Issue No. 15 April 22, 2008 
 
Plant Disease of the Week
 
In This Issue
Rusts of Acacia koa #1 - Atelocauda digitata
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Plant Disease of the Week is a series of online bulletins about plant diseases that affect farms, nurseries, gardens, landscapes and forests in Hawaii. You are welcome to forward this message to anyone who might benefit from the information by using the link at the bottom of the page. You may unsubscribe at any time by using the "SafeUnsubscribe" link at the bottom of this page.

 
 
Rusts of Acacia koa 
 
I. Atelocauda digitata (gall rust)
 
 
The woody monarch of Hawaiian forests, Acacia koa Gray (koa), hosts at least five distinct rust diseases in Hawaii. The name rust derives from the uniquely powdery texture and brownish to orange coloration of fungal spore masses that appear on plants, and in the case of koa, mainly brownish spore masses on diseased phyllodes, flowers and fruits. 
 
A general diagnosis of "koa rust" is readily determined by the presence of these distinctive and typical spore masses. To narrow the diagnosis to one of the specific rust diseases of A. koa requires an understanding of symptom expression and the fungal morphology associated with a disease and its pathogen.
 
One of the most widespread and important rust diseases of A. koa in Hawaii and one of the most important of all diseases of Acacia mangium in Java, Sumatra and Indonesia is caused by Acacia koa Graythe rust fungus, Atelocauda digitata. This is one of the rare macrocyclic rust fungi in Hawaii, meaning that it produces all five spore stages that are typical of macrocyclic rust fungi and diseases in general. 
 
Atelocauda digitata occurs on all major islands, except it has yet to be reported from Lanai.
 
The disease caused by A. digitata is known as phyllode rust or gall rust, and it can cause witches' brooms on some Acacia species. The brooms are the result of the rust pathogen's systemic infection of A. koa. This endophytic relationship causes hormonal changes in A. koa organs (phyllodes, flowers, fruits) which result in unusually swollen or galled tissues and abnormal branching and floral reversion. Many rust diseases of plants do not infect their hosts in this systemic fashion, so this is an unusual disease.
 
Photo: An old and majestic forest specimen of Acacia koa in Hawaii (Photo - J. B. Friday, UH-CTAHR).
 
Much of what we know about the koa rusts in Hawaii stems from the careful research of Don Gardner and his colleagues. In the 1970s, 80s and 90s Gardner working in Hawaii and his colleagues studied and classified the rusts.  They found the "koa rust" in Hawaii was not caused by just one or two species, but by several species, each unique and causing unique disease symptoms and producing unique fungal life cycles. Witches' broom of Acacia koa caused by Atelocauda digitataIf you want more information than that which appears in this brief bulletin, there is a list of references below that is worthwhile reading. 
 
Here we discuss one of the several important koa rusts in Hawaii, a gall rust caused by Atelocauda digitata. We also describe how rusted koa organs attract fungal-feeding rust parasites, generating extraordinarily interesting micro-ecosystems on plant surfaces.
 
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Photo: A young witches' broom on a branch terminal of Acacia koa on Saddle Road on the island of Hawaii in 2005, caused by the plant pathogenic rust fungus, Atelocauda digitata. The brown coloration is due to the masses of erumpent rust spores emerging through the epidermis. The hypertrophic phyllodes are swollen, distorted and twisted. The branch's growth pattern and elongation are abnormal. The fungus will eventually consume all of the plant cells, killing the seasonal or new growth of the branch terminal, and remain dormant inside the koa branch until the next flush of new growth or flowering occurs (Photo - S. Nelson, UH-CTAHR). 
 
Disease name(s): Atelocauda rust, phyllode rust, gall rust, Acacia rust, koa rust
 
Hosts: a wide range of Acacia species, including:
  • Acacia koa
  • Acacia mangium
  • Acacia auriculiformis
  • Acacia aulococarpa
  • Acacia crasicarpa
  • Acacia leptocarpa
  • Acacia mearnsii 
  • Acacia polystacha 
Host common name: koa (the focus of this bulletin)
 
Host family: Fabaceae (bean family).
 
