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Wilt of in East and Central Africa

Diagnostic and Management Guide

E. B. Karamura, F. L. Turyagyenda, W. Tinzaara, G. Blomme, F. Ssekiwoko, S. Eden–Green, A. Molina & R. Markham

Bioversity International Rome, Italy

Bioversity Kampala, Bioversity International is an independent international scientific organization that seeks to improve the well-being of present and future generations of people by enhancing conservation and the deployment of agricultural biodiversity on farms and in forests. It is one of 15 centres supported by the Consultative Group on International Agricultural Research (CGIAR), an association of public and private members who support efforts to mobilize cutting-edge science to reduce hunger and poverty, improve human nutrition and health, and protect the environment. Bioversity has its headquarters in Maccarese, near Rome, Italy, with offices in more than 20 other countries worldwide. The Institute operates through four Programmemes: Diversity for Livelihoods, Understanding and Managing Biodiversity, Global Partnerships, and Commodities for Livelihoods. The international status of Bioversity is conferred under an Establishment Agreement which, by January 2008, had been signed by the Governments of Algeria, Australia, Belgium, Benin, Bolivia, Brazil, Burkina Faso, Cameroon, Chile, China, Congo, Costa Rica, COte d’lvoire, Cyprus, Czech Republic, Denmark, Ecuador, Egypt, , Ghana, Greece, Guinea, Hungary, India, Indonesia, Iran, Israel, Italy, Jordan, , Malaysia, Mali, Mauritania, Mauritius, Morocco, Norway, Oman, Pakistan, Panama, Peru, Poland, Portugal, Romania, Russia, Senegal, Slovakia, Sudan, Switzerland, Syria, Tunisia, Turkey, Uganda and Ukraine. Financial support for Bioversity’s research is provided by more than 150 donors, including governments, private foundations and international organizations. For details of donors and research activities please see Bioversity’s Annual Reports, which are available in printed form on request from bioversity-publicationscgiar.org or from Bioversity’s Web site (www. bioversityinternational.org). The geographical designations employed and the presentation of material in this publication do not imply the expression of any opinion whatsoever on the part of Bioversity or the CGIAR concerning the legal status of any country, territory, city or area or its authorities, or concerning the delimitation of its frontiers or boundaries. Similarly, the views expressed are those of the authors and do not necessarily reflect the views of these organizations. Mention of a proprietary name does not constitute endorsement of the product and is given only for information.

Citation: E. B. Karamura, F. L. Turyagyenda, W. Tinzaara, G. Blomme, A. Molina and R. Markham. 2008. Xanthomonas wilt of bananas in East and Central Africa. Diagnostic and Management Guide. Bioversity International, Uganda.

INIBAP ISBN: 978-2-910810-85-2 Cover photo: William Tinzaara

Bioversity International — Headquarters Bioversity — Uganda Via dei Tre Denari 472a P.o. Box 24384 00057 Maccarese Plot 106, Katalima Road, Naguru Rome, Italy Kampala, Uganda

© Bioversity International, 2008 Contents

Foreword vii Acknowledgements ix 1.0 Bananas in the East and Central Africa (ECA) 1 1.1 Importance of bananas in ECA 1 1.2 varieties and their uses 2 1.3 Challenges to the banana industry in ECA 5 2.0 Xanthomonas wilt of banana in East and Central Africa 9 2.1 Regional distribution 9 2.2 and nomenclature 15 2.3 Disease diagnosis 15 2.3.1 Leaf symptoms 16 2.3.2 symptoms 17 i) Male symptoms 17 ii) symptoms 18 2.3.3 Pseudostem symptoms 20 2.3.4 Confirmatory tests 21 2.4 Disease development and spread 22 2.4.1 Host 22 2.4.2 Movement within plants 25 2.4.3 Movement between plants and fields. 27 i) Insects, bats, birds 27 ii) Contaminated tools 27 iii) Infected /planting material 28 iv) Grazing animals 29 2.4.4 Survival in and plant debris 30 2.5 Control of Xanthomonas wilt of banana 31

iii iv

2.5.1 Raising public awareness 35 2.5.2 Understanding cropping systems (ABB visa-avis AAA) 37 2.5.3 Removing the male bud 40 2.5.4 Disinfecting tools 41 2.5.5 Destruction of infected plant material 44 2.5.6 Use of clean planting materials 44 2.5.7 Host plant resistance/tolerance/escape 45 2.5.8 Exclusion options 46 3.0 Evaluation of the Xanthomonas wilt management guide 48 3.1 Evaluation methods 48 3.1.1 Trainers of trainers evaluation 48 3.1.2 Scoring the criteria 49 3.2 Results and discussion 49 3.3 Conclusion 51 References 52 Plates 57 List of Acronyms 59 Acknowledgements

The field work was made possible with the funding extended to Bioversity International by the Catholic Relief Services (CRS) which together with the International Institute of Tropical Agriculture (IITA) executed the Crop Crisis Control Project (C3P) funded by the USAID. The technical team from Bioversity provided significant input into the planning and testing of the tools, and subsequently into the design of the guide. The field testing was carried out in collaboration with National Agricultural Research Organization scientists and Caritas Community-based trainers, who worked with farmers and collected responses, and provided useful criticisms that were incorporated in the final draft. The National Agricultural Research Organization (NARO-Uganda) provided the technical support in terms of tools, laboratory analysis and expertise during the development of the Guide.

 Foreword

The banana industry in Eastern and Central Africa is a major factor in the region’s food and income security strategy, without which many of the countries would have been net importers of food. Until recently the main biotic threats (weevils, nematodes, fungal and viral diseases) were managed through the use of cultural practices that exploited the differences in resistance / tolerance of the on farm. In this way farmers suffered reduced productivity but maintained a reasonable level of food and income security. However with the arrival of the Xanthomonas wilt (Xw) of bananas in the region, entire crop holdings were wiped out in some areas where highly susceptible genotypes were dominating the farming systems. A number of national and regional organizations declared the Xw, a priority banana production constraint and appealed for support to control the epidemics that were rapidly developing in the region. The Banana Research Network for Eastern and Southern Africa (BARNESA) steering committee meeting, March, 2001, Nairobi, Kenya, declared Xw as a priority production constraint and appealed for resources to search for a solution to the problem. Later, an impact assessment study conducted in Uganda estimated that up to US$4 billions by 2010 could be lost if no measures were taken to arrest the epidemic. Subsequently, the International Network for the Improvement of Banana and Plantains (INIBAP) (now Bioversity International) in collaboration with the Food and Agriculture Organization of the United Nations (FAO) convened a regional stakeholders’ meeting, February, 2005 and developed a strategy that envisioned multi-disciplinary, multi-sectoral approaches in a coherent regional response. It took into account the countries that were Xw-free but threatened; the frontline areas where the disease had just arrived; and the endemic areas where the disease was already established.

