The distribution and extent of parasitism of Cotesia flavipes Cameron (Hymenoptera: Braconidae) on stem borer species attacking maize and sorghum were assessed in three zones of northeastern Ethiopia. Cotesia flavipes was found to be the key larval parasitoid of cereal stem borer species in all areas surveyed. This parasitoid has been introduced into several African countries for the control of Chilo partellus in maize and sorghum, but it has never been released in Ethiopia. The survey results indicated that the distribution and extent of parasitism of Cot. flavipes followed the distribution and severity of its suitable host, C. partellus. A Cotesia flavipes parasitism rate of between 33% and 82% was recorded in sub-moist warm (lowland) AEZs of all zones. In contrast, a parasitism rate of less than 6% was recorded in moist, cool highland areas where Busseola fusca was the predominant species. Cotesia flavipes caused lower rate of parasitism on stem borers in maize (up to 72%) than that of sorghum (up to 82%) in the three zones. In summary, high rates of parasitism of Cot. flavipes were recorded in lowland areas where C. partellus was the dominant borer species and low rates of parasitism were recorded in highland areas where B. fusca was the predominant species. Cotesia flavipes caused the highest parasitism (82%) on C. partellus. This result verified that Cot. flavipes contributed to the reduction of C. partellus population in lowlands, regardless of the zone, and its rate of parasitism varied between crop stages, crop types, elevations, host, and host stages. Findings of this study have particularly relevant information on the contribution of Cot. flavipes to the population reduction of stem borers, time or stage of its occurrence in relation to host stages and crop stages, and its distribution in relation to the availability of a suitable host across each zone. In conclusion, this larval parasitoid plays an important role in reducing stem borer populations and can be used as one component of integrated stem borer management in northeastern Ethiopia.
Introduction
Lepidopteran stem borers, Busseola fusca Fuller (Lepidoptera: Noctuidae) and the exotic Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) are the most damaging field insect pests of maize and sorghum in East Africa.123 Cotesia flavipes Cameron (Hymenoptera: Braconidae), a gregarious koinobiont endoparasitoid of C. partellus larvae in Asia, was introduced into Kenya for a classical biological control program from Pakistan and later from India in 1991.4 It was first released in the coastal areas of Kenya in 1993 and readily established during the same season.5 Following the release of Cot. flavipes, the populations of C. partellus, C. orichalcociliellus, and S. calamistis declined by about 30%, with C. partellus particularly affected (more than 50%). Maize yield, on the other hand, increased by 10%.3,6 Parasitism in western Kenya, where it was not released purposely, was low when compared to the coast and eastern provinces, which was likely due to the presence of two unsuitable hosts, B. fusca and E. saccharina, both of which were considered as a sink for population growth.6 Following the success in Kenya, Cot. flavipes was released in east and southern Africa. Cotesia flavipes from the same laboratory colony in Kenya was released in Mozambique in 1996, followed by a release in Uganda and Somalia in 1997.4 In Uganda, Cot. flavipes was recovered with parasitism of 31% on C. partellus and 12% on B. fusca.7 The success of the introduced Cot. flavipes was demonstrated by its establishment and spread from the release points, increasing parasitism, and decrease in stem borer density by 70%.8 Another indication of success was the positive economic impact associated with the introduction.9,10
In Ethiopia, Cot. flavipes was recorded for the first time in 1999 by Emana et al, without being released.2 The source of Cot. flavipes population in Ethiopia is unknown but is most likely the source released by ICIPE in Somalia, Kenya, Tanzania and Uganda.2,11 Based on the molecular analysis results of Emana12 and Yossef et al,13 the Cot. flavipes population established in Ethiopia was closely related to the populations released against C. partellus in maize in other parts of Africa, which were themselves derived from the original population imported from Pakistan; its dispersal rate was estimated to be 200 km per year. Yossef14 showed that Cot. flavipes was recovered from Sesamia calamistis in the central sugarcane-producing region of Ethiopia. It caused up to 50% parasitism on C. partellus in sugarcane in the northeastern parts of the country.14 The relative importance of Cot. flavipes in the different AEZs will provide a basis for identifying future release sites and help aid population enhancing conservation measures. The objectives of this study therefore were to assess the distribution and extent of Cot. flavipes of stem borers on maize and sorghum in different agroecological zones (AEZ) of northeastern Ethiopia, under natural conditions.
