Plant Disease of the Week No. 5 (Cephaleuros: the plant-parasitic green algae)

1. Introduction

2. General information

3. Cephaleuros virescens leaf spot of avocado

4. Cephaleuros virescens and Cephaleuros parasiticus leaf and fruit spots of guava

5. Integrated management of Cephaleuros diseases

6. Strigula elegans - a lichenized form of Cephaleuros

1. Introduction

Cephaleuros species are filamentous green algae and parasites of higher plants worldwide. In Hawaii, at least two of horticultural importance are known: Cephaleuros virescens and Cephaleuros parasiticus.

Cephaleuros species generally cause minor diseases, negligible leaf spots. Yet certain crops in moist environments suffer great damage. Typically harmless, the algal diseases can cause economic injury to stems, leaves and fruits.

Symptoms and crop damage can vary greatly depending on the combination of Cephaleuros species, hosts and environments. The most adverse combination of elements in Hawaii is probably the "Cephaleuros parasiticus-guava-moist environment" combination. Spots caused by C. parasiticus on guava are top-down, intercellular, full-thickness necrosis, destroying both upper and lower epidermal cell layers and all intervening tissues. Then, a bright but relatively sparse orange algal bloom bursts forth from the undersides of leaf lesions, rather than from the upper side of leaves as is usually the case with with Cephaleuros virescens, the more common species.

The distinctive and much more common spots caused by C. virescens on many hosts in Hawaii appear on the upper leaf surface as raised yet flattened, textured, burnt-orange to brown or rust-colored, circular areas up to about 2-cm diameter, having indistinct, filamentous margins and fuzzy surface topographies. Yet, this species is generally a harmless, subcuticular leaf parasite.

Here we discuss these two pathogens. For information on other Cephaleuros species and their diseases in our region, please refer to the technical report by Fred Brooks. To see images of Cephaleuros minimus on noni, please visit the Hawaii Pest & Disease Image Gallery, and click on "noni."

2. General information

Disease name(s): algal leaf spot, algal fruit spot, green scurf; Cephaleuros infections on tea and coffee plants have been called "red rust."

Disease symptoms and signs: on leaves - symptoms vary according to the Cephaleuros species - host species combination. For Cephaleuros virescens, leaf spots are usually raised, velvety in appearance, in shades of orange or brown, on upper leaf surface. Leaf spots caused by Cephaleuros parasiticus on guava are top-down, full-thickness necrosis, destoying both epidermal layers (abaxial and adaxial) and all intervening tissues. The bright but relatively sparse orange algal bloom occurs on the undersides of leaves, rather than the upper. On some Psidium types a chlorotic, yellow halo surrounds the lesions. On fruits - spots on guava are slightly sunken, cracked, when severe lend a scabby appearance to fruit skin. On twigs and branches - twig and branch lesions may lead to dieback and loss of distal organs.

Type of pathogen: aerophilic filamentous green algae (although aerophilic and terrestrial, they require a film of water to complete their life cycles).

Pathogen genus: Cephaleuros; a member of the Trentepohliales and a unique order

Algal leaf spot of avocado caused by Cephaleuros virescens

Chlorophyta (Chlorophyta - photosynthetic organisms known as green algae).

Species of Cephaleuros: C. biolophus Thompson & Wujek; C. diffusus Thompson & Wujek; C. drouetii Thompson; C. expansus Thompson & Wujek; C. henningsii Schmidle; C. karstenii Schmidle; C. lagerheimii Schmidle; C. minimus Karsten; C. parasiticus Karsten; C. pilosus Thompson & Wujek; C. solutus Karsten; C. tumidae-setae Thompson & Wujek; C. virescens Kunze.

Species of Cephaleuros known in Hawaii: there are at least two Cephaleuros species in the main Hawaiian islands, C. virescens and C. parasiticus.

Photo: Algal leaf spot of avocado (Persea americana) in Hilo, Hawaii, caused by Cephaleuros virescens (Photo: S. Nelson, UH-CTAHR)

Host plants: species of Cephaleuros are very common on the leaves of such economically important tropical trees and shrubs as tea (Camellia sinensis), kava (Piper methysticum), pepper (Piper nigrum), magnolia (Magnolia grandiflora), coffee (Coffea arabica), oil palm (Elaeis guineensis), avocado (Persea americana), vanilla (Vanilla planifolia), mango (Mangifera indica), breadfruit (Artocarpus p.), guava (Psidium guajava), coconut (Cocos nucifera), cacao (Theobroma cacao), as well some citrus (Citrus spp.) cultivars. Cephaleuros infections can cause death (necrosis) of the cells just beneath the algal thallus and injure the host plants.

