DISEASE CONTROL BLACK SIGATOKA

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1 BLACK SIGATOKA Randy Ploetz of the Tropical research & Education Center at the University of Florida in the USA discusses the management of the most important disease of banana and plantain Introduction During 1987, an ad hoc committee set up by the Federal Department of Agriculture of Nigeria recognized the outbreak of black Sigatoka in Nigeria as an ecological disaster, destroying the economies of the states affected. The International Institute of Tropical Agriculture (IITA) has acknowledged that black Sigatoka disease is the most critical research issue for plantain and banana in Africa. Hahn et al. (1990) Black Sigatoka is currently the most important disease of banana and plantain worldwide. The above reactions in West Africa are typical of those that occur once this destructive disease spreads to a new area. Black Sigatoka very significantly reduces the yield and quality of banana and plantain and thereby impacts the food security and economies of the affected regions. Significance of banana and plantain Banana and plantain, the latter being a type of banana, are among the world s most important agricultural products. After rice, wheat and milk, they are the fourth most valuable food. Global output exceeded 87 million metric tonnes (MMT) in 1997, but exported fruit (mainly banana) represented only about 15% of this total. The remaining 74 MMT were produced for local consumption and marketing. Frequently, the producers and end-users of the later fruit are poor, subsistence farmers who utilise banana as a staple food. Black Sigatoka has a tremendous effect on subsistence production. Unfortunately, most of these producers can ill afford the fungicides that are used to control this disease. Thus, relatively little attention is paid to nonexported fruit in this article. Instead, it focuses on the export segment of world banana production which relies heavily on the use of chemicals to control black Sigatoka. Despite their small share of global production, exported bananas are major international commodities. They were valued at US$4.8 billion in 1998, and rank fourth among all exported agricultural commodities and first among all fruit crops (Anonymous). The export trades originated in tropical America in the mid-1800s and remain concentrated in this region (Table 1). The origin, spread and effects of black Sigatoka Black Sigatoka was described originally in the Sigatoka Table 1. The major exporters of banana Country Gross exports in 1997 (1000 tonnes) Ecuador 4446 Costa Rica 1835 Colombia 1509 Philippines 1255 Guatemala 630 Panama 602 Honduras 557 Data are from FAO, Valley of Fiji in However, herbarium specimens and published accounts of banana leaf diseases indicate that the disease was actually widespread in Asia by that time. Only recently has the disease spread outside this region. Black Sigatoka reached the Western Hemisphere (Honduras) in 1972 and Africa (Zambia) in By 1991, the disease had spread to much of the Americas, sub-saharan Africa, and had reached the first island in the Caribbean, Cuba. It is now found in most of the humid tropics in Africa, the Americas and Asia, and continues to spread to the few remaining areas that are free of the disease (Ploetz & Mourichon, 1999). Black Sigatoka and the closely related yellow Sigatoka are the primary leaf spot diseases of banana. They are caused by two ascomycete fungi, respectively, Mycosphaerella fijiensis Morelet (anamorph: Paracercospora fijiensis (Morelet) Deighton) and M. musicola Mulder (anamorph: Pseudocercospora musae (Zimm.)), which produce similar symptoms on banana. Yellow Sigatoka has a wider distribution, but black Sigatoka is more aggressive and has a wider host range; it has displaced yellow Sigatoka as the predominant leaf spot on banana in most of its range. Black Sigatoka affects plantain and banana cultivars that are resistant to yellow Sigatoka, and causes significant defoliation and yield losses (Figures 1 and 2). On the Cavendish cultivars that are used by the export trades, it also causes premature ripening, a serious defect in exported fruit. M. fijiensis produces conidia and ascospores, both of which are infective. They are formed under high moisture conditions, and are dispersed by rain and irrigation water. Due to their greater abundance and small size, ascospores are most important in spreading the disease within plants and plantations. Leaves are infected indirectly via stomata, and the abaxial surface is the primary affected site due to the greater abundance of stomata on this part of the leaf This journal is The Royal Society of Chemistry 2000 Pesticide Outlook February

