Uromycladium spp. that cause gall rusts (Acacia gall rusts)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Latitude/Altitude Ranges
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Impact Summary
- Economic Impact
- Environmental Impact
- Risk and Impact Factors
- Uses List
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Uromycladium spp. that cause gall rusts
Preferred Common Name
- Acacia gall rusts
Other Scientific Names
- Uromyces tepperianum Sacc.
- Uromycladium brachycarpae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium falcatariae Doungsa-ard, McTaggart & R.G. Shivas
- Uromycladium farinosae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium flavescentis Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium holosericeae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium implexae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium leiocalycis Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium ligustrinae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium maslinii Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium merrallii Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium mitchellii Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium morrisii Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium murphyi Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium notabile (F. Ludw.) McAlpine
- Uromycladium paradoxae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium scirpifoliae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium tepperianum (Sacc.) McAlpine emend. Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium tetragonophyllae Doungsa-ard, McTaggart, Geering & R.G. Shivas
- Uromycladium woodii Doungsa-ard, McTaggart, Geering & R.G. Shivas
International Common Names
- Portuguese: wattle gall rust fungus
Local Common Names
- Indonesia: gall rust disease
- New Zealand: Uromycladium rust
- URCLTE (Uromycladium tepperianum)
Summary of InvasivenessTop of page
Gall forming rust fungi of the genus Uromycladium are native to Australasia. They are invasive in New Zealand, the Philippines, East Timor, Malaysia and Indonesia.
Uromycladium murphyi (as Uromycladium notabile in the literature) causes damage to Acacia decurrens grown for tannin and as an ornamental in New Zealand. Other hosts of U. murphyi are A. baileyana, A. dealbata and A. mearnsii. Uromycladium paradoxae infects Acacia paradoxa in New Zealand. Uromycladium species have been found in New Zealand on A. ulicifolia and A. verticillata, but the taxa on these two hosts is uncertain and await phylogenetic studies.
Uromycladium falcatariae causes serious disease in Falcataria moluccana in Southeast Asia. This tree is grown as a shade tree in coffee plantations, for timber and pulp, and for other uses.
Uromycladium morrisii and U. woodii were deliberately introduced into South Africa for the biological control of Acacia saligna and Paraserianthes lophantha, respectively.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Pucciniomycotina
- Class: Pucciniomycetes
- Order: Pucciniales
- Family: Pileolariaceae
- Genus: Uromycladium
- Species: Uromycladium spp. that cause gall rusts
Notes on Taxonomy and NomenclatureTop of page
McAlpine (1905) described the genus Uromycladium and included two species, Uromycladium tepperianum and Uromycladium notabile, that both formed large galls on their hosts and had three one-celled teliospores per pedicel. They were distinguished by the teliospores of U. tepperianum having ridges whereas the U. notabile had warts arranged in lines (broken ridges). U. tepperianum was described as having only spermogonia and teliospores, whereas U. notabile was considered to have spermogonia, urediniospores and teliospores (McAlpine 1905). McAlpine’s species concepts stood for over a century.
Uromycladium spp. have been recorded from over 100 host plants (Gathe, 1971; Morris, 1987, Doungsa-ard et al., 2018), mostly phyllodinous members of Acacia in Australia, but also on Acacia spirorbis in New Caledonia (Mouchacca and Horak, 1998), Paraserianthes lophantha subsp. lophantha [Paraserianthes lophantha] in Western Australia (Gathe, 1971), Paraserianthes lophantha subsp. montana in Indonesia (Magnus, 1892; Boedijn, 1959), and Albizia fulva [Falcataria moluccana] in Papua New Guinea (Shaw, 1984). Uromycladium notabile was recorded from eight Australian Acacia species with bipinnate leaves (Botrycephalae; Farr and Rossman, 2019).
Several authors, such as Burges (1934), noted that were host specific races within U. tepperianum based on field observations. Morris (1987) demonstrated that isolates from three different hosts (Acacia saligna, Acacia implexa and Paraserianthes lophantha) had different host ranges. Phylogenetic studies on specimens from a total of 40 host plants resulted in 15 new species (Doungsa-ard et al., 2015; 2018). Currently U. tepperianum is distinguished as having elongate galls along stems and branches of Acacia ligulata and other closely related hosts. All the other rust species in this complex typically produce rounded or irregularly shaped galls (Doungsa-Ard et al., 2018), on various species of Acacia. Many of the taxa within this species complex are currently known from a single host plant, whilst some occur on a few closely related host plant species (Doungsa-Ard et al., 2018).
Berndt (2011) considered that the type specimen of Uredo notabilis, which McAlpine used as the type specimen for Uromycladium notabile, was identical to the uredinial stage of Endoraecium digitatum, making the name Uromycladium notabile invalid. Doungsa-Ard et al. (2018) described a new species for this taxon – Uromycladium murphyi. All of the Uromycladium spp. that cause gall rusts on Acacia produce spermogonia and teliospores, without urediniospores.
It is likely that additional species will be described within this species complex, as additional specimens on host plants not included in these recent studies become available.
Species of Uromycladium that cause gall rust
Uromycladium tepperianum sensu stricto
DescriptionTop of page
Collectively the Acacia gall rusts produce a range of symptoms that may be very indicative for certain species. In general, galls range from small to very large, reddish brown in colour, on stems, branches, phyllodes/leaves, inflorescences and pods. Witches’ brooms are also produced on some host plants. Spermogonia are produced on young galls (approximately 6 to 8 weeks after infection), and later teliospores. The teliopores en masse cover the galls in a cinnamon coloured, loose powder. Galls may persist for a few months to a number of years. Perennial galls produce spermogonia followed by teliospores on annually produced new growth.
