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Datasheet

Uromycladium tepperianum sensu lato
(Acacia gall rust fungus)

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Datasheet

Uromycladium tepperianum sensu lato (Acacia gall rust fungus)

Summary

  • Last modified
  • 14 February 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Uromycladium tepperianum sensu lato
  • Preferred Common Name
  • Acacia gall rust fungus
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Basidiomycota
  •       Subphylum: Pucciniomycotina
  •         Class: Pucciniomycetes
  • Summary of Invasiveness
  • Uromycladium tepperianum sensu lato is a species complex of gall forming rust fungi native to Australasia. It is invasive in New Zealand, the Philippines, East Timor, Malaysia and Indonesia.

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    Compendia
    CAB International
    Wallingford
    Oxfordshire
    OX10 8DE
    UK
    compend@cabi.org
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Identity

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Preferred Scientific Name

  • Uromycladium tepperianum sensu lato (Sacc.) McAlpine

Preferred Common Name

  • Acacia gall rust fungus

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 sensu stricto (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

EPPO code

  • URCLTE (Uromycladium tepperianum)

Summary of Invasiveness

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Uromycladium tepperianum sensu lato is a species complex of gall forming rust fungi native to Australasia. It is invasive in New Zealand, the Philippines, East Timor, Malaysia and Indonesia.

Uromycladium murphyi (as Uromycladium notabile in the literature) causes damage to a number of Acacia species grown for tannin and as ornamentals in New Zealand, particularly A. decurrens. Other Acacia species such as A. baileyana, A. dealbata and A. mearnsii have also been identified as hosts for U. murphyi. Uromycladium paradoxae infects Acacia paradoxa in New Zealand. U. tepperianum s. lat. species have been found infecting New Zealand A. ulicifolia and A. verticillata, but the taxon that is present on these two hosts is uncertain, as these hosts have not been included in 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 tepperianum s. lat. has also been deliberately introduced in South Africa for the biological control of Acacia saligna and Paraserianthes lophantha. These taxa are now known as Uromycladium morrisii and Uromycladium woodii respectively.

All taxa are potentially invasive where their host plants have been planted.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Basidiomycota
  •             Subphylum: Pucciniomycotina
  •                 Class: Pucciniomycetes
  •                     Order: Pucciniales
  •                         Family: Pileolariaceae
  •                             Genus: Uromycladium
  •                                 Species: Uromycladium tepperianum sensu lato

Notes on Taxonomy and Nomenclature

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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 tepperianum s. lat. was recorded from over 100 host plants (Gathe, 1971; Morris, 1987), 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 there appeared to be host specific races within U. tepperianum s. lat. based on field observations. Morris (1987) demonstrated that isolates from three different hosts (Acacia saligna, Acacia implexa and Paraserianthes lophantha) had different host ranges. A recent molecular phylogenetic study on specimens from a total of 40 host plants resulted in the redefinition of this species in a narrow sense, and a total of 15 new species have been described (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. As currently circumscribed, U. tepperianum occurs only in South and Western Australia (Doungsa-Ard et al., 2018). All records outside of Australia of this name represent other species within this species complex.

Berndt (2011) considered the type specimen of Uredo notabilis, which McAlpine used as the type specimen for Uromycladium notabile, to be identical to the uredinial stage of Endoraecium digitatum. Therefore, the name Uredo notabilis is a synonym of E. digitatum, making the name Uromycladium notabile invalid. Doungsa-Ard et al. (2018) described a new species for this taxon – Uromycladium murphyi. U. murphyi as now circumscribed, does not have urediniospores, and has only spermogonia and teliospores, the same as for all other species within the Uromycladium tepperianum s. lat. species complex. U. murphyi does not occur on Acacia notabilis, the type host of Uredo notabilis and E. digitatum.

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 in the Uromycladium tepperianum sensu lato species complex

Uromycladium tepperianum sensu stricto

Uromycladium brachycarpae

Uromycladium falcatariae

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

Description

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This is a general description for the U. tepperianum s. lat. species complex. Forming small to very large brown galls on host plants, including on stems, branches, phyllodes/leaves, inflorescences and pods. Witches’ brooms also produced on some host plants. Spermogonia 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, easily brushed-off, powder. The galls may live for less than a year 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 erumpent from gall surface, bound by torn epidermal layer, confluent, frequently covering 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.

Within the U. tepperianum s. lat. species complex, species are 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 sensu stricto 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 ornamentation of warts rather than ridges (Doungsa-Ard et al., 2018).

Uromycladium falcatariae has been distinguished from other taxa within the species complex by having only 25–35 equatorial ridges, whereas other species have 30–45 (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 s. lat., with images, are available at Rust Fungi of Australia (2020) and Systematic Mycology and Microbiology Laboratory (2007).

