African Crop Science Journal African Crop Science Society ISSN: 1021-9730 EISSN: 2072-6589 Vol. 7, Num. 4, 1999, pp. 497-502

African Crop Science Journal, Vol. 7. No. 4,  pp. 497-502, 1999

Perfomance of Cotesia sesamiae and Cotesia flavipes (Hymenoptera: Braconidae) as biological control agents against cereal stemborers in Mozambique

D. Cugala, W. A. Overholt¹ , D. Giga² and L. Santos
Eduardo Mondlane University, Faculty of Agronomy and Forest Engineering
P.O. Box 257, Maputo, Mozambique
¹International Centre of Insect Physiology and Ecology, P. O. Box 30772, Nairobi, Kenya
²Department of Crop Science, University of Zimbabwe,  PMB 167, Mount Pleasant, Harare, Zimbabwe

Code Number: CS99040

ABSTRACT

Chilo partellus (Swinhoe) (Lepidoptera: Crambidae), Busseola fusca (Fuller) and Sesamia calamistis Hampson (Lepidoptera: Noctuidae) are the most important stemborers of maize and grain sorghum in Mozambique. Of these, C. partellus is an exotic species which was accidentally introduced into Africa from Asia. Several parasitoids have been recorded from stemborers in Mozambique in previous studies, but the levels of parasitism were typically low. Based on the low parasitism, an exotic parasitoid of C. partellus from Asia, Cotesia flavipes Cameron (Hymenoptera: Braconidae), was introduced at two locations in the southern region of Mozambique in 1996.  Additional releases were made in 1999 in the southern and central regions of the country. Three years after the initial release of C. flavipes, it was recovered in the southern part of the country near one of the 1996 release sites, indicating that it has become established. However, percent parasitism was < 1%. The exotic parasitoid was also recovered from release sites during the second release (1999). The native parasitoid, Cotesia sesamiae Cameron, was the most common natural enemy recovered in the 1999 samples. Parasitism of the native stemborer, S. calamistis, by C. sesamiae was higher than parasitism of C. partellus at all sites, even though C. partellus was the most abundant species. C. flavipes was recovered from B. fusca and the exotic stemborer, C. partellus.

Key Words:  Biological control, establishment, stemborers, natural enemies, parasitoids

RÉSUMÉ

Chilo partellus (Swinhoe) (Lepidoptera: Crambidae), Busseola fusca (Fuller) et Sesamia calamistis Hampson (Lepidoptera: Noctuidae) sont des borers de tige les plus importants du maïs et du sorgho au Mozambique. Parmi eux,  C. partellus est une espèce exotique qui a été introduite accidentellement de l’Asie en Afrique.  Plusieurs parasitoïdes ont été observés chez les borers de tige au Mozambique dans des études précédentes, mais les niveaux du parasitisme étaient faibles.  Suite au parasitisme faible, un parasitoide exotique du C. partellus  d’Asie, Cotesia flavipes Cameron (Hymenoptera: Braconidae), a été introduit dans deux localités dans la région sud du Mozambique en 1996.  Des lâcher supplémentaires ont été faits en 1999 dans les régions sud et centre du pays.  Trois ans après le lâcher initial du C. flavipes, il a été retrouvé dans la partie sud du pay tout prêt de l’un des sites des lâcher de 1996, montrant qu’il était établi.  Cependant, le pourcentage du parasitisme était< 1%. Le parasitoïde exotique a été aussi retrouvé dans les sites de lâcher de 1999 pendant la deuxième période de lâcher.  Le parasitoide natif, Cotesia sesamiae (Cameron),était l’ennemi naturel commun retrouvé dans les échantillons de 1999.  Le parasitisme du borer de tige natif, S. calamistis, par C. sesamiae était plus élevé plus que le parasitsme de C. partellus dans tous les sites, bien que C. partellus était l’espèce la plus abondante.  C. flavipes a été retrouvé chez  B. fusca et chez le borer exotique C. partellus.

Mots Clés: Lutte biologique, establissement, borers de tige, enemis naturels, parasitoïdes

Introduction

Maize (Zea mays L.) is one of the most important cereal crops in Mozambique where it is grown for home consumption and cash income. It is the most widely grown crop occupying more than 30% of the land under cultivation (Ministerio de Agricultura, 1977), and more than 95% of the annual production is produced by small scale farmers. Crop production is limited due to losses caused by pests, often resulting in very low yields (Segeren et al., 1996). Although pesticide use may be effective, they are often not affordable to small-scale farmers (Skoroszewski and van Hamburg, 1987).