Cephaleuros virescens is the most frequently reported algal pathogen of higher plants worldwide and has the broadest host range among Cephaleuros species. It usually occurs on the upper leaf surface of perennial dicotyledonous plants.

A recent survey from American Samoa found susceptible hosts of C. virescens occurring in the following plant families: ACANTHACEAE, AGAVACEAE, ANACARDIACEAE, ANACARDIACEAE, APOCYNACEAE, ARACEAE, ARALIACEAE, ARECACEAE, ASCLEPIDACEAE, BIXACEAE, BOMBACACEAE, BURSERACEAE, CLUSIACEAE, COMBRETACEAE, EUPHORBIACEAE, FABACEAE, LAURACEAE, LEEACEAE, LOGANIACEAE, LYTHRACEAE, MALVACEAE, MARANTACEAE, MELIACEAE, MORACEAE, MYRTACEAE, NYCTAGINACEAE, OLEACEAE, OXALIDACEAE, PANDANACEAE, PIPERACEAE, POLYGONACEAE, RUBIACEAE, RUTACEAE, SAPINDACEAE, SAPOTACEAE, SOLANCEAE, STERCULIACEAE, and VERBENACEAE.

The survey found Cephaleuros parasiticus on plant hosts in the following families: ANACARDIACEAE, ANACARDIACEAE, ARECACEAE, BIXACEAE, HELICONACEAE, LEEACEAE, LYTHRACEAE, MARANTACEAE, MYRTACEAE, ORCHIDACEAE, and SAPOTACEAE.

Cephaleuros species do not affect key subsistence crops in the Pacific such as banana and taro, although coconut and breadfruit are hosts for leaf spots.

Geographic range of hosts: pantropical.

Taxonomy of the pathogen: Cephaleuros is a member of the Trentepohliales, a unique order of aerophilic filamentous green algae (Chlorophyta).The order Trentepohliales is a widespread group of terrestrial green algae. It conists of six genera (Cephaleuros, Phycopeltis, Physolinum, Printzina, Stomatochroon and Trentepohlia). The organisms are predominantly aquatic or marine. Several species are terrestrial, various types are highly specialized.

Photo: algal leaf and fruit spotting of guava (Psidium sp.) caused by Cephaleuros parasiticus near Hilo, Hawaii (Photo: S. Nelson, UH-CTAHR).

Description of genus: Cephaleuros consists of branched filaments that comprise a thallus in the form of irregular discs. The thallus grows below the cuticle or sometimes below the epidermis of the host plant. This pigmented thallus (orange to red-brown) consists of a prostrate portion that is branched irregularly with irregular cells and an erect portion of unbranched hairs, with cylindrical cells, either sterile or fertile, protruding through the cuticle. Haustorial cells are sometimes present inside the plant host's tissue. Sporangiophores bear one or more head cells subtending sporangiate-laterals. Gametangia are terminal or intercalary on the prostrate cell filaments.

Distribution of pathogen: Cephaleuros species are found in tropical and subtropical climates, on all continents and probably all islands between about 33 degrees N and 33 degrees S of the equator, provided the temperature and humidity are suitable for their growth and reproduction. On the U.S. Gulf Coast C. virescens has been recorded on at least 287 plant species and cultivars, including 80 that are subject to stem infections.

Classification of its method of food acquisition: Cephaleuros species are considered obligate epiphytes and occasional plant parasites in some cases, and as plant parasites and pathogens in others.

Life cycle of Cephaleuros sp.: Cephlaeuros is capable of both asexual and sexual reproduction. Cephaleuros has a vegetative thallus from which algal filaments extend beneath the cuticle and sometimes between epidermis and palisade cells into the meosphyll. The C. virescens thallus is disc-like, the C. parasiticus thallus filamentous. Sterile hairs (setae) and asexual zoosporangiophores containing sporangia containing motile zoospores also arise from the vegetative thallus. Through sexual reproduction, the resulting zygote produces a dwarf sporophyte. The life history consists of alternation of heteromorphic generations, with the sporophyte reduced to a dwarf plant (the stalk cell, head cell, one or more suffultory cells, and the meiosporangia). The asexual stage is probably much more important to the typical infection and disease processes.