Spermogonia appear as small black spots on new growth of galls, blister-like, approximately 200 µm in diameter, subepidermal with a flat hymenium.
Telia are erumpent from the gall surface, bound by the torn epidermal layer, confluent, frequently covering the entire gall surface. Teliospores single celled, globose to sub-globose, usually dorsally depressed, immature teliospores are hyaline and mature teliospores yellowish to reddish-brown in colour, with a distinct apical germ pore, 16‒24 × 12‒20 µm, wall 1.5‒3.5 µm thick, ornamented with 25–45 continuous striae (ridges), or striae broken into warts, orientated from apical pore to basal pedicel scar, three teliopores produced per pedicel, readily breaking at joint of spore and pedicel, pedicel with 2 septa so that each spore produced from a different cell at pedicel apex.
Uromycladium species may be distinguished by the identity of their host plants. Identity can be confirmed by sequences of the LSU, ITS and CO3 genes (Doungsa-Ard et al., 2018). U. tepperianum causes elongated, spindle shaped stem galls, whereas the other species cause globose or irregularly shaped galls with rounded lobes, or witches’ brooms. U. mitchellii, on Acacia trudgeniana, and U. murphyi, on members of the Botrycephalae subgenus of Acacia, differ from all other species by having teliospore covered in warts rather than ridges (Doungsa-Ard et al., 2018).
Uromycladium falcatariae has teliospores with 25–35 equatorial ridges on the surface of the wall, whereas other species have 30–45 equatorial ridges (Doungsa-ard et al., 2015).
For further details of descriptions for each taxon, refer to Doungsa-ard et al. (2015; 2018). General descriptions for U. tepperianum, with images, are available at Rust Fungi of Australia (2020) and Systematic Mycology and Microbiology Laboratory (2007).
DistributionTop of page
Native to Australasia, the majority of gall forming Uromycladium spp. are restricted to Australia. Some taxa have been recorded from neighbouring islands, and presumably occur naturally there as their host plants are indigenous – Uromycladium falcatariae in Papua New Guinea (host Falcataria moluccana), and as yet undetermined taxa in New Caledonia (host Acacia spirorbis) and Indonesia (host Paraserianthes lophantha subsp. montana).
Various taxa have dispersed, likely by wind, from Australia to New Zealand, where they established in the early 1900’s when their host plants were introduced and widely planted (Dick, 1985; McKenzie, 1998).
With the widespread planting of F. moluccana throughout Indonesia and neighbouring island states of the Malay Archipelago, U. falcatariae has followed and is recorded as invasive in the Philippines, Malaysia, East Timor and Indonesia. No details are available as to whether this spread was by wind from the presumed native range in New Guinea (where its host occurs naturally), or by human intervention. Dispersal within the Malay Archipelago is likely by wind.
Two taxa (U. morrisii and U. woodii) have been deliberately introduced into South Africa for the biological control of their host plants, which are invasive in that country.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 15 Dec 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|South Africa||Present||Introduced||Uromycladium morrisii: Widespread after being deliberately introduced for biological control of Acacia saligna in 1987. Uromycladium woodii: Localised after being deliberately introduced for biological control of Paraserianthes lophantha in 2016|
|Indonesia||Present||Native and Introduced||Uromycladium falcatariae: introduced and invasive. Present on Bali, Java, Kalimantan, Moluccas and South Celebes. Uromycladium sp.: native and non-invasive. The identity of this taxon has not been determined by phylogenetic studies.|
|-Borneo||Present||Introduced||Uromycladium falcatariae. East Kalimantan|
|-Java||Present, Widespread||Introduced||2003||Invasive||Uromycladium falcatariae|
|-Lesser Sunda Islands||Present, Widespread||Introduced||2006||Invasive||Uromycladium falcatariae. Bali|
|-Maluku Islands||Present||Introduced||1997||Invasive||Uromycladium falcatariae|
|-Sulawesi||Present, Widespread||Introduced||Invasive||Uromycladium falcatariae|
|Malaysia||Present, Localized||Introduced||1992||Invasive||Uromycladium falcatariae. Sabah|
|-Sabah||Present, Widespread||Introduced||1992||Invasive||Uromycladium falcatariae|
|Philippines||Present, Widespread||Introduced||1989||Invasive||Uromycladium falcatariae|
|Australia||Present, Widespread||Native||Uromycladium tepperianum, Uromycladium brachycarpae, Uromycladium farinosae, Uromycladium flavescentis, Uromycladium holosericeae, Uromycladium implexae, Uromycladium leiocalycis, Uromycladium ligustrinae, Uromycladium maslinii, Uromycladium merrallii, Uromycladium mitchellii, Uromycladium morrisii, Uromycladium murphyi, Uromycladium paradoxae, Uromycladium scirpifoliae, Uromycladium tetragonophyllae, Uromycladium woodii. There are likely additional undescribed species in Australia|
|New Caledonia||Present||Native||Uromycladium sp. The identity of this taxon has not been determined by phylogenetic studies|
|New Zealand||Present, Widespread||Introduced||Invasive||Uromycladium murphyi, Uromycladium paradoxae, Uromycladium sp (the identity of one of these species has not been determined by phylogenetic studies). Uromycladium spp. were introduced to New Zealand some time before 1920|
|Papua New Guinea||Present||Native||Uromycladium falcatariae. The host species Falcataria moluccana is native to this island, and presumably therefore the rust fungus as well|
|Tokelau||Present, Widespread||Introduced||1998||Invasive||Uromycladium falcatariae|
History of Introduction and SpreadTop of page
Cunningham (1931) noted that by 1926 Uromycladium murphyi (as U. notabile) was a “serious disease of species of Acacia grown as ornamentals and for tan bark” in New Zealand, in particular Acacia decurrens and Acacia dealbata. This disease was at least partly responsible for preventing the development of a tannin producing industry in New Zealand, which was to be based on plantations of A. decurrens (Dick 1985). At least two species, U. paradoxae and U. tepperianum, also reached New Zealand prior to 1926 (Cunningham, 1931). These may have reached New Zealand via the trans-Tasman airflows, or alternatively they may have been introduced along with planting material (McKenzie, 1998).
