Figure 1. Morphology of Phytophthora palmivora (MFI or S type). Upper row, Variations in shapes of sporangia. Lower row, Globose oogonium with an amphigynous antheridium and an ovoid sporangium with a short pedicel. (Courtesy A. Vaziri; Reproduced from Erwin and Ribeiro, 1996) Click image to see larger view.

 

Figure 2. Culture of Phytophthora palmivora grown on V-8 juice agar. (Courtesy Jean B. Ristaino)

 

Figure 3. Sporangia of Phytophthora palmivora. (Courtesy James O. Strandberg)

 

Figure 4. Phytophthora palmivora.A, Colony. B–E, Sporangia. F, Chlamydospore. G and H, Oogonia and antheridia. B = 20 µm. All at the same magnification except A. (Courtesy Hon H. Ho; Reproduced, by permission of the Institute of Plant and Microbial Biology, from Ho et al., 1995) Click image to see larger view.

 

Figure 5. Oogonium of Phytophthora palmivora with an oval amphigynous antheridium (×1,000). (Courtesy Jean B. Ristaino)

 

Figure 6. Cocoa pod infected with Phytophthora palmivora, the cause of black pod disease. (Courtesy Jean B. Ristaino)

 

Figure 7. Cocoa pods infected with Phytophthora palmivora, the cause of black pod disease. (Courtesy Jean B. Ristaino)

 

Figure 8. Cocoa pod infected with Phytophthora palmivora, the cause of black pod disease. (Courtesy Jean B. Ristaino)

 

Figure 9. Black pod disease of cocoa. (Courtesy Jean B. Ristaino)

 

Figure 10. Cocoa pods infected with Phytophthora palmivora, the cause of black pod disease, on the left and with Moniliophthora rorei, the cause of frosty pod, on the right. (Courtesy Jean B. Ristaino)

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

Introduction

Phytophthora palmivora  (E. J. Butler) E. J. Butler (1919)

 

Phytophthora palmivora was first identified as P. omnivora (Massee, 1899), the cause of black pod disease of cocoa, Theobroma cacao, and as Pythium palmivorum (Butler, 1907), the cause of destructive diseases in palms. The pathogen was later renamed P. palmivora by Butler in 1919 (Butler, 1919). Synonyms of P. palmivora include P. omnivora de Bary (1881), Pythium palmivorum E. J. Butler (1907), P. faberi Maubl. (1909), P. theobromae L. C. Coleman (1910) (=P. palmivora var. theobromae (L. C. Coleman) Orellana (1959)), P. omnivora var. arecae L. C. Coleman (1910) (=P. arecae (L. C. Coleman) Pethybr. (1913)), P. cactorum var. arecae (L. C. Coleman) Sacc & Trotter (1912), Kawakamia carica Hara (1915), P. fici Hori (1915) (considered an invalid name, nom. nud. [Waterhouse, 1963]), P. carica Hara (1918), P. palmivora var. piperis Muller (1936) (considered an invalid name [Waterhouse, 1963]), and P. palmivora var. theobromae (L. C. Coleman) Orellana (1959) (Cline et al., 2008). P. agaves Gandara (1909) was listed as a synonym by Erwin and Ribeiro (1996) but was not examined by Tucker (1931). Waterhouse (1963) considered this an invalid name (nom. nud.). P. arecae was considered a distinct species until recently but is now considered to be synonymous with P. palmivora as originally suggested by Tucker (1931) (Cline et al., 2008; Cooke et al., 2000; Mitchell and Kannwischer-Mitchell, 1983).

 

Phytophthora isolates, first identified as P. palmivora (MF3) were separated into an L type with five or six large chromosomes and an S type (MF1) with 9–12 smaller chromosomes. While the S type is considered to be P. palmivora, the L type was redescribed as P. megakarya and found to be the predominant species causing black pod of cocoa in Nigeria and Cameroon (Brasier and Sansome, 1977). MF2 was found to be a variant of P. palmivora (Brasier et al., 1981). MF4 types were redescribed as P. capsici (Mchau and Coffey, 1995). Aragaki and Uchida (2001) argued for a narrower species concept of the MF4 group of P. palmivora, referring several tropical isolates from cacao, black pepper, and macadamia to the new species P. tropicalis. P. arecae is similar to P. palmivora in morphology and DNA markers (SSCP) and is not a valid species (Gallegly and Hong, 2008). P. palmivora is a group II Phytophthora species (Stamps et al., 1990). The species is described in detail in Stamps (1985) (Fig. 1).

Cultural Characteristics

The optimum temperature for growth is 27.5–30°C (Figs. 2 and 4A), the minimum temperature for growth is 11°C, and the maximum temperature for growth is 35°C (Waterhouse, 1974).

Reproductive Structures

Asexual Structures

 

A range of characteristics for isolates of different hosts can be found in Table 51A.1–A.5 in Erwin and Ribeiro (1996).

 

Sporangiophores:

Sporangiophores are sympodial, and as many as 20 sporangia can form on one sympodium.