vi It also sought to raise the awareness of all stakeholders along the production-consumption chain and empowering them with knowledge and skills for the diagnosis and management of the disease. Hence, awareness-raising and associated training were seen as an integral component of the intervention strategy to control the epidemic and restore productivity in the banana-based farming systems. To achieve this, tools, approaches and innovations were developed and tested to facilitate knowledge generation, learning and sharing in an effort to mobilize stakeholder support and consolidate the fight against the disease. Lessons learnt in the implementation of the regional strategy have been consolidated into the ”Xanthomonas Wilt of bananas in East and Central Africa: Diagnostic and Management Guide” targeting field practitioners (extension providers and planners, researchers and local councils and other policy makers). The guide itself was tested among a cross-section of practitioners from different parts of the region affected by the Xw. It can be used in the development of strategies for stakeholder mobilization, knowledge generation, sharing of information about the disease and training of trainers at country and other levels. In developing the tools, use was made of the wide range of Bioversity experiences with Bugtok () in the Philippines and with Moko (R. solanacearum) in Latin America, both of which have similar symptoms as Xw. Locally, use was made of the experiences gained in Uganda. The tools presented in the guide were deliberately simplified to enable use by a wide range of partners/players. For the same reason a range of management options were proposed to allow practitioners to innovate depending on local circumstances as they use the tools. The regional strategy received a considerable boost with the support of the Crop Crisis Control Project (C3P) funded by the USAID and jointly executed by the Catholic Relief Services (CRS) and the International Institute of Tropical Agriculture (IITA). The project brought together national and regional partners along the production-consumption chain which provided the framework for the testing of the tools in the guide.

vii

1 Bananas in the East and Central Africa (ECA)

1.1 Importance of bananas in ECA Approximately a third of global banana production is grown in sub Saharan Africa where the crop provides more than 25% of food energy requirements for an estimated 70 million people. The sub-region alone produces nearly 20 million tons of bananas annually. The crop is important as a staple as well as a relatively cheap and easily produced source of minerals and vitamins, particularly vitamin A, C and B6. On the east African highlands, AAA cooking and beer bananas predominate, and it is in this region that bananas reach their greatest importance as a staple food crop. In countries such as Uganda, and per capita consumption has been estimated at well over 400- 600kg per year, the highest in the world. Furthermore, banana by-products (peels and pseudostems) provide valuable livestock fodder, especially during the prolonged droughts that affect the regions periodically. The plant has also been used for medicinal purposes (Karamura, 1992), for celebrating marriage and for other rituals (Price, 1995). Virtually all components of the plant have found a variety of uses in the homesteads and domestic industries, including basket-making, carpets, shoes and a host of indoor decorations (Karamura, 1992). A number of industries within the region process a variety of alcoholic and non-alcoholic beverages as well as a diversity of confectioneries from bananas for local and regional markets. Bananas also play an important environmental role within farming systems by combating soil erosion on steep hills and preserving long-term fertility of the soil (INIBAP, 1986). The

  Xanthomonas Wilt of Bananas in East and Central Africa crop’s canopy also provides protection for other crops that are often inter-cropped with it, such as beans, groundnuts, cucurbits and coffee (Karamura, 1992). Once established as a sole crop, bananas enter a phase of continuous growth, creating a “tropical forest” with beneficial microclimatic effects to the soil (Karamura, 1992). Gardens as old as 150 years are common in Uganda (Tothill, 1940).

1.2. Banana varieties and their uses A wide range of varieties of bananas is found in ECA, (Table 1) with different types being specifically adapted to different agro- ecological regions and cultivated for different uses. On the east African highlands, AAA cooking and beer bananas dominate the landscape and the region is considered a secondary diversity centre for bananas. Other types such as plantains (AAB), dessert varieties (Gros Michel and Cavendish AAA) as well as the diploid AB are also grown widely in the region. In addition to local varieties, new banana cultivars developed by the international banana breeding programmes have been introduced in the region and a number of them have already been released to farmers’ respective NARS . Bananas in the East and Central Africa (ECA) 

Plate 1.1: diversity in East and Central Africa. Cultivars in commercial trade

FHIA 17 (AAAA)

Bogoya (AAA) Kayinja (ABB)  Xanthomonas Wilt of Bananas in East and Central Africa

Gonja Nakatansense (AAB) Cavendish (AAA)

Sukali Ndizi (ABB)

FHIA 25 (AAAA) Bananas in the East and Central Africa (ECA) 

In the recent past market forces have tended to force farmers to select and grow only those varieties that readily respond to the needs of urban market consumers. This coupled with population pressure that does not allow the land to rest/rejuvenate its fertility and the selective effects of pests and diseases, has led to increasing genetic erosion in diversity in the region (Karamura, et al 2004)

Table 1: Genome groups and uses of some widely grown bananas in ECA

Genome group Cultivar name End product use Dessert Gros Michel AAA Cooking, roasting Muraru, Mushale Dessert AAA-EAHB Nakitembe Green-cooking AAA-EAHB Kabula Beer

Nakatansese, Ripe-cooking AAB French plantain roasting ABB Kivuvu Ripe-cooking ABB Kayinja (Musa) Beer AB Kisubi Beer AAB Sukali Ndiizi Dessert Dessert, cooking, AAAB FHIA series Beer, chips, figs

Modified from: Karamura DA, 1999

1.3 Challenges to the banana industry in ECA Average yield in these systems ranges from 4-15 tons per hectare, which falls far below the potential levels of 30-40 tons/ha  Xanthomonas Wilt of Bananas in East and Central Africa obtained under research conditions. A host of biotic, abiotic and socio-economic factors stress the industry but by far the biggest challenge is probably posed by the biotic constraints- the pests (banana weevil, nematodes), diseases (black Sigatoka, yellow Sigatoka, Cladosporium speckle, fusarium wilt, , banana streak virus and recently Xw of bananas), in addition to declining soil fertility. Weevils and nematodes are pests of the underground parts of the giant herb, limiting the ability of the plant to access water and nutrients from the soil. However, in the ECA region, a number of genotypes including the ABB (‘’ = ‘Kayinja’), the AB (‘Kisubi’) and some AAA-EAH are variably resistant-tolerant to weevils and nematodes. Similarly, black Sigatoka, yellow Sigatoka and Cladosporium speckle are diseases of the banana leaves, limiting the photosynthetic activity of the plant. Again within the Musa genepool in east and central Africa, a number of genotypes are resistant to the diseases so that households have something to harvest from their crop. Over the years research developed and disseminated cultural management practices that re-enforced farmers’ experiences in controlling the diseases and pests. However this picture dramatically changed with the onset of the Xw of bananas. Apart from the epidemic proportions the disease assumed, being new in the farming systems, all the genotypes succumbed to the disease, leaving no survival options for the communities. Bananas in the East and Central Africa (ECA) 

Plate 1.2: Major pests and diseases of bananas in ECA

Sigatoka

Nematodes

Fusarium  Xanthomonas Wilt of Bananas in East and Central Africa

Viruses

Banana weevil 2 Xanthomonas wilt of banana in East and Central Africa

2.1 Regional distribution In 2001, a banana wilting disease was discovered for the first time in central Uganda (Tushemereirwe et al. 2004). In the same year east Congolese farmers observed the same wilting disease on a few plants at Bwere Hill, Bashali Mokoto village in the Masisi district, in North Kivu Province (Ndungo et al., 2004; 2006). The disease was described as destroying banana fruit bunches and known to result in total loss of production, threatening the livelihoods of millions of people who depend on banana as a food and income source. Subsequently the disease was identified as pathovar musacearum. Previously known only from its attack on Ensete and banana in Ethiopia, in just four years since its discovery in central Uganda, the disease developed into a full- blown epidemic, spreading throughout the eastern, central and north-western districts of the country.