Braza (1997) suggested that the wattle gall rust on Falcataria moluccana was introduced from New Zealand to the Philippines, which is unlikely as U. flacatariae has not been been reported in New Zealand. Rahayu et al. (2010) summarized the spread of the disease through the Malay Archipelago. The first record is from the Philippines (Braza, 1997), which is north-west of New Guinea, where F. moluccana naturally occurs. Thus the monsoon winds from the south-east could have dispersed the rust there. Lee (2004) suggests that the rust fungus spread from the Philippines to Sabah, Malaysia, by wind. From there it appears to have spread southwards down the island of Borneo to Kalimantan, Indonesia, and then elsewhere.
Uromycladium morrisii was first introduced into South Africa in 1987, at a single site (Morris, 1991). From 1988 to 1996 this taxon was established at a further 174 sites, but no further spread was undertaken, as by 1996 galls were visible in every stand of Acacia saligna (Wood and Morris, 2007), a range of approximately 900 km from West to East.
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|New Zealand||Australia||Early 1900s||Yes||No||Cunningham (1931); McKenzie (1998); Gadgil (2005)||Uromycladium murphyi|
|New Zealand||Australia||Early 1900s||Yes||No||Cunningham (1931); McKenzie (1998); Gadgil (2005)||Uromycladium paradoxae|
|New Zealand||Australia||Early 1900s||Yes||No||Cunningham (1931); McKenzie (1998); Gadgil (2005)||Uromycladium sp.|
|Philippines||New Guinea||1989||Yes||No||Braza (1997)||Uromycladium falcatariae|
|Sabah||Philippines||1992||Yes||No||Lee (2004); Rahayu et al. (2010)||Uromycladium falcatariae|
|East Timor||1998||Yes||No||Lestari et al. (2013); Baskorowati et al. (2012); Rahayu et al. (2010)||Uromycladium falcatariae|
|Indonesia||2003||Yes||No||Lestari et al. (2013); Baskorowati et al. (2012); Rahayu et al. (2010)||Uromycladium falcatariae|
|South Africa||Australia||1987||Biological control (pathway cause)||Yes||No||Morris (1991); Morris (1997); Wood and Morris (2007); Wood (2012)||Uromycladium morrisii. Causes high levels of damage, and eventually death. Deliberately introduced for the biological control of Acacia saligna|
|South Africa||Australia||2016||Biological control (pathway cause)||Yes||No||Uromycladium woodii. Deliberately introduced for the biological control of Paraserianthes lophantha|
Risk of IntroductionTop of page
The gall forming Uromycladium spp. are host specific, each being limited to a single host plant species, or several closely related host plant species. Each species is potentially invasive if their host plant species are grown outside of their native range. They may be transported by long distance wind dispersal, depending on prevailing wind directions. Otherwise human intervention (deliberate or accidental) would be required to introduce the taxa. However, as the species are apparently host specific, non-host plant species are unlikely to be attacked and therefore the risk to plant species not known to be hosts is very low.
Once present, the species disperse rapidly and are very difficult to control.
HabitatTop of page
All of the gall forming Uromycladium spp. are associated with the habitats occupied by their host plant species. Depending on the host species ranges, species occupy Mediterranean, temperate and tropical climatic zones. A number of these host species have been introduced to various regions in the world where they are cultivated for many purposes, including timber and pulp, tannin production, ornamentals, and agroforestry. In certain regions, the host plants have become serious invaders of natural habitats and areas disturbed for agricultural purposes.
In their natural habitat, these taxa may be common and widespread (e.g. U. morrisii), or rare and/or localized on their host plants (e.g. U. woodii). In the latter case, some species may well qualify for red data status. Where common, they impact on the population dynamics of their hosts, and are an integral component of the associated ecosystems.
Where host plants have been deliberately planted, and are considered useful plants, the associated rust species can cause economically damaging disease, for example U. falcatariae on Falcataria moluccana. Where the host plants have become invaders, the associated rust species can be valuable biological control agents, for example U. morrisii for the biological control of Acacia saligna in South Africa.
