Pest Status of Acraea acerata Hew. and Cylas spp. in Sweetpotato ( Ipomoea batatas (L.) Lam.) and Incidence of Natural Enemies in the Lake Albert Crescent Agro-ecological Zone of Uganda

Abstract

The present study presents the results of farmers’ field surveys of the sweetpotato butterfly, Acraea acerata Hew., and the two African sweetpotato weevils, Cylas puncticollis Boheman and C. brunneus F. infestation and damage. The objectives of this study were to determine (i) occurrence and distribution of A. acerata and Cylas spp. as well as infestation and losses in sweetpotato (Ipomoea batatas (L.) Lam.), and (ii) the occurrence and abundance of parasitoids of A. acerata in the Lake Albert Crescent (LAC) agro-ecological zone of Uganda. Field surveys were conducted in 240 sweetpotato fields in eight subcounties in Masindi and Buliisa districts at the end of each of the two cropping seasons of 2012 (March to May and September to November). A. acerata and Cylas spp. occurred in 17% and 90% of the fields, respectively. A. acerata did not occur in two subcounties of Buliisa district. A. acerata infestation was low, with up to two and four larvae per plant in the first and second cropping season, respectively, causing minor defoliation of up to 4.1% of the sweetpotato plant. Larvae of Cylas spp. caused root yield losses of up to 56.5% and 47.5% in the first and second cropping seasons, respectively. Parasitism rates of A. acerata larvae ranged from 0.0% to 15.1% in season 1 and 0.0% to 6.3% in season 2. Out of a total of 1020 larvae collected, 8.43% were found to be parasitized. Parasitoids occurred in 56% of fields infested by its host. Charops spp. was the main parasitoid. It was evident that Cylas spp. were more prevalent than A. acerata in the LAC agro-ecological zone of Uganda. Conservation of A. acerata natural enemies may contribute to better management of this pest. Urgent attention for management of Cylas spp. is required.

Keywords

Farmers’ field infestation insect pest severity sweetpotato butterfly sweetpotato weevil parasitoids

Introduction

Sweetpotato, Ipomoea batatas (L.) Lam., is a vitamin A rich staple food crop contributing to household income, food, and nutritional security in Africa.¹ Sweetpotato production, however, continues to be threatened by a complex of biotic constraints, including insect pests, that have led to a decline in crop quality and yields in Africa. The most significant insect pests are the sweetpotato butterfly, Acraea acerata Hew., the two African sweetpotato weevils, Cylas brunneus F. and C. puncticollis Boheman, and the clearwing moth Synanthedon species.^{2

7}

A. acerata and Cylas spp. have been reported in all sweetpotato growing countries in Africa.^5,8,9 A. acerata larvae are voracious herbivores, defoliating plants by up to 100%; during outbreaks plants can fail to establish due to severe leaf and vine damage. Additionally, feeding by larvae of Cylas spp. on the sweetpotato roots and stems can result into 100% root yield loss, especially during long dry seasons.^2,4,10–13

Despite the serious threat to sweetpotato production by A. acerata and Cylas spp., detailed information on their seasonal abundance and distribution in Uganda is limited except for the A. acerata parasitoids abundance surveys conducted between 1994 and 1995 by Lugojja.¹⁴ Charops sp. was the most abundant of the three parasitoid species (Meteorus sp. and Caricelia normula Wyatt) collected in Central Uganda. The current study was therefore conducted to determine (i) occurrence and distribution of A. acerata and Cylas spp. and their damage to sweetpotato and (ii) parasitization of A. acerata larvae in the Lake Albert Crescent (LAC) Agro-ecological zone of Uganda. This region was selected for study as it is one of the leading sweetpotato production zones in Uganda, producing over 100,000 tons per year. In addition, the sweetpotato butterfly and the sweetpotato weevils are ranked first and second most important sweetpotato pests, respectively.^7,15

Information gained in this study can help to understand pest ecology and help to design suitable management options based on pest distribution and severity. It will also guide development of a biocontrol strategy for A. acerata. This baseline survey will fill data gaps on pest severity and efficacy of natural enemies in sweetpotato.

