
Pimenta acris (SW.) Kostel. Pimenta dioica (L.)
Merr.
Pimenta officinalis Lindl. Pimenta dioica (L.)
Merr.
Marlieria edulis Nied. Plinia edulis (Vell.)
Sobral
Myrcia jaboticaba (Vell.)
Baill.
Plinia cauliflora (Mart.)
Kausel
Myrciaria cauliflora (Mart.) O.
Berg
Plinia cauliflora (Mart.)
Kausel
Myrciaria jaboticaba (Vell.) O.
Berg
Plinia cauliflora (Mart.)
Kausel
Phyllocalyx involucratus (DC.)
O.Berg
Eugenia involucrata DC.
Psidium pomiferum L. P. guajava L.
Psidium incanescens Mart.
ex DC.
P. grandifolium Mart. ex DC.
26 A.J. Carnegie, J.R. Lidbetter
Appendix II. Distribution of key hosts of Puccinia psidii
sensu lato in Australia (Australian Virtual Herbarium,
http://avh.rbg.vic.gov.au/avh/)
Syncarpia glomulifera
Gossia inophloiaRhodomyrtus psidioides
Melaleuca quinquenerviaRhodamnia rubescens
Choricarpia leptopetala
Rapidly expanding host range for Puccinia psidii sensu lato 27
References
Alfenas AC, Zauza EAV, Assis TF (2003) First record of Puccinia
psidii on Eucalyptus globulus and E. viminalis in Brazil.
Australas Plant Pathol 32:325–326
Alfenas AC, Zauza EAV, Wingfield MJ, Roux J, Glen M (2005)
Heteropyxis natalensis, a new host of Puccinia psidii rust.
Australas Plant Pathol 34:285–286
Aparecido CC (2004) Estudos Ecológicos sobre Puccinia psidii
Winter—Ferrugem das Mirtáceas. Biológico 66:63
Auer CG, Santos ÁA dos, Bora KC (2010) A ferrugem do eucalipto
na região Sul do Brasil. Communicado Técnico (Embrapa
Florestas) 252.
Baker RED, Dale WT (1948) Fungi of Barbados and the Windward
Islands. Mycolog Pap 25:1–26
Blum LEB, Dianese JC (2001) Padrões de liberação de urediníosporos
e desenvolvimento da ferrugem do jambeiro. Pesquisa Agro-
pecuária Brasileira 36:845–850
Buriticá CP, Pardo-Cardona VM (1996) Flora urediniana Colombiana.
Revista de la Academia Colombiana de Ciencias Exactas, Físicas
y Naturales 20:183–236
Carnegie AJ, Cooper K (2011) Emergency response to the incursion of
an exotic myrtaceous rust in Australia. Australasian Plant
Pathology 40:346–359
Carnegie AJ, Lidbetter JR, Walker J, Horwood MA, Tesoriero L, Glen
M, Priest M (2010) Uredo rangelii, a taxon in the guava rust
complex, newly recorded on Myrtaceae in Australia. Australas
Plant Pathol 39:463–466
Dale WT (1955) A preliminary list of Jamaican Urediniales. Mycol
Pap 60:1–21
de Carvalho Júnior AA, Figueiredo MB, Furtado EL, Hennen JF
(2007) Uredinales sobre blechnaceae, thelypteridaceae, schi-
zaeaceae, myrtaceae, oxalidaceae, rhamnaceae, rubiaceae,
sapindaceae, smilacaceae e vitaceae da reserva florestal
“Armando de Salles Oliveira”, São Paulo, SP, Brasil. Hoehnea
34:481–492
Department of Agriculture, Fisheries and Forestry (2010a) Myrtle rust
(Uredo rangelii) detection. Media Release No. DAFF10/004D.
Available at: http://www.daff.gov.au/about/media-centre/dept-
releases (verified 12 January 2011)
Department of Agriculture, Fisheries and Forestry (2010b) National
Management Group agrees on Myrtle Rust Interim Response
Plan. Media Release No. DAFF10/007D. Available at: http://
www.daff.gov.au/about/media-centre/dept-releases (verified 12
January 2011)
Department of Agriculture, Fisheries and Forestry (2010c). Update on
response to myrtle rust—23 December 2010. DAFF Communiqué, 23
December 2010. Available at: http://www.daff.gov.au/aqis/quarantine/
pests-diseases/myrtle-rust/update_on_response_to_myrtle_rust (veri-
fied 7 March 2011)
Department of Agriculture, Fisheries and Forestry (2011) Myrtle rust
Questions and Answers: 3 March 2011. Available at: http://www.
daff.gov.au/aqis/quarantine/pests-diseases/myrtle-rust/myrtle-rust-
qa (verified 55 March 2011)
de Piza SMT, Ribeiro IJA (1988) Influence of light and temperature on
uredospore germination of Puccinia psidii Winter. Bragantia
47:75–78
Dianese JC, Moraes TS, Silva AR (1984) Response of Eucalyptus
species to field infection by Puccinia psidii. Plant Dis 68:314–
316
Dianese JC, Moraes TS, Haridasan M (1986) Screening Eucalyptus
species for rust resistance in Bahia, Brazil. Trop Pest Manag
32:292–295
Ferreira FA (1983) Eucalyptus rust. Revista Arvore 7:91–109
Furtado EL, Marino CL (2003) Eucalyptus rust management in Brazil. In
Proceedings 2nd IUFRO Rusts of Forest Trees WP Conference.
