African Crop Science Journal African Crop Science Society ISSN: 1021-9730 EISSN: 2072-6589 Vol. 9, Num. 1, 2001

African Crop Science Journal, Vol. 9, No. 1, March 2001, pp. 157-163

Code Number: CS01044

ABSTRACT

The species range, activity and relative abundance of parasitoids attacking the sweetpotato butterfly, Acraea acerata Hew. (Lepidoptera: Nymphalidae) in Uganda was investigated. Samples of eggs and larvae of the sweetpotato butterfly were collected from some of the major sweetpotato growing districts of Uganda to identify the range of parasitoids in the country. Monthly surveys to collect samples of caterpillars from selected sites were also carried out to evaluate percentage parasitism over time. The collected samples were reared in the laboratory for parasitoid emergence. Results showed that the sweetpotato butterfly is attacked by three larval parasitoid species in Uganda, namely, Meteorus sp. (AKW), Charops sp. (AKW) and Caricelia normula Wyatt. No parasitoids emerged from eggs, indicating an absence of egg parasitoids. Charops sp. was the most abundant parasitoid species at all sites, Meteorus sp. had moderate occurrence, while C. normula was the least abundant. Percentage parasitism was found to be rather low to afford significant control on its own. Nevertheless, long term impact of parasitoids is important in moderating pest population dynamics. It is, therefore, important to conserve the native natural enemies by avoiding over use of insecticides.

Key Words: Acraea acerata, biological control, Caricelia normula, Charops sp., Meteorus sp., natural enemies, percentage parasitism, parasitoids, Uganda

RÉSUMÉ

L' étendue d'une espèce de papillons (Acraea acerata Hew.) défoliatrice de la patate douce, son activité et l' abondance relative de ses parasitoides ont été étudiées en Uganda. Des échantillons des oeufs des papillons ont été collectés dans presque tous les grands districts producteurs de la patate douce pour déterminer l'étendue des parasitoides dans le pays. Les enquêtes mensuelles de collection des chenilles à partir des sites sélectionnés ont été aussi conduites pour déterminer le pourcentage du parasitisme dans le temps. Les échantillons collectés étaient élevés au laboratoire pour étudier l'emergence des parasitoides. Des résultats ont montré que les papillons sont attaquées par trois espèces de parasitoides larvaires en Uganda à savoir: Meteorus sp. (AKW), Charops sp. ( AKW) et Caricelia normula Wyatt. Pas de parasitoides émergeant des oeufs signifiant une absence d'oeuf parasitoides. Charop sp était le parasitoide le plus abondant dans tous les sites, Meteorus sp avait une apparition moderée alors que C. normula était le moins abondant. Le pourcentage du parasitisme a été trouvé plutôt faible pour permetre un contrôle significatif par le parasitiode lui-seul. Cependant, un impact à long terme des parasitoides est important dans la moderation du dynamisme des populations de la peste. Il est ainsi important de conserver les ennemis naturels natifs pour éviter l'utilisation des insectides.

Mots Clés: Acraea acerata, contrôle biologique, Caricelia normula, Charop sp, Meteorus sp, ennemis naturels, pourcentage du parasitisme, parasitoides, Uganda

INTRODUCTION

The sweetpotato butterfly (Acraea acerata Hew.) is an important pest of sweetpotato in Uganda (Bashaasha et al., 1993). Outbreaks of this pest normally occur during the dry season, and are especially severe in the highland areas of South-Western Uganda.

Hand picking of caterpillar nests and chemical control are the measures widely recommended for use by farmers (NARO, 1994). Hand picking can only be effective if started early at the onset of the butterfly outbreak, and is most effective when applied regionally because of the concentration and close proximity of farms in some parts of Eastern Africa (Lenné, 1991; Smit et al., 1996). Its biggest limitation is the need for vigilance to monitor infestation, and enough labour force when the outbreak is severe.

The insecticides recommended against A. acerata include carbaryl and pyrethroids (ambush) as foliar sprays (Skoglund and Smit, 1994). Although insecticides provide adequate suppression, they are very expensive, are sometimes unavailable in the rural areas (Venegas and Bashaasha, 1991) and may contribute to environmental contamination. Alternative approaches to sweetpotato butterfly control, such as biological control, are therefore needed.

Since the sweetpotato butterfly is endemic to Eastern Africa (Janssen, 1982; Nyiira, 1982; Ndayiragije, 1984; Ndamage et al., 1992; Allard, 1993; Smit and Matengo, 1995), it is important to consider conservation and augmentation of its indigenous natural enemies rather than importing exotic ones (Debach and Rosen, 1991). However, because the local infrastructure and technical facilities do not allow for large-scale mass rearing and distribution of natural enemies, conservation of the indigenous natural enemies offers the greatest scope for control (Yaninek and Cock, 1989).