Distribution

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Native to Australasia, the majority of taxa in this species complex 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.

In the distribution table, the notes field specifies which species within the U. tepperianum s. lat. species complex is found in that location.

Distribution Table

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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: 14 Feb 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

South AfricaPresentIntroducedZachariades (2018); Morris (1991); Morris (1997); Wood and Morris (2007); Wood (2012); 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

Asia

IndonesiaPresentNative and IntroducedCABI (2020); Magnus (1892); Boedijn (1959); Nielsen et al. (1983); Rahayu et al. (2010)Uromycladium falcatariae: introduced and invasive. Present on Bali, Java, Kalimantan, Moluccas and South Celebes. Uromycladium tepperianum sensu lato: native and non-invasive. The identity of this taxon has not been determined by phylogenetic studies.
-BorneoPresentIntroducedSato et al. (2010)Uromycladium falcatariae. East Kalimantan
-JavaPresent, WidespreadIntroduced2003InvasiveRahayu et al. (2010); Baskorowati et al. (2012); Lestari et al. (2013)Uromycladium falcatariae
-Lesser Sunda IslandsPresent, WidespreadIntroduced2006InvasiveRahayu et al. (2010)Uromycladium falcatariae. Bali
-Maluku IslandsPresentIntroduced1997InvasiveRahayu et al. (2010)Uromycladium falcatariae
-SulawesiPresent, WidespreadIntroducedInvasiveSato et al. (2010)Uromycladium falcatariae
MalaysiaPresent, LocalizedIntroduced1992InvasiveSato et al. (2010)Uromycladium falcatariae. Sabah
-SabahPresent, WidespreadIntroduced1992InvasiveLee (2004); Sato et al. (2010)Uromycladium falcatariae
PhilippinesPresent, WidespreadIntroduced1989InvasiveBraza RD (1997)Uromycladium falcatariae

Oceania

AustraliaPresent, WidespreadNativeDoungsa-Ard et al. (2018); McAlpine (1905); McAlpine (1906); Gathe (1971)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 within this species complex in Australia
New CaledoniaPresentNativeMouchacca and Horak (1998)Uromycladium tepperianum sensu lato. The identity of this taxon has not been determined by phylogenetic studies
New ZealandPresent, WidespreadIntroducedInvasiveGadgil (2005); Cunningham (1931); Dick (1985); McKenzie (1998)Uromycladium murphyi, Uromycladium paradoxae, Uromycladium tepperianum sensu lato. The identity of one of these taxa has not been determined by phylogenetic studies. Uromycladium tepperianum sensu lato was introduced to New Zealand some time before 1920
Papua New GuineaPresentNativeShaw (1984)Uromycladium falcatariae. The host species Falcataria moluccana is native to this island, and presumably therefore the rust fungus as well
TokelauPresent, WidespreadIntroduced1998InvasiveOld and Cristovao (2003)Uromycladium falcatariae

History of Introduction and Spread

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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 other taxa in the species complex, 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. However, since recent molecular phylogenetic studies has demonstrated that the rust fungus that causes this disease, U. flacatariae, is different to any species of Uromycladium present in New Zealand, this cannot be the case. 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.

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous 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 tepperianum sensu lato
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 Introduction

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The various taxa within this species complex are host specific, each being limited to a single host plant species, or several closely related host plant species. Each taxon is therefore potentially invasive if their host plant species is grown outside of its 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 taxa 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.

Habitat

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All species within the U. tepperianum s. lat. species complex are associated with the habitats occupied by their host plant species. Depending on the host species ranges, species within the U. tepperianum s. lat. species complex 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 List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedManaged forests, plantations and orchards Principal habitat Harmful (pest or invasive)
Disturbed areas Principal habitat Natural
Disturbed areas Principal habitat Productive/non-natural
Urban / peri-urban areas Secondary/tolerated habitat Natural
Urban / peri-urban areas Secondary/tolerated habitat Productive/non-natural
Terrestrial ‑ Natural / Semi-naturalNatural forests Principal habitat Natural
Scrub / shrublands Principal habitat Natural

Hosts/Species Affected

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In their native range, the taxa are associated with the following host plants (Doungsa-Ard et al., 2018). The taxa on other host species not listed need to be determined by molecular phylogenetic techniques:

Uromycaldium tepperianum sensu stricto: 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 Affected