Materials and Methods

Survey sites

Masindi and Buliisa districts in the LAC Agro-ecological zone of Uganda were surveyed. The survey area was sub-divided into four sites for sampling. Sampling involved stopping at regular predetermined distances of approximately 1 to 5 km between farmers’ fields along major motorable roads traversing each sampling site. Masindi district is located in the mid-west part of Uganda (01°41'N, 31°44'E). The district is generally a plateau land with an altitude range of 1,100 m to 1,510 m above sea level. The district receives an average of 1,360 mm bimodal rainfall annually which allows for two cropping seasons, the first being from March to May and the second from September to November. Seventy three percent of the population in the district is engaged in smallholder agricultural activities. Major crops grown include sweetpotato (I. batatas), maize (Zea mays ssp. mays L.), cassava (Manihot esculenta Crantz), sugarcane (Saccharum officinalis. L.), and tobacco (Nicotiana tabacum L.). Soils are mainly sandy loams. Long-term min and max temperature for the period 1982 to 2011 are 17 to 31°C for Masindi, but are unknown for Buliisa district due to absence of a meteorological station. Buliisa is a district in northwestern Uganda (02°11'N, 31°24'E) and lies on the floor of the Western Rift Valley at an elevation of 600 to 1,030 m above sea level. The district receives low rainfall (≤800 mm) and is primarily rural with most people being pastoralists, fishers, or subsistence farmers of mainly cassava, sweetpotato, and cotton (Gossypium hirsutum L.). Soils are mainly sandy.

Sampling of A. acerata and Cylas spp. infestation on sweetpotato

One to two month old sweetpotato fields were surveyed for populations of A. acerata while older fields ready for root harvesting (≥3 months after planting) were surveyed for Cylas spp. infestations. A total number of 120 fields were surveyed in the two seasons for each pest, each measuring approximately 0.03 to 0.07 ha in February and September 2012. The survey included 99 fields from four subcounties (Miirya, Pakanyi, Nyangahya, and Bwijanga) in Masindi and 141 fields from four subcounties (Biiso, Kihungya, Buliisa and Ngwedo) in Buliisa. A total of 10 plant stands or hills with at least three vines per hill were assessed along two diagonals in each field.

A. acerata and Cylas spp. infestation

Sweetpotato field infestation rates by A. acerata and Cylas spp., densities of and vine defoliation rates by A. acerata larvae, vine damage, and root yield loss by Cylas spp. were assessed based on the methodology recently reported in Okonya ’ Kroschel.¹⁶ Destructive sampling was used in the assessment of vine and root damage by Cylas spp. The infestation rate of these pests was recorded as the proportion (expressed as a percentage) of farmer fields in which the pests occurred. Since the two African Cylas spp. occur together in the field and cause similar damage, this study did not differentiate between the damage caused by C. puncticollis and C. brunneus.

A. acerata larval parasitization

A total of 1,020 A. acerata larvae were collected from the 21 fields infested by the pest (larvae were randomly searched for in the field if none were found on the 10 sample plants) during the survey. A. acerata larvae were placed in 15 cm diameter transparent plastic containers with fresh sweetpotato vines as diet and labeled appropriately according to location of origin and date of collection. These larvae were reared on sweetpotato vines in a screen house at the National Crop Resources Research Institute (NaCRRI), Namulonge, Uganda (0°32'N, 32°35'E; altitude 1150 m above sea level), until emergence of larval parasitoids. A. acerata larval parasitization by Charops sp. or other larval parasitoids was determined by examining the parasitoid cocoons and any emerged adults. Percent larval parasitization of A. acerata was determined for each field.

Data analysis

Ranked data were square root transformed, percentage data were arcsine transformed while number counts were log (x + 1) transformed.¹⁷ Differences in vine damage severity due to Cylas spp., defoliation due to A. acerata, root yield loss due to Cylas spp., and A. acerata parasitization were analyzed by analysis of variance (ANOVA), using the general linear model (PROC GLM). Mean values were separated using the least significant difference (LSD) test at a significance level of P ≤ 0.05. All data were analyzed using the SAS® program (release 9.2 for Windows).¹⁸

Results and Discussion

A. acerata and Cylas spp. infestation

Both A. acerata and Cylas spp. occurred in the two districts and in both seasons (Table 1). Of the 240 fields sampled (120 for A. acerata and 120 Cylas spp.), 16.5% were infested with A. acerata while 90% were infested with Cylas spp. (Fig. 1). Field infestation was higher in the first cropping season (25% for A. acerata and 97% for Cylas spp.) than the second cropping season (8% for A. acerata and 83% for Cylas spp.). This is the first report on farmers’ sweetpotato field infestation and yield loss by A. acerata and Cylas spp. in Masindi and Buliisa districts. Field infestation rates by A. acerata recorded in this study compare well to those of 18% reported in Kabale district, although they are relatively low.¹⁶ A. acerata does not always occur in sweetpotato fields all year round, or every year, and outbreaks occur once in a while during a prolonged dry season.⁸ The percentages of sweetpotato fields infested with Cylas spp. in this study were significantly higher than those observed for Kabale district (50%). This could be due to higher temperatures (17 to 31°C) in the LAC Agro-ecological zone as compared to those in the southwestern highlands (11 to 25°C).

