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Banana bunchy top disease (BBTD) is a viral disease of bananas and plantains (Musa spp.; hereafter, banana) caused by the banana bunchy top virus (BBTV) (Kumar et al., 2015; Qazi, 2016; Thomas, 2018). BBTD ranks among the top 100 invasive species in the world (Global Invasive Species Database, 2023). In Africa, BBTD was first observed in Egypt in 1900 (Magee, 1927). A second independent introduction happened in the late 1940s or early 1950s at the National Institute for Agronomic Study of the Belgian Congo Yangambi research station in the Democratic Republic of Congo (DR Congo) (Blomme et al., 2013; Wardlaw, 1961). By 1987, the disease was widely spread in the DR Congo, present in Burundi and Rwanda located in the east and central African regions. More recently, BBTD was confirmed in Uganda (Ocimati et al., 2021) and Tanzania (Shimwela et al., 2022), in the East African region.

Severe BBTV infection is characterized by stunted growth with distorted leaves having a bunchy and erect appearance in young plants, while bunches of mature plants fail to fill, as such fruits remain inedible (Magee, 1927; Niyongere et al., 2011). Banana productivity is severely affected, leading to significant yield and economic losses for farmers. The disease has been reported to cause significant yield losses of up to 100% (Caruana-Iskra, 2003; Kumar et al., 2015; Niyongere et al., 2011). In Australia, BBTD almost wiped out the banana industry between 1913 and 1920 (Magee, 1927), while in the 1990s, in Malawi, it reduced the banana production area from 3,500 ha to 800 ha (Soko et al., 2009).

In Uganda, bananas are a vital staple food for a significant proportion of the population, providing essential nutrients and contributing to food security. Uganda, with a daily per capita consumption of approximately 0.7 kg/person, ranks highest in the consumption of bananas in the world (Kilimo Trust, 2012). Additionally, bananas serve as an important source of income for smallholder farmers, supporting their livelihoods and fostering economic development in rural communities. Uganda, with a production of 9.2 to 9.4 million tons between 2019 and 2021 ranks fourth in the production of bananas and plantains combined globally and first in Africa (FAO, 2023; UBOS, 2020). The spread of BBTD into Uganda is thus a serious concern because it can cause significant economic losses and food insecurity, negatively impacting the livelihoods of smallholder farmers and other people depending on this crop along the banana value chain. Following the first report of the disease in the northwestern region of Uganda (Ocimati et al., 2021), further incursions have been confirmed in the Kasese district (Rwenzori subregion) bordering the DR Congo (Ocimati, unpublished results). In affected landscapes within Uganda, individual smallholder farms have reported up to 100% loss in yields and incomes (Ocimati, unpublished results).

The risk of BBTD spread to other banana production zones within Uganda remains high due to several factors including the lack of awareness on BBTD, its symptoms, epidemiology, and control; heavy reliance on suckers sourced from farmers’ own or neighboring farms for planting materials; lack of proper quarantine measures; and limited resources for implementing appropriate control measures. BBTV is known to spread through infected planting materials and via the aphid vector Pentalonia nigronervosa (Magee, 1927) that are omnipresent in all banana-growing regions. The ability of the disease to entrench itself within a landscape given deployment of proper management practices is dependent upon the opportunity for the survival of infective aphids to spread the virus, susceptibility of host plants, and efficiency in detection of infected plants before they become a source of inoculum. In addition to crop management practices, multiple environmental factors including temperature, altitude, precipitation, wind speed, and abundance of the host influence the vulnerability of landscapes to BBTD (Bouwmeester et al., 2023; Niyongere et al., 2013; Raymundo and Pangga, 2011).

In Uganda, management of the disease in currently infected landscapes and prevention of further spread into new production zones require a proper understanding of the vulnerability of the different banana production landscapes to disease introduction and/or establishment. Thus, mapping of the vulnerability of banana production landscapes to BBTD is an essential step toward developing targeted management strategies and implementing preventive measures. By identifying areas at higher risk of disease introduction and/or establishment, stakeholders can prioritize resources and interventions, thereby reducing the overall impact of BBTD on banana production systems. Moreover, mapping vulnerability will aid in decision-making processes, such as implementing disease surveillance programs, designing strategies for disease containment and eradication, and prioritization of limited resources.

This study highlights the findings of initial diagnostic studies conducted on sampled farms in the affected regions and provides a prediction of the risk/vulnerabilities of the different banana production landscapes in Uganda to the establishment and local spread of BBTD. The study utilized a combination of field diagnostic surveys and spatial analysis, to assess past distribution patterns and factors influencing the vulnerability of the banana ecosystem in Uganda to BBTD.