Habitat ListTop of page
|Terrestrial||Managed||Managed forests, plantations and orchards||Principal habitat||Harmful (pest or invasive)|
|Terrestrial||Managed||Disturbed areas||Principal habitat||Natural|
|Terrestrial||Managed||Disturbed areas||Principal habitat||Productive/non-natural|
|Terrestrial||Managed||Urban / peri-urban areas||Secondary/tolerated habitat||Natural|
|Terrestrial||Managed||Urban / peri-urban areas||Secondary/tolerated habitat||Productive/non-natural|
|Terrestrial||Natural / Semi-natural||Natural forests||Principal habitat||Natural|
|Terrestrial||Natural / Semi-natural||Scrub / shrublands||Principal habitat||Natural|
Hosts/Species AffectedTop of page
In their native range, the gall forming Uromycladium spp. are associated with the following host plants (Doungsa-Ard et al., 2018). The Uromycladium species on other host plant species not listed need to be determined by molecular phylogenetic techniques:
Uromycladium tepperianum: Acacia ligulata, Acacia rostellifera, Acacia sclerosperma, Acacia xanthina. Note that the type host is Acacia salacina, however this record is likely Acacia ligulata according to Doungsa-Ard et al. (2018)
Uromycladium brachycarpae: Acacia brachycarpa
Uromycladium falcatariae: Falcataria moluccana (=Paraserianthes falcataria, Albizia falcataria)
Uromycladium farinosae: Acacia farinosa
Uromycladium flavescentis: Acacia flavescens
Uromycladium holosericeae: Acacia holosericea
Uromycladium implexae: Acacia implexa
Uromycladium leiocalycis: Acacia leiocalyx
Uromycladium ligustrinae: Acacia ligustrina
Uromycladium maslinii: Acacia acuminata, Acacia burkittii, Acacia coolgardiensis, Acacia cyclops, Acacia gibbosa, Acacia incognita, Acacia latior, Acacia patagiata, Acacia resinimarginea, Acacia sibina, Acacia yorkrakinensis
Uromycladium merrallii: Acacia merrallii
Uromycladium mitchellii: Acacia trudgeniana
Uromycladium morrisii: Acacia saligna
Uromycladium murphyi: Acacia baileyana, Acacia dealbata, Acacia decurrens, Acacia elata, Acacia mearnsii, Acacia penninervis, Acacia rubida
Uromycladium paradoxae: Paraserianthes lophantha subsp. montana, Acacia paradoxa (= Acacia armata), Acacia stricta, Acacia verniciflua
Uromycladium scirpifoliae: Acacia scirpifolia
Uromycladium tetragonophyllae: Acacia tetragonophylla
Uromycladium woodii: Paraserianthes lophantha
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page
SymptomsTop of page
Brown woody galls develop on main stems, branches, inflorescences, seed pods and phyllodes or leaves of the host plants (Burges, 1934). Generally, galls on main stems can become very large and survive for several years, whereas those on smaller plant parts are themselves smaller. Infected phyllodes/leaves and inflorescences often drop from the plants several months after infection. McAlpine (1906) recorded the largest single gall he saw to be approximately 1.4kg (3lb) in weight, typically they are smaller. Galls are variously shaped, depending on host plant and organ infected. Witches’ brooms may also develop on some hosts when a growth tip or an axillary bud is infected. Hundreds (Rahayu et al., 2010) to thousands (Wood, 2012) of galls can infect a single tree.
Infection is not latent, but the first sign of developing galls occurs approximately six weeks or more after infection.
List of Symptoms/SignsTop of page
|Fruit / galls|
|Inflorescence / galls|
|Leaves / abnormal forms|
|Stems / galls|
|Stems / witches broom|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page
Burges (1934) stated that the first signs of gall development of U. paradoxae (as U. tepperianum) on Acacia stricta in eastern Australia occur in February or March. By the end of March, teliospores are produced. The galls continue to grow and sporulate throughout the year until around August when they die, unless growing from a main stem, in which case they are perennial. This phenology may be common to those species which occur in temperate summer rainfall climates, with infection occurring during the early summer rains when the host plants are growing (October to December in the Southern Hemisphere).
In South Africa, the first signs of gall development of U. morrisii occur in approximately September, and spermogonia are produced between November and January during the hot dry summer. Teliospores are produced throughout the winter rainfall season, from May onwards. In contrast, galls of U. woodii develop throughout the winter rainfall season, from April to November.
The timing of infections, gall development and spermogonia and teliospore production have not been recorded for other taxa. Each taxon may differ in the specific timing of these events due to differences in host phenology and climatic conditions. A generalized assumption can be made that teliospores will be produced in periods when infection can occur, which is during the host plant’s growth period, which would usually be associated with the rainy season and when cool temperatures occur.
Physiology and phenology
All hosts are perennial woody bushes or trees. Any young expanding host tissue is susceptible to infection, whereas nearly fully expanded to mature tissue is immune. Thus any growing branch tips, or new phyllodes/leaves or inflorescences can be infected. These rust fungi can survive unfavourable weather periods (e.g. dry season) within the galls.
Typically galls on main stems live for several to many years, and can reach a large size. Galls on phylodes or leaves, inflorescences or minor side branches typically live for one, or less than one, year. Sometimes the pedicel or peduncle are also infected, in which case the gall survives for longer. In general, the larger the supporting plant structure, the larger the gall can grow and the longer it can live.
Teliospores have melanised thickened walls, a trait which is associated with teliospores remaining viable for a relatively long time, although there is no published data on teliospore longevity. Teliospores of U. morrisii have been observed to remain viable when stored at 5°C for between 3 and 9 months after harvesting.
Galls grow and teliospores are produced when the host plants are actively growing. The phenology of the host therefore determines the season and duration of gall growth and when infection occurs.
Population size and density
Gall density appears to be host density dependent (Wood, 2012). Where the host is densely planted, or occurs in large dense invasions, incidence of mature trees may be up to 100% (Wood, 2012), unless environmental conditions are unfavourable for the fungi. The severity of infection differs widely between plants, as well as between years on individual plants. This is reflected by trees of Acacia saligna which, as they mature, can have a rapidly increasing number of galls from one year to the next, going from tens to hundreds if not thousands of galls in a single year (Wood, 2012).