Pathogen name: Atelocauda digitata (G. Winter) Cummins & Hiratsuka. However, based on a revision of the genus by Walker (2001), the pathogen has been renamed Racospermyces digitatus (G. Wint.) J. Walker comb. nov. We chose not to use that new name in this bulletin.
 
Pathogen order: Uredinales
 
Pathogen synonyms: Racospermyces digitatus (G. Wint.), J. Walker comb. nov.Uromyces digitatus Winter; Uromyces phyllidiorum (B. and Br.) McAlp. 
 
Phyllode rust of Acacia mangium (caused by Atelocauda digitata): this is a disease with potentially devastating effects in Acacia plantations in Java, Sumatra and Indonesia. The pathogen can cause severe damage to foliage and young stems in nurseries and young plantations. Seeds pods may be heavily damaged and deformed. Severe infections result in foliar deformation, defoliation, reduced growth and stunting. On Acacia mangium, infected phyllodes, shoot tips, petioles and even fruits may suffer gross malformation or have galls or blister-like swellings. Acacia mangium trees in young stands cam become severely infected. Young shoots may be malformed and branches may develop multiple stems. Severely infected plants are prone to premature defoliation. Where the disease occurs in A. mangium nurseries, the entire stock of plants may be infected and subject to being destroyed by the grower. The surface of older lesions may be colonized by fungal parasites (e.g., fungi, insects).
 
Historical remarks: Atelocauda digitata was first recorded from Australia (Berkeley and Broom, 1881 - 1887).
 
Species variability: Reports indicate that Atelocauda digitata is a genetically variable fungal species. 
 
Pathogen dispersal: wind; although the pathogen infects seed pods and seeds, A. digitata is not regarded as seed borne, however the large number of spores produced on lesions and the capacity of the pathogen to infect flowers and fruits makes contamination of seed lots a possibility.
 
Sites of infection: shoots, phyllodes, flowers, seed pods, juvenile leaves.
 
Type of rust disease: systemic infection creating deformity and witches' brooms at branch terminals. The pathogen forms an endophytic system within the host and affects the host hormonal balance.
 
Host phenology and disease seasonality: Spermagonia and aecia of the koa rust pathogen A. digitata coincide with the seasonal initiation of flowering and shoot growth of Acacia koa in Hawaii. This depends upon elevation and may vary among years. The aeciospores appear on the witches brooms in the several months after flowering and shoot growth begin.  
 
Pathogen life cycle: Atelocauda digitata in Hawaii is a macrocyclic rust, with five distinct spores stages, all occurring on A. koa.
 
Table 1. Spores types and generally associated symptoms for koa rust caused by Atelocauda digitata in Hawaii.

Spore type

Where found on A. koa

Symptoms

urediniospore

Scattered on normal phyllodes or juvenile leaves

Spots/pustules on phyllodes (uredinial-telial sori)

teliospore

Scattered on normal phyllodes or juvenile leaves, often produced in same sorus as urediniospores

Spots/pustules on phyllodes (uredinial-telial sori)

sporidia

(basidiospores)

Scattered on normal phyllodes or juvenile leaves

Spots/pustules on phyllodes (uredinial-telial sori)

 

aeciospore

Associated with hypertrophied tissues

Vary with host and location. Witches' brooms, galls, hypertrophy of shoots, flowers, seed pods and phyllodes

spermatia

Associated with aecia on hypertrophied tissues

Vary with host and locations. Witches' brooms, galls, hypertrophy of shoots, flowers, seed pods and phyllodes

 
Disease cycle: New cycles of disease probably occur every year on a given koa tree, and for the life of that tree. Yearly disease cycles always occur on fresh host growth. Infection and symptoms occur on the growth at the branch terminals (growth tips, phyllodes, flowers, seed pods). New cycles of disease derive from the systemic infection of branches; when new growth blooms the systemic infections become active and move into the young tissues, distorting them and sporulating upon them. Initial infections of new trees and/or branch terminals or phyllodes or juvenile leaves is most likely by windborne aeciospores or urediniospores. 
 
