Pichia Captophila

Biotic pathogenic agents of cactus pear diseases

Bacterial Diseases

Bacterial spot (Erwinia carotovora, E. cacticida) Crown gall (Agrobacterium tumefaciens) Yeast Diseases

Soft rot (Candida boidimi) Fungal Diseases

Armillaria rot (Armillaria mellea) Alternaria golden spot (Alternaria alternata) Foot rot (Phytophthora cactorum, P. nicotianae) Gray mold (Botrytis cinerea)

Other fungal agents: Aecidium sp., Cercospora sp., Colletotricum sp., Cytospora sp., Hansfordia sp., Fusarium oxysporum, Gleosporium herbarum, Mycospherella sp., Phoma sorghina, Phyllosticta opuntiae, Phyllosticta concava, Pleospora herbarum, Sclerotinia sclerotiorum Phytoplasmalike and Viruslike Diseases Cladode enlargement Flower proliferation ease in areas where winter or spring frosts and hailstorms wound cladodes or fruits. High summer temperatures arrest the infection, but the bacterium (Erwina species) becomes active as soon as cooler, moist conditions prevail (Cortés and Fucikovsky 1986; Alcorn and Orum 1988; Fucikovoky 1990; Granata and Varvaro 1990; Varvaro et al. 1993). The main pathogenic organism of bacterial spot is Erwinia carotovora (Table 14.2), which is rod-shaped, gram-negative, motile by perytrichois flagella, and aerobic. This bacterium grows at temperatures up to 36°C, but the optimal temperature is 10 to i5°C. In addition to cactus pear, it can also infect other species of Opuntia. Symptoms appear on the cladodes in the spring and consist of translucent spots that coalesce, darken, and eventually turn black. Parenchymatous tissues under the integument are initially water-soaked and then turn brown to nearly black. The superficial infected tissues dry, develop into a scab, and are frequently cracked (Fig. 14.6A). To control the disease, the infected cladodes must be removed. They must not be buried in the plantation area and burning is recommended. Two copper-based fungicide applications are recommended in the winter-spring where the disease is widespread and after hailstorms or other events that cause plant wounds. In Mexico the black soft rot on cactus pear is caused by Erwinia cacticida and coffee rot is caused by Erwinia carotovora subsp. atrospetica (Hernandez et al. 1997) Crown gall is another bacterial disease that occurs on cactus pear in Mexico under the name "Agalla del Nopal" (Gutiérrez 1992) and is present worldwide. The pathogenic agent is Agrobacterium tumefaciens (Table 14.2), which affects diverse species of plants. It lives in the soil as a saprophyte and colonizes the upper roots and the crown of a plant. Symptoms consist of tumoral masses at the base of the stem. The tumors can become i0 cm in diameter, are dark in color, and are cracked when mature. A dark amber exudate, which oozes from the stem near the tumor, can be mistaken for fungal infections. In reality, the tumor does not substantially damage the plant, but it should still be removed and destroyed. Copper-solution treatments can control the disease, and wound closure using gum mastic is recommended.

Yeasts

Yeasts are larger than bacteria and possess some morphologic and structural features placing them between bacteria and other fungi (Lodder 1974; Kreger 1984). They are single-celled organisms and, unlike bacteria, are eukaryotes (possess a nucleus) and can develop under both aerobic and anaerobic conditions. Yeasts respire and promote fermentation utilizing monosaccharide sugars, i.e., sugars with six carbon atoms that often derive from disaccharides (e.g., sucrose) cleaved by enzymes. Yeasts attack plants that have been debilitated by fungal or bacterial infection; they are more destructive than bacteria, as fermentation eventually kills the entire infected organ.

The yeast disease cladode soft rot (Fig. 14.6B) is frequently associated with bacterial spot (Phaff et al. 1978, 1985; Starmer et al. 1978; Granata and Varvaro 1990). The pathogenic agent, Candida boidimi (Table 14.2), is most active at temperatures between 20 and 35°C. The initial symptoms are black areas caused by internal tissue infection on the cladodes and fruits, followed by internal tissue rot, after which the plant becomes a deliquescent mass. The entire cladode surface blackens, but the external tissue does not rot and thus the cladodes resemble a limp handbag containing a foul-smelling liquid. Control is most effective when the infected cladodes are removed and destroyed followed by a 1% Bordeaux mixture treatment. Treatments used against bacterial diseases, such as bacterial spot, are also efficacious.