Lestari et al. (2013) noted lower levels of disease incidence, and low severity, in various agroforestry systems in central Java. Average temperatures during this study were between 34 and 40.9°C, and the higher temperatures were associated with lower incidence and severity.
The gall forming Uromycladium spp. are obligate biotrophs that obtains all nutrients from the plant host.
Teliospores of U. morrisii germinate at temperatures between 10 and 20°C. Morris (1987) obtained infection on Acacia saligna at temperatures of 18–20°C for this taxon. In contrast, Widyastuti et al. (2013) infected Falcataria molucanna with U. falcatariae at 25–30°C.
ClimateTop of page
|Af - Tropical rainforest climate||Tolerated||> 60mm precipitation per month||Associated mostly with higher altitude areas|
|Cs - Warm temperate climate with dry summer||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Preferred||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Erechthias mystacinella||Herbivore||not specific|
|Holocola triangulana||Herbivore||not specific|
|Stathmopoda cephalaea||Herbivore||not specific|
|Thaumatotibia leucotreta||Herbivore||not specific|
|Trichothecium roseum||Pathogen||not specific|
Notes on Natural EnemiesTop of page
Seven species of Lepidoptera were reared from galls, in which they tunnel and feed, of U. murphyi on Acacia decurrens in Melbourne, Australia (New, 1982). The three most common species together made up 91% of the total number of moths reared. Galls had up to five species of moth present, and although the average number of moth individuals per gall was 10.1, a few galls had 80 or more individuals each (New, 1982). Dick (1985) comments that insect larvae frequently bore through the galls in New Zealand. Old and Cristovao (2003) noted that insects and fungi were colonizing galls in East Timor, and Triyogo and Widyastuti (2012) recorded that a lepidopteran (Heliozelidae) completed its development in galls in Indonesia. Braza (1997) recorded that Lepidopteran larvae frequently fed on and destroyed galls, reducing the impact of the disease in at least one province of the Philippines.
Seymour and Veldtman (2010) recorded that a number of Lepidoptera formed associations with galls of U. morrisii in South Africa, although only one species was identified, the polyphagous Thaumatotibia leucotreta. A total of 24 Lepidoptera have been recorded in South Africa on morphologically similar galls caused by Ravenelia macowaniana on Vachelia karoo [Acacia karoo] (Krüger, 1998). At least some of these indigenous moth species have spread to galls of U. morrisii. Morris (1999) records three fungi attacking galls of Uromycladium morrisii. These fungi are widespread and common parasites of rust fungi, or generalist mycopathogens.
Galls on plants caused by Uromycladium spp. are commonly fed on by a range of insects, particularly Lepidoptera (polyphagous gall or fruit feeders), and rust specific or generalist mycopathogens. This is both in their native range and where they have been introduced or invaded. These organisms can be abundant, so that many galls survive for less than a year, when they could potentially live for several years. Most of the associated organisms have not been identified to species level.
Means of Movement and DispersalTop of page
Teliospores are wind dispersed. Teliospores may remain viable for several months after production.
Vector transmission (biotic)
The majority of spores would be wind dispersed, however any organism coming into contact with the spores may potentially disperse them. Triyogo and Widyastuti (2012) demonstrated that a moth (Lepidoptera; Heliozelidae) which tunneled within galls of U. falcatariae had teliospores adhering to adults which had emerged from sporulating galls. Melanterius maculatus (Coleoptera; Curculionidae), imported into South Africa as biological control agents for use against Acacia mearnsii, were found to carry teliospores of U. murphyi, even though these beetles are seed feeding and not associated with galls (Dennill et al. 1999). Several other species of Melanterius have also been introduced to South Africa (Dennill et al. 1999), but none have introduced any Uromycladium species.
No cases of accidental introduction have been reported, as it is supposed that the introduction of taxa to New Zealand, the Philippines and Malaysia was by wind. However, the possibility of teliospores being transported on packaging or other human manufactured objects can’t be discounted, and likely does happen. Once the teliospores are dispersed to another area, the teliospores would need to be lifted from the object by wind and deposited on a susceptible host, a requirement which is likely a major bottleneck.
Uromycladium morrisii and U. woodii were been deliberately introduced as biological control agents of their host trees in South Africa.
Pathway CausesTop of page
|Biological control||Deliberately introduced for biological control of host plants which are invasive||Yes||Yes||Morris (1991); Morris (1999)|
|Self-propelled||Dispersed by wind from Australia to New Zealand. Likely also dispersed by wind between and within Papua New Guinea, Indonesia, Malaysia, Philippines||Yes||Yes||McKenzie (1998); Lee (2004)|
Pathway VectorsTop of page
Impact SummaryTop of page
Economic ImpactTop of page
Falcataria moluccana has been planted extensively throughout the Malay Archipelago. It is used as a timber crop and as a shade cover crop in coffee plantations, amongst other uses. Since the early 1990’s, U. falcatariae has spread through the Philippines, Malaysia, Indonesia and East Timor, causing crown thinning, branch dieback and, in severe cases, death of the host plant (Braza, 1997; Old and Cristavo, 2003; Rahayu et al., 2010). This has resulted in the reduced productivity of timber plantations, or required the replanting of alternative trees to provide shade in coffee plantations.
Acacia decurrens and Acacia mearnsii would be at risk if U. murphyi was introduced to regions where they are cultivated as crops. U. murphyi contributed to the failure of the incipient Acacia decurrens plantation industry in New Zealand in the 1920s (Dick, 1985).