Effects of this disease on A. koa plants: This rust disease is not fatal to koa trees. Severe symptoms (witches' brooms) are mainly confined to several or more branch terminals. Seed pods can be severely affected. The rust can destroy all seed pods on a given tree, and do so on a yearly basis. The disease  symptoms can vary significantly among koa genotypes and locations.
 
Disease management:
 
Note - Trimming off witches' brooms does not cure the plant of infections; the disease is systemic in branch terminals. However, trimming of witches' brooms can help to reduce the number of rust spores in the environment.
  • In nurseries - preventive sprays of approved fungicides for rust control may protect young plants from infection, however this disease is probably not a problem for most A. koa nurseries in Hawaii, unless the nursery is in or near a koa forest. However, the disease is reported to be very severe in A. mangium nurseries in some locations outside of Hawaii. This could be due to local conditions or enhanced virulence in the rust populations. Do not outplant rusted Acacias.
  • protecting young forest plantings of Acacia species- sanitation (removal of witches brooms and diseased seed pods from nearby trees) might help to delay the inevitable disease development on the newly planted, uninfected plants.
  • quarantine - avoid moving rusted plants to any other locations, especially areas where the disease is not reported to occur.
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Disease symptoms and signs
 
 
1. Witches' brooms and hypertrophy at branch terminals
 
The twisted, gnarled, swollen, deformed, spore-covered witches' brooms at the branch terminals is a diagnostic symptom of gall rust of Acacia koa caused by the fungal plant pathogen Atelocauda digitata. Appearance of the brooms is annual-seasonal and coincides with flowering and fruit production.
 
The witches' brooms for this disease can grow approximately 15 cm tall. Witches' brooms do not appear on all types of Acacia koa that are infected by this pathogen. They are covered with powdery brown spore masses that are easily rubbed off. From one to many brooms may occur on a tree.
 
incipient witches' broom Witches' broom
Left: Incipient witches' broom. Stem and phyllodes are distorted, erumpent rust sporulation emerges through the epidermis. Right: Phyllodes are swollen and twisted, covered with rust pustules; stems are twisted, swollen and with unusual branching patterns (Photos - S. Nelson, UH-CTAHR).
 
Witches' broom Witches' broom
Left: Phyllodes are swollen and twisted, covered with rust pustules; stems are twisted, swollen and with unusual branching patterns. Right: etiolated stems and reduced phyllodes in a witches' broom at a koa branch terminal (Photos - S. Nelson, UH-CTAHR).
 
The A. digitata witches' brooms produce aeciospores and spermatia of the pathogen.
 
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2. Flowers - hypertrophy, reversion
 
Koa flower organs may undergo reversion and hypertrophy. As the erumpent pathogen bursts through the epidermis with pustules full of powdery brown spores, the infected flowers resemble miniature witches' brooms.
 
The distortion and hypertorphy and abnormal expression of plant hormones in reproductive organs of the host exemplify the growth-altering effects that typify systemic rust diseases of plants.
 
Hypertrophic inflorescence Hypertrophic inflorescence
Left: compare and contrast normal koa flowers with a swollen, diseased inflorescence that has undergone reversion and hypertrophy of floral organs. Right: incipient abnormal symptom in a flower of A. koa, caused by A. digitata rust (Photos - S. Nelson, 2005).
 
Hypertrophic inflorescence, with erumpent rust spores 
Above: Powdery brown spore masses of the erumpent pathogen, Atelocauda digitata, burst through the epidermis of an Acacia koa inflorescence. The infected flower has undergone reversion of floral organs and hypertrophy and resembles miniature witches' broom (Photo - S. Nelson, UH-CTAHR). 
 
