Summary
Bananas (Musa spp.) are considered the most important fruit crop in Kenya, grown mostly by smallholder farmers. However, in the past two decades production has declined and has largely been attributed to plant pathogens, including plant-parasitic nematodes. To assess the understanding and awareness that banana farmers have of nematodes, a survey was conducted. The incidence, abundance and distribution of nematodes in relation to altitude were determined for different banana types on 180 farms and the pathogenicity of Pratylenchus goodeyi, originating from three different altitudinal locations, was compared on two banana cultivars. Just 2.3% of farmers were aware of nematode damage and symptoms, none of whom applied any management measures. The highest abundance of nematodes was recorded at an altitude range of 1601-2000 m a.s.l., with Pratylenchus, Meloidogyne and Helicotylenchus being the predominant genera. Across all altitudinal locations, cooking banana had higher densities of nematodes than dessert bananas. In pots, P. goodeyi populations from Embu (1300 m a.s.l.) appeared more aggressive and with higher levels of multiplication than the population from Oyugis (1100 m a.s.l.). Cooking banana (‘Ng’ombe’) was more susceptible than dessert banana (‘Sukari Ndizi’). Nematode damage is more prominent in areas at higher altitude and on cooking banana cultivars. The findings provide key information in guiding informed and suitable management decision thresholds in relation to potential climate change.
In East and Central Africa, bananas (Musa spp.) are an immensely important staple food crop, fruit crop and source of income for millions of people. In Kenya, bananas are the most important fruit crop, accounting for 35.6% of the total fruit production, and represent the top fruit income earner (Kneoma, 2018). Bananas are often grown across a range of environments, providing a cost-effective source of food energy year-round as well as an ideal infant food when other crops are off-season (Mbaka et al., 2008). Both dessert and cooking types are grown on an estimated 82 000 ha with a total production of 1.43 million MT (Kneoma, 2018). The most important areas of production include Meru (14%), Kirinyaga (12%), Embu (10%), Bungoma (8%), Taita Taveta (7%), Kisii (7%) and Murang’a (6%) (Ministry of Agriculture, Fisheries and Livestock, 2017). Production is mainly under smallholder conditions (Ng’ang’a et al., 2011).
The current rapid rate of population growth in Kenya, combined with evolving changes in food behaviour, provides an ideal opportunity for increasing banana production in the country. Despite showing great production potential, however, banana yields have declined significantly over the past two decades (FAO, 2015). This reduction has been attributed to increased incidence of pests and diseases, including plant-parasitic nematodes (Reddy et al., 2007), worsened by a lack of effective control strategies (Inzaule et al., 2005).
Globally, nematodes are reported as major pests of banana (Coyne & Kidane, 2018), causing yield losses of 30-60% (Kamira et al., 2013; Sikora et al., 2018). This yield reduction is especially notable in Africa, where nematodes may cause up to 50% loss in East African highland bananas (‘EAHB’) (Gaidashova et al., 2009; Coyne et al., 2018). In Kenya, a community of nematode species remains a threat to banana production, with Radopholus similis, Pratylenchus goodeyi and Helicotylenchus multicinctus reported as the main pathogenic nematodes affecting Musa spp. (Gichure & Ondieki, 1977; Inzaule et al., 2005; Reddy et al., 2007; Waweru et al., 2014). When nematodes attack roots they create tissue damage, exposing the roots to secondary infections from fungal, bacterial and viral pathogens (Okafor et al., 2015; Smiley, 2015). Damaged roots are also less able to access adequate water and nutrients (Risède et al., 2010), suppressing plant growth, lengthening the fruiting period, reducing bunch weight and shortening the production life of mats (Wachira et al., 2013). Due to poor anchorage from damaged root systems, fruit-bearing plants may easily topple, especially during storms and strong winds (Coyne & Kidane, 2018).
Crop productivity is heavily influenced by climate, which also strongly affects pest and disease infestation (Das et al., 2011). Historical records demonstrate an increase in global temperatures since the late 19th century (Kirtman et al., 2014) with Africa identified as probably the most vulnerable continent to climate change and climate variability (Niang et al., 2014). Consequently, changing climates will enable pests and diseases to colonise new localities and to survive outside their historic ranges (Harvell et al., 2002), including nematodes (Talwana et al., 2015; Erima et al., 2017).