Among the insect pests attacking maize and sorghum in Mozambique, lepidopteran stemborers are the most economically important group. Three species are commonly found; the exotic spotted stalk borer, Chilo partellus Swinhoe (Lepidoptera: Crambidae), the maize stalk borer, Busseola fusca (Fuller), and the pink stemborer, Sesamia calamistis Hampson (Lepidoptera: Noctuidae).  Among these, C. partellus and B. fusca are considered to be the most important species (Gonalves, 1970; Segeren et al., 1991). C. partellus is an introduced Asian species, while the other two stemborers are indigenous to Africa. It is thought that C. partellus invaded Mozambique sometime before 1958 when it was first found in neighbouring South Africa (van Hamburg, 1979). Stemborer infestation levels reaching 100%, and yield losses of more than 50% have been reported from small-scale farms in the areas where C. partellus is the most abundant species (Berger, 1981). Attempts at controlling stemborers in Mozambique have been based on the cultural and chemical methods on commercial farms (Ariyanayagan, 1983; Oever, 1990). In small scale farming systems, the use of pesticides is minimal (Leeuwen and Zucula, 1987).

In Mozambique biological control is viewed as an alternative strategy for the management of the exotic stemborer, C. partellus.  A parasitoid of C. partellus from India and Pakistan, Cotesia flavipes Cameron (Hymenoptera: Braconidae) was introduced into southern Mozambique in November 1996 by the Mozambique Plant Protection Department, in collaboration with the International Centre of Insect Physiology and Ecology (ICIPE). ICIPE had earlier introduced C. flavipes into Kenya, which has resulted in its permanent establishment (Overholt, 1998).

The first attempt to introduce C. flavipes into Africa was made in 1968 by the Commonwealth Institute of Biological Control (CIBC).  Releases in Uganda, Tanzania and Kenya did not result in establishment (CIBC 1968-72). Later, intro-ductions were made in Ghana, Côte d’Ivoire  and South Africa, but all reportedly failed to establish  (Scheibelreiter, 1980; Breniere and Bordat, 1982;  Skoroszewski and van Hamburg, 1987). One possible explanation for the failures to establish C. flavipes in some areas of Africa, and the success in others, is the suitability of various stemborer populations for the development of C. flavipes (Overholt, 1998).

This paper reports the introduction and colonisation of Cotesia flavipes in Mozambique. This information may eventually help to explain the success or failure of the biological control project.

Materials and Methods

Establishment and spread of C. flavipes from the 1996 release sites. During 1996/97 growing season (early November), the exotic parasitoid C. flavipes was introduced for the first time in Moamba and Marracuene districts, Maputo Province, in the southern region of Mozambique. About 100 cocoons masses were released at each place according to the method described by Overholt et al. (1994a).

During the 1998/99 growing season, 20 farmers’ fields located in Marracuene District in Maputo Province (southern Mozambique), within a radius of 20 km of the 1996 release site, were randomly selected when maize plants were at the tasselling stage. As much as possible, the fields were evenly distributed in all directions from the release fields.  The exact location (latitude and longitude) of the fields was recorded using a GPS (geographic position system).

In each field, 20 plants of maize were randomly selected, inspected and the presence/absence of symptoms of stemborer infestation was recorded. Where the randomly selected plant exhibited signs of infestation (leaf feeding, entrance holes in the stem), it was removed from the field, taken to the laboratory and dissected. If the selected plant did not appear to be infested, the nearest plant showing symptoms of stemborer infestation was taken. The samples were taken twice (i.e., once in January and once in February) during the season to obtain a large sample of stemborer larvae and to ensure reliable estimation of parasitism.

As C. flavipes attacks only medium- and large-sized stemborer larvae (Ngi-Song et al., 1995), only larvae in these size categories were collected and placed individually in vials with fresh cut maize. Stemborers were identified and reared until they pupated, died or parasitoids emerged. All parasitoids which emerged were recorded and identified. Any larva dying (before parasitoid or cocoon emergence), aestivating, escaping or injured was excluded from the calculations.

