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Indigenous Natural Enemies Attacking Fall Armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Ghana



Umar Sanda Issa, Kofi Frimpong-Anin, Ibrahim Adama, Moses Brandford Mochiah, Haruna Braimah and Patrick Obeng
 
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ABSTRACT

Background and Objective: The Fall Armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) is a novel invasive pest in Africa but has established as a major pest of maize. Maize fields across six ecozones were surveyed for indigenous natural enemies of S. frugiperda in Ghana. Materials and Methods: Fifty maize plants showing signs of S. frugiperda infestation were sampled from three farms in each of the forty-eight districts blocked within all the six agro-ecological zones of Ghana. Collected S. frugiperda eggs and larvae were cultured in a laboratory for parasitoid emergence and percent parasitism determined. Results: Five species of egg and larval natural parasitoids comprising three Braconidae Coccygidium luteum Brullé, Chelonus sp. and Cotesia sp., one Ichneumonidae Campoletis sonorensis (Cameron) and one Tachinidae Exorista sp were identified. Among the predators recorded were coccinellids (Harmonia octomaculata [F.] and Coccinella transversalis [F.]) (Coleoptera: Coccinellidae), earwigs and spiders. C. luteum was the dominant natural parasitoid and also exhibited the highest field parasitism level, 6.38-10.71%. Parasitism levels of the other parasitoids ranged between 2.56-3.45%. The seemingly low field parasitism observed could be attributed to the high application of broad-spectrum insecticides which inadvertently is inimical to their development. Conclusion: Some indigenous parasitoids are adapting to S. frugiperda. Further exploration and protection of natural enemies through ecofriendly practices in a comprehensive IPM program is imperative for sustainable management of S. frugiperda.

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Umar Sanda Issa, Kofi Frimpong-Anin, Ibrahim Adama, Moses Brandford Mochiah, Haruna Braimah and Patrick Obeng, 2021. Indigenous Natural Enemies Attacking Fall Armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Ghana. Journal of Entomology, 18: 1-7.

DOI: 10.3923/je.2021.1.7

URL: https://scialert.net/abstract/?doi=je.2021.1.7
 
Received: June 09, 2020; Accepted: October 29, 2020; Published: December 15, 2020


Copyright: © 2021. This is an open access article distributed under the terms of the creative commons attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

INTRODUCTION

Fall armyworm (J.E. Smith 1797) (Lepidoptera: Noctuidae) has been the greatest threat to food security, besides climate change, to sub-Saharan Africa since the pest was officially recorded in the continent in 20161-3. This is because of the conductive tropical African environment for its survival and preference for maize, which is an important commodity and widely cropped in sub-Saharan Africa. It is a prime staple crop for many smallholder farmers but also an important cash crop for all categories of farmers4,5. In Ghana, maize is an important staple food for human consumption, in poultry feed production and in the brewery industry. It accounts for 62% of local cereal production4,6,7 and contributes 3.3% to total agricultural production value8,9. Estimated mean yield loss of maize attributed to S. frugiperda in 2018 was 470 000 t amounting to US$177.3 million compared to years prior to the invasion3.

To salvage the wanton destruction by the pest at the height of the invasion, rapid response strategy mainly by the use of chemical insecticides was employed10. Locally available insecticides, mainly broad-spectrum chemical insecticides were found to be the antidote and were mass applied albeit health and environmental implications. Although this turn out to be effective at the onset, it is not the best option for the long term due to the possibility of the pest developing resistance to a broad spectrum of insecticides, issue of residues especially in fresh corn, killing of beneficial insects and other non-target organisms. For these reasons, alternative methods with less deleterious effects are imperative in the development of Integrated Pest Management (IPM) strategies to contain the pest. Viable alternatives include the use of biorationals, natural enemies and habitat manipulation such as the push-pull.

In the Americas where the S. frugiperda is indigenous, several natural enemies have been identified, with a substantial number assessed for their effectiveness in suppressing the pest11,12. It is believed that the natural enemies, particularly natural parasitoids did not come to Africa alongside the pest hence population explosion, with its attendant destruction, soon after its arrival13. It is in this vein that conscious effort to explore sustainable alternative management options that a study to identify natural enemies is being carried out in Ghana by Crops Research Institute. This study has two components: scouting for indigenous natural enemies and Laboratory and field behavioral assessment of efficiency of the identified natural enemies as part of an integrated management strategy against S. frugiperda. This report, however, covers the scouting aspect.