Pathogen dispersal: wind; splashing water.

Sites of infection: leaves; fruits; stems; twigs.

Cephaleuros disease cycle:

Dispersal - splashing raindrops or wind-driven rain or strong winds dislodge sporangia or thallus fragments of Cephaleuros from diseased host tissue.
Inoculation - sporangia or thallus fragments with sporangia are deposited on susceptible host tissue.
Infection - motile zoospoores are released from sporangia, penetrate the host cuticle, and generate a disc-like algal thallus with threadlike algal filaments.
Disease development - on some hosts the algal filaments ramify throughout the host tissue intercellularly, on others the thallus remains beneath the cuticle only; the effects of the spots on plants are 1) photosynthetic area of leaves is reduced; 2) defoliation of leaves; 3) loss of fruit marketability; 4) twig dieback; 5) tissue necrosis, etc.
Pathogen reproduction - asexual (zoosporangia); sexual (sporophyte, homothallic)
Pathogen survival - in spots on leaves or stems, in fallen debris for some time

Infection: occurs on the upper leaf surface predominantly, initiated by motile zoospores or dislodged pieces of algal thallus; algal filaments extend from the thallus beneath the cuticle and sometimes between epidermal and palisade cells into the mesophyll.

Environmental conditions favoring disease development: warm and wet conditions; dissemination of sporangia and infection are favored by frequent rains and warm weather.

Predisposing factors: frequent rain; poor plant nutrition; poor soil drainage; stagnant air.

Crop damage, C. virescens vs. C. parasiticus: we may separate Cephaleuros species and the damage damage they cause in two groups on the basis of their mode of parasitism: subcuticular vs. intercellular or within the cell matrix. C. virescens is a subcuticular parasite, while C. parasiticus is an intercellular parasite. The thallus of C. virescens grows between a plant's cuticle and its epidermis and creates only negligible tissue damage (but it can in some cases be severe). C. parasiticus extends its thallus intercellularly, ramifying vegetatively within the host, and emerging through the epidermis with a bloom of carotenoid pigment-rich zoosporangiophores. This latter mode of parasitism permits more tissue damage than subcuticular parasitism.

On some hosts and with some Cephaleuros species, there may be no obvious damage or symptom other than the orange-colored downy growth on leaves in the lower part of the canopy. On other hosts, cell and tissue death can occur beneath the algal thallus. Economic damage is possible on fruits of guava, citrus and avocado (reduced marketability).

Damage to leaves: depends mainly on the Cephaleuros species-host combination and the environment. Generally, on most hosts, leaf infection is of little direct economic importance and is confined to low-hanging branches near ground level. On more susceptible hosts such as guava (Psidium sp.) there can be significant tissue necrosis, extensive defoliation, economic injury and crop loss, and reduced photosynthesis and loss of vigor.

Photo: algal leaf spot of magnolia (Magnolia grandiflora) in Kurtistown, Hawaii caused by Cephaleuros virescens (Photo: S. Nelson, UH-CTAHR).

Damage to limbs, twigs and shoots: in Hawaii, the damage does not seem to be important. Elsewhere, C. virescens can attack limbs, twigs and shoots of some hosts, causing dieback. For example, it is reported as a pathogen of longan, guava and citrus twigs. On carambola (starfruit, Averroha carambola L.) in Florida, twigs and limbs may be attacked by C. virescens. Symptoms include rough circular greenish-grey or rusty-red areas and shoot dieback.

Damage to fruits: Most fruit damage from Cephaleuros in Hawaii probably occurs on guavas (presumably caused by C. parasiticus). Elsewhere in the world, problems have been reported on avocado, citrus and other fruits. Damage to guava fruits in Hawaii is limited to the skin of the fruit; no soft rot is caused by the alga. The spots are slightly sunken and cracked with a dark, somewhat corky aspect. When severe, the fruits appear scabbed.

Miscellany: several transitional forms of algae between epiphytes and parasites have been found in the family Trentepohliaceae, suggesting to some scientists that parasitic forms evolved from epiphytic forms. C. virescens was once reported as a very serious pathogen of tea in India and Indonesia. Cephaleuros was first discovered in Florida in 1894. The pigments astaxanthin and B-carotene (yellow-green to dark reddish-orange) color the Cephaleuros thallus brilliantly.