Figure 1.

Infestation rate by Acraea acerata and Cylas spp. in sweetpotato crop in 2012.

Table 1.

Infestation rates of Acraea acerata and Cylas spp. in sweetpotato crop during 2012.

SURVEY SITE (SUBCOUNTIES)	INFESTATION RATE (%)
	A. ACERATA		CYLAS SPP.
	SEASON 1: MAR–MAY	SEASON 2: SEP–NOV	SEASON 1: MAR–MAY	SEASON 2: SEP–NOV
Masindi North (Pakanyi + Miirya)	50.00 (8)^*	18.75 (16)	100.00 (8)^*	92.86 (14)
Masindi South (Bwijanga + Nyangahya)	25.00 (16)	8.33 (12)	87.50 (16)	88.89 (9)
Buliisa upper (Biiso + Kihungya)	41.18 (17)	7.14 (14)	100.00 (17)	94.12 (17)
Buliisa lower (Buliisa + Ngwedo)	0.00 (19)	0.00 (18)	100.00 (19)	65.00 (20)

Number of fields surveyed.

Infestation intensity

The average level of A. acerata infestation intensity was slightly higher in season 2 (1.16 A. acerata larvae per plant) than in season 1 (0.90 A. acerata larvae per plant) (Table 2). Although the highest numbers of A. acerata larvae per plant (2.03 larvae) occurred in sweetpotato fields of Masindi South during the first cropping season, this was not the case during the second cropping season as the highest A. acerata larvae density (4.11 larvae per plant) occurred in sweetpotato fields in Buliisa upper. In both cropping seasons of 2012, no A. acerata larvae occurred in the surveyed fields in Buliisa lower. Sweetpotato fields surveyed during the first cropping season experienced higher defoliation rates by A. acerata larvae (2.17%) than those surveyed during the second cropping season (0.04%). Masindi North had the highest sweetpotato plant defoliation by A. acerata larvae during both the first and the second cropping seasons at 4.06% and 0.16%, respectively. Defoliation levels of this magnitude do not significantly reduce root yield, unlike during outbreaks when plant defoliation levels of over 50% occur. However, quantitative studies on the effect of A. acerata defoliation on root yield are lacking. A. acerata larvae in Masindi South and Buliisa upper caused no defoliation during the second cropping season as A. acerata larvae were too young and still clustered (1st instar) and had barely started to feed. Voracious feeding by A. acerata larvae has been observed to start in the solitary 4th instar larvae.¹⁹ The relatively low A. acerata densities and very low defoliation rates detected in this study are probably due to the fact that this survey was conducted when there was neither an outbreak of A. acerata in Masindi nor Buliisa district. Secondly, there was also no distinct or prolonged dry season, to allow high pest populations to build up in Masindi and Buliisa districts during both cropping seasons of 2012.

Table 2.

Infestation intensity and defoliation of Acraea acerata in sweetpotato crop in 2012.

SITE (SUBCOUNTIES)	SEASON 1		SEASON 2
SITE (SUBCOUNTIES)	INFESTATION INTENSITY (LARVAE/PLANT)	DEFOLIATION (%)	INFESTATION INTENSITY (LARVAE/PLANT)	DEFOLIATION (%)
Masindi North (Pakanyi + Miirya), n = 24	0.64 ± 0.30a	4.06 ± 1.56a	0.53 ± 0.51a	0.16 ± 0.16a
Masindi South (Bwijanga + Nyangahya), n = 28	2.03 ± 1.53a	2.50 ± 1.27ab	0.30 ± 0.30a	0.00a
Buliisa upper (Biiso + Kihungya), n = 36	0.98 ± 0.56a	3.38 ± 1.23a	4.11 ± 4.11a	0.00a
Buliisa lower (Buliisa + Ngwedo), n = 31	0.00a	0.00b	0.00a	0.00a
Total mean	0.90 ± 0.44A	2.17 ± 0.55A	1.16 ± 0.97A	0.04 ± 0.04B

Means followed by the same letter within a column (small letter) and within the last row (capital letter) are not significantly different according to the LSD-test at P ≤ 0.05.