This study builds on the first report of BBTD in the West Nile region of Uganda (Ocimati et al., 2021). The study comprised i) field surveys in high-risk zones of Uganda, that either border or are close to the borders of the DR Congo, Rwanda, and Tanzania that are either hot spots or have reported cases of BBTD; and ii) mapping of the disease risk [introduction and spread] for the Ugandan banana-producing landscapes using statistical tools.

Bananas are an important food and income crop in Uganda with high production concentrations, respectively, in the southwestern, midwestern, and central regions of Uganda. Banana production in the country has been greatly constrained by Xanthomonas wilt of banana, a bacterial disease. The report of BBTD in the northwestern part of the country (Ocimati et al., 2021) and the mid-southwestern district of Kasese (Ocimati, unpublished results) puts more strain on the banana production systems. This study documents the potential spread factors of BBTD at the farm level, delimits the geographical spread of the disease, and maps the vulnerability of the production systems across Uganda, as a basis for proactive interventions to contain its spread.

The banana production systems were dominated by smallholders with a mean farm area of 0.4 ha. Natural capital such as access to land greatly influences the farmers’ decisions to adopt or dis-adopt innovations and may have implications on future efforts to manage BBTD. Deressa et al. (2009) and Langyintuo and Mulugetta (2008) associated larger farms with greater wealth and thus larger-scale farmers to have the means to adapt and the capacity to bear risks. Thus, most farmers in the studied regions could be constrained by resources to manage BBTD in case of an outbreak. Pagnani et al. (2021) observed that the farmers’ willingness to eradicate the banana bacterial disease was subject to the importance they attribute to bananas as a food and income crop, whereas the adoption of the full package may be too demanding for farmers who have extensive banana production.

The farms in the midwestern and central regions and much of northern Uganda are in low to mid altitudes which are suitable for aphid-vectored BBTV transmission (c.f. Supplementary Figure 1A ). High BBTV transmission efficiency and banana aphid survival have been reported at lower altitudes with warmer conditions (Niyongere et al., 2013). The high variability in altitude within the southwestern sites (c.f. Supplementary Figure 1A ) suggests the presence of niches that could still harbor the inoculum in case of disease introduction. The northwestern region that has been confirmed to have BBTD (Ocimati et al., 2021) had the youngest plantations. This region is traditionally a non-banana-growing area. Over the past decade, there has been an increasing interest in banana production in the region. The search for banana planting materials for new fields, with farmers going beyond their communities to other districts and even to neighboring DR Congo, makes this landscape vulnerable to new disease introductions and could partly explain the current introduction and rapid spread of BBTD in the region.

Intercropping though at differing levels of intensity dominated across the studied zones. This could benefit the landscapes through suppression of the BBTV aphid vector. Crop diversification through, e.g., intercrops promote the buildup of a high functionally diverse population of natural enemies, reducing pest densities (Estrada-Carmona et al., 2022; Greenop et al., 2020; Jaworski et al., 2023). High crop species diversity alters crop signals like leaf/stem color and volatile organic compounds necessary for pests to identify their host plants or host patches, reducing pest burden on crops (Cook et al., 2007; Doring and Kirchner, 2022). High levels of monocultures were observed in southwestern Uganda and could increase the risk of BBTD spread across these farms in case of disease introduction.

The presence of BBTD over a period of 0.5 to 4.4 years on at least 9% of the farms in the northwestern and mid-southern region suggests that the disease was within the landscapes for a long period of time before detection and official reporting. The fact that some farms had just observed the disease is evidence that the disease is actively spreading within landscapes. This coupled with the observed high yield losses (75% to 91%) highlights the need for urgent action to contain the disease. Symptoms were observed in diverse banana varieties and genotypes including the East African highland banana that are the most important and cultivated group in East Africa. Though the survey did not exhaustively observe all the banana varieties in the country, Ferreira et al. (1997), Niyongere et al. (2011), and Ngatat et al. (2017) reported all banana varieties to be susceptible, with susceptibility varying from one variety to another. Genotypes with A genomes are reported to be more susceptible, while those with at least one or two B genomes are more tolerant to BBTV (Hapsari and Masrum, 2012; Niyongere et al., 2011).

Farmers’ responses to diseases including BBTD were documented as a measure for their likelihood to adopt BBTD control measures. Cutting of single disease stems was common across the study sites. This can be attributed to the wide promotion of the practice for managing banana bacterial wilt disease, which is prevalent in the region (Blomme et al., 2014; Kikulwe et al., 2022; Ocimati et al., 2019). Rouging of entire banana mats, which is also an important IPDM component for managing BBTD, was common though more widely used in the southwestern region. Rouging is a cumbersome exercise and the fact that farms are already using it could suggest a possible positive response toward the practice for managing BBTD in affected landscapes. The northwestern region had over 60% of the farmers abandoning diseased plants or entire farms and would thus need more effort in terms of training, awareness creation, and motivation to manage the disease.