 10 Xanthomonas Wilt of Bananas in East and Central Africa

Plate 2.1a: Distribution and spread of Xw in C3P districts of Uganda

Yumbe Moyo Adjumani Kitgum Kotido Arua Pader Gulu

Nebbi Moroto Lira

Apac Katakwi Kaberamaido Nakapiripirit Masindi Soroti Hoima Kumi Nakasongola Kapchorwa Pallisa Sironko Kiboga Kamuli Mbale Kibale Luweero Bundibugyo Kayunga Iganga Tororo Kyenjojo Mubende Jinja Fort Portal Mityana Mukono Bugiri Wakiso Njeru Mayuge Busia Kasese Kamwenge Mpigi Kampala Sembabule Entebbe Masaka Kalangala Bushenyi Mbarara Rukungiri Rakai Kanungu Ntungamo Kisoro Kabale

Although the disease was first observed in 2001, in the Democratic Republic of Congo, it was only confirmed in 2004. The disease was confirmed in a 10 km radius around Bashali Mokoto village. Later, a new disease outbreak was observed 20 km from the first, which lessened the chances of containment and eradication (Ndungo et al., 2004; 2006). Xanthomonas wilt of bananas in East and Central Africa 11

Plate 2.1b: Distribution and spread of Xw in eastern DR Congo

In Rwanda the disease has been confirmed in the districts of Rubavu, Rulindo, Rutsiro and Karongi in the northwest of the country, close to the border with North Kivu province of D R Congo. This is the most important banana production area for east African highland beer banana (AAA-EA). Fortunately, the other highland banana production region of Kibungo, bordering and north east Burundi remains free from the disease. 12 Xanthomonas Wilt of Bananas in East and Central Africa

Plate 2.1c: Distribution and spread of Xw in Rwanda Xanthomonas wilt of bananas in East and Central Africa 13

In Tanzania Xanthomonas wilt was first identified in Muleba District Kagera region in January 2006; subsequently the disease has been reported in Bukoba, Karagwe, Biharamulo, in Kagera region and Tarime District in Mara region. The other banana growing regions- Meru-Kilimanjaro axis, Kigoma region, the southern highlands bordering Malawi and Monzambique and the islands of Pemba and Zanzibar are free from the disease. Plate 2.1d: Distribution and spread of Xw in Kagera, Tanzania 14 Xanthomonas Wilt of Bananas in East and Central Africa

In Kenya, Xanthomonas wilt was first discovered in 2006 in Teso, Bungoma and Busia in Western province. In the year 2007 the disease has also been reported in Kakamega district in Western province and Siaya in Nyanza province. The highland agro- ecologies of Kisii, the rift valley and central Kenya remain disease- free and so does the coastal regions. Plate 2.1e: Distribution and spread of Xw in western Kenya Xanthomonas wilt of bananas in East and Central Africa 15

The presence of Xw in Burundi remains unclear. Initial reports indicated that the disease was cited in Cibitoke province in the northwest and Makamba province in the south-east but this remains to be confirmed. It is possible that due to symptomatic resemblance of Panama disease and nutrient deficiency symptoms (e.g. Mn) with Xw of bananas, errors could have been made in field identifications. Nevertheless, given the current regional movement of the epidemic, it will be a question of time before the disease reaches Burundi. It is therefore necessary for contingent plans to be put in place to manage outbreaks as soon as they are reported.

2.2 Taxonomy and nomenclature Aritua et al. (2006; 2007a) have done molecular studies on X. campestris pv. musacearum and found it to have close homology to strains of and suggested that most likely Xw of bananas in ECA belong to this species. The authors have therefore proposed the name X. vasicola to replace X. campestris pv. musacearum but this has not been formally approved as a new combination of names (Tindall et al., 2006; Young et al., 2001, Smith et al., 2007). This may require revisions with regard to memberships within X. vasicola; the pathovar status of strains therein will require revision. The limited pathogenicity studies undertaken to date have provided evidence for strains from enset and banana to be designated as X. vasicola pv. musacearum. However, to confirm the pathovar status within X. vasicola, more studies involving more representative strains of the putative pathovars on appropriate differential hosts needs to be undertaken (Smith et al., 2007).

2.3 Disease diagnosis Correct diagnosis is essential for prescribing and/or application of correct and timely interventions against the disease. The disease symptoms in general are related to the phenological stage of the plant attacked, the mode of infection and/or the farming system in question. The disease will affect any phenological stage of the plant and accordingly the symptoms also vary with plant’s phenology. 16 Xanthomonas Wilt of Bananas in East and Central Africa

2.3.1 Leaf symptoms Characteristically, and to differentiate it from other wilting diseases of bananas, Xw-mediated wilting begins with any leaves (probably depending on the site of initial infection); commonly the central heart leaf at the apex may wilt first to be followed by yellowing and wilting of newly expanded leaves of the infected plant. This may be contrasted with Fusarium oxysporum cubense f. sp (Foc)-mediated wilting that starts from older leaves and spreads to younger leaves. In the case of Xw-mediated wilting in bananas, the leaves are dull yellow like they have been passed through a fire flame (held above a fire). In addition the Xw–infected leaves will tend to snap about one-third the leaf length from the leaf tip. This again is contrasted with Foc-infected leaves which snap at the leaf petioles. Plate 2.2a: Xanthomonas wilt leaf symptoms Xanthomonas wilt of bananas in East and Central Africa 17

Plate 2.2b: Fusarium wilt leaf symptoms

2.3.2 Inflorescence symptoms i) Male bud symptoms In insect-mediated infection, especially in ‘Kayinja’ (ABB)-based cropping systems, the male flower (bud) is usually the point of entry by the disease. The colour of of infected male may fade from deep purple to dark brown or grey. They shrivel and 18 Xanthomonas Wilt of Bananas in East and Central Africa eventually dry up as the portion of the flower stalk immediately above the bud dries up and/or rots. Male bud infection proceeds through the rachis and real stem down to the corm from where it moves into suckers adjoined to the mother plant. Plate 2.2c: Male bud symptoms

In intensively managed Matooke (AAA) production systems where male buds are routinely removed to improve bunch characteristics, male-bud infection is not common partly because they do not stay long enough to be infected and partly because Matooke buds do not appear to attract a lot of foraging insects (Tinzaara, personal communication). ii) Fruit symptoms Both in Kayinja (ABB)-and Matooke (AAA)-based farming systems, premature ripening of the fruit is diagnostic of Xw infection though this is more commonly observed in Kayinja than Matooke systems (as more flower infections occur in Kayinja plantations). The become hardened and rotten and unpalatable to both humans and animals. A cross-section through the fruits will reveal a dark brown discolouration of the pulp. Under conditions not yet clearly Xanthomonas wilt of bananas in East and Central Africa 19 understood, outwardly the fruits may not show signs of infection (e.g. rotting and premature ripening) but on cross-section cutting of the same fruits, the disease symptoms will be revealed. In addition, when the fruits are cut in cross section the yellow-orange pus-like fluid would be observed. Plate 2.2d: Fruit symptoms Premature ripening Internal discolation