2 Figure 1. Initial lesions of black Sigatoka on a leaf of Dwarf Cavendish. As these lesions enlarge and coalesce, they usually develop a water-soaked appearance. Figure 3. Penetration of a banana stomata by Mycosphaerella fijiensis. Note that the germtube has arisen from an ascospore (photo: R. H. Stover) (Washington et al., 1998) (Figure 3). The unfurled new leaf, referred to as the candela in Latin America, provides an ideal microclimate for infection and it is in this structure that significant infection by ascospores occurs (Figure 4). Free moisture is required for infection by ascospores, and the minimum optimum, and maximum temperatures for this event are, respectively, 12 C, 27 C and 36 C. In many production areas conducive conditions occur year-round. Without the frequent use of fungicides, the export trades could not control black Sigatoka and, thus, would be unable to produce profitable quantities of high quality fruit. The trades depend almost entirely on a single Cavendish cultivar, Grand Nain. Grand Nain produces large bunches of uniformly sized fruit, and has a short stature that aids harvesting operations and makes the plant more stable than taller cultivars during tropical storms and hurricanes. Unfortunately, Grand Nain is also very susceptible to black Sigatoka. The export plantations are usually vast monocultures (Figure 5). These huge plantings lend themselves to highly mechanized harvesting and packing operations but, since they are also uniformly susceptible, are also prone to devastating outbreaks of black Sigatoka (Figure 6). In order to treat such large areas with fungicides, helicopters or fixed wing aircraft are used (Figure 7). This is an expensive practice since it also involves permanent landing strips, facilities for mixing and loading the fungicides, and the high recurring expense of the spray materials themselves. These expenses total about US$1000 per hectare per year and, by the time the fruit reach a retail destination in the importing countries, are responsible for 25% of the retail price. Fungicidal control of the Sigatoka leafspots Chemical control of the Sigatoka leaf spots has evolved considerably since the mid-1930s (Stover, 1990). Until the mid-1970s, all efforts were focused on yellow Sigatoka in the Caribbean and Central America. Bordeaux mixture, the first fungicide that was used, was followed by fixed coppers and the dithiocarbamates. Applications were made initially with permanent spray equipment that relied on highpressure pumps and complex underground plumbing in the plantations. Eventually aircraft replaced these permanent systems, and these remain the primary means by which fungicides are applied in these settings. Figure 2. Severe black Sigatoka damage on Dwarf Cavendish in the absence of fungicidal control measures. Petroleum oils Beginning in the late 1950s petroleum oils began to be used in Sigatoka control programs (Stover, 1990). Oils were first used as adjuvants, but it was soon realized that they were also somewhat effective when they were used alone. Oils possess several notable characteristics. They act as spreading and sticking agents and aid the retention and movement of fungicides on the leaf surface. Oils also assist the penetration of the leaf by systemic fungicides, reduce conidium germination, germ tube growth and appressorium formation, and increase the pathogen s incubation period. Finally, they retard the growth and development of the pathogen within the host leaf. 20 Pesticide Outlook February 2000

3 Figure 4. An unfurled new leaf of banana, the candela. The interior of the cylinder that this leaf forms is a primary site of infection for Mycosphaerella fijiensis. (photo: R. H. Stover) Figure 5. Large monoculture of Grand Nain in Honduras that is typical of export plantations. Saturated, aromatic and non-hydrocarbon fractions of heavy and light paraffinic oils were tested first (Stover, 1990). Many of these products were phytotoxic and not very effective. However, as their properties became better understood, effective and less damaging naphthenic and paraffinic oils were developed. Currently, oils with unsulfonated residues of less than 90%, aromatic contents of 12% or less, and distillation ranges between 346 C and 354 C at 760 mm Hg are deemed acceptable. However, in the absence of disease pressure, even these refined products reduce transpiration, photosynthesis and yields by 5 10% (Israeli et al., 1993). Systemic fungicides Fixed copper and dithiocarbamate fungicides in oil were the standard methods of control until the first systemic fungicide, benomyl (Benlate), appeared. Initially tested against yellow Sigatoka in Honduras in 1967, it was used widely by Benomyl and subsequent benzimadazoles were very effective and enabled much improved control over that provided by the dithiocarbamates. The introduction of benomyl and subsequent systemics heralded a new era of Sigatoka control (Stover, 1990). Unlike the protectants, systemics inhibited the development of symptoms after they first appeared. This curative action allowed the frequency of application to be reduced since it was no longer necessary to have susceptible plant surfaces continually protected from infection. About the same time that benomyl was introduced another systemic fungicide, tridemorph (Calixin), was tested. It was the first sterol biosynthesis inhibitor (SBI) and remains the primary morpholine fungicide to be used against black Sigatoka. Since it was not as effective as benomyl, it was not used to any great extent until benomyl resistance problems and black Sigatoka had become widespread in the 1980s. Reintroduction of protectant fungicides During the late 1970s and early 1980s, new strategies were devised to combat this disease (Stover, 1990). Phytotoxicity from the oils began to cause greater concern among export producers, and means by which the amount of oil that was used could be reduced were sought. At this time two new protectant fungicides, a flowable formulation of mancozeb (Dithane F) and chlorothalonil (Bravo 500) were introduced that were applied in water, rather than oil. Although neither product was very effective by itself during periods of high rainfall and disease pressure, these fungicides were effective during drier periods when oils were assumed to cause the