 

Sporangia:

Sporangia size varies considerably for isolates from different hosts (Brasier and Griffin, 1979). Most sporangia are elongated, ellipsoid to ovoid, and prominently papillate (Erwin and Ribeiro, 1996). Sporangia are caducous (deciduous) and have short pedicels (<5 µm). Sporangial size varies, but the average is 25–35 × 40–60 µm (Figs. 3 and 4B–E). Sporangia are stimulated by light (Brasier, 1969) and, when incubated in water, discharge approximately 10–40 zoospores (Holliday, 1980). The length–breadth ratio is 1.3–1.8 µm (average 1.5 µm).

 

Chlamydospores:

Chlamydospores are abundant, globose to subglobose, and terminal or intercalary on mycelium of most isolates of P. palmivora (Mchau and Coffey, 1994). Chlamydospores are 32–42 µm in diameter (Holliday, 1980) and average 33 µm according to Waterhouse (1974), 36 µm according to Ashby (1929), and 36.2 ±9.6 µm according to Mchau and Coffey (1994) (Fig. 4F).

 

Hyphae:

Hyphae are coenocytic and 7–10 µm in diameter.

 

Sexual Structures

 

P. palmivora is heterothallic. A range of characteristics for isolates from different hosts can be found in Table 51A.1–A.5 in Erwin and Ribeiro (1996).

 

Antheridia:

Antheridia are amphigynous, spherical or oval, and 9–10 × 12–15 µm.

 

Oogonia:

Oogonia are spherical and 22.3–34.8 µm in diameter (Brasier and Griffin, 1979).

 

Oospores:

Oospore characteristics vary for different hosts. Oospores are 17–29 µm in diameter (average 22.8 µm) (Dantanarayana et al., 1984) and aplerotic (Figs. 4G and H and 5). The oospore wall is 2 µm thick.

Host Range and Distribution

P. palmivora causes disease on a wide variety of host species and symptoms include black pod, stem canker, patch canker, and bud, flower, and root rot. Some host species include cocoa, papaya, and para rubber. The pathogen can infect more than 138 species from many plant families. Table 51A.1 in Erwin and Ribeiro (1996) has an extensive host range list.

 

P. palmivora is capable of infecting a variety of hosts because of its ability to form sporangia and abundant zoospores on diseased tissue when free water is present. To control diseases caused by P. palmivora, copper fungicides such as Bordeaux mixture can be applied to the infected plant. Systemic fungicides may also be useful in controlling P. palmivora, but these are expensive and may be washed off during heavy rains. Cultural practices that can be used to limit disease occurrences include proper spacing between plants and a reasonable amount of sunlight and fertilization.

Symptoms

Black Pod of Theobroma cacao (Cocoa):

Pods or cherelles (immature pods) may be infected at any place on the surface, but infection is most often initiated at the tip or stem end (Figs. 6–8). The first symptom is the development of a brown to black spot on the pod, which spreads rapidly in all directions, eventually covering the entire pod (Fig. 9). Under humid conditions, a white bloom of mycelium and sporangia forms on the surface of the diseased pods. As the disease progresses to advanced stages, P. palmivora invades the internal tissue and causes discoloration and shriveling of the bean (Fig. 10). Diseased pods eventually turn black and mummify. Black pod disease may create a distinct seaweedlike odor (Sreenivasan and Quesnel, 1977). Contact of diseased pods with healthy ones allows the pathogen to spread.

 

Stem Canker of Theobroma cacao (Cocoa):

The first visible symptom of stem canker is defoliation, which is caused by coalescence of the cankers that girdle the stem or fan branches. In early stages of canker development, the bark can be peeled to reveal wood of a watery gray color, often with reddish streaks that intensify in color after exposure to air. In advanced stages, a reddish fluid exudes from cankers and dries into a rusty deposit. The wood turns brown, and blackish streaks can often be seen. A protuberance or “bottom bulge” may be observed on the surface of diseased trunks that exudes a reddish brown substance. P. palmivora may cause sudden death in plants if associated with the bark beetle, Eccoptopterus spinosus. The disease is spread during heavy rainfalls and with physical contact between diseased and healthy plants.

 

Chupon Wilt of Theobroma cacao (Cocoa):

The chupon is a soft tissue or sucker that emerges at the base of the cocoa tree. Usually, the axil of a young leaf is infected first, and then an angular, necrotic lesion forms. The young shoots are then rapidly girdled, resulting in wilting of the shoot.

 

Purple Blotch and Fruit Rot of Annona squamosa (Sugar or Sweetsop Apple):

When infected, water-soaked lesions develop on green fruits, and the fruits drop and mummify. Lesions on fruits turn purple-brown to black and eventually extend over the entire surface. Internally, infected fruits become brown, and in severe cases, seeds shrivel (Purss, 1953). The disease is most prevalent during heavy rainfalls and in fruits on lower branches that are more easily splashed with inoculum.

 

Fruit Rot of Artocarpus communis (=Artocarpus altilis) (Breadfruit):

Water-soaked lesions with light brown centers appear 48–72 h after infection. Lesions enlarge rapidly, and the fruit completely rots and mummifies (Trujillo, 1970).