20 Xanthomonas Wilt of Bananas in East and Central Africa

2.3.3 Pseudostem symptoms In both Kayinja (ABB) and Matooke (AAA)-cropping systems, the disease attacks the vascular system, which becomes necrotic (very advanced stage) and rots. The necrosis of the vascular bundles is concentrated in the true stem. A cross-sectional cut of the pseudo- stem, leaf petioles or the flower stalk will release yellow-orange bacterial ooze after 5-30 minutes, depending on the turgidity of the plant. Plate 2.2e: Pseudostem symptoms Xanthomonas wilt of bananas in East and Central Africa 21

2.3.4 Confirmatory tests Once the leaf, floral and stem symptoms indicate Xanthomonas wilt, it is necessary to carry out molecular level tests to confirm the presence of the disease in the sample collected. It is also advisable to send samples to more than one laboratory in case the sent material does not reach to target laboratory or that laboratory develops a technical problem. Smith et al. (2007) have summarized the laboratory procedures carried out to isolate the pathogen. In all cases the sample to be used must be fresh and with minimum contamination by other (secondary) microbes. Isolation is recommended from the inflorescence stem using the following procedures: a) Excised plant material (2-5mm3) should be removed aseptically from the internal region of an infected area (stem in cross-section) and placed in a small volume of sterile water (about 1ml) and left for 5 minutes for the bacterium to stream into the water. b) Isolation should be undertaken from the banana-water exudate by streaking onto a growth medium in a manner to obtain single bacterial colonies. A suitable medium for the primary isolation is NA medium, as this is a low-sugar-medium that will reduce excessive growth of competing, faster growing, saprophytes that might otherwise overgrow the X. campestris pv. musacearum colonies. c) Single colonies of X. campestris pv. musacearum will only be evident after 48 hours of incubation at 27-30°C and should be re-streaked to ensure purity on fresh media. A richer growth promoting media, such as YDCA that also buffers against acidification of the medium, is more suitable at this stage. Mwangi and Nakato, (2008) and quoted by Smith et al. (2007) have described a semi-selective media for X. campestris pv. musacearum that is suitable for the isolation and quantification of the bacterium from non-sterile, non-plant backgrounds such as soil. 22 Xanthomonas Wilt of Bananas in East and Central Africa

An array of diagnostic methods are available for the identification and detection of the causal organism, X. campestris pv. Musacearum: i. Lelliott and Stead (1987) and Aritua et al. (2007a) provide additional information on classical and modern approaches to identification. ii. Recent first disease reports for Xw have involved analysis of the bacterium fatty acid profile, DNA (GyraseB gene sequence or rep-PCR profile) and pathogenicity on banana. iii. Diagnostic PCR (real-time and conventional) primers are also available (specific toX. campestris pv. musacearum and X. vasicola strains pathogenic to sorghum, and sugarcane) that have been based on sequencing of a rep-PCR fragment (Aritua et al., 2007b). These primers are currently undergoing field validation in Uganda. It is anticipated that these primers will be useful in the identification, detection and monitoring of the pathogen in plant and non-plant environments (Smith et al., 2007). 2.4 Disease development and spread There is a lot of similarities between the Xw of bananas and other bacterial diseases in terms of disease development and spread. Like Moko or Bugtok (R. solanacearum), Xw infects the vascular systems of its hosts; is transmitted between ABB plants by air- borne vectors; in AAA bananas mainly by working tools; and will not survive under anaerobic conditions for long. Further the development and spread of the disease may be influenced by the host plant phenology (persistent visa-avis dehiscent bracts and flowers) and climate through its influence on arthropod vector distribution.

2.4.1 Host plants In ECA, hosts of X. vasicola pv. musacearum include enset () and banana (Musa) both of which belong to the Xanthomonas wilt of bananas in East and Central Africa 23

Musaceae family, order, Zingiberales. Other family members of the order Zingiberales include: Cannaceae (Cana family), Costaceae (Costus family), Heliconiaceae (Heliconia family), Marantaceae (Prayer-plant family), Strelitziaceae (Birds of Paradise Flower family) and Zingiberaceae (Ginger family) (see -http://plants.usda. gov ). Maize is the only suspected host of the disease that is not of the order Zingiberales (Aritua et al., 2007b). Within Musaceae, however, no banana type is resistant to the disease when artificially inoculated although some cultivars are less susceptible than others. This is said to be related to the physiological and morphological characteristics, management practices and the farming systems in question. Plate 2.3a: Cana Lily 24 Xanthomonas Wilt of Bananas in East and Central Africa

Plate 2.3b: Heliconia

Plate 2.3c: Birds of paradise Xanthomonas wilt of bananas in East and Central Africa 25

2.4.2 Movement within plants In Kayinja (ABB)-based cropping systems, the disease is mainly transmitted from one banana stool to the other by insects (bees, wasps, ants, bats, etc,). Insect-mediated infection is commonly associated with the ABB cultivars (Saba and Cardaba in the Philippines and Kayinja and Kivuvu in east and central Africa). Inflorescence phenology and structure are closely linked to disease etiology and epidemiology. As the inflorescence grows the floral bracts covering the young neuter flowers dehisce and this causes “bleeding” from the scars left by the dehiscent floral bracts. In infected plants the fluid from the scars contain a lot of infective bacterial fluid (=bacterial ooze) which is picked by visiting - collecting/foraging insects. It is postulated that the transmission is mechanical in nature with foraging insects picking the bacterial inoculum from scars on the male bud of infected plants and depositing the on the next uninfected inflorescence visited (the entry points are mainly the male flower/bract scars) thereby initiating new infection on new plants. Four stages of male bud infection have been described in insect- mediated transmission. In stage 1, the outer bracts on the affected male buds begin to shrivel, losing their grip on the main body of the bud. Stage 2 sets in when the male bud bracts dry up, losing the bell shape; the neuter flowers as well as the part of the inflorescence stalk connecting the female and the male flowers may appear dried up and/or rotten. Stage 3 will set in the bunch (=female flower) begins to ripen prematurely. In stage 4 of the infection, the entire bunch is rotten and the upper parts of the pseudo-stem including the youngest leaves are wilted. 26 Xanthomonas Wilt of Bananas in East and Central Africa

Plate 2.4: Stages of male-bud infection

Stage 0: No wilt Stage 1: One bract wilted

Stage 2: Two or more Stage 3: All bracts Stage 4: Flower bracts wilted dry, flower stalk stalk and bud dry drying

In Matooke cropping systems where management is intensive and male buds are regularly removed to improve bunch characteristics, the overriding mode of infection is by contaminated garden tools. Xanthomonas wilt of bananas in East and Central Africa 27

This may involve the upward movement of bacteria through the vascular tissues if infection occurs in the lower parts of the plants (rhizome or pseudostem) or the downward movement of bacteria if the infection site was for example a leaf petiole.