most damage. The new protectants were also used in resistance management programs, either in alternation or in cocktail mixtures with systemics. During episodes of severe disease pressure, cocktails of benomyl or tridemorph with mancozeb in oil and water emulsions were the preferred weapons against the Sigatoka leafspots. New systemic fungicides The first triazole fungicide, propiconazole (Tilt), was introduced for use on banana in 1984 (Stover, 1990). It had high post-infection activity and, thus, could be used on longer application intervals than were possible previously. Along with the adoption of disease forecasting measures (see below), this new fungicide allowed producers to reduce the number of applications in a plantation from as many as 45 to fewer than 20 applications per year. Propiconazole and other sterol demethylation inhibitors (DMIs) now comprise the largest group of systemic fungicides that are used on banana. Despite the large number of triazoles that have been tested against black Sigatoka [e.g. bitertanol (Baycor), cyproconzaole (Alto), difenoconazole (Score), flusilazole (Punch), hexaconazole (Anvil), metconazole (Caramba), and tebuconazole (Folicur)], propiconazole remains the most frequently used fungicide of this group (Romero & Sutton, 1997). Recently, the methoxyacrylate fungicide azoxystrobin (Bankit) has been shown to be effective against this disease. Azoxystrobin is at least as effective against black Sigatoka as the triazoles (Ponsioen & Doco, 1999). Unfortunately, its high cost limits the frequency with which it can be used. Pesticide Outlook February

4 Figure 7. Airplanes are used commonly to apply fungicides in export plantations. (photo: R. H. Stover) Figure 6. Permanent infrastructure, such as this cableway, assists harvesting and packing operations in export plantations. Fungicide resistance An unfortunate attribute of some of the most effective systemic fungicides that have been used against black Sigatoka is the ease with which their efficacy is lost. Within 2 to 3 years of the introduction of benomyl in Central America, resistance began to be observed, and by the late 1970s it could no longer be used effectively in many areas (Stover, 1990). Although benomyl is currently not used to any great extent by the export trades, mention should be made of its re-introduction for black Sigatoka control. After benomyl resistance became a major problem, work in Honduras indicated that sensitive strains of M. fijiensis would displace resistant strains if benomyl use was discontinued; within 15 months, only 10% of the ascospores that were assayed tolerated 10 ppm of benomyl (Stover et al., 1978). In contrast, Romero & Sutton (1998) reported that benomyl resistance actually remained at high levels 3 to 5 years after its use was discontinued in plantations in Costa Rica (42 100% of the strains they studied tolerated 5 ppm). The latter authors recommended that population sensitivities should be assessed before benomyl s reintroduction was considered in a given plantation, regardless of the amount of time that had transpired since its last application. Resistance to propiconazole has developed quite differently. Reduced control with this fungicide became widely evident in Central America in the 1990s. Romero & Sutton (1997) monitored the in vitro response of singleascospore isolates to various propiconazole concentrations and observed a rapid shift towards insensitivity in three different plantations in Costa Rica. However, unlike the situation with benomyl, they observed wide ranges in sensitivity in each plantation, and in no case was there evidence for the predominance of a highly resistant population. Although they speculated that individuals with high levels of resistance were less fit than sensitive strains, the cost of resistance in M. fijiensis to this important fungicide has not been researched. Much less is known about resistance in M. fijiensis to azoxystrobin. After intensive use in a trial site in Costa Rica (>10 consecutive applications), a small population was recovered that was sufficiently insensitive to affect control (Heaney, et al., 1998). Presumably, significant erosion in the efficacy of this fungicide would occur if it was used in an exclusive manner in commercial plantations. Brent & Hollomon (1998) discussed the propensity of different classes of fungicides to lose effectiveness over time. They noted a wide range in the inherent risk of resistance developing in different classes. Among those that have been used against black Sigatoka, the benzimidazoles were ranked as high risk, the DMIs and strobilurins (e.g. azoxystrobin) moderate, and chlorothalonil, copper and the dithocarbamates low. They also classified the risk of resistance developing in various pathosystems. The M. fijiensis:banana system was classified as high risk since the pathogen had a short generation time, sporulated abundantly, and had a sexual cycle that enabled the development of new resistance phenotypes. Based on their combined fungicide and diseaserisk ratings, the benomyl:black Sigatoka scenario was classified as a worse-case situation, an analysis that is clearly corroborated by the short, successful use of this fungicide in banana plantations. Lower, but still very substantial, risk was associated with the use of the DMIs and strobilurins against this disease. In order to prolong the effective life of vulnerable 22 Pesticide Outlook February 2000