Materials and Methods
Survey sites description
Field surveys were conducted in three zones of Amhara Regional State, northeastern Ethiopia (Fig. 1A). A total of six districts, two from each zone, were assessed. The six districts included in the study were Tehulederi (39°40'E and 11°19'N; 1680–2338 m) and Kalu (39°43'E and 11°6'N, 1492–2084 m) from South Wollo; Habru (39°39'E and 11°40'N; 1508–1889 m) and Gubalafto (39°31'E and 11°52'N; 1758–2044 m) from North Wollo and Dawa chefa (39°48'E and 10°51'N; 1419–1669 m) and Bati (39°59'E and 11°11'N; 1412–1657 m) from Oromia zones. Based on the agro-ecological zones (AEZs) classification, almost all zones experienced sub-moist warm (Kola ≤ 1,500 m), dry—warm to moist cool (Woinadega 1,500–2,500 m) and moist cool (Dega 2,500–3,500 m).15
Figure 1.
The relationship between mean percentage of larval parasitism and larval density per plant (N = 16) at booting (A) and at harvest (B) stages of sorghum in Tehulederi district.
Note: The 4 points in the graph showed the mean of 4 replications.
The annual rainfall, temperature (maximum and minimum), and relative humidity of each locality are presented in Table 1. All districts produce sorghum under rain-fed and maize under irrigation. The study areas experience bimodal rainfall, wherein the short rain period is from April to May and the long rain period from June to September. Most farmers prefer to plant late maturing sorghum cultivars using short rain as the cultivars are high yielding (>50 qt/ha). The early maturing cultivars are planted in the main rain period when the short rain fails to come on time. During this study, all fields were covered by late maturing local cultivar, namely Degalit. Therefore, all the samples were taken from this cultivar (in all districts).
Table 1.
Elevation (m), temperature (°C), relative humidity (%) and rainfall of each locality of the three zones of northeast Ethiopia in 2010.
Sampling procedures
Sampling procedures were followed the work of Emana et al2 and Georges et al.16 Three to four peasant associations (PAs) were selected in each district. PAs in transition agro ecological zones (one agro ecology to other) were included. In each selected PA, three to four well managed (weed free, well ploughed, thinned, fertilized, etc) zones were selected. The selected fields were not sprayed with any synthetic chemicals. The minimum size of each field was one hectare. Moreover, all fields were at seedling stages while selected. In each farm, five plots with a size of 3 m × 3 m were sampled in ‘Z’ fashion. Sorghum was sampled at two stages, booting, and harvesting. In addition samples were gathered from irrigated maize (local cultivar) only at harvesting stage. The samples for the different stages were taken from the same sorghum fields.
Larval parasitoid was identified using reports of different authors in the earlier molecular techniques and specimens.12,14 The same authors did molecular investigation to confirm whether the parasitoid recorded in Ethiopia is Cot. flavipes or not by running Polymerase Chain Reaction (PCR) of DNA fragments of Cot. flavipes collected from Ethiopia and other African and Asian countries.
The number of total larvae, parasitized larvae, and dead larvae were recorded from six randomly selected plants. Parasitized larvae were taken to laboratory for the emergence of adult wasps and parasitism rate determination. Geographical coordinates and elevations of each field were recorded using GPS (Garmin eTrex Venture HC GPS Receiver).
Data Analysis
Percent parasitism was calculated as:
The data were arranged in nested design and analyzed using SPSS Version 12 software. The significantly different means (≤0.05) were separated using Student-Newman-Keuls (SNK) multiple range test.17,18 To normalize the data, arcsine and square root transformations were used for percentage and count data, respectively. Correlations of different data were analyzed.
Results
Extent of Cot. flavipes parasitism in South Wollo zone
Tehulederi district
The proportions of B. fusca and C. partellus were 0%–16% and 84%–100% at 1680–1750 meters, 69%–92% and 8%–31% at 1960–1970 meters, and 65%–80% and 9%–35% in 1887–1911 meters, respectively (Table 1). Significantly high Cot. flavipes rates of parasitism were recorded in areas where C. partellus accounted for 8%–100% of the total stem borer population. Cot. flavipes was the most important larval parasitoids in lowland areas where C. partellus was predominant with a parasitism rate of 35%–62% compared to B. fusca in the predominated highland areas. The highest parasitism (62%) was recorded in elevations of 1680–1750 meters and >27 °C while the lowest (5%) was in the 2291–2338 meter range and 21.6 °C (Table 2). Levels of parasitism were higher at the harvesting than booting stage of sorghum and ranged between 5%–62% and 0%–45%, respectively. Because the third and the fourth instars came out at the booting and harvesting stages of the crops respectively, the later larval stages of the host, which is suitable to the parasitoid, were available at later stages of the crop. Higher rates of parasitism were recorded on sorghum (5%–62%) than maize (10%–35%) (Table 2). Percentage of parasitism and borer density had significantly positive relationships at the booting (R2 = 0.98, P = 0.045) and harvesting stages of sorghum (R2 = 0.95, P = 0.045).