Biological control of the sweetpotato butterfly in a conservation strategy is an option compatible with subsistence farming conditions in East Africa. Conservation is a strategy whereby environmental manipulations aim to increase the impact of native natural enemies on indigenous pest populations. At present, no information is available on the sweetpotato butterfly natural enemy situation in Eastern Africa. Yet understanding the present role of parasitoids is an essential step in the development of an Integrated Pest Management (IPM) package for A. acerata. In the present study, therefore, efforts were made to identify the range of parasitoids of A. acerata in Uganda, to assess the level of parasitism at selected sites over time and to establish the relative abundance of the parasitoids at the selected sites.

MATERIALS AND METHODS

This study consisted of field surveys, conducted between January 1994 and June 1995, to collect samples of A. acerata from various sites, which were then reared for parasitoid emergence in the Sweetpotato Laboratory at Namulonge Agricultural Institute, Uganda. A bimodal rainfall pattern is experienced in all the study sites, with December to February and June to August being the dry months.

Identification of the range of parasitoids of A. acerata. Samples of not less than 100 eggs and caterpillars of A. acerata were collected from some of the major sweetpotato growing districts of Uganda between January, 1994 and March, 1995. The districts were Mpigi, Soroti, Mukono, Luwero, Tororo, Kabale, Masaka and Jinja. A. acerata pupae were scarce in the field and therefore data on pupal parasitoids were not collected. The different species of parasitoids that emerged during the rearing were sorted out, and mounted adult parasitoids with their pupal cases were sent to the International Institute of Entomology, IIE , United Kingdom, for identification.

Percentage parasitism of A. acerata larvae and relative abundance of the parasitoids. Two surveys were carried out in the districts of Luwero, Mpigi and Mukono during the periods February - July 1994, and February - May 1995, to establish the levels of A. acerata parasitism at these sites. Samples of 100 caterpillars were collected monthly from farmer's sweetpotato fields in selected villages during the surveys. The villages were Nazalensi, Kiwenda, Nabitalo and Sendusu in Kyadondo County, Mpigi District and Mbalala in Mukono County, Mukono District. Those selected during the second survey were Bombo (Luwero District), Kiwenda (Mpigi), Mbalala (Mukono), Nabbingo (Mpigi) and Ntawo (Mukono).

The number of A. acerata pupae formed and adults enclosed during the rearing were determined. Natural enemies (parasitoids) emerging were recorded to establish percentage parasitism at different sites over time. The relative abundance of the different parasitoids per sample of 100 larvae sampled over the same time period was also established.

RESULTS

Range of parasitoids of A. acerata. Four parasitoid species, three Hymenoptera and one Diptera, were encountered. The dipteran species was Caricelia normula (Tachinidae), while the hymenopterans were Meteorus sp. (Braconidae), Charops sp. and Mesochorus sp. (Inchneu-monidae). Only the first three species were identified as parasitoids of A. acerata. The fourth species was identified as a hyperparasite of one of the parasitoids.

Parasitism of the A. acerata larvae. Data collected during the February - July 1994 survey from the five sites showed significant (P < 0.05) increase in larval mortality with successive months after April, with a peak in June before it declines in July (Table 1). Percentage parasitism was highest in February and March (start of the rainy season), but declined with successive months, being lowest in May and July. There were significant (P < 0.05) differences in percentage parasitism between sites, with Mbalala registering the highest parasitism.

Data collected during the February - May 1995 survey, from the five selected sites, showed that larval mortality in this period increased in successive months (Table 2). There were significant (P<0.05) differences in mortality levels between months and sites, with Bombo registering the highest percentage mortality. Percentage parasitism was significantly (P<0.05) highest in February and March, and decreased in successive months. There were no significant differences in percentage parasitism between sites.

Abundance of the parasitoids varied with species and site during both surveys (Table 3). In the February to July 1994 period, Chrops sp. was the most abundant parasitoid species, with a mean occurrence of 4.0% (range 0 - 19%), while C. normula was the least abundant with a mean incidence of 1.1% (range of 0 B 3%). Mbalala registered the highest percentage (6.7%) of Charops sp. while Kiwenda registered the lowest percentage (0.5%) of C. normula during this period.

In the period February to May 1995, Charops sp. was the most abundant parasitoid species, with a mean incidence of 4.6% and a range of 0 - 19%, while C. normula was the least abundant with a mean emergence of 0.8% and a range of 0 - 3% (Table 3). Kiwenda had the highest percentage (7.5%) of Charops sp. while Mbalala had the lowest percentage (0.5%) of C. normula during this period. It is evident from the data that Charops sp. was the most abundant parasitoid of A. acerata while C. normula was the least abundant over the two survey periods.