August 2002. Yangling, China. Forest Research 16 (Suppl.), 118–
124
Glen M, Alfenas AC, Zauza EAV, Wingfield MJ, Mohammed C (2007)
Puccinia psidii: a threat to the Australian environment and
economy—a review. Australas Plant Pathol 36:1–16
Global Invasive Species Database (2010) Puccinia psidii (fungus).
Available at: http://www.issg.org/database/species/ecology.asp?
si=1538&fr=1&sts=sss&lang=EN (verified 12 January 2011)
Govaerts R, Sobral M, Ashton P, Barrie F, Holst B, Landrum L,
Matsumoto K, Mazine F, Lughadha E, Proenca C, Soares-Silva
L, Wilson P, Lucas E (2011). World Checklist of Myrtaceae. The
Board of Trustees of the Royal Botanic Gardens,Kew. Available
at: http://www.kew.org/wcsp/ (verified 1 August 2011)
Grgurinovic CA, Walsh D, Macbeth F (2006) Eucalyptus rust caused
by Pucinia psidii and the threat it poses to Australia. EPPO Bull
36:486–489
Hennen JF, Figueiredo MB, de Carvelho AA Jr, Hennen PG (2005)
Catalogue of the species of plant rust fungi (Uredinales) of
Brazil. (Instituto de Pesquisas, Jardim Botânico do Rio de
Janeiro: Rio de Janeiro, Brazil)
Joffily J (1944) Ferrugem do Eucalpto. Bragantia 4:475–488
Junghans DT, Alfenas AC, Brommonschenkel SH, Oda S, Mello EJ,
Grattapaglia D (2003) Resistance to rust (Puccinia psidii Winter)
in Eucalyptus: mode of resistance and mapping of a major gene
with RAPD markers. Theor Appl Genet 108:175–180
Junqueira NTV, de Andrade LRM, Pereira M, Lima MM, da Chaves
RC (2001) Doenças da goiabeira no Cerrado. Circ Téc (Embrapa
Cerrados) 15:1–31
Kawanishi T, Uemastu S, Kakishima M, Kagiwada S, Hamamoto H,
Horie H, Namba S (2009) First report of rust disease on ohia and
the causal fungus, Puccinia psidii, in Japan. J Gen Plant Pathol
75:428–431
Killgore EM, Heu RA (2007) A rust disease on ‘Ohi’a, Puccinia psidii
Winter. New Pest Advisory 05–04 (Updated December 2007).
Available at http://www.hawaiiag.org/hdoa/npa/npa05-04-ohiarust.
pdf (verified 14 May 2010)
LaRosa AM, Hauff R (2007) Incidence and Evaluation of a New Rust
Disease on Myrtaceae in Hawaii: Puccinia psidii Winter, Guava
Rust. USDA Forest Service, Forest Health Monitoring Working
Group Meeting Poster Presentation. Available at: http://fhm.fs.
fed.us/posters/posters07/incidence_eval.pdf (verified 20 January
2011)
Laundon GF, Waterson JM (1965) Puccinia psidii.‘C.M.I. Description
of Pathogenic Fungi and Bacteria, No. 56.’(Commonwealth
Mycological Institute, Kew, Surrey, England)
Leahy RM (2003) Plant pathology section. Tri-ology 42(1). Available
at: http://www.freshfromflorida.com/pi/enpp/triology/archive/03-
jan-feb.htm#top (verified 24 June 2011)
Leahy R (2004) Recent history of Puccinia psidii on Myrtaceae in
Florida. Available at http://web.archive.org/web/20050117213153/
http:/extlab7.entnem.ufl.edu/PestAlert/tmm-0209.htm (verified 12
January 2011)
Lindquist JC (1960) Notas Uredinologicas. VI. Rev Fac Agron (La
Plata) 36:101–108
Loope L (2010) A summary of information on the rust Puccinia psidii
Winter (guava rust) with emphasis on means to prevent
introduction of additional strains to Hawaii. U.S. Geological
Survey Open File Report 2010-1002 (U.S. Geological Survey,
Reston, Virginia)
Loope L, La Rosa AM (2008) An analysis of the risk of the introduction
of additional strains of the rust Puccinia psidii Winter (‘Ohi’a rust)
to Hawai’i. U.S. Geological Survey Open File Report 2008-1008
(U.S. Geological Survey, Reston, Virginia)
28 A.J. Carnegie, J.R. Lidbetter
MacLachlan JD (1938) A rust of the pimento tree in Jamaica, BWI.
Phytopathology 28:157–170
Marlatt RB, Kimbrough JW (1979) Puccinia psidii on Pimenta dioica
in south Florida. Plant Dis Rep 63:510–512
Office of the Chief Plant Protection Officer (2007) ‘Puccinia psidii.