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Plant nameFamilyContext
Acacia acuminataFabaceae
Acacia baileyana (cootamundra wattle)Fabaceae
Acacia brachycarpa
Acacia burkittiiFabaceae
Acacia coolgardiensisFabaceae
Acacia cyclops (coastal wattle)Fabaceae
Acacia dealbata (acacia bernier)Fabaceae
Acacia decurrens (green wattle)Fabaceae
Acacia elataFabaceae
Acacia farinosa
Acacia flavescensFabaceae
Acacia gibbosa
Acacia holosericeaFabaceae
Acacia implexaFabaceae
Acacia incognita
Acacia latior
Acacia leiocalyxFabaceae
Acacia ligulataFabaceae
Acacia ligustrinaFabaceae
Acacia mearnsii (black wattle)Fabaceae
Acacia merralliiFabaceae
Acacia paradoxa (kangaroo acacia)Fabaceae
Acacia patagiataFabaceae
Acacia penninervis (black wattle)Fabaceae
Acacia resinimarginea
Acacia rostelliferaFabaceae
Acacia rubidaFabaceae
Acacia saligna (Port Jackson wattle)Fabaceae
Acacia scirpifolia
Acacia sclerospermaFabaceae
Acacia sibina
Acacia stricta
Acacia tetragonophyllaFabaceae
Acacia trudgeniana
Acacia vernicifluaFabaceae
Acacia xanthinaFabaceae
Acacia yorkrakinensis
Falcataria moluccana (batai wood)Fabaceae
Paraserianthes lophantha (brush wattle)Fabaceae
Paraserianthes lophantha subsp. montana

Growth Stages

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Symptoms

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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/Signs

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SignLife StagesType
Fruit / galls
Inflorescence / galls
Leaves / abnormal forms
Stems / galls
Stems / witches broom
Whole plant / plant dead; dieback

Biology and Ecology

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Reproductive biology

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 inflorescensces can be infected. These rust fungi can survive unfavourable weather periods (e.g. dry season) within the galls.

Longevity

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.

Activity patterns

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.

Nutrition

The U. tepperianum s. lat. species complex are obligate biotrophs that obtains all nutrients from plant host.

Environmental requirements

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.

Climate

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ClimateStatusDescriptionRemark
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 Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
18 43

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological 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
Tuberculina Pathogen not specific
Verticillium Pathogen not specific

Notes on Natural Enemies

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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 the U. tepperianum s. lat. species complex 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 Dispersal

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Natural dispersal

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.

Accidental introduction

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.

Intentional introduction

Two taxa of the U. tepperianum s. lat. species complex have been deliberately introduced as biological control agents of their host trees in South Africa, namely U. morrisii and U. woodii.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Biological controlDeliberately introduced for biological control of host plants which are invasive Yes Yes Morris, 1991; Morris, 1999
Self-propelledDispersed 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 Vectors

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VectorNotesLong DistanceLocalReferences
Host and vector organismsPossible but not main means of dispersal. Living infected host material not traded. Yes Yes Triyogo and Widyastuti, 2012; Dennill et al., 1999
WindTeliospores readily dispersed by wind Yes Yes

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Positive

Economic Impact

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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.

Other host species, such as Acacia decurrens and Acacia mearnsii, are at risk if the associated taxon of the U. tepperianum s. lat. species complex were to be introduced to where they are productive crops. U. murphyi contributed to the failure of the incipient Acacia decurrens plantation industry in New Zealand in the 1920’s (Dick, 1985).

Environmental Impact

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In their natural habitat in Australasia, the various taxa within the U. tepperianum s. lat. species complex 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 Factors

Top of page Invasiveness
  • 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
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts forestry
  • Negatively impacts livelihoods
  • Damages animal/plant products
Impact mechanisms
  • Competition - monopolizing resources
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult/costly to control

Uses

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Various host plant species of the U. tepperianum s. lat. species complex have become invasive in natural ecosystems in various countries around the world to which they had been introduced. Each of the various species within the complex 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, using a taxon in this species complex, in Hawaii and other Pacific Islands is a feasible option (Hughes et al., 2013). U. falcatariae would be the appropriate taxon to consider for this purpose.

Uses List

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Environmental

  • Biological control

Diagnosis

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The species complex can be diagnosed by microscopic examination of teliospores, as the teliospores are highly characteristic for the U. tepperianum s. lat. species complex as a whole. The host identity will indicate which species is present. Molecular phylogenetic techniques, comparing the sequences of the LSU and ITS ribosomal genes, and the CO3 mitochondrial gene to sequences available in databases such as Genbank (Benson et al., 2003), can be used to confirm which species is present.

Detection and Inspection

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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/Conditions

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All taxa within the U. tepperianum s. lat. species complex are distinguished from other Uromycladium species by having three single-celled teliospores per pedicel and no 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.

Single teliospores of taxa within the U. tepperianum s. lat. species complex are readily distinguished from teliospores of other genera of Pucciniales, as they 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.

Prevention and Control

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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.

SPS measures

Uromycladium tepperianum s. lat. is listed as a regulated pest by the USDA (Cline and Farr, 2006). It was 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 taxa within the U. tepperianum s. lat. species complex, 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.