DISCUSSION

This study showed that the sweetpotato butterfly is attacked by a narrow range of parasitoids in Uganda. No parasitoids emerged from eggs of A. acerata. Percentage parasitism at the selected sites was rather too low for the parasitoids to afford much control on their own, but indicated that it is important enough to warrant conserving the natural enemies. Charops sp. was the most abundant parasitoid species at the selected sites, Meteorus sp. had moderate occurrence, while C. normula was the least abundant. Lefervè (1948) also identified Meteorus and Charops spp. as parasitoids of A. acerata in Congo. A fourth natural enemy, Mesochorus was encountered, and this was previously identified by Lefervè (1948) as a hyperparasite of Charops sp.

Results obtained further showed that the parasitoids occurred at all the sample sites. However, Charops sp. was generally the most abundant and C. normula the least. A possible explanation for this may be that Charops sp. has higher population build-up in the environment than the other two natural enemies. It may also have a competitive advantage over the other two species, being more efficient at searching for and attacking A. acerata (Lugojja, 1996). In the study, no parasitoids emerged from eggs, indicating an absence of egg parasitoids. This is in agreement with Lefervè's (1948) findings in Congo.

The parasitoids attacking A. acerata contributed relatively little towards the mortality of the butterfly in the laboratory. The biggest mortality was due to other factors, including the fungal pathogen, Beauveria bassiana. These other mortality factors are probably the ones largely responsible for suppressing the butterfly populations, particularly during the rainy season when fungal infection is at its highest. These mortalities seem to explain the outbreaks of the sweetpotato butterfly during dry seasons, and the low or no butterfly outbreaks during wet seasons.

It is concluded from this study that natural enemies are important factors in the dynamics of A. acerata populations. However, further studies should focus on understanding the roles of pathogens in the occurrence of sweetpotato butterfly pest outbreaks.

ACKNOWLEDGEMENTS

This work was conducted at Namulonge Agricultural and Animal Production Research Institute when the first author was a Graduate Student at Makerere University, Kampala. The International Potato Centre (CIP) financed the research. The support of the three institutions is greatly acknowledged. The International Institute of Entomology (IEB, UK) taxonomists are thanked for insect identification.

REFERENCES

Allard, G.B. 1993. Integrated Control of Arthropod pests of Root Crops. Annual Report 1992. CAB International Institute of Biological Control, Kenya Station, Nairobi, Kenya. 95 pp.

Bashaasha, B., Mwanga, R.O.M., Ocitti P'Obwoya, C. and Ewell, P.T. 1993. Sweetpotato in the Farming and Food Systems of Uganda. A Farm Survey Report. 63 pp.

Debach, P. and Rosen, D. 1991. Biological Control by Natural Enemies. Cambridge University Press, Cambridge.

Janssens, M.J.J. 1982. Sweetpotato improvement in Rwanda. In: Root Crops in Eastern Africa. Proceedings of a Workshop held at Kigali, Rwanda, 23 - 27 November 1980. IDRC, Ottawa, Canada B 103. 99 pp.

Lefervè, P.C. 1948. Acraea acerata Hew. parasite de la patate douce. Bulletin Agricole Cong Belge 39:49 B 76.

Lenné, J.M. 1991. Diseases and Pests of Sweetpotato: South-east Asia, the Pacific and East Africa. Natural Resources Institute Bulletin No. 46 viii + 116 p.

Lugojja, F. 1996. Aspects of the biology of the sweetpotato butterfly (Acraea acerata) and impact of its defoliation on sweetpotato. M.Sc. Thesis, Makerere University, Kampala. 120 pp.

National Agricultural Research Organisation (NARO), 1994. Sweetpotato. Growers' Guide. NARO, Uganda.

Ndamage, G., Ntwawuruhunga, P. and Mulindangabo, J. 1992. Progress de la recherche sur les plantes a racines et tubercules au Rwanda. ISAR, Butare, Rwanda, IDRC, Ottawa, Canada.

Ndayiragije, P. 1984. Phytosanitary problems of roots and storage roots in Burundi. In: Proceedings of the Second Eastern and Southern Africa Regional Workshop. December 10 -15, 1984 Kampala, Uganda.

Nyiira, Z.M. 1982. Country report Uganda. In: Root Crops in Eastern Africa. Proceedings of a Workshop held at Kigali, Rwanda, 23- 27 November 1980. IDRC, Ottawa, Canada.

Skoglund, L.G. and Smit, N.E.J.M. 1994. Major Diseases and Pests of Sweetpotato in Eastern Africa. International Potato Center (CIP), Lima, Peru. 33 pp.

Smit, N.E.J.M. and Matengo, L.O. 1995. Farmers' cultural practices and their effects on pest control in sweetpotato in South Nyanza, Kenya. International Journal of Pest Management 41:2-7.

