Vertical Distribution of Plant-Parasitic Nematodes in Sweet Potato

Sixteen nematode genera were observed across Central (16), Manyatta (13), and Nembure (12) regions of Embu. Two-way ANOVA indicated a significant variation in abundance of Psilenchus (P < 0.0001), Hemicycliophora (P = 0.01), and Hoplolaimus (P = 0.01) across the regions. A significant region × depth interaction was observed for Tylenchus (P = 0.01) (Table 1; Figs. 2 and 3). From the simple main effects analysis, it could be ascertained that there were lower populations of Tylenchus in Central region at 30 cm to 60 cm depth compared to Manyatta and Nembure. At 0 cm to 30 cm depth, the populations were higher in Central than in Nembure. For all the other nematode genera, there were no significant variations in the abundance at 0 cm to 30 cm and 30 cm to 60 cm depths. However, Helicotylenchus, Meloidogyne, and Scutellonema occurred in relatively high numbers at both depths in all the regions. Pearson’s phi coefficient of association showed that Scutellonema was significantly associated with 0 cm to 30 cm depth (r = 0.262; P = 0.017). Region and depth significantly influenced Shannon–Weaver (P = 0.04) and Simpson (P = 0.05) diversities (Table 1). Across all regions, Shannon–Weaver and Simpson diversity indices were higher at 0 cm to 30 cm depth (Table 2) while Pielou’s evenness was similar at both depths (J = 0.81 ± 0.02, 0–30 cm; J = 0.79 ± 0.02, 30–60 cm).

Figure 2

Figure 3

Diversity partitioning of genus richness, Shannon–Weaver, and Simpson diversities across the three regions, at 0 cm to 30 cm and 30 cm to 60 cm depths, indicated that β component contributed 61.9%, 35.6%, and 22.6% of γ diversity, respectively (Fig. 4). In the NMDS analysis, nematode community structure was not clearly differentiated at the two depths in all the regions and the average dissimilarity was 67.4% (Fig. 5; PERMANOVA, R² = 0.005, F = 0.44, P = 0.99; PERMDISP, F = 0.015, P = 0.90). The most influential genera that contributed to the NMDS structure were Helicotylenchus, Meloidogyne, Scutellonema, Tylenchus, and Pratylenchus. Across the three regions, there were significant differences in N, C, Mn, Zn, Na, and silt at 0 cm to 30 cm depth (Table 3). According to CoIA, there was significant covariation (RV = 0.13, P = 0.05; Monte Carlo test) between nematode genera and soil properties. The first and second axes accounted for 60.4% and 27.6% of the total variance, respectively. There were positive correlations between pH, Ca, Mg, and Scutellonema. Population density of Tylenchus was positively linked to N, C, silt, and Zn while Meloidogyne was associated with high Cu levels (Fig. 6).

Figure 4

Figure 5

Figure 6

Vertical distribution of PPN determines the effectiveness of control strategies (Ingham et al., 2000). Helicotylenchus, Meloidogyne, and Scutellonema occurred in relatively high numbers at 0 cm to 30 cm and 30 cm to 60 cm depths in all the regions but the abundance was not significantly different. However, Scutellonema showed a specific association with 0 cm to 30 cm depth. Similarities in nematode genera at the two depths were also depicted in the NMDS analysis. These nematodes have been previously reported in association with sweet potato in Kenya (Njuguna and Bridge, 1998). Lack of significant differences at the two soil depths may be due to the influence of crop growth stage on PPN population dynamics whereby similar numbers of nematodes may be present either in the soil or within the plant at a particular time (Sharma et al., 1992). Root density (Robinson et al., 2005) and architecture also influence the vertical distribution of PPN (Pudasaini et al., 2006, Wesemael and Moens, 2008). The population density of PPN within plant roots at 0 cm to 30 cm and 30 cm to 60 cm depths was not tested in the current study, and this avenue of study warrants further investigation. Based on soil conditions, the sweet potato root system may occur up to 2-m deep (Woolfe, 1992), which may explain the uniform distribution of most of the PPN genera within the soil profile (Fan-xiang et al., 2005). At depths below 40 cm, Rodriguez-Kabana and Robertson (1987) also observed constant distribution of Meloidogyne arenaria, which they attributed to light soil texture.