Traditionally, some species of nematodes infecting banana have been distributed through a conspicuous temperature gradient, such as R. similis, which is traditionally found at lower altitudes with warmer temperatures (Blomme et al., 2012), while P. goodeyi traditionally occurs at higher altitudes where temperatures are cooler (Kashaija et al., 1994; Luambano et al., 2018). It is worth noting that these two species have different damage potentials as they present different levels of aggressiveness, with R. similis reported to be more damaging than P. goodeyi (Price, 2006; Plowright et al., 2013). Given that banana responds poorly to climate change, in relation to impacts on food and nutritional security assessments, the quantification of the climatic conditions for banana production is of particular importance to assess banana’s climate sensitivity and, thereafter, to predict the potential impacts of climate change on banana production systems (Varma & Bebber, 2019).
Owing to the shift in temperatures (King’uyu et al., 2000) along the altitudinal gradient linked to climate change in the East African Highlands, it is possible that the distribution of R. similis to higher altitudes, overlapping with P. goodeyi, will detrimentally impact ‘EAHB’ productivity (Coyne et al., 2018). To determine the incidence, abundance and distribution of nematodes at different altitudes on bananas in Kenya, both cooking and dessert type bananas were assessed for nematodes in key banana-growing localities. The differential pathogenicity of three populations of P. goodeyi recovered from three different altitudinal zones was also assessed.
Materials and methods
Field sampling in mid (1100-1600 m a.s.l.) and high (1601-2000 m a.s.l.) altitude areas
Banana farms from 12 major banana-producing areas of Kenya were sampled in Kisii (1100-1600 m a.s.l.), Migori (1100-1600 m a.s.l.), Homabay (1100-1600 m a.s.l.), Kakamega (1601-2000 m a.s.l.), Embu (1100-1600 m a.s.l.), Meru (1601-2000 m a.s.l.), Kiambu (1601-2000 m a.s.l.), Murang’a (1601-2000 m a.s.l.), Kirinyaga (1100-1600 m a.s.l.), Nyeri (1601-2000 m a.s.l.), Busia (1100-1600 m a.s.l.) and Bungoma (1601-2000 m a.s.l.) between November 2018 and July 2019 (Fig. 1). In each area, 15 distant farms were selected for sampling, resulting in a total of 180 sampled farms. In each farm, soil and roots were collected from two banana types: ‘EAHB’ (cooking type) and ‘Cavendish’ (dessert type), from a hole measuring 20 × 20 × 20 cm dug using a spade ca 1 m from the banana plant/mat. Five functional roots measuring ca 10 cm each were also sliced longitudinally to assess percentage root damage using the Root Necrosis Index (RNI) according to Speijer & De Waele (1997) and Coyne et al. (2014). The geographical coordinates and altitude were recorded for each farm.
Awareness of plant-parasitic nematodes on bananas and nematode evaluation
The study assessed farmers’ knowledge levels and perceptions of nematodes as pests affecting banana production. This was executed through a structured questionnaire with each of the 180 selected farmers.
Extraction and processing of plant-parasitic nematodes
In the laboratory, banana roots were washed, blotted dry on tissue paper, then chopped to ca 1 cm length pieces. Nematodes were extracted from 5 g roots and 100 cm3 of soil for 48 h, using the modified Baermann technique (Coyne et al., 2014). Nematodes were counted and examined under a Leica MZ12 dissecting microscope with under-stage lighting at ×20 magnification. Nematodes were killed using the hot water bath method at 65°C (Roy et al., 2014) and fixed in 4% formalin (Coyne et al., 2014) to facilitate identification. Nematodes were identified to genus level using a Leica 2500 compound microscope at 40× magnification, based on morphological features described by Hooper et al. (2005). Photos were captured at 40× magnification.
Pathogenicity pot trial assessment
Data analysis
Data from questionnaires were coded and analysed using Statistical Package for Social Sciences (SPSS) version 16.0. The nematode count data were transformed by
Results
Awareness by farmers of plant-parasitic nematodes on bananas
The majority of the farmers growing bananas (97.8%) did not know that nematodes are pests of bananas, with just 2.2% of farmers being aware. None of the interviewed farmers was aware that their banana fields were infested and damaged by nematodes, even though some (2%) were familiar with bananas toppling over but were unaware of the cause. The majority (98%) of farmers had not noticed bananas toppling in their farms.
