spp.) was ranked the world’s sixth in production in 2017 (FAO data), with an annual production of about 144.6 million Mg [1
]. Less than 10% of the global annual production enters the commercial market, indicating that the crop is more important for local consumption than for export [2
]. The East African Highlands and the Great Lakes region—Burundi, Kenya, Rwanda, Western Tanzania, Uganda, the Democratic Republic of Congo and the Republic of Congo—are zones of secondary diversity for bananas, with a large number of locally adapted AAA-EA groups of cultivars and landraces for various uses including cooking, dessert, plantain, and multiple use types [4
]. Genetic diversity is important for cropping system resilience and sustainability. It enables farmers and plant breeders to adapt to diverse and changing environmental conditions and to provide genes for breeding for disease tolerance [6
In Burundi, a higher diversity is recorded for beer and cooking banana types compared to dessert and plantain types [7
]. Most of these varieties arise from the AAA-EA genome subgroup through clonal variation and farmer selection and are shared locally through informal seed systems. Although not yet contributing significantly to the global banana breeding gene pool, the genetic diversity of banana in Burundi is interesting in its richness, incomplete documentation, and potential as a source of genetic traits for breeding adaptable bananas for production resilience in changing environmental conditions such water availability, dwindling soil fertility, pests, and diseases. It therefore presents an excellent model for studying such phenomena in seed systems, especially of vegetative propagated crops, which are little included in regulatory frameworks. With the increased regulation of seeds, this system would be invaluable in assessing the interphase between the formal and informal seed system and the framework for evaluating the consequences of seed degeneration in formal and informal interphases [8
]. The conservation of this existing diversity in this area is important to service a diversity of current needs and to mitigate potential future biotic and environmental challenges or to meet social and economic needs [9
It is the informal seed system that ensures the conservation and the distribution of locally adapted varieties with farmer-desired characteristics for many vegetatively propagated crops. Through their networks, farmers multiply and share their preferred varieties including those with traits not produced by formal breeding, such as tolerance of characteristic local stress, or particular organoleptic qualities [6
]. Acceptable genotypes from formal breeding also enter the informal seed system networks once adopted. In addition, disease invasions present a powerful force of genetic selection favouring crop varieties that are tolerant, resistant, or evasive of infection. This is the case for the Banana Bunchy top disease (BBTD) invasion, which was especially important since small scale farms and informal seed systems were dominant in maintaining and sharing the rich diversity of East African Highland bananas (AAA-EAH group) and because no resistant genotypes are known. The management of such diseases creates room for the introduction of new varieties and trials with cultivars with hitherto non-valued benefits or constraints to the production and seed system on a local scale.
The introduction of Banana Bunchy Top Disease (BBTD) in Burundi in the late 1980s presented a significant, rapidly spreading constraint to local banana production [13
]. It is one of the most devastating diseases affecting bananas in the world [14
], which are among the top 100 of the world’s most important invasive alien species [16
]. BBTD is presently spreading in Africa and has been reported in at least 18 countries, with five having been invaded in the last ten years alone [17
]. Once introduced into an area through infected seed, it quickly establishes and spreads locally through the banana aphid, Pentalonia nigronervosa
(Homoptera; Aphididae), leading to a gradual collapse of production. It is especially severe because it attacks both the production capacity and clean seed systems of bananas [22
]. The early symptoms of BBTD are usually barely detectable, and often asymptomatic infections exist [25
]. By the time advanced symptoms begin to appear, a large number of plants are likely infected asymptomatically, leading to a lack of clean seeds [8
]. No BBTD-resistant cultivars are known [27
], although there is a wide range of susceptibility and symptom expression among Musa
]. The outbreak of BBTD may therefore affect the ability of the seed system to preserve, propagate and share existing genetic diversity [31
] if control measures are not applied.