Release trials. Trial releases were made in two ecologically different areas, selected according to differences in the stemborer species complex. One area was Nhacoongo village (24º19’41'’S; 35º 12’82'’E; elevation 40 m), a warm, lowland area in the southern province of Inhambane where previous surveys had shown that C. partellus was the dominant stemborer (>90% of the population), followed by S. calamistis  (<10% of the population).  B. fusca has not been recorded from this area (Segeren et al., 1991). The second area was Machipanda (18º52’16'’S; 32º47’96'’E; elevation 800 m), a mid to high elevation, cooler zone located in the Central Province of Manica.  In Machipanda, both B. fusca and C. partellus occur with nearly equal frequency (40% and 60% of the population for B. fusca and C. partellus, respectively) (unpublished data). The selected areas are located 400 km and 1300 km away, respectively, from the locations where C. flavipes had been previously released in 1996.

Four plots of about 1/4 ha each of maize and grain sorghum were sown during the 1998/99 rainy season at each site. Each plot was divided into 4 sub-plots of about 100 m² each; two for maize and two for grain sorghum. Sub-plots were monitored for stemborer infestation during the growing season (November- April) of 1998/99. Insects were allowed to infest plants naturally and no insecticides were applied.

About 60,000 cocoons of C. flavipes were released three times in Nhacoongo in February and about 21,000 cocoons were released once in Machipanda in March, according to the method described by Overholt et al.  (1994a).  Releases were timed to coincide with the presence of suitable larval instars (third and larger). Parasitoids were released both as cocoons and adults. Releasing cocoons is a preferred method as it maximises the effective life span of the adults in the field (Overholt et al., 1997). To protect the cocoons from predators and rainfall, they were placed in a ‘release station’ (Overholt et al., 1994b). The cocoons were shipped to Mozambique from ICIPE’s rearing laboratory  in Nairobi. Two weeks after release, all cocoon masses were collected and the number of adults that did not emerge was estimated by counting the number of dark cocoons or adults dead inside release cage.

Samples of 20 plants were randomly selected from each sub-plot twice in Nhacoongo and once in Machipanda during the growing season. The plants were taken to the laboratory and then dissected, and all stemborer larvae and pupae were removed. All third instar and larger larvae were individually provided fresh pieces of maize or sorghum stem in glass vials (2.5 cm diameter and 7.0 cm high or 3.5 cm x 8.0 cm) and covered by cotton wool and reared until death, pupation or parasitoid emergence. Pupae were individually kept in glass vials without providing them food and covered by cotton wool and reared until death, adult emergence or parasitoid emergence.

Results and Discussion

Establishment and spread of Cotesia flavipes. C. flavipes was found parasitising stemborer larvae up to 20 km from the release sites, and was recovered from 8 out of the 20 sampled sites.  In total, 14 stemborers parasitised by C. flavipes were found in the 20 fields.  However, parasitism was quite low (1%) (Table 1). This was the first time that C. flavipes was recovered from the area where it was previously released in 1996, and indicated that this exotic parasitoid has been established in southern Mozambique. The low level of parasitism is expected and is probably due to the fact that the population build-up of C. flavipes is not sponteneous.  In Kenya, where C. flavipes was released in 1993, the population density remained very low for the first 4 years, and then increased dramatically (Overholt, 1998). The same phenomena has been reported after the release of C. flavipes in Barbados (Alam et al., 1971) and Madagascar (Greathead, 1971).  It appears that the population simply needs time to build up and spread from the release sites. The majority of recoveries were made in fields located more than 10 km from the release sites.  However, the native larvae parasitoid, C. sesamiae, was far more abundant than the introduced species. Parasitism by the native species was 21% on C. partellus and 25% on S. calamistis (Table 1).  The level of parasitism by C. sesamiae found in this study was considerably higher than the 5% previously reported by Segeren et al. (1991) and Davies et al. (1995).

Table 1. Parasitism of stemborer larvae by Cotesia flavipes and C. sesamiae in farmer’s fields in southern Mozambique

Cs - C. sesamiae; Cf – C. flavipes; sex ratio (Female:Male) and progeny produce were estimated from Cs only

The number of progeny emerging from parasitised larvae varied by host; an average of 30 cocoons were produced from C. partellus larvae and 40 from S. calamistis larvae.  It was observed that small larvae (< 3rd instar) produced smaller cocoon numbers than larger larvae of both parasitoid species. One possible explanation is that higher numbers of progeny emerged from S. calamistis because it is larger than C. partellus.  Mohyuddin (1971) reported an average of 105 and 101 C. sesamiae adults emerging from B. fusca and S. calamistis, respectively, and that early larvae instar produced few cocoons. Ngi-Song et al. (1995) reported the highest progeny produced of C. flavipes from C. partellus (36.5) and 35.2 of C. sesamiae from S. calamistis.