Table 2.
Elevation (m), stem borers species composition (%) and natural parasitism rates of Cot. flavipes on maize and sorghum in South and North Wollo zones in 2010/11.
Kalu district
There were significant differences between elevations in rates of Cot. flavipes parasitism (Table 2). Significantly high parasitism (76%) was recorded at elevations of 1492–1527 meters, where C. partellus was the only borer species attacking sorghum and maize. Extents of Cot. flavipes parasitism reduced with the increase in elevation and thus parasitism rates of 19%–55%, 12%–37% and 3%–24% were recorded at elevation ranges of 1841–1857 meters, (25.6 °C), 1834–1842 meters (26.2 °C), and 1923–2084 meters (24.6 °C) respectively. In all elevations, a higher percentage of larval parasitism was recorded on sorghum at the harvesting (24%–76%) than at the booting stage (10%–48%). Higher rates of parasitism were recorded on sorghum (24%–76%) than maize (3%–42%) (Table 2).
A strong positive relationship between the borer density and Cot. flavipes parasitism was obtained both at the booting (R2 = 0.85, P = 0.048) and harvesting (R2 = 0.92, P = 0.023) stages of sorghum (Fig. 2).
Extent of Cot. flavipes parasitism in North Wollo zone
Habru district
C. partellus was the only stem borer species recorded at an elevation between 1508–1670 meters but B. fusca and C. partellus shared 51%–73% and 27%–49% at 1850–1889 meters, respectively (Table 2).
High rates of parasitism (34%–68%) were recorded in the lowland (1508–1670 meters, >28.8 °C) areas where C. partellus was the only borer species on both maize and sorghum (Tables 1). In contrast, low rates of parasitism (4%–39%) were recorded at 1850–1889 meters, with mean temperature of 26.5 °C where B. fusca was the dominant and accounting for 51%–72%. High rates of parasitism were recorded on stem borer larvae on both maize at harvesting and sorghum at different stages. Rates of parasitism were higher at harvesting (39%–68%) than at the booting (4%–49%) stage of sorghum. On the other hand, rates of parasitism were higher on sorghum (4%–68%) than on maize (21%–39%) in different elevations (Table 1). Generally, this study's results showed that the efficiency of Cot. flavipes was highly determined by distribution of its suitable host, host stages, elevations, and crop stages (Table 1).
Rate of Cot. flavipes parasitism and borers’ density had significantly positive relationships at booting (R2 = 0.99, P ≤ 0.0342) and harvesting (R2 = 0.97, P ≤ 0.0041) stage of sorghum, respectively (Fig. 3).
Gubalafto district
Busseola fusca was the dominant stem borer, sharing 69%–88% as compared to C. partellus which shared 12%–31% at elevations of 1856–2044 meters (Table 2). Rates of parasitism of Cot. flavipes on stem borer larvae were low in maize (5%–13%) and sorghum (2%–8%). Rates of parasitism were slightly higher at harvesting (4%–8%) than at booting (2%–4%) stage of sorghum. Rates of parasitism were higher on maize (5%–13%) than sorghum (2%–8%) (Table 1). Because of low population of C. partellus, rate of parasitism was low on both maize and sorghum in the district and the result depicted that the parasitism rate of Cot. flavipes was highly influenced by the distribution of its suitable hosts, host stages, elevation, and crop stages (Table 1). Cotesia flavipes and borers’ density had weak and negative relationships (R2 = 0.03, P = 0.412 and R2 = 0.003, P = 0.541) at booting and harvesting stage of sorghum, respectively (Fig. 4).
Extent of Cot. flavipes parasitism in Oromia zone
Dawachefa district
Chilo partellus is the predominant species, accounting for 100% of the total borer in all districts of the Oromia administrative zone with elevations less than 1670 meters and temperature greater than 29 °C (Table 3).