Fungi

Fungi cause both plant and animal diseases. To date about 100,000 species of fungi have been studied and over 800 possess more or less virulent plant pathogenic action. Fungal infections cause physiological alterations in host plant transpiration, respiration, and nutrition and lead to damage ranging from stunted growth and production to death of the whole plant, or part thereof. Indeed, fungi are the most common pathogenic agents in the plant world, including the Cactaceae. Characterized by a vegetative stage made up of mycelium (hyphae) that ensures fungal growth, fungi have a parasitic relationship with the host plant. Hyphae produce spores by agamic processeses or conidia. Spores and conidia are propagation forms that enable fungal diffusion in the environment. When they come into contact with receptive hosts under suitable environmental conditions, they germinate and produce hyphae, some of which penetrate intact surfaces or access the plant through natural openings, e.g., stomata or wounds. As previously noted, cacti have few natural openings and a tough waxy epidermis, thus pathogenic agents rarely penetrate the skin and cell wall; however, they are vulnerable to pathogenic attack through wounds. Fungal diseases can be diagnosed by typical symptoms and microscopic examination of the structure and reproductive bodies of the fungus on the colonized organs or in artificial media (Agrios 1978).

Armillaria root and stem rot (Table 14.2) is a slowly progressing disease that leads to the death of a plant. It is caused by Armillaria mellea, a basidiomycetous fungus that

Opuntia Diseases
Figure 14.6. (A) Cladode of Opuntia ficus-indica with symptoms of bacterial spot and (B) dark areas of cladode caused by the yeast disease, soft rot.

colonizes the shoot and main roots of the plant and produces white mycelium and cordons of hyphae that spread from the infected tissues and contaminate neighboring plants. The presence of hyaline, elliptical, and smooth ba-sidiospores produced by carpophores are characteristic of infections caused by this disease. Infected plants suffer a decline in tissue turgor and chlorosis resulting from phloem disorganization and altered water and mineral nutrition. Fruits borne by the infected plant are small and do not ripen. The infected tissue at the stem base eventually rots and releases a viscous exudate. A white mycelium emitting a characteristic fungus smell is found under the bark. The contaminated portion of the shoot has a bright-red border (Redfern 1968, 1973; Raabe 1979; Mangano di San Lio and Tirro 1983). This fungus is ubiquitous, polyphagous, and often remains in the soil in residues from previous cultivations, thus inevitably infecting new crops. It is advisable not to cultivate Armillaria-infected soil for 2 or 3 years and to remove sources of inoculum (roots of previous cultures). Effective chemical control of the disease is not yet available.

Alternaria golden spot (Fig. 14.7A) has been reported in Mexico under the name of "Mancha de Oro" and is also present in Italy and South Africa. It is caused by the fungus Alternaria alternata (Table 14.2) that generally penetrates the plant near the spines of cladodes. A slightly raised round spot appears close to the site of penetration; the underlying tissue then changes from dark to light green and the spot becomes golden. Spots can also appear on the fruits. Spraying with a copper- or Captan-based fungicide can be an effective control for this disease. Ideally, treatment should be applied to potentially vulnerable plants prior to the onset of the symptoms.

Phytophthora cactorum (Fig. 14.7B) and P nicotianae are the pathogenic agents of foot rot (Table 14.2) and are found in cultivations of cactus pear and other Cactaceae (Cacciola and Magnano di San Lio 1988). These fungi live in the soil and usually attack the plant shoot and roots, es pecially in irrigated areas where surface water is present. Gum begins to ooze from the stem base of infected plants at the end of the spring, exuding the greatest amounts during the summer. Diseased innermost tissues rot and turn reddish. The rot may involve the entire stem circumference and kill the plant. Infected plants become chlorotic, growth slows, and cladodes wilt, causing the plant to fall over. Clay soils where water stagnates are prone to infection with Phytophthora species. Thus, cactus pear should be cultivated in sandy soils, and applications of specific fungicides are recommended wherever this disease prevails.