The control of BBTD in Burundi has involved the double risk reduction strategy of eliminating affected banana mats, sources of infection and the use of tissue culture clean planting material. Although a level of recovery has been achieved in Burundi [19
], the persistence of parallel formal and informal seed systems meant that the introduced clean plants would eventually enter into informal seed exchange. It is yet unknown how these interactions have influenced farmer seed exchange and selection. The effect of the BBTD invasion on the seed system may also influence cultivar diversity. This assessment would require a comparison of the varieties on a disease frontier lying in the same agroecological zone, to account for local diversity existence. Since banana is a perennial crop with a low seed replacement rate, such a frontier study is complicated, but a comparison of disease-free and infected areas is more feasible. This study was, therefore, carried out to assess the effect of BBTD on banana seed systems, the disease sweep and recovery on cultivar diversity, and the interaction between formal and informal seed systems in distributing and conserving banana diversity in areas of high secondary diversity (e.g. AAA-EA in the great lakes region), as well as the potential of local seed systems in a high diversity region for the AAA-EA in the East African Highlands in Burundi. We sought to investigate the hypothesis that the effect of disease on seed diversity may be detected in seed selection practices, cultivar preference and seed dissemination channels of different varieties. Understanding this information would inform seed systems linked to such regions and offer a means of engaging vegetative propagated crop seed systems.
2. Materials and Methods
Three sites in Burundi were selected for the study. Two BBTD endemic in Collins of Cibitoke Province (Munyika and Gitebe) and one BBTD free zone in Gitega Province (Muremera) (Figure 1
). Gitebe is located in Mugina commune with an average altitude of 1375 m above sea level (a.s.l.), Munyika in Rugombo commune with an average of 900 m. a.s.l., and Muremera in Giheta commune with an average of 1800 m. a.s.l. Diversity and seed selection variables were compared between the three zones. Within the BBTD endemic area, farmers actively involved in BBTD control were also compared with those not participating but living in the same locality. This allowed for the investigation of BBTD-linked variables while controlling potential cross site differences.
Quantitative and qualitative data were collected using structured questionnaires (Supplementary Data
) in a household survey (n
= 120) and twelve focus group discussions (FGDs) with eight participants in each. For the household survey, 40 households were selected per site, targeting the principal banana manager for each household. In Cibitoke, the BBTD endemic region, half of participants were randomly selected from 130 banana growers who participated directly in a BBTD control project at the pilot sites, and the rest were selected from their neighbours who grow bananas but did not participate in the project. For the control site Gitega, participants were randomly selected from the banana growers. Structured questionnaires were used for the household survey. For the qualitative study, focus group discussions were used considering sex and age disaggregated groups. Age disaggregation grouped participants as 40 years old and below or above 40 at the time of the study. The FGD guide of open-ended questions was used, led by a facilitator of the same sex as the interviewees. Data and observations were recorded verbatim by a note taker in the same session.
Data were collected on the recall of diversity of bananas planted in 2006, 2010, and currently in 2016; the varieties desired for the next planting; seed usage and preference; seed sourcing standards; and criteria for seed acceptance or rejection linked to biotic stress. Data from focus group discussions were analysed by combining and interpreting the answers to each of the articulated questions [33
]. Data from the survey were analysed using Statistical Package for the Social Science (SPSS) version 20 [34
]. Descriptive statistics (percentages, frequencies and crosstabs) were performed to assess the trends in banana diversity and preference, the type of seeds used and desired, the sources of seeds used in 2016 and their corresponding source and access conditions, and the criteria and symptoms recognized while selecting planting material. The 4 square methods were used to assess changes in the prevalence of variety groups between 2006 and 2016. Univariate Analysis of Variance (UNIANOVA) was carried out to assess the average number of varieties grown by a farmer in 2006, 2010 and 2016; and the average number of planting material used in 2016. Differences between study areas and farmers’ categories were assessed using Pearson’s chi-square (χ2
) for categorical variables and an independent t-test for numerical variables.