2.4.3 Movement between plants and fields i) Insects, bats, birds Like with Moko and Bugtok (R. solanacearum) diseases, X. vasicola pv. musacearum transmission in ABB bananas has been associated with insects, bats and birds (Buddenhagen, 2006). However the bacterium has only been isolated from insects collected from infected banana flowers (Tinzaara et al., 2006). It would appear that the bacterium has no symbiotic relationship with the insects and that transmission is only mechanical. The insects visiting banana flowers for nectar mechanically pick bacterial ooze and on visiting other disease-free plants contaminate the latter to start a new infection site. The potential of bats and birds to transmit the disease has been demonstrated (H. Buregyeya, unpublished report). An inventory of insects visiting banana flowers in Uganda identified potential vectors. The most common insects were stingless bees (Family Apidae), fruit flies (Family Drosphilidae) and grass flies (Family Chloropidae). The bacterium was isolated from stingless bees, honey bees (Apis mellifera), fruit flies and grass flies that had been collected from male flowers of symptomatic and asymptomatic plants (Tinzaara et al., 2006; Gold and Bandyopadhyay, 2005; and Jones et al., 2007). The importance of insect-transmission in ABB bananas through the male buds has been underlined by the fact that early de-budding (i.e. right after the formation of the last hand) readily arrests disease spread. ii) Contaminated tools Many aspects of crop husbandry involve the use of pruning/de- leafing/digging tools. At a farm level, the use of these toolsis not only routine; it is also a daily occurrence, as the farmer weeds, 28 Xanthomonas Wilt of Bananas in East and Central Africa de-suckers, de-trashes or harvests bananas. If the tool(s) used is contaminated by the disease, transmission will occur at the point on the plant where cuts are made. The spread of disease by contaminated tools is, therefore, a key mechanism by which the disease is spread locally (Blomme et al, 2006; Eden-Green, 2006) within the same field (as is the case of a farmer working in his/her garden) as much as between fields when contaminated tools are used to harvest bananas on different farms (Karamura, 2006). iii) Infected plant/planting material Infected plant and planting material may account for many of the long distance disease transmission cases. In Tanzania, a farmer unsuspectingly moved infected planting material from the Kagera region close to the Rwandese border to the Mara region on the Kenya border, where a new outbreak was started weeks after planting the infected sucker. The sucker wilted soon after planting and the unsuspecting farmer cut it down and continued working using the tools (without decontamination). As more plants got sick they were cut down and the disease moved on till a 20 x 10 km banana enclave was brought under attack. The disease may also be moved in infected fruit; mulching material, especially piles of the rachis that are left at collection centres when the bunches are de-handed to load the fruit onto lorries for distant markets, and when infected male buds are used to seal plastic containers (beer or water). Xanthomonas wilt of bananas in East and Central Africa 29

Plate 2.4b: Male bud and banana finger used as corks for water plastic containers

iv) Grazing animals Domestic herbivores (goats, sheep and cows) tend to feed on banana suckers selectively. Although it has not been studied quantitatively, it suspected that a feeding animal could easily transmit the disease mechanically from an infected plant to a clean one when browsing. 30 Xanthomonas Wilt of Bananas in East and Central Africa

2.4.4 Survival in soil and plant debris The pathogen is also reported to survive in the soil (or debris) for up to two weeks during which they can serve as primary inoculum. Use of unsterilized soil in plant nurseries can also transmit the same to the seedlings and usually these die within weeks of infection. A quick check under field conditions can be instituted by planting tissue culture seedlings, sword or maiden suckers in a suspected infected environment or drenched with the disease and they will quickly wilt and die. Under anaerobic conditions however it is estimated that the disease will have died out from the soil within three months and the field can be replanted with banana (Molina, 2006). Plate 2.5: Plantlet dying after planting in infected soil Xanthomonas wilt of bananas in East and Central Africa 31

2.5 Control of Xanthomonas wilt of of banana poses special problems with respect to its control and management because of its ability to assume epidemic proportions in a matter of weeks. Being a new disease, with new symptoms, new mode of attack, new control measures and more destructive than other diseases that are endemic in the banana-based agro-ecologies in the region, it may take time for researchers, extension and farmers to adjust and/or respond to it appropriately. Moreover it requires more than just control measures at the farm level; something has to be done all along the production- consumption chain and this calls for multidisciplinary and multi- sectoral collaboration to bring the full weight of stakeholders to bear on the disease and minimise the impact of the epidemic on the farming communities. In planning Xw management therefore, it is critical to identify the objectives, which may include: i. To prevent the disease from crossing local and international borders ii. To eradicate the pockets of the disease before moving out of outbreak areas iii. To arrest the epidemic from reaching damaging levels iv. To put in place strategies and/or measures that will incorporate Xw management into the overall national (or regional) integrated pest and disease management programme when the disease epidemic has been controlled but not eradicated. The actions to be undertaken will depend on the disease typology prevailing in the target area (Table 3). In disease-free but threatened areas, the focus is to raise general public’s awareness of disease recognition symptoms; de-budding techniques; disease eradication techniques; how to use disease surveillance and reporting tools. In the frontline and out break areas the strategy would be to promote ‘best bet’ options for slowing down epidemic spread and coping with outbreak by extension. In endemic regions, however a broader focus is needed that shifts to the development of skills/ 32 Xanthomonas Wilt of Bananas in East and Central Africa tools for validating and deploying best bet options for slowing down the epidemic and enabling farmers to cope with outbreak through farmer field schools (FFS). Farmers in these areas need to be empowered to develop and use tools for evaluating the effectiveness of disseminated information and technologies. In all areas the stakeholders need to be equipped with skills for correct application of Xw management techniques. Xanthomonas wilt of bananas in East and Central Africa 33

Table 3: Confronting the threat of banana Xanthomonas wilt of bananas in East and Central Africa Goal: To assure food security and household incomes in banana-based systems in East and Central Africa Purpose: To strengthen the capacity of the banana sub-sector to successfully manage the outbreak of banana Xanthomonas wilt Outputs: 1. Communities in unaffected 2. Communities in outbreak 3. Communities in 4. Response to areas mobilized to prepare areas equipped to respond endemic areas equipped Xw effectively for outbreaks (Burundi, to the epidemic (Rwanda, to sustain production coordinated Kenya) Uganda, Tanzania & systems (Rwanda, (BARNESA) Democratic Republic of Uganda, Tanzania & Congo) Democratic Republic of Congo) Activities: Raising awareness of threat Advocating an enabling policy Policy dialogue continued Establishing national among decision-makers environment for national level to sustain resource Coordinating and mobilizing of resources action (awareness – lobbying) commitment at national Committees or Working (National Action Plans) level Groups Raising awareness of actions Advocating an enabling policy Policy dialogue continued Monitoring, evaluating needed among implementers environment at local level to sustain resource and assessing impact and training of actors (Local (awareness – lobbying) commitment at local level - tools developed, Action Plans) disseminated, harmonized at regional level Raising general public’s Strengthening knowledge base Understanding Monitoring, evaluating awareness of threat and on disease recognition and susceptibility and control and assessing impact solutions (facilitating dialogue management (demonstrations, methods through FFSs, - implemented at amongst grassroot stakeholders) exchange visits, workshops, established in endemic national and regional etc) regions level 34 Xanthomonas Wilt of Bananas in East and Central Africa