Environmental ImpactTop of page
In their natural habitat in Australasia, the gall forming Uromycladium spp. are indigenous, and an integral part of the natural ecosystems. Where their host plant species have been introduced outside of their native range, no indigenous plants or animals are threatened by the presence of these rust fungi, despite any potential economic damage. Where the host plants are themselves invasive, these rust fungi are useful as biological control agents, reducing the impact of the host plants themselves on the natural ecosystem.
Risk and Impact FactorsTop of page
- Proved invasive outside its native range
- Has a broad native range
- Abundant in its native range
- Tolerant of shade
- Highly mobile locally
- Long lived
- Has high reproductive potential
- Host damage
- Negatively impacts agriculture
- Negatively impacts forestry
- Negatively impacts livelihoods
- Damages animal/plant products
- Competition - monopolizing resources
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult/costly to control
UsesTop of page
Various host plant species of the gall forming Uromycladium spp. have become invasive in natural ecosystems in various countries around the world to which they had been introduced. Each species is therefore a potential biological control agent of its host plant, where that plant has become invasive. U. morrisii was introduced to South Africa for the control of Acacia saligna in 1987, where it has proven to be both safe and effective (Morris, 1991; 1997; 1999; Wood and Morris, 2007). Following this success, Uromycladium woodii has also been introduced into South Africa for the control of Paraserianthes lophantha.
It has been suggested that biological control of Falcataria moluccana in Hawaii and other Pacific Islands is feasible (Hughes et al., 2013). U. falcatariae would be the appropriate taxon to consider for this purpose.
Uses ListTop of page
- Biological control
DiagnosisTop of page
In many cases, the gall forming Uromycladium spp. can be identified by microscopic examination of teliospores, together with the identity of the host species. Comparison of the sequences of the LSU and ITS ribosomal genes, and the CO3 mitochondrial gene to ex-type sequences available in databases such as Genbank (Benson et al., 2003), are required to confirm species identity.
Detection and InspectionTop of page
Infected plants are easily identified by visual inspection. Large brown, woody galls are produced on stems, branches, phyllodes/leaves, inflorescences or seed pods of Australian Acacia and closely related plant species. Teliospores produced in abundance on the gall surface, usually during the rainy season, so that galls appear covered in a dry brown powder.
Detection of viable teliospores carried unintentionally on vectors is difficult as the teliospores are approximately 20 µm in diameter and require a light microscope with a minimum of 100 × magnification.
Similarities to Other Species/ConditionsTop of page
Teliospores of gall forming Uromycladium spp. are depressed globose in shape and ridged (or warted), with a single germ pore in the apical depression and with a pedicel scar in the basal depression, which readily distinguishes them from other genera of Pucciniales.
They are distinguished from other Uromycladium species by having three single-celled teliospores per pedicel without a vesicle. In addition, the teliospore walls are ornamented with ridges (striae), these may be continuous or broken into warts. All other species of Uromycladium have only one or two teliospores with apparently smooth walls (as seen using a light microscope), and with or without a vesicle.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Gall forming Uromycladium spp. are listed as regulated pests by the USDA (Cline and Farr, 2006). They were considered to have a high risk potential to Acacia koa, which is endemic to Hawaii, due to the broad host range recorded (DeNitto et al., 2015). However, of the currently recognized gall forming Uromycladium spp., only U. implexae is potentially a threat in Hawaii, as its host plant (Acacia implexa) is one of the species most closely related to Acacia koa (Brown et al., 2012).
Where the host plants are cultivated and are considered to have economic value, away from their natural range, each of the taxa of the species complex would pose a threat to their specific host plants. Quarantine regulations should be applied.
Once established, eradication will be impossible as the wind-borne teliospores would rapidly spread the disease both within populations and to distant populations.
Chemical control would in most cases be impractical, due to the large size of the hosts and the cost of applying chemicals on a frequent basis.
Old and Cristovao (2003) suggested that a practical method of control of U. falcatariae was to replace infected trees with an alternative tree that is not a host. They also suggested that breeding for resistance may be possible and efforts towards this goal are being undertaken (e.g. Rahayu et al., 2009; Baskorowati et al., 2012).
Gaps in Knowledge/Research NeedsTop of page
The taxonomy of the gall forming Uromycladium spp. is not yet complete. Material from additional hosts not yet included should be examined to complete our knowledge of the species and their natural host range.
Infection studies have only been carried out on only two taxa, U. morrisii (Morris, 1987) and U. falcatariae (Rahayu et al., 2010; Widyastuti et al., 2013). There are contradictions in the process described in the two papers dealing with U. falcatariae, which requires resolution.
ReferencesTop of page
Baskorowati L, Susanto M, Charomaini M, 2012. Genetic variability in resistance of Falcataria moluccana (Miq.) Barneby & J.W. Grimes to gall rust disease. Journal of Forestry Research, 9, 1-9.
Berndt R, 2011. Taxonomic revision of Endoraecium digitatum (rust fungi, Uredinales) with description of four new species from Australia and Hawaii. Mycological Progress, 10, 497-517.
Braza RD, 1997. Gall rust disease of Paraserianthes falcataria in the Philippines. Forest, Farm, and Community Tree Research Reports, 2, 61-62.