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3. Seed pods and fruits - galling and distortion
 
The rust can destroy the developing seeds by attacking the pods while still green. Pods are distorted, twisted, deformed, swollen or galled, with erumpent rust spores masses bursting though the galled tissues. 
 
Galled, rusted koa seed pod Galled, rusted koa seed pod
Galled, rusted koa seed pod Galled, rusted koa seed pod
Above: Atelocauda digitata can cause severe disease of Acacia koa seed pods in Hawaii. Aeciospores are commonly found on these tissues (Photos - S. Nelson, UH-CTAHR).
 

Koa tree with all seed pods rusted

Above: Acacia koa tree with most seed pods heavily rusted by Atelocauda digitata, from Saddle Road on the island of Hawaii in 2005. There were very little to no viable seeds produced by this tree (Photo - S. Nelson, UH-CTAHR).
 
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4. Phyllodes - uredinial-telial sori
 
 
rust pustules on phyllode of Acacia koa rust pustules on phyllode of Acacia koa
Above: Raised, sporulating pustules; the uredinial-telial sori that typically appear on rusted koa phyllodes infected by Atelocauda digitata (photos - S. Nelson, UH-CTAHR).
 
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Habitat
 

Acacia koa in a rust habitat

Above: one of the habitats of Atelocauda digitata rust of Acacia koa. This is a small, high-elevation kipuka near Saddle Road on the island of Hawaii near Pu'uhuluhulu and the Mauna Kea Observatory Road (Photo - S. Nelson, UH-CTAHR).
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The pathogen: Atelocauda digitata
 
 
 Teliospores of Atelocauda digitata Teliospore of Atelocauda digitata
Above: Teliospores of Atelocauda digitata (highly magnified) showing typical apical finger-like projections (Photos - S. Nelson, UH-CTAHR).
 

Aeciospores of Atelocauda digitata

Above: Here are mainly aeciospores of the gall rust pathogen, Atelocauda digitata, recovered from an aecial-spermagonial broom from a branch terminal of an infected Acacia koa tree (highly magnified)(Photos - S. Nelson, UH-CTAHR).
 
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The fungus Tuberculina maxima Rostrup.
 
a hyperparasitic, biological control agent for Atelocauda digitata
 
 
Advanced-stage rust brooms usually have naturally occurring rust hyperparasites or fungal-feeding insects that consume the rust spores. In August, 2005 we noted insects and fungi as parasites and consumers of the koa rust spores (Atelocauda digitata).
 
There can occur on the witches' brooms an unusual hyperparasite, the fungus Tuberculina maxima, a hyperparasite of Atelocauda digitata, the gall rust pathogen.
 
Tuberculina maxima is a brightly colored fungus, in shades of deep violet (see photo below). Expanding colonies of T. maxima become established on lawns of rust spores on the brooms. As the Tuberculina colonies expand, they are fringed with their own whitish mycelium, lending the colonies a white-halo effect.
 
 Tuberculina maxima (purple fungus) as a hyperparasite of Atelocauda digitata aecia
Above: Tuberculina maxima (purple areas and whitish rings) as a parasite of Atelocauda digitata on phyllodes of Acacia koa. The witches' brooms for this disease can grow approximately 15 cm tall. (Photo - S. Nelson, UH-CTAHR).
 
Spores of Tuberculina maxima recovered from witches' broom A spore of Tuberculina maxima (smaller) parasitizing an aeciospore of Atelocauda digitata
Left: purplish Tuberculina maxima spores and brownish colored Atelocauda digitata aeciospores, scraped from the lawn of spores on a rusted koa phyllode. Right: a spore of Tuberculina maxima sends an attacking attachment tube-like appresorium to begin its parasitism of an aeciospore of Atelocauda digitata (Photos - S. Nelson, UH-CTAHR).