Eradication

Once established, eradication will be impossible as the wind-borne teliospores would rapidly spread the disease both within populations and to distant populations.

Control

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 Needs

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The taxonomy of the U. tepperianum s. lat. species complex 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, so the correct details need to be confirmed. Also, other taxa need to be examined to determine if the pattern observed in these two hosts is common across the whole species complex.

References

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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.

Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., Wheeler, D. L., 2003. GenBank. Nucleic Acids Research, 31(1), 23-27. doi: 10.1093/nar/gkg057

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.

Boedijn, K. B., 1959. The Uredinales of Indonesia. Nova Hedwigia, 1, 463-496.

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.

Dick, M., 1985. Uromycladium rusts of Acacia. Forest Pathology in New Zealand, Forest Research Institute, New Zealand, (No. 15), 8pp.

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/

Gadgil, P. D., 2005. Fungi of New Zealand. Vol. 4 Fungi on Trees and Shrubs in New Zealand, Hong Kong, China: Fungal Diversity Press.437 pp.

GATHE, JANETTE., 1971. Host range and symptoms in Western Australia of the gall rust, Uromycladium tepperianum. Journal and Proceedings of the Royal Society of Western Australia, 54(4), 114-118 pp.

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.

Lee, S. S., 2004. Diseases and potential threats to Acacia mangium plantations in Malaysia. Unasylva (English ed.), 55(217), 31-35.

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.

McAlpine, D., 1906. The Rusts of Australia, Melbourne, Australia: Government Printer.

McKenzie, E. H. C., 1998. Rust fungi of New Zealand - An introduction, and list of recorded species. New Zealand Journal of Botany, 36(2), 233-271.

Morris, M. J., 1987. Biology of the Acacia gall rust, Uromycladium tepperianum. Plant Pathology, 36(1), 100-106. doi: 10.1111/j.1365-3059.1987.tb02183.x

Morris, M. J., 1991. The use of plant pathogens for biological weed control in South Africa. Agriculture, Ecosystems and Environment, 37(1-3), 239-255.

Morris, M. J., 1997. Impact of the gall-forming rust fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa. Biological Control, 10(2), 75-82. doi: 10.1006/bcon.1997.0560

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.

Mouchacca, J., Horak, E., 1998. Annotated checklist of New Caledonian Basidiomycota. II. Rusts and Smuts. Mycotaxon, 69, 13-30.

New, T. R., 1982. Lepidoptera from Uromycladium galls on Acacia. Australian Journal of Zoology, 30(2), 357-364. doi: 10.1071/ZO9820357

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.

Shaw, D. E., 1984. Research Bulletin, Department of Primary Industry, Papua New Guinea, (No.33) . vii + 344 pp.

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.

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. http://www.springerlink.com/content/k231m4x3765427g5/ 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

Distribution References

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.

Boedijn K B, 1959. The Uredinales of Indonesia. Nova Hedwigia. 463-496.

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.

Dick M, 1985. Uromycladium rusts of Acacia. Forest Pathology in New Zealand, Forest Research Institute, New Zealand. 8pp.

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. 221-238. DOI:10.3767/persoonia.2018.40.09

Gadgil P D, 2005. Fungi of New Zealand. Vol. 4 Fungi on Trees and Shrubs in New Zealand. Hong Kong, China: Fungal Diversity Press. 437 pp.

Gathe Janette, 1971. Host range and symptoms in Western Australia of the gall rust, Uromycladium tepperianum. Journal and Proceedings of the Royal Society of Western Australia. 54 (4), 114-118 pp.

Lee S S, 2004. Diseases and potential threats to Acacia mangium plantations in Malaysia. Unasylva (English ed.). 55 (217), 31-35.

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.

McAlpine D, 1906. The Rusts of Australia. Melbourne, Australia: Government Printer.

McKenzie E H C, 1998. Rust fungi of New Zealand - An introduction, and list of recorded species. New Zealand Journal of Botany. 36 (2), 233-271.

Morris M J, 1991. The use of plant pathogens for biological weed control in South Africa. Agriculture, Ecosystems and Environment. 37 (1-3), 239-255.

Morris M J, 1997. Impact of the gall-forming rust fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa. Biological Control. 10 (2), 75-82. DOI:10.1006/bcon.1997.0560

Mouchacca J, Horak E, 1998. Annotated checklist of New Caledonian Basidiomycota. II. Rusts and Smuts. Mycotaxon. 13-30.

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

Shaw D E, 1984. Research Bulletin, Department of Primary Industry, Papua New Guinea. vii + 344 pp.

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

Principal Source

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Draft datasheet under review

Contributors

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Original text by:

Alan R. Wood, Agricultural Research Council – Plant Health and Protection, Stellenbosch, South Africa

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