Effect of altitude and banana type on root damage
Root necrosis was greater (
Occurrence of plant-parasitic nematode genera
Fourteen nematode genera belonging to eight families in the orders Tylenchida, Dorylaimida and Triplonchida were found associated with banana (Table 1). Pratylenchus goodeyi was the most commonly recovered (66.1%) species followed by H. multicinctus (16.3%) and Meloidogyne spp. (8.9%), while R. similis (0.3%) was rarely observed (Table 2). These nematodes were recovered from both soil and roots across altitudinal ranges and in both ‘EAHB’ and ‘Cavendish’ bananas (Figs 2, 3). On the effect of altitude on plant-parasitic nematode density, cooking banana showed greater densities (
Distribution of plant-parasitic nematodes across banana production areas in Kenya
Greater densities (
Effect of banana type on plant-parasitic nematode density
‘EAHB’ supported higher (
Effect of Pratylenchus goodeyi populations on banana root damage
The percentage root necrosis following inoculation with the three populations of P. goodeyi did not differ (
Effect of banana cultivar and trial site on Pratylenchus goodeyi population density
Across the two trial sites, the mean density of P. goodeyi was 346 (5 g root)−1 for Nairobi and 266 (5 g root)−1 for Kisii, although there was no significant difference (
Reproductive factor of three Pratylenchus goodeyi populations across two trial sites
From the two trial sites, the RF was similar for the three P. goodeyi populations in Kisii, compared with Nairobi (
Correlation between Pratylenchus goodeyi densities in banana roots and root damage
A positive (
Discussion
The current study shows clearly that P. goodeyi is the most prominent nematode at higher altitude areas (>1600 m a.s.l.) of Kenya, compared to its occurrence in mid altitude areas (<1600 m a.s.l.), reflecting previous studies from across the region (Kashaija et al., 1994; Gaidashova et al., 2004; Reddy et al., 2007; Kamira et al., 2013). However, recent findings by Luambano et al. (2017) show that both P. goodeyi and P. coffeae occur at lower altitudes, such as on the islands of Zanzibar and across the Tanzanian coast. Luambano et al. (2018) further reported P. coffeae on banana in mainland Tanzania, where the nematode had previously not been reported. Therefore, Pratylenchus species, and in particular P. goodeyi (Mgonja et al., 2019), appear to be shifting from their ‘known’ distribution in East Africa to outside their traditional ranges. Previous studies have demonstrated an altitudinal demarcation for P. goodeyi distribution (Talwana et al., 2003; Gaidashova et al., 2009; Kamira et al., 2013), while the current study shows P. goodeyi occurring at lower altitudes in the mid altitude belt. Pratylenchus goodeyi was seldom observed in low altitudinal elevations in East Africa until recently when the nematode was encountered in Tanzania (Luambano et al., 2017), raising questions as to whether variations in ecotypes, which are more tolerant of higher temperatures, are developing (Coyne, 2009). Although P. goodeyi infection can affect banana root efficiency (Wang et al., 2009) and expose plants to secondary infections (Tanimola et al., 2013; Smiley, 2015) at high altitudes, it is yet to be determined how this impacts bananas at higher temperatures in lower altitudes.
From the current study, H. multicinctus was recovered from elevations above 1600 m a.s.l., unlike earlier reports (Kashaija et al., 1994; Gaidashova et al., 2004) where the nematode was observed in all sites below 1600 m a.s.l. but not above. This could relate to the mixed banana production systems observed in most of the farms surveyed. Helicotylenchus multicinctus is recognised as a key nematode constraint to Musa production, especially plantain in West Africa (Coyne, 2009) but also on ‘EAHB’ (Hartman et al., 2010). Comparatively, H. multicinctus is not viewed as being as aggressive as R. similis, but where it occurs in high populations it can cause severe root damage (Tanimola et al., 2013).
Meloidogyne spp. was widely distributed in both mid and high altitude areas (<1600 m a.s.l.) in low densities. Although Meloidogyne spp. have been similarly encountered in mid altitude areas in the region (Kamira et al., 2013), the nematodes have not regularly been encountered at high altitudes but are more prevalent at lower altitudes (<1400 m a.s.l.) (Kashaija et al., 1994; Talwana et al., 2003; Reddy et al., 2007). Whilst studies have shown that Meloidogyne spp. can affect bunch weight (Van den Bergh et al., 2000) and cause root galling (Coyne et al., 2014), Meloidogyne spp. are generally not considered a major pest of bananas in East Africa (Tanimola et al., 2013).
Interestingly, R. similis, a damaging species and prevalent elsewhere in the region, was rarely detected in the current study, further supporting observations by Reddy et al. (2007) who observed it infrequently. This observation could be ascribed to the increasing use and popularity of tissue culture plants in Kenya, which would limit the spread of R. similis as the distribution of this species results mainly from the dissemination of infected banana planting materials (Price, 2006; Blomme et al., 2012). Radopholus similis has also traditionally been found at altitudes below 1400 m a.s.l. (Kashaija et al., 1994; Gaidashova et al., 2004; Reddy et al., 2007) where temperatures are higher, although in the current study the nematode was detected only infrequently across all survey sites.