Gray mold of cactus pear fruits is caused by the fungus Botrytis cinerea (Fig. 14.8A). It can start anywhere on the plant, but it generally begins in wounds caused when removing fruits from the cladodes. The infected areas are usually gray and round. When peeled, the underlying fruit tissues appear decayed and soft. The infection spreads in hot humid areas, with the entire fruit becoming a soft, decaying mass. Typical green or blue colonies of Penicillium are often observed on the diseased fruit surface (Fig. 14.8A). Gray mold is difficult to control on cactus pear fruits, as the spines and glochids on fruits cause wounds that promote infection during harvesting and processing.

Cactus pear is host to many other fungi that can cause damage under particular environmental and host conditions. Aecidium species induces the disease called "Roya" in Peru, leading to small chlorotic spots on the cladodes and fruits in the early summer; the spots enlarge and give rise to pustules with orange-colored centers that deform the fruit. Infected fruit do not ripen fully. Cercospora spp. induce circular (1.0-1.5 cm diameter) necrotic wounds on the cladodes (Fig. 14.8B) and fruits and is the most serious cactus disease in Peru and Bolivia. In Mexico Colletotricum spp. cause dark brown spots with reddish tints that generally start at the edges and then extend over the entire clad-ode or fruit. Cytosporaspp., Gleosporium spp., Mycospherella spp., Phoma sorghina (Fig. 14.8C), and Pleospora herbarum also produce necrotic spots on cactus pear cladodes and are found in various countries. Fusarium oxisporum f.s. opun-tiarum, the causal agent of "Fusarium wilt," affects the vascular tissues and causes wilting of cladodes and fruit, leading to a reddening of infected tissues. Phyllostica concava and Phyllostica opuntiae occur in Mediterranean areas and Mexico, respectively, and produce small, round, rust-colored "scabies" for cactus pear; the fungal fructifications appear as black spots. A Phyllostica species is also causing damage to Opuntia ficus-indica cultivated in Argentina (Wright 1997). Sclerotiniasclerotiorum causes a cottony rot on cladodes of cultivated cactus pear in Chile and on native Opuntia species in Argentina. The cuticle softens, the contaminated tissue then darkens, flakes off, and is covered with white wool; soon numerous black sclerotia appear from the decayed tissues. Hansfordia species are other fungi found in Mexico that cause black spots (Hernandez 1992).

Native Fungi on Cacti

Very few surveys have been made of native cactus diseases within North and South America. South African patholo-gists have surveyed for potential pathogens to be used for the biological control of jointed cactus, Opuntia aurantia-ca (Moran and Annecke 1979; Mildenhall et al. 1987). Some of these diseases may switch to cultivated Opuntia species once the areas under cultivation in the Americas and elsewhere increases. The most prominent diseases within native Opuntia species are Aureobasidium pullulans, Fusarium proliferatum, and Microdochium lunatum (Mildenhall et al. 1987). The latter disease already occurs widely on native and cultivated Opuntia species in Argentina, the southwestern United States, South Africa, Australia (Dodd 1940), and the Canary Islands (Von Arx 1984), and on Opuntia ficus-indica in Spain (Wollenweber and Reinking 1935). This disease was studied in South Africa as a potential biocontrol agent against O. aurantiaca (Witbooi 1991). The disease forms circular necrotic spots that eventually collapse and fall out, leaving a clear circular opening. Under certain conditions, the fungus can cause rotting of entire cladodes.

Other Diseases

A disease leading to cladode enlargement has been reported in Mexico under the name of "Engrosamiento excesivo de cladodios" and can occasionally develop into a serious problem for cactus pear cultivation in that country (Pimienta-Barrios 1974; Gutierrez 1992); the causal agent is unknown (Hernandez 1992). The characteristic symptoms of this disease are stunted plant growth, followed by cladode swelling and gradual loss of the plant's green color. Flower production is reduced and flowers generally form on the flat part of the cladodes, whereas on healthy cladodes flowers form on the upper edge. Fruit production is poor in terms of both number and weight. Cladodes from vigorous, healthy plants should be chosen for planting. During the first years, any plants manifesting the symptoms of cladode enlargement in new cactus-pear plantations should be removed and replaced with healthy ones. In old plantations, infected plants must be eliminated and destroyed.