Cylas spp. infestation intensity

External vine damage scores by Cylas spp. ranged from 1.47 to 1.74 in season 1 and 1.18 to 1.89 in season 2 (Table 3). Similarly, internal vine damage scores by Cylas spp. ranged from 1.50 to 1.89 in season 1 and 1.12 to 2.11 in season 2. However, external and internal vine damage scores by Cylas spp. did not significantly differ between seasons and were relatively low. Although different sweetpotato varieties were assessed for vine damage in this study, Muyinza et al¹² reported comparable vine damage scores of between 0.9 and 3.3. Root yield loss was higher in the first cropping season (42.80%) than in the second cropping season (26.64%). Buliisa upper had the highest root yield loss during both the first and second cropping seasons at 56.53% and 47.54%, respectively. Root yield losses due to Cylas spp. damage reported in this study are lower than those observed in the drought-prone Soroti district (98.0%) but equal to the highest damage levels (55.6%) reported in Serere district.^4,12 Damage by Cylas spp. has been shown to increase with reduced rainfall amounts, less number of rainy days, and shorter below ground root storage time.² Since early harvesting is the main cultural method used by farmers to avoid Cylas spp. root damage in most regions of Uganda (Okonya ’ Kroschel, unpublished), farmers in Masindi district did not leave sweetpotato in the fields for more than six months after planting, making it impossible to register root infestation levels of near 100% during this survey.

Table 3.

Vine damage and root yield loss by Cylas spp. in sweetpotato crop in 2012.

SITE (SUBCOUNTIES)	MEAN ± SE
	SEASON 1			SEASON 2
	VINE DAMAGE (SCORE)^*		ROOT YIELD LOSS (%)	VINE DAMAGE (SCORE)^*		ROOT YIELD LOSS (%)
	EXTERNAL	INTERNAL	ROOT YIELD LOSS (%)	EXTERNAL	INTERNAL	ROOT YIELD LOSS (%)
Masindi North (Pakanyi + Miirya), n = 22	1.50 ± 0.19a	1.50 ± 0.19b	43.40 ± 8.71ab	1.64 ± 0.13a	1.93 ± 0.16a	28.70 ± 5.94ab
Masindi south (Bwijanga + Nyangahya) n = 25	1.50 ± 0.13a	1.69 ± 0.12ab	35.81 ± 5.24b	1.89 ± 0.11a	2.11 ± 0.20a	25.12 ± 7.95b
Buliisa upper (Biiso + Kihungya), n = 34	1.47 ± 0.12a	1.59 ± 0.12ab	56.53 ± 4.16a	1.18 ± 0.10b	1.12 ± 0.08b	47.54 ± 5.40a
Buliisa lower (Buliisa + Ngwedo), n = 38	1.74 ± 0.10a	1.89 ± 0.07a	36.13 ± 4.94b	1.65 ± 0.17a	1.70 ± 0.13a	8.12 ± 4.16c
Total mean	1.57 ± 0.06A	1.70 ± 0.06A	42.80 ± 2.85A	1.55 ± 0.08A	1.65 ± 0.08A	26.64 ± 3.36B

Basal segment vine damage scores: 1 = 0%; 2 = 1–25%; 3 = 26–50%; 4 = 51–75%; 5 = 76–100%; Means followed by the same letter within a column (small letter) and within a row (capital letter) are not significantly different (P ≤ 0.05).

Though not targeted in this study, relatively high infestation rates by the clearwing moth (Synanthedon spp.; Lepidoptera: Sesiidae) which occupies the same ecological niche (basal vines) as Cylas spp. were observed to occur in approximately 75% of fields in lower Buliisa, causing over 75% of basal stem damage. Therefore, studies on how Cylas spp. interact with Synanthedon spp. in the field might be of interest. Nderitu et al⁶ indicated that Synanthedon spp. was an important insect pest of sweetpotato in Eastern Kenya. Management of Synanthedon spp. in Uganda had been reported to not be necessary, however this was probably because Buliisa district was never surveyed or may have changed due to other factors such as climate change.^11,20

Parasitism, parasitoid diversity, and distribution

Out of the 21 fields infested with A. acerata larvae, 56% of the fields had larvae which were parasitized. All the fields in Buliisa upper had larvae that were parasitized while fields in Buliisa lower had no A. acerata larvae and therefore no parasitoids. Eighty six parasitoids emerged out of the 1,020 A. acerata larvae (parasitism rate of 8.43%) collected from 15 sweetpotato fields during the two cropping seasons. Three different parasitoid species were recorded in this study, belonging to two orders: Hymenoptera (1 sp.) and Diptera (2 spp.) (Table 4). One of the dipteran parasitoids was not identified. Charops spp. (Hymenoptera: Ichneumonidae) was the most dominant parasitoid identified in this survey (96.51%). This species represented 93.62% and 100% of the three parasitoids reared in the first and second cropping seasons, respectively. Larval parasitoid Charops sp. was also the most dominant species in Buliisa upper, Masindi North, and Masindi South.

Table 4.

Parasitism rates of Acraea acerata in sweetpotato crop in 2012.