Brown, G. K., Murphy, D. J., Kidman, J., Ladiges, P. Y., 2012. Phylogenetic connections of phyllodinous species of Acacia outside Australia are explained by geological history and human-mediated dispersal. Australian Systematic Botany, 25(6), 390-403. http://www.publish.csiro.au/nid/150.htm doi: 10.1071/SB12027
BURGES, A. , 1934. Studies in the genus Uromycladium (Uredineae). I. General introduction, the anatomy of the galls, and the cytology of the vegetative mycelium and pycnia of Uromycladium tepperianum (Sacc.) McÂlp. on Acacia stricta Willd. Proceedings of the Linnean Society of New South Wales, 59(3-4), 212-228 pp.
Cline, E. T., Farr, D. F., 2006. Synopsis of fungi listed as regulated plant pests by the USDA Animal and Plant Health Inspection Service: notes on nomenclature, disease, plant hosts, and geographic distribution. Plant Health Progress, (May), 1-44. http://www.plantmanagementnetwork.org/php/
Cunningham GH, 1931. The rust diseases of New Zealand, Dunedin, New Zealand: John McIndoe Ltd.261 pp.
DeNitto, G. A., Cannon, P., Eglitis, A., Glaeser, J. A., Maffei, H., Smith, S., 2015. General Technical Report - Pacific Southwest Research Station, USDA Forest Service, Berkeley, USA: Pacific Southwest Research Station, USDA Forest Service (No.PSW-GTR-250), 171 pp. http://www.fs.fed.us/psw/publications/documents/psw_gtr250/psw_gtr250.pdf
Dennill, G. B., Donnelly, D., Stewart, K., Impson, F. A. C., 1999. Insect agents used for the biological control of Australian Acacia species and Paraserianthes lophantha (Willd.) Nielsen (Fabaceae) in South Africa. In: Biological control of weeds in South Africa (1990-1998) [ed. by Olckers, T., Hill, M. P.]. Pretoria, South Africa: Entomological Society of Southern Africa.45-54.
Doungsa-ard, C., McTaggart, A. R., Geering, A. D. W., Dalisay, T. U., Ray, J., Shivas, R. G., 2015. Uromycladium falcatarium sp. nov., the cause of gall rust on Paraserianthes falcataria in south-east Asia. Australasian Plant Pathology, 44(1), 25-30. http://link.springer.com/article/10.1007%2Fs13313-014-0301-z doi: 10.1007/s13313-014-0301-z
Doungsa-Ard, C., McTaggart, A. R., Geering, A. D. W., Shivas, R. G., 2018. Diversity of gall-forming rusts (Uromycladium, Pucciniales) on Acacia in Australia. Persoonia, 40, 221-238. https://www.ingentaconnect.com/content/nhn/pimj/2018/00000040/00000001/art00010# doi: 10.3767/persoonia.2018.40.09
Farr DF, Rossman AY, 2019. Fungal databases. Systematic Mycology and Microbiology Laboratory, USDA-ARS.http://nt.ars-grin.gov/fungaldatabases/
Hughes, R. F., Johnson, M. T., Uowolo, A., 2013. The invasive alien tree Falcataria moluccana: its impacts and management. In: Proceedings of the XIII International Symposium on Biological Control of Weeds, Waikoloa, Hawaii, USA, 11-16 September, 2011 [Proceedings of the XIII International Symposium on Biological Control of Weeds, Waikoloa, Hawaii, USA, 11-16 September, 2011], [ed. by Wu, Y., Johnson, T., Sing, S., Raghu, S., Wheeler, G., Pratt, P., Warner, K., Center, T., Goolsby, J., Reardon, R.]. Hilo, USA: USDA Forest Service, Pacific Southwest Research Station, Institute of Pacific Islands Forestry. 218-223.
Krüger, M., 1998. Identification of the adults of Lepidoptera inhabiting Ravenelia macowaniana Pazschke (Uredinales) galls on Acacia karroo Hayne (Fabaceae) in southern Africa. African Entomology, 6(1), 55-74.
Lestari P, Rahayu S, Widiyatno, 2013. Dynamics of gall rust disease on sengon (Falcataria moluccana) in various agroforestry patterns. Procedia Environmental Sciences, 17, 167-171.
Magnus P, 1892. (Zur kenntniss der verbreitung einiger pilze). Bericht der Deutschen Botanischen Gesellschaft, 10, 195-200.
McAlpine D, 1905. A new genus of Uredineae – Uromycladium. Annales Mycologici, 3, 303-323 and Plates VI-IX.
Morris, M. J., 1999. The contribution of the gall-forming rust fungus Uromycladium tepperianum (Sacc.) McAlp. to the biological control of Acacia saligna (Labill.) Wendl. (Fabaceae) in South Africa. In: Biological control of weeds in South Africa (1990-1998) [ed. by Olckers, T., Hill, M. P.]. Pretoria, South Africa: Entomological Society of Southern Africa.125-128.
Nielsen, I., Guinet, P., Baretta-Kuipers, T., 1983. Studies in the Malesian, Australian and Pacific Ingeae (Leguminosae-Mimosoideae): the genera Archidendropsis, Wallaceodendron, Paraserianthes, Pararchidendron and Serianthes (part 2). Bulletin du Muséum National d'Histoire Naturelle, B (Adansonia), 5(4), 335-360.