In line with earlier reports (Anhalt and Almeida, 2008; Bouwmeester et al., 2023; Niyongere et al., 2013), BBTD presence on farms was influenced by temperature variables, wind speed, precipitation variables, presence of the susceptible host, and NDVI (c.f. Figure 3 ).

Temperature affects the aphid vector biology and movement, virus spread and transmission efficiency, and the rate of disease symptom development (Allen, 1978; Anhalt and Almeida, 2008; Raymundo and Pangga, 2011; Robson et al., 2007). Temperatures between 25°C and 30°C have been reported to be ideal for aphid population buildup, declining with increasing or decreasing temperatures, respectively, above and below this optimum temperature range (Anhalt and Almeida, 2008; Robson et al., 2007; Wu and Su, 1990). For cereal aphids, low temperatures of approximately 14°C to 15°C (Walters and Dixon, 1984) and high temperatures of approximately 31°C (Robert, 1987) and above have been shown to inhibit or delay migration. Wu and Su (1990) reported no BBTV transmission at 16°C. Temperature variables also had a strong correlation to solar radiation that affects the BBTV aphid vector due to its effects through heat (see discussions on temperature above) and visible light. Slosser et al. (1992) reported a significant, negative correlation between solar radiation and the population of cotton aphids. Auclair (1967) observed a higher feeding and survival of cotton aphids under low light intensity, while Hoyt and Madsen (1960) observed the highest migration of the first instar nymphs of the woolly apple aphid in the late afternoon when there is less light. Solar radiation also influences the activity of natural enemies of the BBTV aphid vectors. For example, Elliott et al. (2012) reported an increase in the number of aphids predated upon per minute by adult convergent lady beetles, Hippodamia convergens with increasing intensity of solar radiation.

High precipitation, despite improving the suitability of the host to the BBTV aphid vectors, raindrops, and runoff water directly dislodge aphids off the plants, thus reducing their populations on plants (Kaakeh and Dutcher, 1993). Niyongere et al. (2013), for example, observed a higher aphid population in the dry season months. Thus, production zones with higher precipitation will have a lower buildup and BBTV spread relative to those with drier conditions. The increase of BBTD presence with precipitation in the driest months suggests that extreme dryness, which could be associated with high temperatures and desiccation, is detrimental to the aphids and the virus. This agrees with the findings of Anhalt and Almeida (2008); Robson et al. (2007), and Wu and Su (1990) who reported high temperatures above the optimal to deter aphid buildup. Thus, precipitation in dry periods moderates the environment making it suitable for the aphid and the virus.

The negative association of BBTD presence with wind speed could be attributed to the direct dislodgement of BBTV aphid vectors by wind. Previous studies, however, paint a mixed picture of the effect of wind on aphids. Singh et al. (1986) reported a negative effect of wind speed on the population of mustard aphid (Lipaphis erysimi). Devegili et al. (2019) observed wind to trigger the detachment of aphids and their movement toward the unexposed side of the stems; thus, a non-windy condition could expand aphid foraging and infestation rates. Thus, production zones exposed to higher wind speeds could experience lower rates of BBTD spread by banana aphids. In contrast, Singh et al. (2007) only reported a negative wind effect in the declining phase of aphid infestation. Barton (2014) reported wind speed to indirectly lead to an increased aphid density due to alteration of aphid predator behavior. Wind has also been reported to support the dispersal of the alate (winged) aphids over both short and long distances, though wind speeds higher than 8 km h⁻¹ delay or deter aphid migration (Haine, 1955).

As expected, disease presence was positively correlated to the banana production variable, i.e., banana presence in 2016. The high presence of the host plant creates a suitable environment for the BBTV aphid vector to thrive and thus a higher chance for BBTV spread. Normalized difference vegetation index had a strong negative correlation with BBTD presence. NDVI quantifies the health and density of vegetation and could reflect the role of a healthy and diverse vegetation in creating a suppressive landscape toward the aphid vector. This result, however, contrasts with the findings of Bouwmeester et al. (2023) who found a positive correlation between NDVI and BBTD presence. It is thus possible that the current BBTV infections occur in poorly managed production systems that reflect a lower NDVI score.