PARASITOID TAXA	PARASITISM RATE (%)
	MASINDI NORTH (PAKANYI + MIIRYA), n = 6		MASINDI SOUTH (BWIJANGA + NYANGAHYA), n = 11		BULIISA UPPER (BIISO + KIHUNGYA), n = 4		BULIISA LOWER (BULIISA + NGWEDO), n = 0
	SEASON
	I	II	I	II	I	II	I	II
Hymenoptera: Ichneumonidae Charops spp.	0.0(0)	6.1 (18)^*	11.1 (33)	6.3 (21)	15.1 (11)	0.0 (0)	0.0 (0)	0.0 (0)
Diptera: Tachinidae Caricelia spp.	0.0 (0)	0.0 (0)	0.3 (1)	0.0 (0)	1.4 (1)	0.0 (0)	0.0 (0)	0.0 (0)
Diptera (unidentified sp.)	4.8 (1)	0.0 (0)	0.0 (0)	0.0 (0)	0.0 (0)	0.0 (0)	0.0 (0)	0.0 (0)
Total larvae	21	297	296	333	73	0	0	0

n = number of fields;

= number of parasitoids in parentheses.

Improper use of broad-spectrum insecticides such as cypermethrin, dimethoate, and permethrin against A. acerata (Okonya ’ Kroschel, unpublished) could be responsible for the low parasitoid diversity and abundance recorded in this study as some farmers practice routine insecticide applications. Low parasitism of A. acerata larvae is consistent with the observation of Azerefegne et al³ in Ethiopia and Lugojja et al²¹ in Uganda. Although no mycosis tests were carried out on larvae dead due to fungal infections in this study, Lugojja et al²¹ observed the entomopathogenic fungi Beauveria bassiana (Bals.-Criv.) Vuill. to be responsible for the death by factors other than parasitism. Also, handling of larvae might have increased larval mortality.

Conclusion and Recommendations

A. acerata and Cylas spp. are significant insect pests in Masindi and Buliisa districts. Pest pressure of the previously neglected or underestimated Synanthedon spp. is significantly higher in Ngwedo and Buliisa subcounties and requires a detailed study. This information should aid the decision-making process for insect pest management in the two districts and surrounding districts with similar agro-ecologies, such as Hoima, Kiryandongo, Kibaale, Mubende, Kiboga, Bundibugyo, Kyenjojo, Kabarole, and Kamwenge.

Suggestions for an integrated pest management (IPM) strategy aiming at reduction of damage from insect pests include: a) adequate cultural practices and proper sanitation involving removal of any infested crop roots and vines from the field and its surroundings to prevent re-infestation; b) use of healthy planting material; c) regular monitoring of pest populations, for example through the use of pheromone traps for Cylas spp. or the occurrence of A. acerata larvae on the foliage; d) avoidance of calendar insecticide spraying as this would worsen the situation especially for A. acerata as in years without outbreaks, A. acerata pest populations and infestation would not require any intervention as shown in this study; e) use of biopesticides such as Bacillus thuringiensis sp. kurstaki to control larvae of A. acerata; and f) as the last option, use of less-toxic insecticides considering all safety measures during application and storage of the insecticide. It would be extremely useful to activate a basic education program on essential elements of IPM, such as increased crop rotation duration of at least 12 months since adult females of C. puncticollis can live for up to 309 days (Okonya ’ Kroschel, unpublished), the basics of insect pest biology, and the use of biological control.

Author Contributions

Conceived and designed the survey protocol: JSO, JK. Analyzed the data: JSO. Wrote the first draft of the manuscript: JSO. Contributed to the writing of the manuscript: JSO. Agree with manuscript results and conclusions: JSO, JK. Jointly developed the structure and arguments for the paper: JSO, JK. Made critical revisions and approved final version: JSO, JK. Both authors reviewed and approved of the final manuscript.

Footnotes

Acknowledgment

The authors wish to thank James DJ Gilbert for comments on the manuscript, Katja Syndikus and Robert OM Mwanga for helpful discussions, Zaamu Ssempa for assistance with laboratory work, and Esther L Nampeera, and agricultural extension workers of the surveyed subcounties for assistance with fieldwork.

As a requirement of publication the authors have provided signed confirmation of their compliance with ethical and legal obligations including but not limited to compliance with ICMJE authorship and competing interests guidelines, that the article is neither under consideration for publication nor published elsewhere, of their compliance with legal and ethical guidelines concerning human and animal research participants (if applicable), and that permission has been obtained for reproduction of any copyrighted material. This article was subject to blind, independent, expert peer review. The reviewers reported no competing interests.

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