Smit, N.E.J.M., Lugojja, F. and Ogenga-Latigo, M.W. 1996. The sweetpotato butterfly - a review. International Journal of Pest Management. In Press.

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Yaninek, J.S. and Cock, M.J.W. 1989. Identifying pest problems in relation to implementing biological control in Africa. In: Biological Control: A Sustainable Solution to Crop Pest Problems in Africa. Proceedings of the Inaugural Conference and Workshop of IITA Biological Control Program Center for Africa, 5 - 9 December 1988, Contonou.

TABLE 1. Percentage mortality and parasitism of A. acerata larvae collected during the period February to July, 1994

Month	Collection site	No. of larvae	Percentage mortality
			Parasitism	Others
February	Nazalensi	100	13	19
	Kiwenda	100	6	19
	Nabitalo	100	18	22
	Sendusu	100	9	33
	Mbalala	100	6	48
March	Nazalensi	100	10	15
	Kiwenda	100	14	9
	Nabitalo	100	9	6
	Sendusu	100	5	31
	Mbalala	100	29	16
April	Nazalensi	100	14	13
	Kiwenda	100	5	13
	Nabitalo	100	9	17
	Sendusu	100	6	33
	Mbalala	100	15	16
May	Nazalensi	100	1	55
	Kiwenda	100	2	62
	Nabitalo	100	3	73
	Sendusu	-	-	-
	Mbalala	100	6	62
July	Nazalensi	100	6	78
	Kiwenda	100	0	67
	Nabitalo	-	-	-
	Sendusu	-	-	-
	Mbalala	100	8	64

TABLE 2. Percentage mortality and parasitism of A. acerata larvae for samples collected during the February to May, 1995 survey

Month	Collection site	No. of larvae	Percentage mortality
			Parasitism	Others
February	Mbalala	100	8	33
	Ntawo	100	9	45
	Nabbingo	100	12	27
	Kiwenda	100	17	26
	Bombo	100	10	47
March	Mbalala	100	12	33
	Ntawo	100	13	35
	Nabbingo	100	9	45
	Kiwenda	100	22	29
	Bombo	100	10	55
April	Mbalala	100	5	53
	Ntawo	100	1	65
	Nabbingo	100	3	66
	Kiwenda	100	3	74
	Bombo	100	2	82
May	Mbalala	100	2	79
	Ntawo	100	3	90
	Nabbingo	100	4	84
	Kiwenda	100	3	87
	Bombo	100	1	87

TABLE 3. Mean number (x + SE) and range of parasitoids emerging per sample of 100 larvae collected from different sites in Mukono, Luwero and Mpigi districts during the periods February - July, 1994 and February - May, 1995.

Time periods	Site	Parasitoid species
		Charops	Meteorus	C. normula
	Nazalensi (X±SE) range	4.5± 1.5	2.2 ±0.7	1.3± 0.4
		1.0 - 9.0	0.0 - 5.0	0.0 - 3.0
	Kiwenda (X±SE) range	2.5 ± 1.0	1.8 ± 0.7	0.5 ± 0.3
		0.0 - 7.0	0.0 - 5.0	0.0 - 2.0
February to July, 1994	Nabitalo (X±SE) range	4.2± 1.4	2.3 ± 1.0	0.7 ± 0.5
		0.0 -10.0	0.0 - 6.0	0.0 - 2.0
	Sendusu (X±SE) range	2.0 ±0.9	1.0 ± 0.4	0.7 ± 0.5
		0.0 - 5.0	0.0 - 2.0	0.0 - 3.0
	Mbalala (X±SE) range	6.7 ± 2.6	3.2 ±0.9	2.3 ± 0.2
		2.0 -19.0	1.0 - 7.0	2.0 - 3.0
	Mbalala (X±SE) range	4.5 ± 1.8	1.5 ± 0.7	0.5 ± 0.5
		1.0 - 8.0	0.0 - 3.0	0.0 - 2.0
	Ntawo (X±SE) range	3.8 ± 1.9	1.8 ± 1.0	1.0 ± 0.4
		1.0 - 9.0	0.0 - 4.0	0.0 - 2.0
February to May, 1995	Nabbingo (X±SE) range	4.3 ± 1.4	1.8 ± 1.0	1.0 ± 0.4
		2.0 - 8.0	1.0 - 3.0	0.0 - 2.0
	Kiwenda (X±SE) range	7.5 ± 3.2	3.0 ±1.2	0.8 ± 0.8
		2.0 - 13.0	1.0 - 6.0	0.0 -3.0
	Bombo (X±SE) range	2.8 ± 1.7	1.8 ± 1.2	1.3 ± 0.3
		0.0 - 7.0	0.0 - 5.0	1.0 - 2.0