 

Root and Fruit Rot of Carica papaya (Papaya):

Leaves of affected plants wilt, turn yellow, and hang limply. In advanced stages, all of the leaves drop. Lateral roots and taproots are entirely destroyed when infected, and a foul odor often emanates from diseased trees. When plants are wounded, a trunk rot may develop and infection spreads up the trunk, causing leaf- and fruit-bearing trees to collapse. On ripening fruit, rot initially appears as small, circular, water-soaked lesions and then progresses into larger, white, circular or elliptic lesions. Under humid conditions, a whitish mass of sporangia and mycelium is visible on the surface of the fruit. Ripe fruits are more susceptible to infection than green fruits (Hine et al., 1965). Optimal conditions for disease development include temperatures between 20 and 30°C, excessive soil moisture, and rainy weather.

 

Bud Rot and Premature Nut Fall of Cocos nucifera (Coconut) and Other Palms:

The first symptom includes a yellow-brown discoloration of the emerging young heart leaf, which eventually wilts and dies. The bud rot spreads from the heart leaf outward and invades the entire central whorl of leaves and spathes (Ashby, 1920). Older leaves often remain green and fall after maturity, leaving the tree bare. If the plant is infected by a secondary invader, such as bacteria, an offensive odor may develop (Ocfemia, 1934). In palms, rows of brown spots across the leaf pinnae denote incipient infection. The infected portions of the trunk turn soft. Bud rot is most severe at temperatures of 16–20°C and under conditions of high relative humidity.

 

Patch Canker of Durio zibethinus (Durian):

The first symptom is an exudation of a dark red fluid around the collar region. Cankers grow and girdle the tree, and infected cortical tissue changes from its normal pink or light brown to a red, dark brown, or black color. The lesion is bordered by a margin. Leaves fall and branches die back. In the end, all of the leaves drop and the tree dies. Infection occurs mainly during periods of high rainfall.

 

Diseases of Hevea brasiliensis (Para Rubber):

Several Phytophthora species have been described as the cause of diseases of the rubber plant, but P. meadii and P. palmivora are the most frequently isolated.

 

Black Stripe or Black Thread of Hevea brasiliensis (Para Rubber):

The first symptom of the disease is the occurrence of sunken, discolored areas on the bark just above the tapping cut. As the disease progresses, vertical fissures in the bark occur. When scraped away, the bark portrays a characteristic vertical black line extending beyond the tapping cut. Splits and cracks may also occur in the bark. The disease spreads by moist air currents and infested tapping knives.

 

Patch Canker, Lump Canker, or Foot Disease of Hevea brasiliensis (Para Rubber):

Infection starts under the bark and can be seen when the outer bark is peeled back. The disease can spread up and down the trunk for some distance before external symptoms are visible. The cortex may have a distinctive claret color and the cambium may die. During the dry season, when the callus tissue regenerates over the coagulated latex, a lumpy canker forms (Chee, 1968). P. palmivora spreads quickly during cool, moist weather.

 

Secondary Leaf Fall and Green Pod Decay of Hevea brasiliensis (Para Rubber):

Symptoms include dull, ash gray spots that develop at the stem end of fruit and gradually spread across the entire surface of the fruit, coalescing in the end. Drops of latex, which eventually turn black, may also exude from the spots. Under humid conditions, a whitish fuzz of mycelium and sporangia may cover the infected portion. The fruits turn dark and become soft, and in severe cases, every fruit on the tree may become infected. Individual leaves may turn yellow or red, and during the fruit rot phase, leaves shed. Dark brown or black lesions with white spots of coagulated latex are usually present in the center of each fallen leaf. Branches eventually die back, and shoots that arise from the branches wilt early (Pillai, 1982). The disease develops a few weeks after the monsoon season begins.

 

Foot Rot of Piper nigrum (Black Pepper):

Symptoms include slight wilting of the vine, pale green leaves, drooping of vines, and premature dropping of leaves. Before leaves drop, their edges may curl inward and leaves may turn yellow. Deep brown lesions appear on leaves near the ground, and leaf infection results in defoliation. Once all leaves drop, the fruit becomes dried and wrinkled. A foul odor may be emitted. Stems and roots are also susceptible to the disease, and stems die back when infected. The disease is most severe during periods of heavy rainfall. The causal organism of pod rot of black pepper was originally attributed to P. palmivora MF4, but other isolates from pepper have been determined to be P. capsici (Tsao and Alizadeh, 1988).

 

Mycoherbicide:

P. palmivora has been used as a biocontrol agent against the strangle vine weed or milkweed (Morrenia odorata) and is sold under the trade name DeVine (Auld, 1990; Charudattan, 1987; Ridings, 1986; Ridings et al., 1976). To control the weed, chlamydospore inoculum of P. palmivora must be applied under the proper growing conditions for this Phytophthora species. P. palmivora grows best in an environment of frequent rainfall or high humidity, either alone or in combination, and optimum temperatures.

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