Old KM, Cristovao CDS, 2003. A rust epidemic of the coffee shade tree (Paraserianthes falcataria) in East Timor. In: Agriculture: New directions for a new nation – East Timor (Timor-Leste). ACAIR Proceedings no. 113 [ed. by da Costa H, Piggin C, da Cruz CJ, Fox JJ]. http://www.gov.east-timor.org/MAFF/ta100/ta120.pdf
Rahayu, S., Lee SuSee, Nor Aini, A. S., 2010. Uromycladium tepperianum, the gall rust fungus from Falcataria moluccana in Malaysia and Indonesia. Mycoscience, 51(2), 149-153. http://www.springerlink.com/content/m03x38215530r110/fulltext.html doi: 10.1007/s10267-009-0022-2
Rahayu, S., Shukor, N. A. A., See LeeSu, Saleh, G., 2009. Responses of Falcataria moluccana seedlings of different seed sources to inoculation with Uromycladium tepperianum. Silvae Genetica, 58(1/2), 62-68. http://www.sauerlaender-verlag.com
Rust Fungi of Australia, 2020. Uromycladium tepperianum. Queensland, Australia: DAF Biological Collections.https://collections.daff.qld.gov.au/web/key/rustfungi/Media/Html/uromycladiumtepperianum.html
Seymour CL, Veldtman R, 2010. Ecological role of control agent, and not just host-specificity, determine risks of biological control. Austral Ecology, 35, 704-711.
Systematic Mycology and Microbiology Laboratory, 2007. Uromycladium tepperianum on Acacia spp. In: Invasive and Emerging Fungal Pathogens - Diagnostic Fact Sheets, USDA-ARS.https://nt.ars-grin.gov/taxadescriptions/factsheets/index.cfm?thisapp=Uromycladiumtepperianum
Triyogo A, Widyastuti dSM, 2012. The role of insect as vector of gall rust disease of Albizia falcataria L. Fosberg. Journal of Agronomy Indonesia, 40, 77-82.
Widyastuti SM, Harjono, Surya ZA., 2013. Initial infection of Falcataria moluccana leaves and Acacia mangium phyllodes by Uromycladium tepperianum fungi in a laboratory trial. Journal of Tropical Forestry Research (Jurnal Manajemen Hutan Tropika), 19, 187-193.
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Wood, A. R., Morris, M. J., 2007. Impact of the gall-forming rust fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa: 15 years of monitoring. Biological Control, 41(1), 68-77. http://www.sciencedirect.com/science/journal/10499644 doi: 10.1016/j.biocontrol.2006.12.018
Baskorowati L, Susanto M, Charomaini M, 2012. Genetic variability in resistance of Falcataria moluccana (Miq.) Barneby & J.W. Grimes to gall rust disease. Journal of Forestry Research. 1-9.
Braza RD, 1997. Gall rust disease of Paraserianthes falcataria in the Philippines. Forest, Farm, and Community Tree Research Reports. 61-62.
CABI, 2020. CABI Distribution Database: Status inferred from regional distribution. Wallingford, UK: CABI
Cunningham GH, 1931. The rust diseases of New Zealand. Dunedin, New Zealand: John McIndoe Ltd. 261 pp.
Lestari P, Rahayu S, Widiyatno, 2013. Dynamics of gall rust disease on sengon (Falcataria moluccana) in various agroforestry patterns. Procedia Environmental Sciences. 167-171.
Magnus P, 1892. (Zur kenntniss der verbreitung einiger pilze). Bericht der Deutschen Botanischen Gesellschaft. 195-200.
McAlpine D, 1905. A new genus of Uredineae – Uromycladium. Annales Mycologici. 303-323.
Nielsen I, Guinet P, Baretta-Kuipers T, 1983. Studies in the Malesian, Australian and Pacific Ingeae (Leguminosae-Mimosoideae): the genera Archidendropsis, Wallaceodendron, Paraserianthes, Pararchidendron and Serianthes (part 2). Bulletin du Muséum National d'Histoire Naturelle, B (Adansonia). 5 (4), 335-360.
Old KM, Cristovao CDS, 2003. A rust epidemic of the coffee shade tree (Paraserianthes falcataria) in East Timor. In: New directions for a new nation – East Timor (Timor-Leste) [ACAIR Proceedings no. 113], [ed. by da Costa H, Piggin C, da Cruz CJ, Fox JJ]. http://www.gov.east-timor.org/MAFF/ta100/ta120.pdf
Rahayu S, Lee SuSee, Nor Aini A S, 2010. Uromycladium tepperianum, the gall rust fungus from Falcataria moluccana in Malaysia and Indonesia. Mycoscience. 51 (2), 149-153. DOI:10.1007/s10267-009-0022-2
Sato H, Ban S, Masuya H, Hosoya T, 2010. Reassessment of type specimens of Cordyceps and its allies described by Dr. Yosio Kobayasi preserved in the mycological herbarium of the National Museum of Nature and Science (TNS). Part 1: The genus Torrubiella. Mycoscience. 51 (2), 154-161. DOI:10.1007/s10267-009-0015-1
Wood A R, 2012. Uromycladium tepperianum (a gall-forming rust fungus) causes a sustained epidemic on the weed Acacia saligna in South Africa. Australasian Plant Pathology. 41 (3), 255-261. DOI:10.1007/s13313-012-0126-6
Wood A R, Morris M J, 2007. Impact of the gall-forming rust fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa: 15 years of monitoring. Biological Control. 41 (1), 68-77. http://www.sciencedirect.com/science/journal/10499644 DOI:10.1016/j.biocontrol.2006.12.018
Zachariades C, 2018. Biological control of invasive alien plants in South Africa: a list of all insects, mites and pathogens released as biological control agents from 1913- 2018., South Africa: Agricultural Research Council. http://www.arc.agric.za/arc-ppri/Documents/Table2-NaturalEnemiesReleased.pdf
ContributorsTop of page
30/09/19 Original text by:
Alan R. Wood, Agricultural Research Council – Plant Health and Protection, Stellenbosch, South Africa
Distribution MapsTop of page
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