Establishing an early Evaluating options for Strengthening the seed Establishing information warning/surveillance system introducing alternative systems to deliver portal - stakeholders and actors varieties (escaping infection quality banana seed to - database, GIS tools, identified and trained (e.g. and acceptable to farmers and farmers. Evaluating and ICT capacity building training in quarantine tools) consumers) disseminating new varieties – and strengthening (incl. strengthening of linkages for information processing-marketing exchange chains) Diagnostic tools developed (incl. Validating/demonstrating Refining and validating Initiating policy e.g. assessment of variability) options for slowing Xw management strategies dialogue at regional and and deployed transmission (e.g. debudding, (incl. new varieties) through international level sanitation, disinfection) participatory research

Information materials developed Developing system for ‘Mainstreaming’ Xw and disseminated (posters, introducing and disseminating management tactics with leaflets, radio/tv talk shows, etc) clean ‘seed’ of new varieties other IPM and NRM options in FFS and other extension efforts Information on Xw included in Promoting ‘best bet’ options extension curricula for slowing epidemic spread and coping with outbreak in extension campaign Validating and deploying best bet options for slowing epidemic spread and coping with outbreak in FFSs Xanthomonas wilt of bananas in East and Central Africa 35

2.5.1 Raising public awareness The battle against Xanthomonas wilt necessarily has to be multi- faceted, requiring the mobilization of all available resources- human as well as financial. Everyone must know and be facilitated to make a contribution towards the control of the disease. In the case of banana in the Great Lakes region of east Africa, due attention may not be difficult to obtain given the importance of the crop in the region. Moreover the flashy symptoms of the disease coupled with the speed of destruction of host plants quickly attract farmers’ attention to do something about it. In some cases, however, the importance people have attached to banana may be a hindrance when it comes to implementing recommendations which they (farmers) consider belittling / abusive to the (sacred) plant and hence refuse to carry them out. The quality of stakeholder response will depend on the quality of messages received. All key stakeholders need to be given clear/ concise and appropriate messages, stating what needs to be done by whom, how, where and when so that they in turn can play their effective roles. The messages should be designed in terms of content the medium and time of transmission/dissemination to bring the maximum and predictable effects on all who receive them. Posters, pamphlets, leaflets, brochures and billboards need to be designed to suit the levels of literacy in the target area and population. The choice and nature of the communication strategies should take into account the capacity (literacy levels, numbers of radio receivers, extension support, etc) available in the target area. A time frame for assessing /evaluating the effectiveness of the messages should be decided before the transmission of the messages and appropriate tools prepared to collect the feedback. It is important to design a two-way information exchange scheme where information sent out elicits a response that can be quantitatively analysed. It frustrates grassroot platforms as much as the task managers of the project, when information sent receive no response. Therefore a fast-track message exchange needs to be instituted so that actions are taken in time and team spirit 36 Xanthomonas Wilt of Bananas in East and Central Africa maintained along the production-consumption chain in the target areas. One extension approach adopted in Uganda was termed “going public” (Nankinga et al., 2006) in which use was made of public gatherings such as market days, Sunday services, school open days, etc to inform the public about the disease and solicit their support. These campaigns have focused on the recognition of disease symptoms and the recommended cultural control practices to be taken. They also serve as surveillance mechanism, where by farmers recognizing the disease from the poster, may inform appropriate authorities who would take action. Xanthomonas wilt of bananas in East and Central Africa 37

Plate 2.6: Going public on market day 38 Xanthomonas Wilt of Bananas in East and Central Africa

2.5.2 Understanding Cropping systems (ABB vis-a-vis AAA) Within ECA, and in respect to Xw of bananas, two distinct banana cropping systems- the Kayinja (ABB) and the east African highland banana (AAA) systems have been recognized. The ABB are generally lower altitude plants used for juice/beer/wine making and are aggressive plants, being resistant to black Sigatoka and tolerant to weevils and nematodes. The cultivar however produces a lot of nectar during flowering which attracts foraging insects, bats and birds. It is those ABB varieties which do not have persistent neuter flowers and bracts that are most at risk from contamination by bacterial ooze-laden insects when they walk over “wounds” of fallen (dehiscent) male flowers (most likely not male bracts). The wound provides an entry point for the bacteria to start an infection. In these systems therefore infection starts at the male bud and progresses to the female fruit and down to the corm via the true stem from where it may enter the suckers attached to the infected mother plant. Unfortunately in many parts of the region, Kayinja gardens are neither pruned nor de-budded or weeded once planted. The farmer only comes to harvest the fruit. This has limited the use of tools and by default tools-mediated infection. Unfortunately this “minimum-attention” approach by farmers for Kayinja gardens has maximized insect mediated infection because male buds are not removed. In contrast, the east African highland bananas (AAA) not only do not attract as much insect life as Kayinja (ABB) (Tinzaara, personal communication) but also are intensively managed with de-budding religiously done to improve bunch characteristics. However intensive management has meant maximum use of garden tools which would spread the disease quickly between plants if contaminated. Hence the movement of the disease is not as straight forward as is the case for insect-mediated infection. In the case of tool-mediated infection, the movement of the disease within the plant will depend on the site of infection and this can be the roots, leaves, the inflorescence or the stem. Xanthomonas wilt of bananas in East and Central Africa 39

Plate 2.7a: Kayinja-based cropping system

Plate 2.7b: Highland banana cropping system 40 Xanthomonas Wilt of Bananas in East and Central Africa

2.5.3 Removing the male bud This is regarded by extension practitioners as the first line of defence against the disease Blomme et al. 2008). In planning a control strategy especially in disease-free but threatened regions, massive de-budding must be instituted in the region to eliminate the possibility of air-born vectors introducing the disease. De-budding needs to be done correctly to eliminate the risk of infecting new plants. The use of cutting knives may promote further infection since this may “inject” the disease at the site of the cut. Conversely the use of a forked stick does not predispose the cut surfaces to the disease and is highly recommended. Plate 2.8: Debudding using a forked stick

Xanthomonas wilt of bananas in East and Central Africa 41

In Matooke this is regularly done and farmers only need to be advised on the correct use of the forked de-budding stick. When correctly used the male bud snaps off and the forked stick does not make contact with the fluids from the cut/injured surface, thereby eliminating the possibility of contamination of the de-budding stick and possible transmission from plant to plant. For effective control of Xw in Kayinja-based systems, de- budding is mandatory because here the mode of infection is through foraging insects on the male inflorescence. In all cases, the use of cutting knives must be discouraged as they will increase the likelihood of plant-to-plant disease transmission. Experiments have demonstrated that the infection rate can be drastically reduced by use of a forked stick (Blomme et al., 2005; Ssekiwoko et al., 2006; Turyagyenda et al., 2006). However farmers tend to resist de-budding in Kayinja because they believe that “bleeding” of the cut male bud reduces the juice quality.

