Black Leaf Streak Disease Is Challenging the Banana Industry

Original article

Black Leaf Streak Disease is challenging the banana industry

Luc de Lapeyre DE BELLAIRE1*, Eric FOURÉ1, Catherine ABADIE2,3, Jean CARLIER2

1 CIRAD-Persyst, UPR Black Leaf Streak Disease is challenging the banana industry. Systèmes bananes et ananas, Abstract — Introduction. Black Leaf Streak Disease (BLSD) is regarded as the most economically TA B-26 / PS4, Blvd. de la important threat that the banana industry has to face. Effectively, this foliar disease affects leaf pho- Lironde, 34398 Montpellier tosynthesis but, above all, reduces the greenlife of fruits, that cannot be exported in cases of severe Cedex 5, France, infestation. Main characteristics of Black Leaf Streak Disease. More than 20 Mycosphaerella species have been described on bananas. Leaf spot diseases of bananas are caused by some species of luc.de_lapeyre_de_bellaire@ this complex, of which M. fijiensis (BLSD) and M. musicola (Sigatoka disease) are the most important. cirad.fr M. fijiensis is an invasive species that has totally replaced M. musicola in most banana-exporting countries, which was conducive to increasing difficulties in banana leaf spot control. BLSD causes increas- 2 CIRAD-Bios, UMR BGPI, ing difficulties for control. Since all banana cultivars grown in the banana industry are highly Campus international de susceptible to BLSD, the control of this disease relies on aerial applications of fungicides according Baillarguet, TA A-54 / K, to either systematic frameworks (mostly contact fungicides) or forecasting strategies (mostly systemic 34398 Montpellier Cedex 5, fungicides). In a banana-exporting country where M. fijiensis has been reported, BLSD control becomes increasingly more difficult. This evolution is essentially due to the rapid emergence of fun- France gicide resistance, and is conducive to a significant increase in the cost of disease control but, above 3 all, to increasing negative environmental effects. Challenges for the banana industry. Because of CIRAD-Bios, UPR the rapid adaptation of M. fijiensis, the banana industry must be prepared for significant evolution. Multiplication végétative, We propose various parameters that should be monitored at different levels (disease assessment Station de Neufchâteau, parameters, evaluation of chemical control efficiency, global evaluation of BLSD economic incidence) Sainte-Marie, 97130 to rationalize such evolution. The modelization of BLSD effects on bunch mass and greenlife should Capesterre-Belle-Eau, enable defining acceptable disease thresholds and optimizing bunch weight and harvest stage according to agronomic practices. On the other hand, fungicide use is conducive to significant environmental Guadeloupe, France impact and must be limited. Forecasting strategies should be used wherever systemic fungicides are still efficient. Finally, the predominance of a unique type of susceptible cultivar is unsustainable and the recourse to resistant varieties in an integrated strategy is undoubtedly the future of BLSD control. France / Musa / disease control / fungal diseases / Mycosphaerella fijiensis / resistance to chemicals La Maladie des Raies Noires défie l'industrie de la banane. Résumé — Introduction. La Maladie des Raies Noires (MRN) est la plus grande menace à laquelle est confrontée l’industrie de la banane. En effet, cette maladie foliaire affecte la photosynthèse des bananiers mais, surtout, elle entraine une réduction du potentiel de conservation des fruits qui ne peu- vent être exportés lorsque les bananiers sont sévèrement atteints. Principales caractéristiques de la MRN. Plus de 20 espèces du genre Mycosphaerella ont été décrites sur le bananier, mais les cercosporioses des bananiers sont principalement le fait de deux espèces M. fijiensis (MRN) et M. musicola (maladie de Sigatoka). M. fijiensis est une espèce invasive qui a totalement remplacé M. musicola dans la plupart des pays exportateurs de bananes, ce qui s’est toujours traduit par un contrôle plus difficile de la cercosporiose. Des difficultés de contrôle croissantes. Comme toutes les variétés de bananes cultivées dans l’industrie de la banane sont très sensibles aux cercosporioses, le contrôle de la MRN repose sur l’application aérienne de fongicides soit selon des programmes systématiques (fongicides de contact), soit sur avertissement (fongicides systémiques). Dans les pays exportateurs de * Correspondence and reprints bananes où M. fijiensis a été détecté, le contrôle de la MRN est devenu de plus en plus difficile. Cette évolution a principalement été le fait de l’apparition de souches résistantes aux fongicides et s’est tra- duite par une augmentation du coût de la lutte et surtout par un accroissement des impacts envi- ronnementaux. Des défis pour l’industrie bananière. Comme M. fijiensis a des capacités d’adaptation très rapides, une des conditions de survie de l’industrie bananière est de se préparer à Received 30 August 2010 d’importantes mutations. Nous proposons une batterie d’indicateurs à différents niveaux (parcelle, Accepted 15 September 2010 efficacité globale de la lutte, incidence économique globale) afin d’objectiver ces évolutions. La modé- lisation des effets de la MRN sur le poids des régimes et la durée de conservation des fruits devrait permettre de définir des niveaux de maladie acceptables mais aussi d’optimiser le poids des régimes Fruits, 2010, vol. 65, p. 327–342 et le stade de récolte en fonction des pratiques agronomiques. Afin de limiter l’emploi des fongicides © 2010 Cirad/EDP Sciences qui ont un impact environnemental important, les stratégies d’avertissement doivent être employées All rights reserved partout où les fongicides systémiques sont encore efficaces. Enfin, la prédominance de cultivars sen- DOI: 10.1051/fruits/2010034 sibles n’est pas durable et le futur de cette industrie passe probablement par l’incorporation dans les systèmes de culture de variétés résistantes. www.fruits-journal.org France / Musa / contrôle de maladies / maladie fongique / Mycosphaerella fijiensis / RESUMEN ESPAÑOL,p.342 résistance aux produits chimiques

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Article published by EDP Sciences and available at http://www.fruits-journal.org or http://dx.doi.org/10.1051/fruits/2010034 L. de Lapeyre de Bellaire et al.

1. Introduction fruit [9], harvested still green at a pre-climacteric stage before being ripened artificially Bananas are one of the main agricultural with ethylene in ripening rooms. The time productions in the world, and the main fruit between harvest and the climacteric rise is crop, with an annual production of about called the greenlife and reflects the potential 110 Mt [1]. International trade of bananas of fruit conservation [10], which should be represents 14 Mt·year–1 with a value of more superior to the time between harvest and than 4 billion US$ [2]. The production of artificial ripening. The main effect of BLSD bananas for this international trade is grown is the reduction of the greenlife of harvested in a small number of tropical countries fruits on heavily diseased plants [11]. This is mainly located in Latin America (80%), in why this disease is such a significant threat African and Asian countries, and in the Euro- to the banana industry. Effectively, banana pean community (French West Indies, growers must control BLSD to a level that Canary Islands). In all these countries, this does not alter fruit exportation. This is why industry is economically important and a the different banana companies generally source of direct and indirect employment. perform a systematic control of this disease In the world of the banana industry, Black and use an empiric threshold of remaining Leaf Streak Disease (BLSD) is regarded as leaves at harvest (3–5 leaves according to the most economically important disease [3] the companies) in order to decide which and is considered as one of the most impor- bunches are exportable or not. The eco- tant crop diseases in the world [4]. This sit- nomic incidence of this disease is significant uation is mainly because the banana trade since the cost of control can reach more than relies on a unique banana group of cultivars 25% of the production cost [12]. BLSD inci- (Musa acuminata, AAA, Cavendish sub- dence in the banana industry is regularly group) which are highly susceptible to this increasing and the objective of our paper is disease. The dominance of the Cavendish to highlight the origin of these variations and cultivars results itself from the organization to propose some evolution in the banana of the banana production in an industry industry, driven by research, in order to pre- which is furthermore (i) highly concen- vent a new ‘crisis’ in this industry. trated in multinational groups [2], and (ii) characterized by the presence of an industrial process at the end of the chain 2. Main characteristics since bananas are artificially ripened in industrial ripening houses before marketing. of Black Leaf Streak Disease Black Leaf Streak Disease of bananas is a foliar disease. The first symptoms of this 2.1. A fungal pathogen within disease are reddish-brown streaks (< 1 mm) a complex of species which enlarge and can form lesions of up to 20–30 mm, becoming darker in color [5]. BLSD is caused by an ascomycetous heter- This leaf spotting has two kinds of effects othallic fungus, Mycosphaerella fijiensis on the banana yield. Since BLSD affects the Morelet, which was first described in the photosynthetic area of banana leaves, the island of Fiji in 1963 [13]. Mycosphaerella production of dry matter is reduced by leaf fijiensis produces bicellular ascospores spotting. It has been shown for Sigatoka Dis- while its anamorph Paracercospora fijiensis ease (SD), a related Mycosphaerella foliar forms 1–10 septate conidia which are pro- disease of bananas, that the diminution of duced singly at the apex of conidiophores. the leaf area, induced by severe spotting, Sigatoka Disease, caused by Mycosphaerella had a strong effect on bunch weight [6]. For musicola (anamorph Pseudocercospora BLSD, significant yield losses (20% to 50%) musae), was the first Mycosphaerella foliar were also estimated on plantains [7, 8]. How- disease of bananas described in Java in 1902 ever, another important component of [14]. The two fungi can only be distin- banana yield is the fruit aptitude for conser- guished by the morphology of their vation. Effectively, banana is a climacteric anamorph [15]. More recently, a third

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Mycosphaerella foliar disease of bananas unfurled leaf. Therefore, there is a gradient (Mycosphaerella eumusae, anamorph Pseu- of evolution of the disease from the top to docercospora eumusae) was reported in the bottom of the banana tree, and fungicide Southern and Southeast Asia [16]. Later, a applications should be aimed at the top of broad study revealed that more than banana trees to control new infections. New 20 Mycosphaerella species can be isolated attacks should be detected only on young from banana leaves [17], but, except for leaves, which is particularly important for Mycosphaerella musae causing a leaf disease monitoring in forecasting strategies. freckle, the implication of these other Mycosphaerella species as leaf pathogens of 2.2.2. The duration of the incubation bananas has not been determined. Molecu- period is variable lar diagnostic tools have been developed The duration of the incubation period, as from specific actin or beta-tubulin genes [18] well as the symptom evolution time, is very or ITS sequences [19] to distinguish variable according to climatic variations. M. fijiensis, M. musicola and M. eumusae, This indicates a real possibility for forecast- but these tools should take into account this ing systems to work where climatic condi- broader complex. On the other hand, the tions might be unfavorable to disease potential implication of these species as new development. foliar diseases either on Cavendish, or on other banana cultivars is questionable. The 2.2.3. Ascospores are produced in late predominance of M. eumusae in some Asi- stages atic countries suggests a differential adaptation of the different Mycosphaerella species Although the epidemiological importance and the competitiveness between these spe- of conidia is still not well understood, it is cies should be better understood. accepted that ascospores are predominant in BLSD epidemiology. Therefore, in order 2.2. Main considerations to control field inoculum, it is essential to control the disease before necrotic forma- on the life cycle of BLSD tion. Where leaves are heavily spotted, they should be removed, since they might pro- The life cycle of BLSD has been widely duce ascospores for many months. described [3, 11] and starts with leaf infection by either ascospores or conidia. After 2.2.4. Inoculum is wind-dispersed a period of epiphyllic growth of generally 2–3 days, germ tubes penetrate stomata. In As wind-transported ascospores can dis- good conditions, the first symptoms appear seminate the disease over long distances, generally 10–14 days after. The symptoms BLSD has a strong potential progression in then gradually evolve from stage 1 to stage landscapes where Musa genotypes are quite 6. Conidia are produced on young stages of frequent, which is the case in most tropical the disease (stage 2–4) and have been con- countries where bananas are grown. Con- sidered as water dispersed at short dis- trol of the disease should be maintained by tances, even if they are also present in the all growers of one region, using the same airspora [20]. Ascospores are produced at technical guidelines because disease and the later stage and are wind-dispersed after pathogen evolution in a specific geographic perithecia burst. They are considered to be area has potential influence over a wider dispersed at longer distances than conidia area. [21]. It is important to highlight some charac- 2.3. BLSD, a disease still teristics of this life cycle that are useful for in worldwide expansion BLSD control. At the beginning of the banana industry, 2.2.1. Infection starts in young leaves Sigatoka Disease was present in all countries Because of antagonism on old leaves, infec- located in tropical humid conditions and the tion mainly occurs on the cigar and the first control of this disease was easier and less

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expensive than for BLSD. In all countries has been in the African continent, probably where M. fijiensis has been reported, this from a hypothetical initial introduction in pathogen rapidly replaced M. musicola. Zambia in 1973 [3, 27]. In Cameroon, BLSD The economic consequences of the emer- was reported in 1980 and totally replaced gence of BLSD in such countries were very Sigatoka disease in the commercial banana significant, and the case of the expansion of farms in less than 2 years. Population struc- this pathogen in Latin America showed var- ture analysis of M. fijiensis from the global ious significant effects such as (i) significant to local scales have allowed us to under- losses due to premature ripening, (ii) signif- stand better the dispersal processes under- icant increases in production costs, and lying this recent pandemic [26, 28, 29]. (iii) the abandoning of significant commer- Particularly, founder effects were detected cial areas for exportation and for plantain in the global population structure of production [22]. M. fijiensis is more aggres- M. fijiensis, suggesting rare migration sive than M. musicola, and particularly on events among continents through move- plantains [23], which are an important food ments of infected plant material. crop in many countries and particularly in Depending on environmental conditions, Africa and Latin America. Since the aggres- BLSD may have a rapid geographic expan- siveness of M. musicola is very low on plan- sion, mainly because ascospores can be tains, growers were not prepared for leaf wind-transported over long distances. spot disease control, and the emergence of Therefore, M. fijiensis is a quarantine organ- BLSD on this food crop had a dramatic inci- ism in all countries where this disease is not dence, leading to significant crop losses and present, the best control method being the to the abandoning of significant commercial prevention of its introduction. Specific con- areas [22]. However, in the ecological control measures were therefore established to ditions of highlands (Cameroon, Colombia), prevent the dissemination of this disease to M. musicola was pathogenic on plantains new countries [30]. These measures include: [24] and the substitution of M. musicola by (i) specific communication to the popula- M. fijiensis has been delayed [25]. tion; (ii) coordination of sanitary services on The genetic structure of M. fijiensis pop- a regional scale; (iii) monitoring programs ulations around the world shows that this in order to detect the progression of the fungus originated from South-East Asia and pathogen, this work being now facilitated has been brought to other continents by the development of molecular methods through limited introductions due to germ- [18, 19]; and (iv) specific legislation to plasm transportation [26]. From the original restrict germplasm movement and for oblig- center, two recent and rapid continental atory control measures in new infested expansions have occurred and are still in areas. Once introduced into a new country, progress. The most important for the banana BLSD expansion has been fast because industry started in the American continent bananas are not only grown in industrial from Honduras in 1972 [3, 27]. Progressively plantations, but also in gardens and food- all central American countries have been producing plots. Thus, bananas are scat- colonized, and tropical and subtropical tered regularly in tropical countries, favor- South American and North American coun- ing a gradual expansion of the disease. As tries were also colonized (figure 1). This a consequence, in most countries where expansion is still in progress in the Carib- BLSD has been introduced, eradication has bean islands from a first northern introduc- not been achieved, except in Australia tion in Cuba in 1990 and a probable where (i) an intensive surveillance program southern independent introduction in Trini- based on performing diagnostic tests, and dad in 2003. Only a few islands, including (ii) an efficient elimination of infected and Martinique, Dominica and Guadeloupe, neighboring bananas have been imple- remain free of BLSD, the most recent report mented [19]. Therefore, chemical control is being in St-Vincent and Ste-Lucia in 2009 the only control method that enables BLSD and 2010, where its expansion has been management in all of the banana industry very fast. The second continental expansion [31].

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3. BLSD causes increasing This strategy allowed a significant limitation Figure 1. difficulties for control of chemical use to 12–14 treatments per Geographic expansion of Black year. Nevertheless, the development of fun- Leaf Streak Disease in the Americas. In a banana-exporting country where BLSD gicide resistance led to the progressive has been introduced, the history of disease abandoning of this rational strategy at the control always shows that control is increas- expense of systematic use of contact fungi- ingly more difficult. Then, the number of cides that must be applied every week (40– chemical treatments necessary for disease 50 applications per year). In all these coun- control increases with time. This is the case tries, this evolution has led to a significant in Costa Rica where about 30 fungicide increase in the cost of disease control [33] applications per year were realized at the but, above all, to an increase in negative beginning of the 90s [21]. A recent survey environmental effects. In systematic strate- –1 –1 of pesticide use carried out in 2007 for the gies, 30–40 kg active ingredient·ha ·year –1 –1 Pesticide Reduction Plan for Banana (PRPB) are applied versus 2–4 kg a.i.·ha ·year in showed that more than 50 applications per the forecasting strategy. year are now necessary in this country [41]. This increase is essentially due to the Another illustration of increasing control dif- rapid adaptation of the fungus, that ficulties is the case of Cameroon, where becomes resistant to the systemic fungicides BLSD was reported for the first time in 1980. which have a curative effect on the disease In the banana farms of Cameroon, a fore- [31]. The strong adaptation potential of this casting strategy, relying on timing of appli- fungus is a consequence of its biological cations of highly curative systemic fungicides characteristics: importance of recombina- according to biological observations [32], tion, high population levels and high dis- was elaborated and applied with success. persion capacities [34]. Two types of

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fungicides have been used for BLSD control products for which the emergence of resist- [31]: contact fungicides and systemic fungi- ant strains has been very fast in some coun- cides. tries such as Honduras, where they have Contact fungicides (mancozeb, chlorotha- been reported after only 2–3 years of con- lonil) have only a preventive effect and do tinuous use [37]. Fungicide resistance to not penetrate the banana leaf. They are gen- strobilurins has also been very fast in most erally applied every week in systematic banana-growing countries, and did not frameworks because all new unfurling exceed 3 years' use in Costa Rica [38]. A sig- banana leaves must be protected. They nificant shift in the sensitivity to DMI fungi- inhibit fungal germination by a multisite cides was also reported in Costa Rica after action and so do not induce the develop- these fungicides had been used for more ment of resistant strains. than 7 years [39]. After the emergence of resistance, first in a localized area, resistant Systemic fungicides penetrate the banana strains progressively diffuse in most of the leaf. The systemic properties of these fun- banana plantations of the same country [33, gicides are variable: some have only a 38]. Today, fungicide resistance to benzim- translaminar transport and others can be dis- idazole and to strobilurins is widespread in tributed in the whole banana plant [35], and the Latin American banana-exporting coun- the biokinetics of these fungicides confer a tries [40]. A similar evolution has been more or less pronounced curative effect. observed in Cameroon where systemic fun- The curative effect is more pronounced on gicides have been applied in a forecasting young streaks (stages 1, 2), but lower on strategy [33], although this evolution has older lesions (stages 3, 4) and without any been delayed (more than 10 years) in com- effect on necrotic stages (stages 5, 6), parison with other areas where systemic although sporulation might be temporarily fungicides have been used in systematic decreased. Different chemical families have frameworks. However, fungicide resistance been used, which are in chronological is still not established in some banana plan- order: i) antimitotic products that inhibit tations of Ivory Coast where systemic fun- tubuline polymerization (benzimidazoles); gicides have been used in a forecasting ii) inhibitors of ergosterol biosynthesis that strategy for more than 10 years (de Lapeyre inhibit eburicol demethylation (DMI fungi- de Bellaire, unpubl. data). cides mostly belonging to the triazole family); iii) a second group of inhibitors of In order to prevent the emergence of fun- ergosterol biosynthesis that inhibit several gicide resistance, specific measures should enzymes such as reductases and isomerases be implemented [40]: (amines); iv) mitochondrial respiration – non-cross-resistant fungicides should be inhibitors that bind to the cytochrome b used in alternation in order to limit selection complex (QoI inhibitors of the strobilurin pressure, and particular attention should be family); and (v) pyrimethanil, a supposed paid to the number of applications per year, inhibitor of methionine biosynthesis whose that should be limited; mode of action is still not clearly established. – systemic fungicides should not be applied Only systemic fungicides can be used in on high population sizes in order to limit the forecasting systems that rely on early dis- risk of emergence of resistant strains. ease detection and a strong curative effect of fungicide applications [36]. For this pur- Nevertheless, the history of systemic fun- pose, systemic fungicides are used in oil gicide use in the banana industry shows that mixtures. Nevertheless, since the mode of these conditions were not fulfilled: action of these fungicides is a single target, – The first reason is that, in many cases, non- they provoke the emergence of resistant cross-resistant fungicides could not be used strains. in alternation because they were not avail- Systemic fungicides have been widely able at the same time. Therefore, in many used in the banana industry and the devel- cases, a new group of fungicides replaced opment of resistance is frequently reported. a group that had been discarded because of This has been the case for benzimidazole the emergence of resistant strains.

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Figure 2. History of Black Leaf Streak Disease (BLSD) control in banana plantations in Cameroon from 1985 to 2008.

– Also, because of their curative effect, sys- BLSD will probably never be finished. temic fungicides have been intensively used Therefore, the banana industry must be pre- on high population sizes in order to achieve pared for significant changes as a condition rapid disease control when banana planta- for its survival. However, increasing difficul- tions were damaged. This situation has ties in control will undoubtedly have signif- probably accelerated the emergence of fun- icant repercussions on the sustainability of gicide resistance. This has been particularly chemical control because of increasing envi- the case in Cameroon where systemic fun- ronmental incidences and because of the gicides were first used in a forecasting strat- evolution of the legislation in exporting and egy (figure 2), reducing the selection pres- importing countries driven by consumer sure. Nevertheless, these fungicides were demand [33]. Recent studies have shown later used intensively on plantations where that, where M. fijiensis is present, fungicides control had been lost because of logistic fail- for BLSD control represent the most signif- ures and, as a consequence, resistant strains icant contribution to the pesticide use in the were reported shortly after this period. banana plantations [41]. Therefore, signifi- – Lastly, the strong dispersion capacity of the cant evolution of BLSD control in the future pathogen has probably accelerated the dif- is unavoidable. We present here the evolu- fusion of resistant strains in a production tion that will be needed and the scientific area. gaps that should be overcome.

4.1. Elaboration of reliable tools for strategic decisions 4. Challenges for the banana industry Because changes in control strategies are necessary, it is important to rationalize these Taking into account the rapid adaptation evolutions from objective information at dif- capacity of M. fijiensis, the “battle” against ferent levels.

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Figure 3. Illustration of the Stage of Evolution of Disease's (SED) potential to monitor the efficiency of the chemical control strategy in banana plantations. All fungicide applications are indicated by an arrow above the SED curve (arrows with different colors correspond to different fungicides applied).

4.1.1. Disease monitoring at field level – The ‘Youngest Leaf bearing Streaks’ (YLSt) The first level of elaboration of reliable tools is the position of the youngest leaf bearing for strategic decisions is to implement a con- symptoms of the disease. A value for YLSt tinuous monitoring of disease evolution in must be scored for all banana plants moni- the field. It is also informative to fit these tored for SED assessment. If none of the weekly data with weekly rainfall, in order 4 leaves monitored have symptoms, the to get a better appreciation of epidemiolog- symptoms should be looked for on the older ical conditions. leaves. If none of the leaves bear any symptoms, the value of YLSt will be N+1, where – The Stage of Evolution of Disease, SED, N is the total number of leaves of the banana is the main parameter that should be tree. The YLSt reflects the incubation period assessed. Disease monitoring methods have of the disease under a spraying program mainly been designed for early warning sys- (figure 4). To interpret this parameter prop- tems and the Stage of Evolution of Disease erly it is important to consider that, under a has been specifically designed for this pur- spraying program, the incubation period pose [36]. Anyway, this parameter is not only will depend on both climatic conditions and useful for timing of decisions, but also to fungicide inhibition of the pathogen. The evaluate the efficiency of the chemical con- progressive evolution of this parameter is trol strategy that is designed to reduce dis- thus important to understand the evolution ease development on the young banana of epidemiological conditions as well as the leaves (figure 3). Therefore, this informa- performance of the chemical strategy in tion should be used whatever the control order to protect the youngest leaves, and strategy performed. This assessment is par- this information is complementary to the ticularly important for systematic strategies SED. in order to detect rapidly any failure in the – The ‘Youngest Leaf Spotted’ (YLS) should strategy mainly due to the quality of appli- be scored according to Stover’s method [42]. cations and to inoculum levels. In this method, the YLS is the youngest leaf However, a larger set of disease parame- bearing at least 10 necrotic lesions. We pro- ters should also be used. These parameters pose here new specifications for the assess- must be evaluated continuously every week ment of this parameter in order to use this on the same banana plot used for the assess- information for a regular diagnosis of the ment of SED in order to provide comple- efficiency of the chemical control strategy. mentary information: Because the absolute value of the YLS

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Figure 4. Illustration of Youngest Leaf bearing Streaks (YLSt) variations according to epidemiological conditions and time of chemical treatments applied in banana plantations. All fungicide applications are indicated by an arrow above the YLSt curve.

depends on the phenological stage of the can conclude that the chemical strategy is banana tree, it is better to consider the efficient in slowing down the necrotic for- weekly evolution of this parameter on the mation (figure 5). same plants. Effectively, the evolution of the – The ‘Number of Functional Leaves at Har- YLS on the same banana plant is a balance vest’ (NLH) also has to be evaluated. It is between the rate of necrotic formation and often considered that a functional leaf the foliar emission rate. Therefore, the evo- should have less than 30% of necrotic sur- lution of this parameter is helpful to under- face, although no scientific data support this stand the efficiency of the fungicide control consideration. The NLH must be evaluated at the level of necrotic formation (i.e.,ata every week on different banana trees and lower level than SED and YLSt). In order to its interpretation is more difficult and impre- use this parameter properly, it is important cise than the other parameters. It is better to consider the evolution of the YLS from the to make this observation on the same plot establishment of a new plot of 10 plants for used for the other parameters. Generally, in SED evaluation up to the flowering of these the banana plantations where partial deleaf- 10 plants. Then, all these plants should be ing of infected leaves is performed, NLH is changed at the same time before flowering calculated as the sum of different portions and the interpretation of the evolution of the of remaining leaves. This parameter is not, YLS should start again at this stage (fig- in time, directly linked to the chemical appli- ure 5). A value should be scored for each cations. Nevertheless, since BLSD mainly banana tree: if none of the leaves bear any affects fruit quality, the NLH is the final esti- necrotic lesion (this is often the case mator of how the control strategy has been because of deleafing in banana plantations, working and a potential indicator of fruit so special attention should be paid by work- exportability. Banana companies generally ers in order to avoid this), the value of YLS use an empiric threshold of NLH (3–5 will be N+1, where N is the total number of according to the companies) in order to leaves of the banana tree. If the YLS is decide which bunches are exportable or assessed in these conditions, it is possible not. Nevertheless, experimental data do not to interpret its evolution: (i) if the value of support this assumption (data not shown) YLS decreases, the chemical control is fail- and the value of NLH should be regarded ing because necrotic formation is faster than mostly as the efficiency of the chemical strat- leaf emission; (ii) if the YLS is increasing, we egy at the harvest stage.

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Figure 5. Illustration of interpretation of the Youngest Leaf Spotted (YLS) from its weekly evolution in banana plantations. Arrows indicate the date at which all the 10 banana plants were changed: the value of YLS is artificially different when the banana plants are changed and this variation should not be considered. YLS is scored according to Stover’s method [40].

4.1.2. Global evaluation of the that significant changes should be made in efficiency of the chemical strategy the control strategy. ECC is also interesting for the comparison of various strategies in The second level of elaboration of reliable the same location (table I). tools for strategic decisions is the global efficiency of chemical control. We propose a 4.1.3. Global evaluation of economic new indicator to evaluate the efficiency of incidence of BLSD the chemical control (ECC): ECC = (SED )× y The third level of elaboration of reliable N , where SED is the average of the weekly y y tools for strategic decisions is the evaluation values of the SED over one year in a location of the global economic incidence of BLSD, and N is the number of fungicide treat- y and there are no existing tools for this pur- ments applied in one year in this same loca- pose. Nevertheless, this evaluation is impor- tion tant because changes in control strategy The lower the ECC, the more efficient the should be legitimated by a global economic chemical control strategy. A low ECC value approach. Generally, data on the cost of means that a good control of BLSD is BLSD control only focus on direct costs for achieved (low average value of SED) with fungicides and fungicide applications. How- a low number of fungicide treatments. ECC ever, this economic impact comprises direct could be an indicator used to monitor the costs (spraying operations, deleafing, etc.), incidence of disease control over time in the but also indirect costs such as (i) disease same area and could be useful for compar- monitoring, (ii) losses (bunches rejected, isons between various locations. The varia- weight reduction, quality reduction), and tion of the ECC in different situations (iii) the cost of environmental measures according to locations with different cli- [33]. This information should be collected in mates (Ivory Coast, Cameroon or Belize) databases and specific models should be and according to various types of chemical defined in order to simulate the potential strategies (forecasting system or systematic benefit of changes in the industry. Only this strategies) have been calculated (table I). A global approach should justify changes in regular increase in ECC over years means the industry.

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Table I. Illustration of the efficiency of the chemical control (ECC) in banana plantations in various situations. ECC = SEDy × Ny, where SEDy (Stage of Evolution of Disease) is the average of the weekly values of the SED over one year in a location, and Ny is the number of fungicide treatments applied in one year in this same location SED.

Zone Banana plantation Year Type of strategy Annual rainfall SEDy Ny ECC (mm)

2002 Forecasting Not determined 399 12 4798 Plantation A 2007 Forecasting 1500 1269 15 19035 Ivory Coast 2009 Systematic 1520 116 34 3944 Plantation B 2007 Forecasting 1388 95 12 1140

2005 Systematic 2700 152 44 6688 Cameroon Plantation C 2009 Systematic 3112 846 46 38916

2006 Systematic 1 3240 746 52 38792 Plantation D1 Belize 2006 Systematic 2 3240 378 50 18900 Plantation E 2006 Systematic 2 3130 131 47 6157

1 Two different systematic strategies (systematic 1 and systematic 2) were applied in plantation D in 2006.

4.2. Definition of acceptable disease Such models should rely on a better under- thresholds standing of disease effect on dry matter accumulation at different phenological The banana industry could probably endure stages and on the differential mobilization a certain disease level instead of a headlong of resources by the different organs at these pursuit of perfect control through an different stages. Since banana is a semi-per- increasing chemical use. ennial crop, such models should integrate successive crop cycles. In this way, experimental deleafing of bananas has shown that bunch weight, the The second component of yield, the first component of yield, is poorly affected greenlife, depends on the stage of fruit as long as 5 to 7 leaves remain on the maturity at harvest, which is determined by banana plant from flowering to harvest [6, thermal sums from flowering to harvest 43–46]. However, the effect of strong deleaf- [50]. Where no stress alters bunch feeding, ing after flowering, which has been poorly bananas harvested at 900 dd reach a grade studied, could probably be important since compatible with market standards [51] and (i) fruit size is determined by the intensity a greenlife satisfactory for shipment [50]. It of cellular divisions which occur 350 degree- has been shown that abiotic stresses alter days (dd) after flowering, and (ii) the rate fruit growth, but have no influence on the of dry matter accumulation in fruit depends greenlife of bananas harvested at a constant on the source-sink ratio from the end of cel- physiological age [52]. Nevertheless, it has lular divisions to harvest [47]. Lastly, banana been shown recently that biotic stresses is a ratoon crop and the next sucker mobi- with the intensity of Sigatoka Disease or lizes a part of the dry matter during bunch Black Leaf Streak Disease damage signifi- feeding [48], so a lack of resources during cantly reduce the greenlife of bananas har- this phase (as a consequence of severe spot- vested at a constant physiological age [53, ting) could compromise the yield of the next 54], arguing for a direct effect of these foliar ratoon [49]. Acceptable disease thresholds diseases on fruit physiology by mecha- should be determined through the modeli- nisms that remain to be discovered. So, zation of the effects of BLSD on bunch mass. specific mechanisms of interactions between

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leaf spotting and greenlife reduction should effective population sizes and such strate- be better understood in order to modelize gies should be interrupted when disease the effect of BLSD on greenlife according to level is too high in order to avoid fungicide the harvest stage. resistance. In such conditions, a temporary This global approach for BLSD on the var- use of contact fungicides could decrease ious components of yield will enable the inoculum levels before going back to the optimization of bunch weight according to forecasting strategy. a fixed stage of harvest (through agronomic Lastly, where fungicide resistance is estab- practices), and vice versa. lished, some data show that the interruption of systemic fungicide use can lead to a 4.3. Limitation of fungicide use decrease in fungicide resistance [33, 40]. This decrease could result from (i) gene flow between unsprayed and sprayed plantations, The forecasting strategies enable BLSD con- and (ii) resistance cost. The acceleration of trol with a limited use of chemicals. In such such evolution combined with incoming sys- strategies, the cost of control is lower but, temic fungicides with a new mode of action above all, the environmental impact is lim- could therefore enable the reintroduction of ited. Such strategies should be preferred to a forecasting strategy. Such fungicide resist- systematic strategies that are conducive to ance management strategies should rely on significant environmental impact and they a better understanding of (i) gene flow should be combined with other measures between unsprayed and sprayed areas; such as sanitation (deleafing), drainage, (ii) selection pressures, and (iii) competi- under-cover irrigation and good fertilization tiveness of resistant strains [33, 55]. practices. Forecasting strategies have faced some drawbacks in some countries, espe- cially in Cameroon, because of the emer- 4.4. Introduction of resistant gence of fungicide resistance to systemic varieties into the agrosystem fungicides. Nevertheless, such strategies should be implemented in specific condi- Only Cavendish bananas, highly susceptible tions that are encountered in the banana to BLSD, are grown in the banana industry, industry: (i) banana areas free of fungicide but resistant banana cultivars exist and two resistance and particularly those where types of resistance have been described [3]. adverse climatic conditions exist during a The first one is a high resistance character- part of the year (dry season). This is the case ized by the blockage of symptoms at early in some parts of Ivory Coast, Ghana and, stages. This type of resistance is considered probably, in some regions of Latin America to be a hypersensitive reaction of the host (the Dominican Republic, for instance). [56] and is found in cultivars such as Yan- (ii) New countries devoted to the banana gambi km 5 (AAA, Ibota) and in different industry; this is, for instance, the case of diploids used in breeding programs as a Ghana but also Mozambique and Angola, source of resistance (Paka, AA). The second where only Sigatoka Disease is reported. one is a partial resistance characterized by When new plantations are established in a slower evolution of disease symptoms as new areas of a country where fungicide compared with susceptible varieties. This resistance is present, special attention type of resistance is characteristic of culti- should be paid to germplasm movement in vars belonging, for example, to the sub- order to prevent the introduction of resistant groups Pisang Awak (ABB, i.e., Fougamou) strains through planting material. This is, for and Mysore (AAB). Two examples suggest instance, the case in Cameroon and Ivory a potential adaptation of M. fijiensis on Coast. resistant cultivars: In such situations, the sustainability of the – The first one is the observation of virulent forecasting strategy would be a significant strains of M. fijiensis on Paka in the Cook challenge. From former unsuccessful sto- Islands [57]. These authors consider that ries, we should remember that systemic fun- these strains are widespread in the Pacific gicides should not be applied on high Islands and also mention that they are

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virulent on Yangambi km 5 which is also References considered as highly resistant to BLSD. – The second one results from the release [1] Lescot T., La banane en chiffres : le fruit pré- of FHIA 18 and FHIA 21, two partially resist- féré de la planète, FruiTrop 140 (2006) 5. ant cultivars that have been grown over [2] Loeillet D., Le commerce international de la 18 000 ha in Cuba. In 2003, 10 years after banane : entre évolution et révolution, Frui- the introduction of these cultivars into the Trop 129 (2005) 2–19. central region of Cuba, an increase in dis- [3] Jones D.R., Diseases of banana, abaca and ease expression has been reported and enset, CAB Int., Wallingf., U.K., 2000. aggressiveness changes in the fungal population have been suspected [58]. Neverthe- [4] Pennisi E., Armed and dangerous, Science less, this evolution could reflect changes in 327 (2010) 804–805. host-pathogen interactions due to environ- [5] Fouré E., Les cercosporioses du bananier et mental factors (mineral nutrition, effect of leurs traitements. Comportement des varié- climatic conditions) and such adaptation of tés. Études de la sensibilité variétale des M. fijiensis to partially resistant cultivars is bananiers et plantains à Mycosphaerella still not demonstrated. fijiensis Morelet au Gabon (maladie des raies noires). I. Incubation et évolution de la mala- Although the present organization of the die, Fruits 37 (1982) 749–759. banana industry is an obstacle to the diver- [6] Ramsey M.D., Daniells J.W., Anderson D.J., sification of banana cultivars in the com- Effects of Sigatoka leaf spot (Mycosphaer- modity chain, the predominance of a unique ella musicola Leach) on fruit yields, field rip- type of susceptible cultivar is unsustainable ening and greenlife of bananas in North and recourse to resistant varieties in an inte- Queensland, Sci. Hortic. 41 (1990) 305–313. grated strategy is probably the future of BLSD control. Since M. fijiensis has signifi- [7] Stover R.H., Effet du cercospora noir sur les plantains en Amérique centrale, Fruits 38 cant adaptation capacities, the type of resist- (1983) 326–329. ance used should be polygenic instead of monogenic. So, it is hypothesized that par- [8] Mobambo K.N., Gauhl F., Pasberg-Gauhl C., tially resistant cultivars would be more dura- Zuofa K., Season and plant age effect eva- ble than highly resistant cultivars. Few luation of plantain for response to black conventional breeding programs focus on sigatoka disease, Crop Prot. 15 (1996). the creation of such tolerant cultivars [59]. [9] Burg S.P., Burg E.A., Relationship between Partially resistant cultivars exist but their ethylene production and ripening in bana- adaptation to an industry adapted for Cav- nas, Bot. Gaz. 126 (1965) 200–204. endish cultivars is still problematic. How- [10] Peacock B.C., Blake J.R., Some effects of ever, a better understanding of the genetic non-damaging temperatures on the life and basis of resistance to BLSD is needed for respiratory behaviour of bananas, Qld. J. adequate breeding. Agric. Anim. Sci. 27 (1970) 147–168. We hypothesize that the partial introduc- [11] Stover R.H., Banana, plantain and abaca tion of resistant cultivars into the agro-sys- diseases, Commonw. Mycol. Inst., Kew, Sur- tem could contribute to a decrease in rey, U.K., 1972. epidemic development of BLSD on spatial [12] Stover R.H., Simmonds N.W., Bananas, scales that remain to be determined. How- Longman, Essex, U.K., 1987. ever, partially resistant varieties could be introduced into agro-systems in different [13] Leach R., A new form of banana leaf spot in Fiji, black leaf streak, World Crops 16 (1964) ways and the development of spatial epide- 60–64. miological models would contribute to define the most efficient strategies on these [14] Zimmerman A., Über einige tropisher Kultur- spatial scales [60]. Lastly, models to predict pflanzen beobachtete Pilze, Zentralblatt für potential changes for aggressiveness traits in Nakteriologie, Parasitenkunde, Infek- fungal populations are also needed to tionskrankh. Hyg. 8 (1902) 219. define deployment strategies for durable [15] Meredith D.S., Lawrence J.S., Black Leaf resistance [61]. Streak Disease of bananas (Mycosphaerella

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[35] Bartlett D.W., Clough J.M., Godwin J.R., Hall black Sigatoka (Mycosphaerella fijiensis) A.A., Hamer M., Parr-Dobrzanski B., Review: disease, Int. J. Pest Manag. 55 (2009) 19–25. the strobilurin fungicides, Pest Manag. Sci. [47] Jullien A., Munier-Jolain N., Malézieux E., 58 (2002) 649–662. Chillet M., Ney B., Effect of pulp cell number [36] Fouré E., Ganry J., A biological forecasting and assimilate availability on dry matter system to control Black Leaf Streak disease accumulation rate in a banana fruit [Musa of bananas and plantains, Fruits 63 (2008) sp., AAA, group 'Grande Naine' (Cavendish 311–317. subgroup)], Ann. Bot. 88 (2001) 321–330. [37] Romero R.A., Sutton T.B., Characterization [48] Eckstein K., Robinson J.C., Davie S.J., Phy- of benomyl resistance in Mycosphaerella siological-responses of banana (Musa-aaa, fijiensis, cause of black Sigatoka of banana, Cavendish subgroup) in the subtropics. in Costa Rica, Plant Dis. 82 (1998) 931–934. 3. Gas-exchange, growth analysis and [38] Amil A.F., Heaney S.P., Stanger C., Shaw source-sink interaction over a complete crop M.W., Dynamics of QoI sensitivity in Mycos- cycle, J. Hortic. Sci. 70 (1995) 169–180. phaerella fijiensis in Costa Rica during 2000 [49] Dens K.R., Romero R.A., Swennen R., Turner to 2003, Phytopathology 97 (2007) 1451– D.W., Removal of bunch, leaves, or pseu- 1457. dostem alone, or in combination, influences [39] Romero R.A., Sutton T.B., Sensitivity of growth and bunch weight of ratoon crops in Mycosphaerella fijiensis, causal agent of two banana cultivars, J. Hortic. Sci. & Bio- Black Sigatoka of banana, to Propiconazole, technol. 83 (2008) 113–119. Phytopathology 87 (1997) 96–100. [50] Jullien A., Chillet M., Malézieux E., Pre-har- [40] Anon., Minutes of the banana working vest growth and development, measured as group, in: www.frac.info (Ed.), 2010. accumulated degree days, determine the post-harvest green life of banana fruit, J. [41] Risède J.M., Lescot T., Cabrera Cabrera J., Hortic. Sci. & Biotechnol. 83 (2008) 506–512. Guillon M., Tomekpé K., Kema G.H.J., Côte F., From science to field. Banana case study [51] Ganry J., Meyer J.P., Recherche d'une loi – Guide number 1, Challenging short and d'action de la température sur la croissance mid-term strategies to reduce pesticides in des fruits du bananier, Fruits 30 (1975) 375– bananas, in: ENDURE (Ed.), Montpellier, 392. France, 2010. [52] Chillet M., Hubert O., Ribes M.J., de Lapeyre [42] Stover R.H., A proposed international scale de Bellaire L., Effects of the physiological for estimating intensity of banana leaf spot age of bananas on their susceptibility to (Mycosphaerella musicola Leach),Trop. wound anthracnose due to Colletotrichum Agric. 48 (1971) 185–196. musae, Plant Dis. 90 (2006) 1181–1185. [43] Daniells J.W., Lisle A.T., Bryde N.J., Effect of [53] Abadie C., Hubert O., Ngando Essoh J., bunch trimming and leaf removal at flowe- Ngoh G., Mbéguié-A-Mbéguié D., de ring on maturity bronzing, yield, and other Lapeyre de Bellaire L., Chillet M., Evidence aspects of fruit-quality of bananas in North of the effects of Mycosphaerella leaf spot Queensland, Aust. J. Exp. Agric. 34 (1994) diseases on fruit quality, in: Borja J.S., 259–265. Orrantia C., Paladines R., Quimí V., Tazán L. [44] Lassois L., Bastiaanse H., Chillet M., Jullien (Eds.), XVIIIth ACORBAT Meet., 10–14 A., Jijakli M.H., de Lapeyre de Bellaire L., November 2008, Guayaquil, Ecuador, 2008. Hand position on the bunch and source-sink [54] Chillet M., Abadie C., Hubert O., Chilin- ratio influence the banana fruit susceptibility Charles Y., De Lapeyre de Bellaire L., Siga- to crown rot disease, Ann. Appl. Biol. 156 toka disease reduces the greenlife of bana- (2010) 221–229. nas, Crop Prot. 28 (2009) 41–45. [45] Robinson J.C., Anderson T., Eckstein K., The [55] de Lapeyre de Bellaire L., Rieux A., Ngando Influence of functional leaf removal at flower Essoh J., Zapater M.F., Carreel F., Ravigne emergence on components of yield and V., Carlier J., An integrated approach to photosynthetic compensation in banana, J. define management strategies of fungicide Hortic. Sci. 67 (1992) 403–410. resistance in populations of the plant patho- [46] Vargas A., Araya M., Guzman M., Murillo G., genic fungus Mycosphaerella fijiensis, in: Effect of leaf pruning at flower emergence of Bertrand J.C., Bonis A., Caquet T., Franc A., banana plants (Musa AAA) on fruit yield and Garnier E., Olivieri I., Thébaud C., Roy J.

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La enfermedad de las rayas negras desafía a la industria de la banana. Resumen — Introducción. La enfermedad de las rayas negras (ERN) es la amenaza más grande a la cual se enfrenta la industria de la banana. Efectivamente, dicha enfermedad foliar afecta la fotosíntesis de los bananos, pero, sobre todo, conlleva una reducción del potencial de conservación de los frutos que no pueden exportarse cuando los bananos están severa- mente afectados. Principales características de la ERN. Se describieron en el banano más de 20 especies del género Mycosphaerella, pero las cercosporiosis de los bananos son principalmente el resultado de dos especies M. fijiensis (ERN) y M. musicola (enfermedad de Siga- toka). M. fijiensis es una especie invasiva que remplazó totalmente a M. musicola en la mayor parte de los países exportadores de bananos, lo que siempre se tradujo por un control más difícil de la cercosporiosis. Dificultades de control crecientes. Dado a que todas las variedades de bananos cultivados en la industria de la banana son muy sensibles a las cercosporiosis, el control de la ERN se basa en la aplicación aérea de fungicidas, tanto según programas sistemáticos (fungicidas de contacto), como por prevención (fungicidas sistemáti- cos). En los países exportadores de bananos donde se detectó M. fijiensis, el control de la ERN se ha vuelto cada vez más difícil. Dicha evolución se debe principalmente a la aparición de cepas resistentes a los fungicidas y se tradujo por un aumento del coste de la lucha, pero sobre todo por un incremento de los impactos medioambientales. Desafíos para la industria bananera. Dado a que M. fijiensis posee capacidades de adaptación muy rápida, una de las condiciones de supervivencia de la industria bananera es la preparación a importantes mutaciones. Proponemos un conjunto de indicadores de diferentes niveles (parcela, eficacia general de la lucha, incidencia económica general) con el fin de objetivar estas evoluciones. La modelización de los efectos de la ERN en el peso de los regímenes y la duración de conservación de los frutos debería permitir definir los niveles de enfermedad aceptables. Debería asimismo permitir optimizar el peso de los regímenes y el estado de cosecha en función de las prácticas agronómicas. De modo a limitar el uso de los fungicidas que tienen un impacto medioambiental importante, las estrategias de prevención deben emplearse ahí donde los fungicidas sistemáticos aún son eficaces. Por último, el predominio de cultivares sensibles no es duradero y el futuro de esta industria pasa probablemente por la incorpora- ción de variedades resistentes en los sistemas de cultivo. Francia / Musa / control de enfermedades / enfermedades fungosas / Mycosphaerella fijiensis / resistencia a productos químicos

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