Overall, this study revealed that the BBTD outbreak and control in Burundi was associated with changes in banana cultivar diversity, seed systems and seed selection standards. These changes involved the replacement of some varieties with others and a greater penetration of formal seeds in local plantings. Changes in seed selection indicators were observed and linked to a greater acceptance of formal seeds in BBTD areas compared with non-outbreak area. This study also reveals the susceptibility of the informal seed system to disease invasions. The seed-system-linked interventions weakened the informal seed sector creating a potentially unintended variety turnover. Thus, a lower inflow of these cultivars coupled with the removal of infected plants gradually diminishes their availability, leading to reduced overall diversity and an unintended variety turnover.
The invasion of BBTD created an opportunity for rapid cultivar turnover associated with both disease outbreak and management. Varietal susceptibility and resistance has been associated with such changes in other systems. For example, worldwide, Fusarium race 1 was responsible for the replacement of Gros Michel by Cavendish, though preferred to the commercial dessert banana. In Burundi, Kayinja (Pisang’ Awak) has been replaced by Yangambi Km5 as the principal beverage banana in the Great lakes region due to the Fusarium invasion. Although all banana varieties are assumed to be susceptible to BBTD, significant variation in disease susceptibility has been reported [30
]. In this study, reduction of the local East African Highland banana varieties was observed in the endemic area, which could contribute to the decline of provisioning, regulating, and cultural ecosystem services as reported before [35
]. A large number of these varieties exist in Burundi in not yet affected areas, principally maintained as perennial plantations with seed exchange occurring through the informal seed sharing system. These present an increased relative risk to BBTD due to minimal quality assurance and the general longevity of plantations. Indeed, although farmers recognized BBTD symptoms and mentioned considering them in seed selection, symptomatic seed selection misses asymptomatic plants in the incubation period, which is common in BBTD [8
]. Varietal changes could also arise due to the limited availability of diverse local cultivars in the tissue culture system and to the available varieties with other beneficial characteristics (e.g. high yield and adaptability) introduced during the disease mitigation projects. Typically, projects attempt to distribute preferred varieties, or comparable ones, in disease mitigation efforts, often leading to the unavailability of some preferred varieties, replacement with ‘comparable’ hybrids, or non-consideration of peripheral local cultivars. This replacement is a concern over the loss of germplasm diversity [6
]. Indeed, in this study, we observed both an introduction of different varieties (hybrids FHIAs and Pro-Vitamin A) but also an increased demand from local cultivars, where these varieties were most dominant.
Changes in the sourcing of seed, supply channels and standards were also observed in this study. An increase in the acceptance of tissue culture plantlets observed in BBTD endemic areas was related to them being perceived as disease free but also to their desirable high yielding varieties. Farmers in this area were also more likely to pay for planting materials. In contrast, the non-BBTD endemic area considered agronomic potential, varietal identity and observable symptoms as key selection qualities, although old plantations served as preferred sources of planting material. They were relatively more trusted as sources of adaptable planting materials, lower in cost and favoured for the potential to observe the garden and mother plant in seed selection. Interestingly, farmer demand for new planting varieties contrasted with their existing stand, demonstrating an ongoing desire for crop improvement. Farmers in the BBTD endemic region desired less available local varieties, citing organoleptic properties, adaptability and agronomic suitability in the local production system; while those in the non-endemic area desired hybrids citing reported high yield levels. This confirms the previous findings [37
]. Together, these observations show the dynamic considerations related to varieties and underline the possibility of seed-based interventions achieving unintended outcomes or collapsing altogether. For example, the trends of seed demand in BBTD areas might push farmers towards unconfirmed seed sources, increasing the risk of BBTD reinvasion.
We concluded that BBTD has triggered a reduction of diversity in the informal seed system and affected the potential of local seeds systems to produce clean planting material in BBTD endemic areas. It has influenced the farmers’ choice of banana varieties and the planting material type, motivating actors in the seeds systems to introduce improved varieties while revealing more preferred banana varieties per site. This information on specific variety demand should guide the choice of banana varieties to be introduced into these areas. To ensure the sustainability of banana diversity, it is necessary and urgent to identify and promote more tolerant, or BBTD-tolerant, varieties in infested areas while managing the disease before the reintroduction of susceptible varieties, which may quickly disappear again.