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3. Cephaleuros leaf spot of avocado

Pathogen:

Cephaleuros virescens

Algal leaf spots are commonly seen on avocado (Persea americana). The symptoms are responsible for many of the questions raised by backyard growers. The disease usually attacks leaves on low-hanging branches. Often, there will be no spots at all on the upper leaves. Damage to avocado plant vigor and yield is generally insignificant.

Typical raised, velvety, coppery brown algal spots on leaves of avocado (Persea americana) caused by Cephaleuros virescens. The spots consist of the brightly pigmented thallus of the plant parasitic algae. Click on images to see their larger versions (Photo: S. Nelson, UH-CTAHR, left - S. Kona, right - Hilo).

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4. Cephaleuros leaf and fruit spots of guava

Pathogens:

a. Cephaleuros virescens

b. Cephaleuros parasiticus

Cephaleuros can cause substantial damage to some varieties of guava (Psidium spp.) in Hawaii. Leaf spots can be severe, leading to reduced plant vigor and defoliation. Fruit spots can affect marketability of fresh fruits and cause fruits to be rejected by harvesters or at juicing facilities. The disease occurs commonly wherever Psidium species are growing in relatively wet conditions, such as the eastern half of the island of Hawaii or in many of Hawaii's coastal forests. There are two main types of symptoms on guava leaves: velvety spots and non-velvety spots.

a. Cephalueros virescens

Cephaleuros virescens leaf spots on guava consist of velvety patches of algal bloom on the upper leaf surface. Fruits can be severely spotted.

Right: velvety spot symptom on wild Psidium sp., Hakalau, HI. The damage to the

Cephaleuros virescens leaf spots on gauva (Hawaii)

underside of the leaf may be minimal with this symptom type, and there is usually no emergence of the alga on that side of the leaf. (Photos: S. Nelson and Fred Brooks, UH-CTAHR.).

Below: fruit symptoms (left) and leaf and fruit symptoms (right) for guava infected by C. virescens in American Samoa. Cephaleuros fruit infections on guava remain confined to the skin of the fruit and do not directly cause interior fruit rot (although opportunistic fungi and bacteria can enter the cracked lesions). The sunken lesions on fruits appear cracked and corky. A yellowish-orange, velvety algal bloom on the upper leaf surface covers a hefty percentage of the total leaf area and blocks sunlight (Photos: Fred Brooks, UH-CTAHR).

Cephaleuros virescens fruit spots on guava in American Samoa

Cephaleuros virescens fruit spots (left) and leaf spots (right) on guava (American Samoa)

b. Cephaleuros parasiticus

Cephaleuros parasiticus causes a non-velvety spot type. There is no discernable algal bloom on the upper leaf surface, but there are brightly colored Cephaleuros fructifications emerging from the underside of the diseased leaf. This symptom mimics a rust disease.

Algal leaf spot on Psidium sp. (upper leaf surface)

Fruiting bodies of Cephaleuros parasiticus on Psidium sp.

Left: Cephaleuros parasiticus spots on guava leaves appear initially as tiny, dark brown specks that enlarge into roughly circular lesions with ash-colored centers and dark brown to blackened margins (Hakalau, Hawaii). Right: On the underside of the same leaf, spots appear as dark gray, circular and watersoaked. The brightly pigmented algal thallus and sporagiophores emerge in yellowish-orange clusters within rings in the dark, watersoaked lesions. Lesions tend to form along the leaf midrib, and as damage progresses the vein(s) can collapse and die (Hakalau, Hawaii) (Photos: S. Nelson, UH-CTAHR).

Right: Cephaleuros parasiticus algal thallus emerging through the epidermis of the underside of a guava leaf (Psidium sp., highly magnified). This brightly pigmented alga is often mistaken for a rust fungus. The hematochrome pigments, astaxanthin and B-carotene, lend a yellow-green to dark reddish-orange color to the thallus of Cephaleuros (Photo: S. Nelson and B. Bushe, UH-CTAHR, from infected material near Hilo, Hawaii).

Right: Cephaleuros parasiticus thallus and

sporangiophores. Upon making a slide mount in a drop of water, zoospores may be relseased immediately (Photo: Fred Brooks, UH-CTAHR, from material collected in American Samoa.)

Below: Cephaleuros parasiticus leaf spots on some Psidium species or cultivars have yellow, chlorotic halos around them (below left) and fruits of all developmental stages may be heavily spotted. Leaves may turn yellow and defoliate prematurely (near Hilo, Hawaii) (Photos: S. Nelson, UH-CTAHR).