Flower proliferation is a cactus-pear disorder that has been encountered only in Mexico, on a limited number of natural and cultivated varieties. The disease is spreading in Mexico and could pose serious damage to cactus-pear cultivations if not controlled by selection. This disease is char-

Phoma Life Cycle
Figure 14.8. (A) Gray mold caused by Botrytis cinerea on fruit, with secondary fungus Penicillium sp.; (B) cladode infected by Cercospora; and (C) necrotic spots caused by Phoma sorghina.

acterized by excessive flower production all over the cladode surface, early detachment of flowers (receptacles), and premature spine abscission. The young cladodes are deformed, and new fruits may differentiate from the upper part of fruits. Finally, some phytoplasma and virus-like cactus pear diseases can be transmitted by grafting but the pathogenic agents are not known. The microorganisms involved cause alterations in the phloem and consequent stunted plant growth, yellowing, and low productivity.

Conclusions and Future Prospects

The cactus-feeding insects associated with subfamily Opuntioideae are well documented, but those associated with the other subfamilies, Cactoideae and Pereskioideae, are little known and need further study, particularly in some South American countries. The known insect guild is characterized by a high degree of specificity and unique adaptations to the Cactaceae. The insect families Pyrali-dae, Cerambycidae, and Curculionidae dominate the guild, and all their cactus-feeding species are endo-phagous. Of the nine species in the Dactylopiidae, which are all associated with Cactaceae, four species have become well known as highly successful biological control agents against invasive Opuntia species and a fifth one, Dac-

tylopius coccus, is reared commercially as a source of the red dye, carmine.

With the increasing importance of commercial cactus plantings and larger areas under cultivation, some of the key pests will find their way to new targets. Knowing and understanding the potential threats may help to prevent unwanted arrivals. The dispersal of Cactoblastis cactorum and its subsequent invasion of mainland America is a case study. The chances of insects from non-cactus hosts adapting to become pests on cactus cultivations are small, and the recruitment of new pests in the major cactus growing countries will depend mainly on natural dispersal and human intervention of existing cactus pests. This applies particularly to cactus-pear cultivation in countries outside of the Americas. The recruitment of new pests from the large source of cactus-feeding insects and diseases native to the Americas is also possible in time.

The internal feeding habits of most cactus-feeding insects will make conventional control methods, e.g., insec-ticidal control, very difficult. Biological control has been attempted against only one cactus pest, Diaspis echinocacti, but biological control projects are now being considered against C. cactorum and other species. Research will continue on the use of host-specific, cactus-feeding insects for the biological control of cactus invaders outside their natural distribution. The selection of host-adapted biotypes of Dactylopius tomentosus for the biological control of Opuntia rosea is presently being examined in South Africa, which is expected to provide further useful information on the existence of host-adapted biotypes. Studies on biological control of cactus weeds have provided valuable information on many of the key cactus-feeding insects (Moran and Zimmermann 1984). Likewise, research on C. cactorum by South African and Australian entomologists will provide useful information when formulating a strategy to prevent its invasion or, eventually, its control on the North American continent (Zimmermann et al. 2000).

Cactus diseases are not extensively studied, as revealed by the relatively few publications. Most research on cactus diseases has emerged from Mediterranean countries, e.g., Italy. Even less research has been conducted on the natural diseases found on native cactus species in the Americas. With increased cultivation of cactus pear in America and elsewhere, some of the less host-specific latent diseases are expected to gain in importance when switching to commercial plantations.

Acknowledgments

Thanks are expressed to the following persons for providing information on cactus pests and selected literature: Mayra Perez-Sandi y Cuen, Antonio Bustamante, Yosef Mizrahi, Carmen Saenz, Carlos Nostas, and Enrique Lobo. Hildegard Klein provided valuable criticism and edited the draft manuscript.

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