Forestry, rural and urban biosecurity plan. Pest specific contin-
gency plan.’(Australian Government Department of Agriculture,
Fisheries and Forestry: Canberra)
Old KM, Alfenas A, Wingfield MJ, et al (2002) Assessment of
Eucalyptus rust as a pathogen of Eucalyptus spp. and other
Myrtaceae and development of sensitive methods for its detection
in germplasm. ACIAR Project No. FST/1996/206. Second
Annual Report, Client Report No. 1161
Old KM, Alfenas A, Wingfield MJ, et al (2004) Assessment of
Eucalyptus rust as a pathogen of Eucalyptus spp. and other
Myrtaceae and development of sensitive methods for its detection
in germplasm. ACIAR Project No. FST/1996/206. Final Report
Pérez CA, Wingfield MJ, Altier NA, Simeto S, Blanchette RA (2010)
Puccinia psidii infecting cultivated Eucalyptus and native
myrtaceae in Uruguay. Mycological Progress doi:10.1007/
s11557-010-0698-x
Ramsfield T, Dick M, Bulman L, Ganley R (2010) Briefing document
on myrtle rust, a member of the guava rust complex, and the risk
to New Zealand. (Scion: Rotorua, New Zealand). Available at:
http://www.nzffa.org.nz/images/design/Briefing-paper-myrtle-
rust.pdf (verified 12 January 2011)
Rangel E (1916) Contribuição para o estudo das Puccinias das
Myrtaceas. Archivos do Museu Nacional do Rio de Janeiro
18:149–158
Rayachhetry MB, Elliot ML, Van TK (1997) Natural epiphytotic of a
rust fungus (Puccinia psidii)onMelaleuca quinquenervia in
Florida. Plant Dis 81:831
Rayachhetry MB, Van TK, Center TD, Elliott ML (2001) Host range
of Puccinia psidii, a potential biological control agent of
Melaleuca quinquenervia in Florida. Biol Control 22:38–45
Ruiz RAR, Alfenas AC, Ferreira FA (1989) Influência da temperatura,
luz e origem do inóculo sobre a produção de uredosporos e
teliosporos de Puccinia psidii. Fitopatol Bras 14:70–73
Simpson JA, Thomas K, Grgurinovic CA (2006) Uredinales species
pathogenic on species of Myrtaceae. Australas Plant Pathol
35:549–562
State of California Department of Food and Agriculture (2007) Hawaii
restrictions on importation of all Myrtaceae plants. Phytosanitary
Advisory No. 33-2007. Available at: http://www.cdfa.ca.gov/
countyag/postings/files/PSA_33-2007_Hawa.pdf (verified 20
January 2011)
Tommerup IC, Alfenas AC, Old KM (2003) Guava rust in Brazil—a
threat to Eucalyptus and other Myrtaceae. N Z J For Sci 33:420–
428
Uchida JY, Loope LL (2009) A recurrent epiphytotic of guava rust on
rose apple, Syzygium jambos, in Hawaii. Plant Dis 93:429
Viégas AP (1945) Alguns fungos do Brasil. IV. Uredinales. Bragantia
5:1–144
Viégas AP (1961) ‘Índice de Fungos da América do Sul.’(Instituto
Agronômico: Campinas, São Paulo, Brazil)
Vieira ALPA, Ghini R, Bettiol W, Auer CG, dos Santos AF (2011)
Puccinia psidii XEucalyptus benthamii: patogenicidade e efeito
do aumento da concentração de CO
2
do are m sala climatizada.
Summa Pahytopathologica 37:Supplement. Available at: http://
ainfo.cnptia.embrapa.br/digital/bitstream/item/35258/1/Summa.
pdf (verified 23 June 2011)
Walker J (1983) Pacific mycogeography: deficiencies and irregularities
in the distribution of plant parasitic fungi. Aust J Bot Supple-
mentary Series 10:89–136
Walker J, Hartigan D, Bertus AL (1974) Poplar rusts in Australia with
comments on potential conifer rusts. Eur J For Pathol 4:100–118
Wilson PG, O’Brien MM, Heslewood MM, Quinn CJ (2005)
Relationships within Myrtaceae sensu lato based on matK
phylogeny. Plant Systemat Evol 251:3–19
Winter G (1884) Repertorium. Rabenhorstii fungi europaei et
extraeuropaei exsiccati cura Dr. G. Winter, Centuria XXXI et
XXXII. Hedwigia 23:164–172
Zambino PJ, Nolan PA (2011) First report of rust caused by Puccinia
psidii on paperbark, Melaleuca quinquenervia, in California.
Plant Disease “First Look”http://apsjournals.apsnet.org/doi/
pdfplus/10.1094/PDIS-05-11-0436
Zandvoort R, Groenewegan CAM, Zadoks JC (1968) On the
incubation period of Puccinia horiana. Neth J Plant Pathol
74:128–130
Zauza EAV, Alfenas AC, Old KM, Couto MMF, Graça RN, Maffia LA
(2010) Myrtaceae species resistance to rust caused by Puccinia
psidii. Australas Plant Pathol 39:405–411
Rapidly expanding host range for Puccinia psidii sensu lato 29