2.5.4 Disinfecting tools Working tools if they come in contact with the bacterial ooze would transmit the disease from one plant to the other. This has been the main medium of Xw transmission in intensively managed systems such as the Matooke system in east and central Africa and the commercial systems in the Philippines and Latin America. Since the disease is systemic, any knife cut through the vascular system of an infected plant would pick the bacteria on to the surfaces of the knife, which potentially can transmit it to the next plant if not decontaminated. The tools can be disinfected by washing them in Sodium hypochlorite solution locally sold in east Africa under the trade name “Jik.” This is mixed with water at the ratio of one cup of Jik in five cups of water. If Jik is not accessible, the metal implements may be flamed in fire until they are too hot .to touch Many farmers find the use of fire to disinfect the tool too laborious to apply especially because tools have to be flamed before use on the next plant. Equally, the use of Jik has posed problems of cost and accessibility in the rural areas. 42 Xanthomonas Wilt of Bananas in East and Central Africa

Plate 2.9a: Disinfecting tools with “JIK”

Xanthomonas wilt of bananas in East and Central Africa 43

Plate 2.9b: Disinfecting tools with fire 44 Xanthomonas Wilt of Bananas in East and Central Africa

In Matooke systems, one approach adopted to eliminate the disease from pockets of infection was to avoid the use of cutting tools in the garden for six months, during which all infected mats die off and the disease is eliminated. However this approach would work better when there is a lot of discipline and/or when the farmer can afford not to use the garden for so long.

2.5.5 Destruction of infected plant material In traditional systems removing a that is older than several human generations is not readily accepted. A lot of convincing would be needed to force farmers to cut their banana trees, let alone remove the entire mat. This situation has not been helped by the limited research on the movement of the disease in tool-mediated infection. For this option to be effective there must be regular inspection of gardens for symptoms but this is only done for highland green-cooking and beer bananas but not so commonly in Kayinja systems. Several approaches / methods have been proposed. First, the plants could be uprooted and buried but this has been found to be labour intensive. Second the infected mats/ plants could be cut, heaped and left to rot undisturbed. This may require fencing off and labelling to avoid accidental interference. The other option demonstrated has been the use of herbicides but associated costs and health risks for poor farmers can not be over- emphasized. In insect-mediated infection where the disease moves unidirectional along the true stem from the male bud to the corm in the ground, it is possible to remove the affected tree (not the whole mat) if the infection is detected early e.g. at stage 1 as seen in Plate 2.4 (Ssekiwoko et al., 2006).

2.5.6 Use of clean planting materials In many instances latent infection is moved over short and long distances in planting materials (just as in plant residues), hence the need to avoid planting material from fields whose Xw status is not ascertained. Where possible, use should be made of tissue culture material or of clean seed from known clean seed mother Xanthomonas wilt of bananas in East and Central Africa 45 gardens. Where applicable, farmers should be facilitated to use macro-propagation techniques to produce their own clean seed.

2.5.7 Host plant resistance/tolerance/escape A number of inoculation experiments have not revealed robust host plant resistance among the cultivated varieties in the region. However , an ornamental wild banana was reported to recover after showing signs of wilting. These experiments will need to be repeated to confirmM. balbisiana as a potential source of host resistance. Under field conditions, however, the east African highland bananas (AAA) were also reported to be 50% less likely to be infected than Kayinja bananas (ABB) but it is not yet clear if the former has some physiological (tolerance) mechanisms or the plants are simply escaping due to agronomic factors. In both AAA and ABB genome subgroups, however, the presence of persistent / indehiscent neuter flowers and male bud bracts enables the plants to escape natural infection. That the plants are merely escaping, is proved when the plants are artificially infected, readily succumb to the disease. 46 Xanthomonas Wilt of Bananas in East and Central Africa

Plate 2.10: Persistent neuter flowers and male-bud bracts

2.5.8 Exclusion options Exclusion options will help to delay the arrival of the disease but rarely prevent it. Nevertheless exclusion measures would help to delay the arrival while contingent plans are made to manage it. In all situations rigorous monitoring and surveillance would be needed to ensure that the arrival is detected as soon as possible and corrective measures are taken in time. In distinctly isolatable Xanthomonas wilt of bananas in East and Central Africa 47 locations, such as islands, rift valleys or mountain ecologies, it may be helpful if quarantine measures are imposed to stop the movement of banana materials into and out of the target region. However, when the borders of the target district, country or region are porous, exclusion measures tend to be ineffective. Quarantine measures can be re-enforced with bye-laws and other policy innovations but this would also require appropriate institutional frameworks such as task force formation/ implementation and associated resource commitments to make them work. 3 Evaluation of the Xanthomonas wilt management guide

The draft Diagnostic and Management Guide is targeted on researchers, the extension teams, local councils, NGOs and CBOs involved in the training of trainers at the regional and national levels. This is the cadre of practitioners involved in on-farm planning and execution of management strategies for the control of Xanthomonas wilt (Xw) of bananas. Subsequently the guide was used as a basis for the development national level wilt control/ management strategies, such as training tools in different local languages. It was therefore necessary to establish its effectiveness both at the technical and farm level. At the technical level the trainers of trainers were targeted for the easiness with which the various components of the guide lent themselves to the training objectives at various (tier) levels. At the farm level, the guide was evaluated on the competences attained by farmers with respect to Xw disease recognition, mechanisms of spread and control.

3.1 Evaluation methods

3.1.1 Trainers of trainers’ evaluation The exercise was carried out in a workshop attended by the C3P country project managers, national research institute researchers, extension managers/officers, university lecturers), and NGOs. The team was facilitated to agree on the basic Xw management practices which were divided into four categories-

48 Evaluation of the Xanthomonas wilt management guide 49

1. Capacity building and public awareness 2. Diagnosis/symptoms 3. Control of the disease 4. Institutional mechanisms The team then discussed and agreed on the criteria along with associated scoring system for each criterion as follows:

3.1.2 Scoring the criteria

A 1. Probability of success (High =1; Medium=3, Low = 5) B 1. Cost of delivering the practice/tools (Low =1; Medium=3; High = 5) 2. Local availability of associated tools/equipment. (Readily available = 1; Easy = 3; Difficult to obtain = 5) 3. Personal safety of participants. (Quite safe =1; Low risk = 3; High risk = 5) 4. Existing experiences in target beneficiaries (Plenty of experience =1; Some experience = 3) No experience = 5) 5. Applicability under a broad range of agro-ecologies (Readily applicable =1; Limited areas =3 ; to specific areas = 5) C 1. Time taken to realize changes (Very short =1; Medium =3; Very long = 5) D 1. Beneficial to the environment (Very friendly = 1; Friendly under some conditions=3; Not friendly = 5) 2. Harmful to the environment (Indirectly = 1; Neutral=3; Directly = 5) E. 1. Sustainability of practices 3.2 Results and discussion Most practitioners found the guide was easy to use with respect to de-budding, diagnosis of symptoms and the destruction of infected plant and planting material (Table 4a). Conversely they found that 50 Xanthomonas Wilt of Bananas in East and Central Africa using the tool, it was not possible to confirm the disease through application of molecular tools; develop and enforce bye-laws; formulate action plans or develop frameworks for accessing clean planting materials at farm level. However, most people thought the guide was useful in forming task forces and in establishing monitoring and evaluation activities. With respect to the activities targeting the mobilization of stakeholders (Table 4b), the practitioners thought the guide was most helpful in developing brochures, posters, pamphlets and leaflets for farmers and extension. Equally important was the radio / television talk shows and the use of farmer exchange visits. They thought however that the guide could not be used in certificate training. In general, all the tactics in this category have cross- cutting effects, being broad spectrum in their effects and hence must be used in combination with bio-cultural control options to get good results.