 
References
 
 
(1) Berkeley, M. J., and Broome, C. E. 1881-1887. List of fungi from Brisbane, Queensland, with descriptions of new species. Part II. Trans. Linn. Soc. 2:53-74.

(2) Chen, W.-Q., D. E. Gardner, and D. T. Webb. 1996. Biology and life cycle of Atelocauda koae, an unusual demicyclic rust. Mycoscience 37: 91-98.

(3) Gardner, D. E. 1985. Spore surface morphology of Hawaiian Acacia rust fungi. Mycologia 77:575-596.
 
(4) Gardner, D. E. 1988. Revisions to endemic Hawaiian rusts. Mycologia 80: 747-749.
 
(5) Gardner, D. E. 1991. Atelocauda angustiphylloda n. sp., a microcyclic rust on Acacia koa in Hawaii. Mycologia 83:650-653.
 
(6) Gardner, D. E. Rusts on Acacia koa (koa) (Fabaceae) (University of Hawaii at Manoa website, accessed April 15, 2008).
 
(7) Gardner, D. E. Rusts on Acacia koa: Atelocauda digitata (University of Hawaii at Manoa website, Accessed April 15, 2008).
 
(8) Gardner, D. E. Acacia koa: a review of its diseases and associated fungi (University of Hawaii at Manoa website, accessed April 15, 2008).

(9) Gardner, D. E., T. Miller, and E. G. Kuhlman. 1979. Tuberculina and the life cycle of Uromyces koae. Mycologia 71: 848-852.

(10) Hodges, C. E., and Gardner, D. E. 1984. Hawaiian forest fungi. IV. Rusts on endemic Acacia species. Mycologia 76:332-349.
 
 
(12) Old, K. M., Vercoe, T. K., Floyd, R. B., Wingfield, M. J., Roux, J., and Neser, S. 2002. Acacia spp. - FAO/IPGRI Technical Guidelines for the Safe Movement of Germplams No. 20.
 
(13) Ramsden, M., McDonald, J., and Wylie, F. R. 2002. Forest pests in the South Pacific region: a review of major causal agents of tree disorders. Department of Primary Industries, Agency for Food and Fibre Sciences, Forestry Research, Queensland, Australia.
 
(14) Walker, J. 2001. A revision of the genus Atelocauda (Uredinales) and description of Racospermyces gen. nov. for some rusts of Acacia. Australian Mycologist 20:3-28.
 
Acknowledgements: Don Gardner, for correspondence regarding the rust disease and Tuberculina maxima; Pat Conant (HDOA) for identifying an insect that feeds on the aeciospores of A. digitata on the spermagonial-aecial witches' brooms; Brian Bushe (UH-CTAHR) for assistance with microphotography; J. B. Friday (UH-CTAHR) for photography.  
 
Thank you for reading about this plant disease.  Please feel free to contact me if you have any questions or comments about the information provided in this message or if you would like to see a specific plant disease treated in this series. 
 
Aloha!
 
Dr. Scot C. Nelson
University of Hawaii at Manoa
College of Tropical Agriculture and Human Resources
Department of Plant and Environmental Protection Sciences
Cooperative Extension Service
875 Komohana St., Hilo, HI 96720
 
The information given herein is for educational purposes only. Reference to commercial products or trade names is made with the understanding that no discrimination is intended and that no endorsement by the Cooperative Extension Service is implied. The University of Hawai'i is an equal opportunity/affirmative action institution.
 
Author: Scot C. Nelson
 
For more and larger photographs of this and other plant diseases in Hawaii, please visit the Hawaii Pest and Disease Image Gallery.
University of Hawaii at Manoa
College of Tropical Agriculture and Human Resources
Department of Plant and Environmental Protection Sciences
Cooperative Extension Service
875 Komohana St.
Hilo, Hawaii 96720
tel: 808-981-5199
fax: 808-981-5211