5 fungicides in high-risk situations, working groups of the Fungicide Resistance Action Committee (FRAC) of the Global Crop Protection Federation (an international consortium of agrochemical producers) have created use guidelines. In general, these recommendations specify that effective fungicides with different modes of action should be used on an alternating basis or in mixtures. With regard to black Sigatoka, FRAC collaboration with the export companies ensures that there is industry-wide adoption of the guidelines. Once there is agreement among the respective parties on the most effective use patterns, plantation managers utilise, on a regional basis, an integrated approach for management. Regional coordination addresses the ease with which M. fijiensis moves among plantations as well as the view that resistance management strategies would not be very effective if less than full compliance was achieved in a given area. Disease forecasting Application schedules in the plantations are now routinely determined with disease-forecast models (Stover, 1990). In general, these systems incorporate data on disease severity and environmental factors that are known to affect infection and disease development. The models are based on the use of oils and systemic fungicides only since protectant fungicides have no curative effect on symptom development. When these epidemiological tools were first used in Cameroon, they enabled producers to control black Sigatoka with annual applications (Stover, 1990). In tropical America, where control is more difficult, typical schedules of applications per year could be reduced by more than one-half when disease forecasting was first used. However, increased tolerance to the DMI fungicides in Central America has recently made it necessary to again increase applications to previous frequencies of times per year. How the introduction of azoxystrobin in black Sigatoka control programs has affected application frequencies in this region has not been reported. Outlook Undoubtedly, the management of black Sigatoka represents one of the most significant and ongoing challenges in all of production agriculture. Given the dependence of the export trades on Grand Nain, it is clear that this disease will remain a severe constraint in the foreseeable future. Despite recent advances in banana breeding, there are currently no resistant cultivars that could be used to replace Grand Nain. Thus, fungicidal control of this disease will remain an absolute necessity in order for the trades to continue producing high quality fruit in the humid tropics. The success of these efforts will depend in no small part on the trade s abilities to effectively manage fungicide resistance problems, and on the development of new, effective chemistries. In the absence of both of these requirements, banana could again become an expensive and uncommon tropical fruit in the developed world. References Anonymous. FAOSTAT online database at: Brent, K. J.; Hollomon, D. W. (1998) Fungicide Resistance: The Assessment of Risk. FRAC Monograph No. 2. Global Crop Protection Federation. Brussels. Hahn, S.; Vuylsteke, D.; Swennen, R. (1990) First reactions to ABB cooking bananas distributed in southeastern Nigeria. In: Fullerton, R. A., and Stover, R. H. (Eds.) Sigatoka Leaf Spot Diseases of Banana. INIBAP. Montpellier, France. pp Heaney, S.; Lorenz, G.; Appel, J.; Butler, J. N.; Staub, T.; Dalton, I. (1998) STAR (Stobilurin Type Action and Resistance). In: 1998 Status Report & Recommended Fungicide Resistance Management Guide. FRAC. Global Crop Protection Federation. Brussels, pp Israeli, Y.; Shabi, E.; Slabaugh, W. R. (1993) Effect of banana spray oil on banana yield in the absence of Sigatoka (Mycosphaerella sp.). Scientia Horticulturae 56, Ploetz, R. C.; Mourichon, X. (1999) First report of black Sigatoka in Florida. Plant Disease 83, 300. Ponsioen, G.; Doco, H. (Eds.) (1999) MUSARAMA. vol. 12, bibliography numbers 5196 and Romero, R.A.; Sutton, T. B. (1997) Sensitivity of Mycosphaerella fijiensis, causal agent of black Sigatoka of banana, to propiconazole. Phytopathology 87, Romero, R. A.; Sutton, T. B. (1998) Characterization of benomyl resistance in Mycosphaerella fijiensis, cause of black Sigatoka of banana, in Costa Rica. Plant Disease 82, Stover, R. H. (1990) Sigatoka leaf spots: Thirty years of changing control strategies: In: Fullerton, R. A., and Stover, R. H. (Eds.) Sigatoka Leaf Spot Diseases of Banana. INIBAP. Montpellier, France. pp Stover, R. H.; Slabaugh, W. R.; Grove, M. D. (1978) Effect of chlorothalonil on a severe outbreak of banana leafspot caused by benomyl tolerant Mycosphaerella fijiensis var. difformis. Phytopathology News 12, 268. Washington, J. R.; Cruz, J.; Lopez, F.; Fajardo, M. (1998) Infection studies of Mycosphaerella fijiensis on banana and the control of black Sigatoka with chlorothalonil. Plant Disease 82, Randy Ploetz has been a research plant pathologist at the University of Florida s Tropical Research & Education Center in Homestead since He is an authority on diseases of tropical fruit crops, in particular those that affect avocado, banana and mango. He has written extensively on these diseases, has edited Fusarium Wilt of Banana and the Compendium of Tropical Fruit Diseases, both published by APS Press, and is in the midst of editing a new book, Diseases of Tropical Fruit Crops, that will be published later this year by CAB International. With the recent outbreak of black Sigatoka, he now intends to investigate this important disease in the Homestead area. Pesticide Outlook February