Cephaleuros parasiticus leaf spots with yellow halos on guava leaf

Cephaleuros parasiticus fruits spots on guava

Cephaleuros parasiticus fruit spots on guava fruits

Cephaleuros parasiticus leaf snd fruit spots on guava fruits

Cephaleuros parasiticus leaf spots on some guava cultivars are surrounded by yellow halos and the associated fruit damage can be significant (near Hilo, Hawaii) (Photos: S. Nelson, UH-CTAHR).

Cephaleuros parasiticus leaf spots on three guava cultivars

Three guava cultivars express the algal spot symptoms somewhat differently. Leaves of three different Psidium species or cultivars growing side-by-side in a collection at the University of Hawaii, each displays a unique reaction to its association with Cephaleuros parasiticus (near Hilo, Hawaii) (Photo: S. Nelson, UH-CTAHR).

5. Integrated management of Cephaleuros diseases

Accurate diagnosis of the disease is by microscopic examination of the alga. The common diagnostic mistake is to confuse al algal leaf spot with a rust disease. Therefore, submit a sample to your local extension service office or a trained plant pathologist for a correct diagnosis.

Check to see if you can rub the algae off the leaves with your fingers. Non-parasitic algae do not penetrate the cuticle and are easily rubbed off leaves. Also, non-parasitic algae do not have corresponding lesions on the opposite side of the leaf.

Diseases caused by Cephaleuros virescens (or its lichenized form, S. elegans) in Hawaii rarely warrant management, except in the case of guava in wet environments. However, they may be a nuisance in landscapes. To control these parasites, integrate a combination of the following practices:

Sanitation - remove spotted leaves by hand from lightly diseased plants; prune low hanging branches that are affected by the disease; collect and discard all fallen leaves.
Pruning - prune overhanging trees around diseased plants (this will reduce relative humidity and speed up leaf drying after rains).
Reduce plant stress - keep plants well fertilized; improve soil drainage.
Weed control - keep weeds around affected plants under control (this will reduce relative humidity in the plant canopy and reduce plant stress); prevent climbing and vine-like weeds from establishing on the host plant.
Fungicides - some fungicides will provide control; use chemicals only according to directions on the label; the Bordeaux mixture is commonly recommended.
Intercropping - interplant very susceptible hosts with less susceptible hosts.
Variety selection - try to select a more tolerant variety (for example, of guava) where the crop is grown in a wet environment.
Choice of planting location - for highly susceptible crops, select a planting location with moderate rainfall, well-drained soil and good air circulation.
Plant spacing and thinning to improve aeration and light exposure.

Finding a number of different algal species on a leaf is common in shaded, moist environments. Most of the algae are not parasitic on plants. If you can easily rub off algae with your fingers, they are probably not plant parasitic.

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6. Cephaleuros as a lichen symbiont

Strigula elegans - the lichenized form of Cephaleuros

Cephaleuros in its lichenized form is also plant-parasitic. Cephaleuros becomes lichenized due to being parasitized by a number of species of phyllosphere fungi. One of the resultant lichens is Strigula elegans. Thus, in this union of fungus and alga, Cephaleuros parasitizes the plant while its fungal symbiont parasitizes Cephaleuros.

The lichenized form of Cephaleuros causes leaf spots on dozens of hosts in the Pacific. Spots occurr in moist areas, shaded but with some exposure to sunlight. Spots most commonly exist on the foliage of low-hanging branches or in shaded recesses within the plant canopy.

The spots normally don't seem to cause any major problems for the infected plants.

Strigula elegans leaf spots on two sides of longan (Dimocarpus longan) leaves. Left: darkened, circular areas correspond to leaf spots on the other side of this leaf. Sporangiophores of C. parasiticus emerge through the spots that have complete necrotic burn-through from the spots on the top side of the leaf. Right: Leaf spots of the lichenized from of Cephaeluros parasiticus, Striga elegans. Spots have whitish centers and greenish-orange margins, they are slightly raised and roughly circular. Magnified images are shown below. (near Hilo, Hawaii) (Photos: S. Nelson, UH-CTAHR).

Strigula elegans "spots" on the upper surface of a longan leaf (magnified). Spots are whitish in color with pale green or orange-tinged margins. Bright orange setae ("sterile hairs") emerge from the lichenized thallus of Cephaleuros (near Hilo, Hawaii) (Photos: S. Nelson and B. Bushe, UH-CTAHR).

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