Cotesia flavipes release trial. Adults successfully emerged from more than 95% of the cocoons at both release locations. All stemborer species found at each release site, C. partellus and S. calamistis at Nhacoongo, and C. partellus, B. fusca and S. calamistis at Machipanda, were parasitised by Cotesia spp. At Nhacoongo, 594 stemborers were found in maize and 433 in grain sorghum.  Of the borers in maize, 95% were C. partellus and 5% S. calamistis. In sorghum at the same location, 97% were C. partellus and 3% were S. calamistis.  At Machipanda, 241 larvae were collected of which 61% were C. partellus, 32% B. fusca and 7% S. calamistis (Table 2). Thus, C. partellus was the most abundant stemborer at both places.

Cocoons of C. flavipes were recovered at both release sites during the 1998/99 growing season from C. partellus and B. fusca, but not from S. calamistis. Mohyuddin (1971) and Rajabalee and Govendasamy (1988) reported that C. flavipes could not develop in S. calamistis. In contrast, Ngi-Song et al. (1995) found in laboratory trials that S. calamistis was a suitable host for C. flavipes, and Overholt (1998) reported field recoveries of C. flavipes from S. calamistis in Kenya.

The rate of parasitism varied according to stemborer species, location and crop. The highest rate of parasitism by C. sesamiae was found on S. calamistis on grain sorghum (46%) at Nhacoongo, while in Machipanda, 24% of parasitism was reported on grain sorghum (Table 2).  At Machipanda, recoveries of C. flavipes were made only from B. fusca (3%). This is an interesting result because in Kenya it was found that C. flavipes could not successfully develop in B. fusca (Ngi-Song et al., 1995), except in cases where the B. fusca larva was already compromised by another invader.  For example, laboratory work in Kenya showed that when B. fusca was stung by both C. flavipes and C. sesamiae, C. flavipes emerged in some cases (Overholt, unpubl.).  Similar observations have been made on B. fusca larvae attacked by entomogenous nematodes, and then parasitised by C.flavipes (Overholt, unpubl.).  However, Skoroszewski and Van Hamburg (1987) also reported field recoveries of C. flavipes from B. fusca.  Thus, either the immune system of the B. fusca population in southern Africa is sufficiently different from that in East Africa as to allow C. flavipes to develop, or the larvae recovered in this study were also attacked simultaneously by other natural enemies.

 Table 2.  Percent parasitism of cereal stemborers by C. sesamiae and C. flavipes at the  trial release sites

Cs =C.sesamiae; Cf = C.flavipes; sex ratio (Female:Male) and progeny produced were estimated from Cs only

The recoveries of C. flavipes from C. partellus and B. fusca at Nhacoongo and Machipanda in both maize and sorghum provide clear evidence that C. flavipes was able to successfully colonise these areas.  Establishment in these areas can only be determined after several seasons.

Other parasitoids that were found during the sampling period included the pupal parasitoids, Pediobius furvus (Gahan) (Hymenoptera: Eulophidae), and Dentichasmias busseolae Heinrich (Hymenoptera: Ichneumonidae).  Larval parasitoids included Stenobracon (=Euvipio) rufa Szepligeti (Hymenoptera: Braconidae), Goniozus indicus Ashmead (Hymenoptera: Bethylidae) and the egg parasitoid Trichogramma sp. or spp.  The hyperparasitoid Aphanogmus fijiensis. (Ferriere) (Hymenoptera: Ceraphronidae) was recorded from cocoons of Cotesia spp. at both places.

Conclusions

Recoveries of C. flavipes from the 1996 release sites indicated that this parasitoid had established in southern Mozambique. However, the population numbers and percent parasitism were very low and the native parasitoid, C. sesamiae, was still the most abundant. It is expected that the abundance of C. flavipes will increase in the coming years.  C. flavipes was also recovered at the trial release sites, indicating that the parasitoid had colonised the two areas during the growing season.

Acknowledgement

The Rockefeller Foundation’s Forum on Agricultural Resource Husbandry, supported this research. We would like to thank Dr. S. Kimani for parasitoid species identification and Dr. C. Omwega for providing parasitoids and comments. We are grateful to the staff at Nhacoongo Agricultural Research Station and Extension Net at Manica District Directorate of Agriculture and Fisheries for providing and maintaining the maize and sorghum field trials. We also thank M. A. Mucavele and F. Rodrigues for assistance in laboratory work.

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