Table 3.
Elevation (m), stem borers species composition (%) and natural parasitism rates of Cot. flavipes on maize and sorghum in Oromia zone in 2010/11.
Stem borers larval parasitism ranged between 32%–63% on maize and 33%–75% on sorghum in the Dawachefa district. Parasitism rates increased through time and were higher at harvesting (60%–75%) compared to booting (33%–46%) stage of sorghum. Regarding crop types, rates of parasitism were higher on sorghum (33%–75%) than maize (32%–63%) (Table 3).
Parasitism rates and borer density had positive relationships at booting (R2 = 0.84, P = 0.058) and harvesting (R2 = 0.75, P = 0.1518) stages of sorghum (Fig. 5).
Bati district
C. partellus is the predominant species accounting for 100% in all localities of Bati district having an elevation less than 1670 meters and temperature greater than 28 °C (24).
In Bati district, larvae parasitism ranged from 55%–73% on maize and 45%–82% on sorghum. Rates of parasitism were higher at harvesting than at booting stage of sorghum, with a range of 45%–53% and 61%–82% at the respective stages. Regarding crop types, rates of parasitism were relatively higher on sorghum (45%–82%) than on maize (54%–73%) (Table 3). Of all the zones in which the study was carried out, the highest rate of parasitism (82%) was recorded in this district.
The percentage of parasitism and borer density had a significantly positive relationship at booting (R2 = 0.69, P = 0.04) and harvesting (R2 = 0.96, P = 0.02) stages of sorghum (Fig. 6).
Discussion
This research showed that the distribution and extent of parasitism of this parasitoid varied with agroecological zones and subsequently affected its major host, C. partellus. Moreover, C. partellus was a dominant species in lowlands (≤1750 meters) with high temperatures (28 °C–32 °C). Rates of parasitism were higher in lower elevated areas where C. partellus was the dominant species. In contrast, the rate of parasitism was lower in highlands (.1850 meters) where B. fusca was dominant. Other workers also reported that geographic distribution of these two species depends on elevation, with C. partellus being lowland and B. fusca a mid-altitude to highland species.1,19,20 Cugala et al21 described that rate of Cot. flavipes parasitism varied with agro ecology. Kfir et al22 also reported that Cot. flavipes dramatically reduced populations of stem borers in East Africa, although its impact and rate of parasitism varied from one agro-ecological zone to another because of availability of the suitable host, C. partellus. Tillman et al23 and Mendel et al24 reported that parasitization was affected by elevation—which is related to temperature and relative humidity—and host factors such as host stage and host quality. Additionally, low temperature (highland areas) could negatively affect the establishment of Cot. flavipes. Zhou et al25 showed that Cot. flavipes caused a 50% reduction in stem borer population in the warmer coastal region of Kenya (lowlands), but that the impact of the parasitoid was reduced in cooler climates (highlands). Low temperature (≤25 °C) affected the host development and age structure of C. partellus—in all likelihood younger and smaller host instars are available for a longer period in cooler climates than at higher temperatures (.27 °C).25 Growth and development, as well as host searching of Cot. flavipes, were highly influenced by altitude, which subsequently affected the temperature, relative humidity, and the host.5,8,26
In our study, higher parasitism rates (82%) were recorded than the earlier reports in Ethiopia (11%–73%),11,14,27,28 in Uganda (12%–31%),7 in India (30%),29 and in Kenya (76.4%).30 In Ethiopia, the parasitism rate of Cot. flavipes on larvae of C. partellus increased through time since its first record from 7.5% in 1999, 11%–20% in 2002, 58.8% in 2005, and 73% in 2007.11,28
This research results showed that a low rate of Cot. flavipes parasitism was recorded on B. fusca. Similarly, Ngi-Song et al29 reported that Cot. flavipes parasitized 76.4% on C. partellus, 63.2% on Chilo orichalcociliellus, 42.2% on Sesamia calamistis, and nil on B. fusca. The same author indicated that if Cot. flavipes was to be released in areas where suitable and unsuitable hosts occurred sympatrically, the parasitoid population would suffer mortality in the unsuitable host, B. fusca. Similarly, a high rate of Cot. flavipes parasitism was recorded on C. partellus (31%) compared to B. fusca (0%–12%) in Uganda.7,31 Variation in elevation affected the efficiency of Cot. flavipes parasitization, mainly through the availability of its suitable host, C. partellus. B. fusca was acceptable for oviposition but no parasitoid progeny developed to maturity.5 Overholt4 suggested that B. fusca is not suitable for the development Cot. flavipes, but the presence of acceptable but unsuitable hosts would create a sink for Cot. flavipes eggs and depress population growth. Ngi-Song et al32,34 also reported that Cot. flavipes successfully developed only on C. partellus. Cugala et al21 showed that B. fusca was partially suitable for the development of Cot. flavipes, with 6.7% of the larvae stung producing cocoons compared with 29.4% in C. partellus. Emana28 and Emana et al33 reported that C. partellus and S. calamistis were the most suitable host for Cot. flavipes and it developed in only two populations of B. fusca.