MATERIALS AND METHODS

Study areas: The survey was conducted in all sixteen regions of Ghana, from June, 2018 to August, 2019. The entire country was first zoned into six broad areas based on ecological considerations (Coastal Savanna, Tropical Rainforest, Semi-Deciduous Rainforest, Forest-Savanna Transition, Guinea Savanna and Sudan Savanna). These were further blocked such that all ecological zones within each of the 16 political regions were covered. Thus, three districts per region and three maize farms were randomly selected from major maize growing areas within the regions (Fig. 1). Coordinates and elevation of sampled farms were taken and later marked on Ghana map using, ArcGIS Release 10.6. Maize farms that had not been sprayed since planting and those that had not been sprayed for at least 3 weeks were the benchmarks for selecting a farm for sampling. This was based on farmers’ assertions on insecticide spraying timelines.

Sampling for natural enemies: Sampling for fall armyworm larvae in maize was conducted in all the sixteen regions during the major cropping season (June-August) in the transitional to the coastal ecological zones in the south. That of the Guinea and Sudan Savanna zones was in July-August. Fifty maize plants showing signs of S. frugiperda infestation (frass, window panes, maize leaf blades showing characteristic chewing signs) were then randomly sampled from each farm. Eggs were collected by cutting sections of the maize leaves with egg masses and put into labelled 1 litre plastic jars and the open end covered with fine nylon mesh fastened with rubber bands.

The type of predators and their activities such as capturing of larva of S. frugiperda at the time of examining infested maize plants was also observed.

Both alive and dead S. frugiperda larvae of different instars were also collected from randomly selected infested maize (i.e., signs of fresh frass, leaves with holes/window panes). Larval lengths were measured and categorized into different instars: < 1 cm (1st-2nd instar), 1-2 cm (3rd-4th instar) and >2 cm (5-6th instar). Each specimen was put into a separate 350 mL disposable plastic cup and covered as in the jars.

Rearing immature fall armyworm for natural parasitoids: Samples were taken to and kept in the laboratory at 28-30°C, pending emergence of natural parasitoids from eggs, larvae and pupae. The live S. frugiperda larvae were fed with fresh-cut young maize leaves daily until they pupated or died. Larval droppings were cleaned every other day.

Fig. 1:Map of surveyed areas and locations where natural parasitoids were collected

Set up was observed daily, observing any changes in the S. frugiperda larvae/pupae as well as the collection of emerged parasitoids. The parasitoids that emerged from the eggs or larvae were recorded every 24 hrs until pupation. Samples of the parasitoids preserved in 70% ethanol were sent to the University of Ghana and CABI-Ghana for identification. The percentage parasitism of each parasitoid was calculated based on the proportion of parasitoids that emerged from the total number of S. frugiperda larvae per farm14:

RESULTS AND DISCUSSION

Natural parasitoids: Five natural parasitoid species belonging to three insect families, which include Braconidae, Ichneumonidae and Tachinidae emerged from the cultured S. frugiperda collected from the field. One species, Chelonus sp. is an egg parasitoid while four species, comprising Coccygidium luteum Brullé, Cotesia sp., Campoletis sonorensis (Cameron) and Exorista sp. are larval parasitoids. The natural parasitoids identified in the study and brief descriptions of their attributes as natural enemies are presented in Table 1.

The distribution of the parasitoids, as shown in Fig. 1, data indicated they were more predominant in the eastern corridor of the country. These hotspots are predominantly characterized by Coastal and Transitional ecological conditions. These ecological zones are moderately dryer compared to the forest zones but comparatively wetter than the Guinea savanna. Nevertheless, the observed pattern probably reflects the direction from where the pest entered Ghana and first established. Based on the evidence that S. frugiperda moved in from the eastern part of West Africa (possibly Nigeria)2 and probably colonized these areas earlier, affirmed by the first official report in Ghana coming from Eastern Region (Fig. 1)10. