**3. Lessons drawn from various experiences and perspectives**

Beyond the biological and technical components there are economic, political, logistical, environmental and social issues that are key points to consider in a holistic approach, otherwise leading to unpredictable failures.

An Integrated Approach to Control the Black Leaf Streak

fungicide applied (de Lapeyre de Bellaire et al., 2009)

**3.1 Short-term solutions** 

**3.2 Long-term solutions** 

from the Comoros archipelago).

BLSD control.

Mysore (AAB).

Disease (BLSD) of Bananas, while Reducing Fungicide Use and Environmental Impact 219

The introduction of more eco-friendly fungicides would be beneficial to address environmental and health impact of contacts fungicides. In the past 5 years, organic fungicides or bio-fungicides, such as essential oils, alimentary additives, organic acids, potassium carbonates, leachates of decomposed banana material (bunch stems, fruits), and bio-control agents have been experimented in Cameroon. None of these fungicides gave good control of BLSD under high inoculum pressure. However, recent experimental data suggest that the combination of some bio-control agents (*Bacillus subtillis* and *B. pumilis*) applied in mixtures with contact fungicides could enable the reduction of the amount of

In addition, forecasting strategies should be devoted and implemented in areas where specific conditions are fulfilled: (i) areas free of fungicide resistance, (ii) new banana areas, (iii) low disease pressure areas. Where fungicide resistance is established, the reintroduction of forecasting strategies relies on possible fungicide resistance reversion and incoming of new mode of action fungicides with a high curative effect. For instance, in situations where the current fungicide resistance is reversible as shown in Cameroon (see § 2.1), it is possible to carefully reintroduce adequate curative fungicides and thus implement warning strategies.

As already mentioned at the beginning, only Cavendish bananas, highly susceptible to BLSD, are grown in the banana industry, which is a high risk for the sustainability of the industry. For this reason and although the current market organization of the banana industry that is an obstacle to the diversification of banana cultivars in the commodity chain, recourse to resistant varieties in an integrated strategy is certainly part of the future of an integrated

Resistant banana, edible or wild, already exist and two types of resistance have been

The first one is a high resistance due to a hypersensitive reaction of the host and characterized by the blockage of symptoms at early stages. It is found in cultivars such as Yangambi km 5 (AAA, Ibota) and in various diploids already used in breeding programs as a source of resistance (Paka, AA and some genotypes from the Mlali group and originated

The second one is a partial resistance characterized by a slower evolution of disease symptoms as compared with susceptible varieties. This type of resistance is characteristic of cultivars belonging, for example, to the subgroups Pisang Awak (ABB, *i.e*., Fougamou) and

Since *M. fijiensis* has significant adaptation capacities, already observed in some situations3, the type of resistance used should be polygenic instead of monogenic and thus the breeding

3 Virulent strains of *M. fijiensis* were observed on Paka in the Cook Islands (Fullerton & Olsen, 1995)3. These authors consider that these strains are widespread in the Pacific Islands and also mention that

they are virulent on Yangambi km 5 which is also considered as highly resistant to BLSD.

**3.2.1 At the cross-road between genetics and landscape management** 

described (Fouré et al., 1990,Beveraggi et al., 1995, , Jones, 2000).

Chemical control of BLSD would not appear sustainable in the long term. In several countries, fungicide resistance to systemic fungicides is increasing, and chemical control using these fungicides is becoming no longer efficient. In such situations, a systematic use of contact fungicides, as shown in the case studies of Belize and Cameroon, needs to be implemented. As a consequence, warning strategies, which could help reduce costs and environmental impact of chemical control, are becoming useless, because of systematic and frequent sprays. As a consequence, fungicides for BLSD control are the most important contribution to the annual amount of pesticide used in all countries were BLSD is present and where favorable conditions prevail (Risède et al., 2010). In the FWI, fungicide resistance is particularly worrying since the SBI of group 1 are the only fungicides approved. The introduction of very restrictive legislation significantly affects the sustainability of chemical control (table 4). More restrictive legislation aimed to further protect human and environmental health may be passed in the future. New solutions are then necessary to guarantee the sustainability of banana cropping systems (de Lapeyre de Bellaire et al., 2009).


Table 4. Number of fungicide products registered in various countries for BLSD or SLSD control in 2006. (from de Lapeyre de Bellaire et al., 2009)

Fig. 8. Estimated total pesticide quantities used by the dessert banana industry in some countries, including European Community areas (2006-2007).© *Thierry Lescot, CIRAD, France*

#### **3.1 Short-term solutions**

218 Fungicides for Plant and Animal Diseases

Chemical control of BLSD would not appear sustainable in the long term. In several countries, fungicide resistance to systemic fungicides is increasing, and chemical control using these fungicides is becoming no longer efficient. In such situations, a systematic use of contact fungicides, as shown in the case studies of Belize and Cameroon, needs to be implemented. As a consequence, warning strategies, which could help reduce costs and environmental impact of chemical control, are becoming useless, because of systematic and frequent sprays. As a consequence, fungicides for BLSD control are the most important contribution to the annual amount of pesticide used in all countries were BLSD is present and where favorable conditions prevail (Risède et al., 2010). In the FWI, fungicide resistance is particularly worrying since the SBI of group 1 are the only fungicides approved. The introduction of very restrictive legislation significantly affects the sustainability of chemical control (table 4). More restrictive legislation aimed to further protect human and environmental health may be passed in the future. New solutions are then necessary to guarantee the sustainability of banana cropping systems (de Lapeyre de Bellaire et al., 2009).

Active ingredient group Belize Cameroon Guadeloupe

Table 4. Number of fungicide products registered in various countries for BLSD or SLSD

Fig. 8. Estimated total pesticide quantities used by the dessert banana industry in some countries, including European Community areas (2006-2007).© *Thierry Lescot, CIRAD, France*

mancozeb 8 7 0 chlorothalonil 2 5 0 SBI group 2 1 3 0 pyrimidins 1 2 0 strobilurins 2 2 0 antimitotics 1 1 0 SBI group1 5 7 2

control in 2006. (from de Lapeyre de Bellaire et al., 2009)

The introduction of more eco-friendly fungicides would be beneficial to address environmental and health impact of contacts fungicides. In the past 5 years, organic fungicides or bio-fungicides, such as essential oils, alimentary additives, organic acids, potassium carbonates, leachates of decomposed banana material (bunch stems, fruits), and bio-control agents have been experimented in Cameroon. None of these fungicides gave good control of BLSD under high inoculum pressure. However, recent experimental data suggest that the combination of some bio-control agents (*Bacillus subtillis* and *B. pumilis*) applied in mixtures with contact fungicides could enable the reduction of the amount of fungicide applied (de Lapeyre de Bellaire et al., 2009)

In addition, forecasting strategies should be devoted and implemented in areas where specific conditions are fulfilled: (i) areas free of fungicide resistance, (ii) new banana areas, (iii) low disease pressure areas. Where fungicide resistance is established, the reintroduction of forecasting strategies relies on possible fungicide resistance reversion and incoming of new mode of action fungicides with a high curative effect. For instance, in situations where the current fungicide resistance is reversible as shown in Cameroon (see § 2.1), it is possible to carefully reintroduce adequate curative fungicides and thus implement warning strategies.

#### **3.2 Long-term solutions**

#### **3.2.1 At the cross-road between genetics and landscape management**

As already mentioned at the beginning, only Cavendish bananas, highly susceptible to BLSD, are grown in the banana industry, which is a high risk for the sustainability of the industry.

For this reason and although the current market organization of the banana industry that is an obstacle to the diversification of banana cultivars in the commodity chain, recourse to resistant varieties in an integrated strategy is certainly part of the future of an integrated BLSD control.

Resistant banana, edible or wild, already exist and two types of resistance have been described (Fouré et al., 1990,Beveraggi et al., 1995, , Jones, 2000).

The first one is a high resistance due to a hypersensitive reaction of the host and characterized by the blockage of symptoms at early stages. It is found in cultivars such as Yangambi km 5 (AAA, Ibota) and in various diploids already used in breeding programs as a source of resistance (Paka, AA and some genotypes from the Mlali group and originated from the Comoros archipelago).

The second one is a partial resistance characterized by a slower evolution of disease symptoms as compared with susceptible varieties. This type of resistance is characteristic of cultivars belonging, for example, to the subgroups Pisang Awak (ABB, *i.e*., Fougamou) and Mysore (AAB).

Since *M. fijiensis* has significant adaptation capacities, already observed in some situations3, the type of resistance used should be polygenic instead of monogenic and thus the breeding

<sup>3</sup> Virulent strains of *M. fijiensis* were observed on Paka in the Cook Islands (Fullerton & Olsen, 1995)3. These authors consider that these strains are widespread in the Pacific Islands and also mention that they are virulent on Yangambi km 5 which is also considered as highly resistant to BLSD.

An Integrated Approach to Control the Black Leaf Streak

Angola, China.…)

components.

fungicides.

adaptation.

**5. Acronyms** 

AA: diploid Acuminata AAA: triploid Acuminata

BGA: Banana Growers Association

minimize economic impact and environmental damages as well.

Disease (BLSD) of Bananas, while Reducing Fungicide Use and Environmental Impact 221

on a sufficiently long period, can master the agricultural risk related to the disease and

The limited use of fungicides through this system is more sustainable than the systematic strategy, and more than ever it is important to adopt such an approach in the control of the BLSD. Particularly this strategy should be used wherever it is possible, and particularly where fungicide resistance does not prevent it. This assumption should be especially considered in the frame of new banana projects either in traditional banana growing countries (Cameroon, Ivory Coast,….) or in new banana growing countries (Mozambique,

It is clear that any failure in the implementation of one component of the system is condemning all the system, jeopardizing any effort done in the implementation of any other

For instance, if the inoculum density is becoming too high, due to some failure in leaf removal, in the control of "hotspots", or in the timing of the sprays, the effectiveness of the control will be strongly reduced. Thus, the control strategy would not be able to reduce the inoculum density which will continue to increase, if nothing is done to cut such an amplifying effect. In such a situation, the priority is to reduce drastically the inoculum density through appropriate measures (strong leaf removal, systematic applications with contact fungicides to prevent the emergence of resistant strains to systemic fungicides…) and to consider that it is an essential punctual investment necessary for the sustainability of this strategy. The potential benefit of a temporary shift to a systematic use of protectants is probably the most important lesson that should be learnt from the experience in Cameroon, and specific adaptations of the strategy must be adopted in order to manage efficiently fungicide resistance and thus the sustainability of this system that relies on systemic

Taking into account that such a control strategy is dealing with a pathogen with a high evolutionary potential, there could not be any "routine" behavior. On the contrary a permanent "alert" behavior is needed to anticipate any new evolution. The control strategy

It is the case with the emergence of resistant strains to curative fungicides, which requires permanent efforts for fungicide resistance management and also to bring curative fungicides with new mode of action. It is also the case with the increasing social pressure related to environment and health in production areas. In this context, it will be probably essential, in the future, to consider the use of resistant varieties to BLSD, at least in certain critical situations (residential areas, hotspots,...). A permanent innovation is the corollary of an integrated and sustainable approach to control the Black Leaf Streak Disease of bananas. It is the reason why a strong interaction must be kept between the technical services in charge of its implementation and research teams able to provide support for anticipation and

must be shaped to be prepared to evolve and adapt to new constraints.

strategy must aim at producing partially resistant rather than highly resistant cultivars. As genetically modified bananas are facing consumer resistance and legislation constraints in most importing countries, the more promising way is to look at innovative ways of conventional breeding.

Few programs are currently focusing on the creation of resistant cultivars through such an approach (Abadie et al., 2009).

Some partially resistant hybrids issued from these programs are already tested but their adaptation to an industry exclusively based on Cavendish cultivars is not an easy task. Consumer and market requirements are major constraints, and selection of suitable export cultivars, if at all possible, is a very long process.

The introduction of resistant cultivars into the agro-system could contribute to a decrease in epidemic development of BLSD on spatial scales that remain to be determined, from field to landscape (Ganry, 2004).

### **3.2.2 Definition of acceptable disease thresholds**

Instead of only targeting a perfect control of the disease through chemical control, the banana industry would probably have better question the economically acceptable level of disease, and define the disease management accordingly. Acceptable disease thresholds should be determined through the modeling of the effects of BLSD on bunch mass. Such models should rely on a better understanding of disease effect on dry matter accumulation at different phenological stages and on the differential mobilization of resources by the different organs at these different stages. Since banana is a semi-perennial crop, such models should integrate successive crop cycles.

This global approach for BLSD on the various components of yield will enable the optimization of bunch weight according to a fixed stage of harvest (through agronomic practices), and *vice versa*.

#### **3.2.3 A more integrated approach based on strategic decision tools**

While data on the cost of BLSD control are generally only focusing on direct costs for fungicides and fungicide applications, it is necessary to take into account other components including direct costs (spraying operations, leaf removal, etc.), but also indirect costs such as (i) disease monitoring, (ii) losses (bunches rejected, weight reduction, quality reduction), and (iii) the cost of environmental measures (de Lapeyre de Bellaire et al., 2009).

It is the reason why it is important to think about reliable tools for strategic decisions is the evaluation of the global economic incidence of BLSD, as there are no existing tools for this purpose. Such information should be collected in databases and specific models should be defined in order to simulate the potential benefit of changes in the industry. Only this global approach should justify changes in the industry.

#### **4. Conclusion**

The experience gained in the control of the Sigatoka leaf spot diseases, compared to situations of concern observed in Latin America, shows that an integrated approach applied on a sufficiently long period, can master the agricultural risk related to the disease and minimize economic impact and environmental damages as well.

The limited use of fungicides through this system is more sustainable than the systematic strategy, and more than ever it is important to adopt such an approach in the control of the BLSD. Particularly this strategy should be used wherever it is possible, and particularly where fungicide resistance does not prevent it. This assumption should be especially considered in the frame of new banana projects either in traditional banana growing countries (Cameroon, Ivory Coast,….) or in new banana growing countries (Mozambique, Angola, China.…)

It is clear that any failure in the implementation of one component of the system is condemning all the system, jeopardizing any effort done in the implementation of any other components.

For instance, if the inoculum density is becoming too high, due to some failure in leaf removal, in the control of "hotspots", or in the timing of the sprays, the effectiveness of the control will be strongly reduced. Thus, the control strategy would not be able to reduce the inoculum density which will continue to increase, if nothing is done to cut such an amplifying effect. In such a situation, the priority is to reduce drastically the inoculum density through appropriate measures (strong leaf removal, systematic applications with contact fungicides to prevent the emergence of resistant strains to systemic fungicides…) and to consider that it is an essential punctual investment necessary for the sustainability of this strategy. The potential benefit of a temporary shift to a systematic use of protectants is probably the most important lesson that should be learnt from the experience in Cameroon, and specific adaptations of the strategy must be adopted in order to manage efficiently fungicide resistance and thus the sustainability of this system that relies on systemic fungicides.

Taking into account that such a control strategy is dealing with a pathogen with a high evolutionary potential, there could not be any "routine" behavior. On the contrary a permanent "alert" behavior is needed to anticipate any new evolution. The control strategy must be shaped to be prepared to evolve and adapt to new constraints.

It is the case with the emergence of resistant strains to curative fungicides, which requires permanent efforts for fungicide resistance management and also to bring curative fungicides with new mode of action. It is also the case with the increasing social pressure related to environment and health in production areas. In this context, it will be probably essential, in the future, to consider the use of resistant varieties to BLSD, at least in certain critical situations (residential areas, hotspots,...). A permanent innovation is the corollary of an integrated and sustainable approach to control the Black Leaf Streak Disease of bananas. It is the reason why a strong interaction must be kept between the technical services in charge of its implementation and research teams able to provide support for anticipation and adaptation.

#### **5. Acronyms**

220 Fungicides for Plant and Animal Diseases

strategy must aim at producing partially resistant rather than highly resistant cultivars. As genetically modified bananas are facing consumer resistance and legislation constraints in most importing countries, the more promising way is to look at innovative ways of

Few programs are currently focusing on the creation of resistant cultivars through such an

Some partially resistant hybrids issued from these programs are already tested but their adaptation to an industry exclusively based on Cavendish cultivars is not an easy task. Consumer and market requirements are major constraints, and selection of suitable export

The introduction of resistant cultivars into the agro-system could contribute to a decrease in epidemic development of BLSD on spatial scales that remain to be determined, from field to

Instead of only targeting a perfect control of the disease through chemical control, the banana industry would probably have better question the economically acceptable level of disease, and define the disease management accordingly. Acceptable disease thresholds should be determined through the modeling of the effects of BLSD on bunch mass. Such models should rely on a better understanding of disease effect on dry matter accumulation at different phenological stages and on the differential mobilization of resources by the different organs at these different stages. Since banana is a semi-perennial crop, such models

This global approach for BLSD on the various components of yield will enable the optimization of bunch weight according to a fixed stage of harvest (through agronomic

While data on the cost of BLSD control are generally only focusing on direct costs for fungicides and fungicide applications, it is necessary to take into account other components including direct costs (spraying operations, leaf removal, etc.), but also indirect costs such as (i) disease monitoring, (ii) losses (bunches rejected, weight reduction, quality reduction),

It is the reason why it is important to think about reliable tools for strategic decisions is the evaluation of the global economic incidence of BLSD, as there are no existing tools for this purpose. Such information should be collected in databases and specific models should be defined in order to simulate the potential benefit of changes in the industry. Only this global

The experience gained in the control of the Sigatoka leaf spot diseases, compared to situations of concern observed in Latin America, shows that an integrated approach applied

**3.2.3 A more integrated approach based on strategic decision tools** 

and (iii) the cost of environmental measures (de Lapeyre de Bellaire et al., 2009).

conventional breeding.

landscape (Ganry, 2004).

practices), and *vice versa*.

**4. Conclusion** 

approach (Abadie et al., 2009).

cultivars, if at all possible, is a very long process.

**3.2.2 Definition of acceptable disease thresholds** 

should integrate successive crop cycles.

approach should justify changes in the industry.

AA: diploid Acuminata AAA: triploid Acuminata BGA: Banana Growers Association

An Integrated Approach to Control the Black Leaf Streak

*Fruits*, Vol. 11, pp. 435-441

Montpellier, France. 25 p.

France. 120 p.

180

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BLSD: Black Leaf Streak Disease

CARBAP : Centre Africain de Recherches sur Bananiers et Plantains

CIRAD: Centre de Cooperation Internationale en Recherche Agronomique pour le Développement.

FRAC: Fungicide Resistance Action Committee

FWI: French West Indies

GPS: Global Positioning System

IBS: Inhibitors of ergosterol biosynthesis

IFAC: Institut Français de Recherches Fruitières Outre-Mer

IRFA: Institut de Recherche sur les Fruits et Agrumes

LER : leaf emission rate

Mt : Million tons

NLH: number of functional leaves at harvest

PE: Piche evaporation

SEDb: The Stage of Evolution of the Black Leaf Streak Disease

SEDs : the Stage of Evolution of the Sigatoka Disease

SLSD: Sigatoka Leaf Spot Disease

YLS: the youngest leaf spotted

YLSt: the youngest leaf bearing streaks

#### **6. References**


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CARBAP : Centre Africain de Recherches sur Bananiers et Plantains

BLSD: Black Leaf Streak Disease

FRAC: Fungicide Resistance Action Committee

IFAC: Institut Français de Recherches Fruitières Outre-Mer IRFA: Institut de Recherche sur les Fruits et Agrumes

SEDb: The Stage of Evolution of the Black Leaf Streak Disease

SEDs : the Stage of Evolution of the Sigatoka Disease

IBS: Inhibitors of ergosterol biosynthesis

NLH: number of functional leaves at harvest

Développement.

FWI: French West Indies GPS: Global Positioning System

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PE: Piche evaporation

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**11** 

*USA* 

**Yield Response to Foliar** 

Michael Zwingman and P. Stephen Baenziger

Stephen Wegulo, Julie Stevens,

*University of Nebraska-Lincoln* 

**Fungicide Application in Winter Wheat** 

Fungicides are routinely applied to control fungal diseases of wheat and other cereal crops, with the main goal of preventing yield loss (or increasing yield) and hence maximizing economic returns. In North America, the fungicides used to control foliar fungal diseases of wheat belong to two major classes with a broad spectrum of activity against fungal pathogens. These are the strobilurins and triazoles. Fungicides in both classes are used as foliar fungicides and seed treatments. The strobilurins are named in recognition of a mushroom, *Strobilurus tenacellus,* the original source of the chemical compound that formed the basis of the chemistry of this fungicide class. They are quinone outside inhibitors (QoI) and work by interfering with energy production in fungi (Vincelli, 2002). They act as local systemics by inhibiting fungal spore germination and early infection, and are highly effective when applied preventively. The strobilurins have a single-site mode of action. Examples of strobilurin fungicides used in cereal crop production in North America are

The triazoles are characterized by having a five-membered ring of two carbon atoms and three nitrogen atoms. They are curative and move systemically through the plant xylem. Triazoles slow fungal growth through the inhibition of sterol biosynthesis (Buchenauer, 1987). Sterols are essential building blocks of fungal cell membranes and are inhibited at a single site by triazoles. Because of their curative activity against early fungal infections and their ability to redistribute in the crop, triazoles are highly effective and reliable (Hewitt, 1998). Examples of triazoles used in cereal crop production in North America are

In the Great Plains of the United States, the most common foliar diseases of winter wheat are leaf rust (*Puccinia triticina*), powdery mildew (*Blumeria graminis* f. sp. *graminis*), tan spot (*Pyrenophora tritici-repentis*) (anamorph: *Drechslera tritici-repentis*), Septoria tritici blotch (*Mycosphaerella graminicola*) (anamorph: *Septoria tritici*), spot blotch (*Cochliobolus sativus*) (anamorph: *Bipolaris sorokiniana*), and Stagonospora nodorum blotch (*Phaeosphaeria nodorum*) (anamorph: *Stagonospora nodorum*). Stripe rust (*Puccinia striiformis* f. sp. *tritici*) and stem rust

**1. Introduction** 

azoxystrobin, pyraclostrobin and trifloxystrobin.

metconazole, propiconazole, prothioconazole, and tebuconazole.

(*Puccinia graminis* f. sp. *tritici*) also occur, but less commonly.