Most female adult wasps were found to deposit their eggs on late instars host larvae during physiological maturity of sorghum (before harvesting). These results corroborate findings by Jiang et al34 that high parasitism rates of Cot. flavipes at later host instars in Kenya. Ngi-Song et al35 and Setamou et al36 reported that the proportion of successfully parasitized C. partellus larvae by Cot. flavipes was higher in larger (ie, 4th and 5th instars) than smaller larvae (ie, 3rd instar).
A laboratory investigation on parasitization of different host ages of C. partellus larvae by Cot. flavipes at 27 °C ± 2 °C and 75% ± 5% relative humidity showed that higher parasitization and cocoon formation was recorded on the 17 and 20 day old larvae of C. partellus, with 82.6% and 82.46% parasitization and 43.09 and 42.70 cocoon formation, respectively. No parasitization and cocoon was recorded in 5 day old larvae.37,38
However, various differences between maize and sorghum are expected. Cot. flavipes rates of parasitism were lower on maize than sorghum, 3%–43% on maize and 5%–54% on sorghum in South Wollo, 5%–38% on maize and 2%–68% on sorghum in North Wollo, and 32%–72% on maize and 33%–82% on sorghum in Oromia Zone. This result corroborated Setamou et al (2005) and their laboratory work's findings that host plant species significantly affects the rate of successfully parasitized larvae by Cot. flavipes. Because hosts continue to feed after parasitization, the amount and quality of host diet can affect the performance of koinobiont parasitoids. The same author showed that the differential survivorships of parasitized C. partellus suggest that host plant species significantly affects the rate of successfully parasitized larvae by Cot. flavipes. Thus, the quality of host larvae is of paramount importance in the performance of Cot. flavipes.36
In the present study, parasitism rate of Cot. flavipes and borers density had a significantly positive relationship, which was in agreement with the work of Matama et al,7 who showed percentage parasitism by Cot. flavipes was positively associated with C. partellus densities in Uganda.
Information on the distribution and extent of Cot. flavipes parasitism that is reflected in its ecological requirement, host suitability, and host stages are the prerequisite in priority setting for stem borer control. The findings from this study are particular relevant as information on the contribution of Cot. flavipes in the population reduction of stem borers, time or stage of its occurrence in relation with host stages and crop stages, and its distribution in relation to the availability of suitable hosts across each zone or district of northeastern Ethiopia. It revealed that Cot. flavipes distribution and rate of parasitism varied with elevation that could affect the availability of suitable host, C. partellus. Its efficiency is affected by host stages—higher at later than early instars—that are active at later instars of the host and the crops.
Author Contributions
Conceived and designed the experiments: AD. Analysed the data: AD. Wrote the first draft of the manuscript: AD. Contributed to the writing of the manuscript: AD. Agree with manuscript results and conclusions: AD, EG, FA, AA. Jointly developed the structure and arguments for the paper: AD, EG, FA, AA. Made critical revisions and approved final version AD, EG, FA, AA. All authors reviewed and approved of the final manuscript.
References
Notes
[1] Conflicts of interest As a requirement of publication author(s) have provided to the publisher signed confirmation of compliance with legal and ethical obligations including but not limited to the following: authorship and contributorship, conflicts of interest, privacy and confidentiality and (where applicable) protection of human and animal research subjects. The authors have read and confirmed their agreement with the ICMJE authorship and conflict of interest criteria. The authors have also confirmed that this article is unique and not under consideration or published in any other publication, and that they have permission from rights holders to reproduce any copyrighted material. Any disclosures are made in this section. The external blind peer reviewers report no conflicts of interest.