The current study identified more species of nematodes on cooking banana than on dessert bananas, with high densities of the dominant P. goodeyi observed on ‘EAHB’ compared to ‘Cavendish’, confirming earlier findings (Reddy et al., 2007), where more lesion nematodes were observed on ‘EAHB’ in most Kenyan districts surveyed. This observation could be explained in part by the endemic and dominant cultivation of ‘EAHB’ in the cooler highlands (Karamura et al., 1998), as opposed to lowland areas (Gaidashova et al., 2004).
In the pathogenicity study of P. goodeyi populations, the higher densities of P. goodeyi from the Nairobi trial (1600 m a.s.l.), compared to that of Kisii (1300 m a.s.l.), could be due in part to the existence of an inherent degree of variability in aggression and infectivity between temperatures and within the pathogen biology (Talwana et al., 2003). This current observation of P. goodeyi at altitudes of 1300 m a.s.l. indicates that the temperature range of the nematode is shifting, as it is now occurring in areas at lower altitudes where it has previously not been reported (Luambano et al., 2017; Mgonja et al., 2019), challenging observations that the nematode is confined to higher altitudinal ranges above 1500 m a.s.l. (Kamira et al., 2013). The higher root necrosis observed in Nairobi compared with Kisii may be related to the higher average altitude of Nairobi (>1600 m a.s.l.) compared to Kisii (<1300 m a.s.l.). Greater nematode densities and RF was recorded from ‘Ng’ombe’ but, interestingly, with lower root damage, while ‘Sukali Ndizi’ had lower nematode densities and RF but greater root damage. Although root damage varied across sites on both cultivars, ‘Sukali Ndizi’ would appear to be less tolerant of P. goodeyi than ‘Ng’ombe’. These observations reflect the views of Marin et al. (2009) that reproductive fitness of the nematode and the amount of root damage caused on the host may not always be related, suggesting that these attributes could be under the control of different genes (Shaner et al., 1992). In the current study, it was noted that a demonstrable degree of variability in nematode aggressiveness exists and that infection levels vary between temperatures within sites and among the three P. goodeyi populations. This damage could be influenced by factors such as plant cultivar or climate (Gauggel et al., 2005), confirming reports by Talwana et al. (2003). The future of banana production in the region, therefore, would benefit from the long-term development of management thresholds to cope with these changing threats.
The variability of root necrosis among the three P. goodeyi populations observed across sites mirrors those found by Speijer & De Waele (1997) and Nega & Fetena (2015), who observed that overall nematode damage levels displayed large variability among different sites in Uganda and Ethiopia. This observation suggests that in rolling out breeding programmes for nematode resistance, banana cultivars that maintain a strong root system when infected with high nematode densities provide a good source of nematode management (Barekye et al., 2000). Comparatively, the Embu population isolated from a temperature of 20°C had a significantly greater RF than the Nairobi (24°C) or Oyugis (26°C) populations. While these observations typify the multiplication indices of plant-parasitic nematodes at higher temperatures (Talwana et al., 2003; Coyne et al., 2014; Wu et al., 2014), they contradict the thermophobic character of P. goodeyi. Further, the results from the current study indicate that P. goodeyi is adapted to a wide range of temperatures despite showing thermal sensitivity in aggressiveness. The current findings indicate that P. goodeyi is spreading geographically, regardless of climatic conditions or altitudinal elevation (Coyne et al., 2018; Mgonja et al., 2020).
The current study has demonstrated that the vast majority of banana growers in Kenya are not aware of nematodes as pests infecting their bananas. These findings confirm other studies (Brooks, 2004; Wang & Hooks, 2009; Chitamba et al., 2016), where most growers are unaware of nematodes as a major cause of Musa production problems and have only limited knowledge of banana nematodes as a pest. In addressing the nematode challenge, therefore, there is a need to raise farmers’ awareness and promote the use of healthy, nematode-free planting materials (Coyne, 2009).
Corresponding author, e-mail: d.coyne@cgiar.org
Acknowledgements
The authors gratefully acknowledge the financial support from the donors who supported this work through their contributions to the CGIAR Fund (https://www.cgiar.org/funders/) and in particular to the CGIAR Research Program for Roots, Tubers and Bananas (CRP-RTB), and also the ‘GCE Phase II: Neuropeptide Nematicides’ project opportunity ID: OPP1130274, led by Queens University, Belfast, and by the European Union project: Microbial Uptakes for Sustainable management of major banana pests and diseases, Grant Agreement 727624.
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