Table 4a: Percentage number of farmers who found the guide easy to use with respect to Xw management practices.

Practice Percentage of farmers De-budding 73 Disinfection of tools (using Jik or fire) 62 Destruction of diseased plants 60 Clean planting materials 52

Table 4b: Percentage of farmers who found the guide useful in targeting tactics for mobilizing stakeholders (awareness creation and capacity building) for the management of Xw

Practice Percentage of farmers Task Forces formation 58 Mobilization of stakeholders 63 Formulation of Action plans 58 Enforcement of by-laws 56 Monitoring , supervision and 59 Evaluation Evaluation of the Xanthomonas wilt management guide 51

3.3 Conclusion The guide has strengths and weaknesses with respect to the planning and execution of a Xw management programme. It should however be understood that no single management option is enough to effectively control the disease. Both biocultural practices and institutional mechanisms must be applied at the same time because they re-enforce one another. Like the disease, the ease of application will have to be monitored closely to obtain lessons learnt by the practitioners and this will be the basis for improving the tool. References

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communication. In: Saddler, G., Elphinstone, J. and Smith, J. (eds) Programmeme and Abstract Book of the 4th International Bacterial Wilt Symposium, 17th-20th July 2006, The Lakeland Conference Centre, Central Science laboratory, York, UK, p. 64. Ndungo, V., Bakelana, K., Eden-Green, S., and Blomme, G. (2004). An outbreak of banana Xanthomonas wilt (Xanthomonas campestris pv. musacearum) in the Democratic Republic of Congo. Infomusa 13(2), 43-44. Ndungo, V., Eden-Green, S., Blomme, G., Crozier, J. and Smith, J. (2006). Presence of banana xanthomonas wilt (Xanthomonas campestris pv. musacearum) in the Democratic Republic of Congo (DRC). Plant Pathology 55, 294. Price, N.S. (1995). Banana morphology part i: roots and rhizomes. In: S. Gowen (editor): Bananas and plantains pp 179-189. Chapman and Hall, London. Smith, J. J., Jones D. R., Karamura E., Blomme, G., and Turyagyenda, F. L. (2007). An analysis of the risk from Xanthomonas campestris pv. musacearum to banana cultivation in Eastern, Central and Southern Africa, PROMUSA Monograph, 23p. Ssekiwoko, F., Turyagyenda, L.F., Mukasa, H., Eden-Green, S. and Blomme G. (2006). Systemicity of Xanthomonas campestris pv. musacearum (Xcm) in flower-infected banana plants. In: Saddler, G., Elphinstone, J. and Smith, J. (eds) Programmeme and Abstract Book of the 4th International Bacterial Wilt Sym- posium, 17th-20th July 2006, The Lakeland Conference Centre, Central Science laboratory, York, UK, p. 61. Tindall, B., Kampfer, P., Euzeby, J.P. and Oren, A. (2006). Valid publications of names of prokaryotes according to the rules of nomenclature: past history and current practice. International Journal of Systematic and Evolutionary Microbiology, 56 2715-2720. Tinzaara, W., Gold, C.S., Ssekiwoko, F., Tushemereirwe, W .,Bandyo- padhyay. R., Abera, A. and Eden-Green, S.J. (2006). The pos- sible role of insects in the transmission of banana Xanthomonas wilt. African Crop Science Journal, 14:105-110. Tothill, J. D (Editor) (1940). Agriculture in Uganda. Oxford Univer- sity Press, Oxford 56 Xanthomonas Wilt of Bananas in East and Central Africa

Turyagyenda, L.F., Blomme, G., Ssekiwoko, F., Mukasa, H. and Eden-Green S.J. (2006). On-farm assessment of banana bacterial wilt control options. In: Saddler, G., Elphinstone, J. and Smith, J. (eds) Programmeme and Abstract Book of the 4th International Bacterial Wilt Symposium, 17th-20th July 2006, The Lakeland Conference Centre, Central Science laboratory, York, UK, p. 58. Young, J.M., Bull, C.T., De Boer, S.H., Firrao, G., Garden, L., Saddler, G.E., Stead, D.E. and Takikawa, Y. (2001). Committee on the taxonomy of plant pathogen bacteria: International standards for naming pathovars of phytopathogenic bacteria. http:// www.isppweb.org/about_tppb_naming.asp Plates

Plate 1.1 Cultivar diversity in East and Central Africa Plate 1.2 Pests and diseases of bananas in East and Central Africa Plate 2.1a Distribution and spread of Xanthomonas wilt in C3P districts of Uganda Plate 2.1b Distribution and spread of Xanthomonas wilt of bananas in DR Congo Plate 2.1c Distribution and spread of Xanthomonas wilt of bananas in Rwanda Plate 2.1d Distribution and spread of Xanthomonas wilt of bananas in Tanzania Plate 2.1e Distribution and spread of Xanthomonas wilt of bananas in Kenya Plate 2.2a Xanthomonas wilt leaf symptoms Plate 2.2b Fusarium wilt leaf symptoms Plate 2.2c Male bud symptoms Plate 2.2d Fruit symptoms Plate 2.2e Pseudostem symptoms Plate 2.3a Canna Lily Plate 2.3b Heliconia Plate 2.3c Birds of paradise Plate 2.4 Stages of male-bud infection Plate 2.4b Male buds used as cokes for water plastic containers Plate 2.5 Plantlet dying after planting in infected soil Plate 2.6 Going public on market day Plate 2.7a Kayinja-based cropping system Plate 2.7b Highland banana-based cropping system

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Plate 2.8 Debudding using a forked stick Plate 2.9a Disinfecting tools with “Jik” Plate 2.9b Disinfecting tools with fire Plate 2.10 Persistent neuter flowers and male-bud bracts List of Acronyms

ADP Area Development Programme ASARECA Association for Strengthening Agricultural Research in Eastern and Central Africa ASC Advisory Steering Committee BARNESA Banana Research Network for Eastern and Southern Africa C3P Crop Crisis Control Project CARITAS Network of Catholic Charitable Organizations working under CBOs Community Based Organizations CBT Community Based Trainers CRS Catholic Relief Services Diocesan and Catholic Conference mandate DRC Democratic Republic of Congo ECA East and Central Africa FFS Farmer Field Schools GIS Geographic Information System IITA International Institute of Tropical Agriculture INERA Institut National pour l’Etude et la Recherche Agronomique INIBAP International Network for the Improvement of Banana and Plantain (now Bioversity International) IRAZ Institut de Recherche Agronomique et Zootechnique ISABU Institut des Sciences Agronomiques du Burundi ISAR Institut des Sciences Agronomiques du Rwanda KARI Kenya Agricultural Research Institute KEPHIS Kenya Plant Health Inspection Services

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ICT Information and Communication Technologies IPM Intergrated Pest Management MINAGRI Ministry of Agriculture (Rwanda) MoA Ministry of Agriculture NAADS National Agricultural Advisory Services (Uganda) NARO National Agricultural Research Organization (Uganda) NARS National Agricultural Research Systems NBRP National Banana Research Programme (Uganda) NGOs Non Governmental Organizations NRM Natural Resources Management USAID United States Agency for International development Xw Xanthomonas wilt