Unexpectedly, a weak negative correlation was observed with altitude (c.f. Figure 3 ), as altitude has been shown to negatively affect the aphid vector’s virus transmission efficiency and disease expression in banana plants. This can be attributed to the presence of BBTD-affected plants/mats at high-altitude locations of the northwestern region, possibly introduced through infected planting materials sourced from BBTD-affected farms and landscapes.

Only six covariates and the interaction between wind speed and LSTD had a significant (i.e., p < 0.05) contribution to the model for BBTD suitability. The effect of the five covariates in the model is generally consistent with the correlations. Isothermality quantifies the extent of day-to-night temperature oscillations relative to the annual temperature oscillations. Its negative association with BBTD presence can be attributed to its effect on the survival, life cycle, and feeding behavior of the BBTV aphid vector. For example, in comparison to constant temperature conditions, oscillating temperature conditions did not affect pea aphid populations under cooler temperature (20°C vs. 16°C/24°C) conditions, whereas smaller populations were produced under warmer (28°C vs. 24°C/32°C) conditions (Valls, 2018). In a separate study, Chen et al. (2013) observed that aphids under oscillating temperature conditions developed slowly with longer generation times despite having a higher net reproductive rate.

The LSTD had a strong and positive influence on BBTD presence. Uganda experiences moderate temperatures throughout the year, with monthly minimum air temperatures of 16.6°C to 18.1°C, monthly maximum of 28.0°C to 31.2°C, and monthly average air temperature varying between 22.3°C and 24.3°C. These temperature conditions are within the conducive range for the survival and spread of BBTV and its aphid vector (Wu and Su, 1990; Robson et al., 2007; Anhalt and Almeida, 2008). The significant negative effect of the interaction between wind speed and LSTD on BBTD presence (c.f. Table 2 ) can be attributed to the increase in temperatures with declining wind speeds, reducing the suitability of landscapes to the banana aphid and BBTV. An inverse relationship has been reported between wind speed and LSTD (Back et al., 2023).

Though altitude did not contribute to the final model, it is highly and negatively correlated to the temperature covariates including LSTD ( Figure 3 and Table 2 ). As explained above, BBTD was observed at high altitudes, possibly transmitted through the introduction of externally sourced infected planting materials. The weak negative association between BBTD and altitude could be suggestive of improvements in the suitability of the mid- to high-altitude landscapes for BBTV transmission by the aphid vector and virus within plant proliferation. This is supported by the fact that several studies have reported temperature increases of up to 1.5°C across most of Uganda, with characteristic rates of warming approximately 0.2°C per decade (Funk et al., 2012; Egeru et al., 2019). A more recent study in Burundi similarly reported BBTD-infected fields at higher altitudes of up to 2,000 masl (Nakato et al., 2023), whereas a decade ago, BBTD-infected mats were only observed up to 1,600 masl.

The BBTD risk map shows swaths of production zones in the northwestern and central Uganda to be suitable for the disease to establish itself. The low-lying production zones with higher temperatures along the River Nile and around Lake Victoria are highly prone to BBTD. Potential BBTD hot spots also exist in the western and southwestern districts that account for the highest banana production in Uganda. Bouwmeester et al. (2023) ranked these production zones of Uganda as highly prone and of high priority due to their adjacent location and high connectivity to eastern DR Congo, a large hot spot for BBTD, and their favorable climatic conditions for BBTD establishment and spread. The observed presence of potential hot spots in the southwestern region and BBTD at higher altitudes and the current trends in global warming also suggest that the higher production zones in the country, especially in the southwest, are increasingly vulnerable to this disease. Despite the lower transmission efficiency at high altitudes, the aphid vectors have been shown to acquire the virus at mid- and high-altitude areas with lower temperatures (Niyongere et al., 2013). Temperature increases of 1.8°C to 2.1°C between 1940 and 2069 and 2.2°C to 4.0°C by the end of the century under different representative concentration pathways have been projected for Uganda (Egeru et al., 2019). These projections suggest that the suitability of key Ugandan banana landscapes for BBTD establishment is likely to improve.

BBTD control has been reported to be extremely challenging once established due to the lack of easy environmentally and economically sound control measures and the omnipresence of the BBTV aphid vector in all banana production landscapes (Omondi et al., 2020). It is also difficult to detect the early stages of infection, especially when dealing with a large number of mats on farms. Given the high production zone connectivity within the country, overreliance on suckers as planting materials, and rising temperatures, the risk for disease spread to new production zones from the current locations in the north- and midwestern regions remains high. Proactive surveillance, quarantines, and safe and sustainable seed systems are thus urgently needed for protecting the currently BBTD-free production zones. Measures to eliminate or reduce the inoculum in the affected areas also need to be urgently rolled out.