Contrary to our observations, Scutellonema and Helicotylenchus have been reported to decrease with depth in most crops. In a groundnut field, >95% of Scutellonema clathricaudatum were found at 0 cm to 30 cm (Sharma et al., 1992) while a higher population of Helicotylenchus was observed at 20 cm to 30 cm in a fallow field (Fan-xiang et al., 2005). Similarly, Araya and De Waele (2011) observed a decline in the number of Helicotylenchus at higher soil depths in a banana field. In the current study, population densities of Tylenchus were variable at both depths in the three regions, which is similar to observations reported elsewhere in the literature (Fan-xiang et al., 2005, Siddiqui, 2007). Meloidogyne species are considered the most economically damaging PPN in sweet potato and they cause 10% to 20% of yield losses (Koenning et al., 1999; Okechalu and Wonang, 2015). The losses resulting from RKN infestation may be variable depending on the nematode species (Overstreet, 2009). Root-knot nematodes also cause necrosis and predispose the storage roots to cracking, which reduces their market value (Lawrence et al. 1986). High population density of Helicotylenchus reduces the weight of tubers, roots, and shoot biomass (Lopez et al., 1981). Although Scutellonema (Njuguna and Bridge, 1998; Coyne et al., 2003) and Tylenchus (Haougui et al., 2011) are associated with sweet potato, there are limited studies on their effects on yield.

Effective control of PPN that were observed in this study will require that information on their vertical distribution is considered. This was demonstrated by Ingham et al. (2000), where Meloidogyne chitwoodi was not controlled by metam sodium, ethoprop, and oxamyl at 0 cm to 30 cm due to migration of the nematode from 120-cm depth to the upper soil layers. In a different study, solarization at 40-cm soil depth was more effective in controlling M. incognita eggs (Nico et al., 2003). Rodriguez-Kabana and Robertson (1987) also suggested that for control of M. arenaria, placement of fumigant nematicides that move upwards should be such that they cover the depth where the nematodes are most prevalent. Low-cost PPN management techniques in sweet potato would be preferred by smallholder farmers in Kenya. The optimal depth at which the treatments would have a higher efficacy against the PPN should be tested on a case-by-case basis.

Shannon and Simpson diversities were higher at 0 cm to 30 cm across Central, Manyatta, and Nembure regions with the a component having a higher contribution to γ diversity. Zheng et al. (2012) also observed a decrease in these indices at higher soil depths, which was corroborated by Zhong et al. (2015) in different cropping systems. Processes that shape PPN populations such as niche differentiation, competition, reproduction, r-k strategies, and feeding methods affect their diversity and influence their response to control agents (Pérez et al., 2000; Pudasaini et al., 2006). Effect of occurrence of multiple PPN on crop damage was demonstrated in sweet potato, whereby competition between M. incognita and R. reniformis during concomitant infection resulted in the dominance of one species (Thomas and Clark, 1983). Co-occurrence of multiple PPN in soil influences the damage that they cause in crops (Thomas and Clark, 1983) and hence the need to consider this aspect when choosing nematode control strategies.

Regional differences that were observed in diversity indices and PPN abundance may be explained by several factors including soil properties (Hoogen et al., 2019; Li et al., 2020). Soil properties are an important factor in shaping distribution of nematode communities at different spatial levels (Nguyen et al., 2020). In the present study, Scutellonema was positively correlated with pH, Ca, and Mg, while Tylenchus was positively correlated with N, C, silt, and Zn. The abundance of Meloidogyne was associated with high Cu levels, as previously observed by Krif et al. (2020). However, according to Noe (1985), Meloidogyne incognita prefers soil with low Cu concentration due to its toxicity. Association of Scutellonema with high pH and Mg was reported in Western Kenya (Kandji et al., 2001). Aït Hamza et al. (2018) reported a positive correlation between clay and Tylenchus, unlike what was observed in the present study. Texture is important in the movement of PPN in the soil profile (Wesemael and Moens, 2008), whereby motility is faster where the silt/clay content is low (Prot and Gundy, 1981).

Apart from soil properties, other factors such as season, crop type (Nguyen et al., 2020), tillage (Lenz and Eisenbeis, 2000), soil aggregates, interactions with other organisms (Liu et al., 2019), and density-and time-dependent factors (Eisenback, 1985), which were not considered in this study, may also contribute to differences in diversity of PPN at different depths. From our results, we find that PPN distributions for most genera were similar across the 0 cm to 30 cm and 30 cm to 60 cm depths. There is a possibility that the abundance of PPN observed in this study was higher at depths >60 cm, an inference that warrants further investigation before a definitive conclusion can be reached. Control of PPN in sweet potato using treatments that are applied at depths below 60 cm may not effectively eliminate a great proportion of the nematodes. Since the population dynamics of PPN in sweet potato fields may be affected by the aforementioned factors, bespoke integrated nematode management schemes in sweet potato cropping systems need to be designed.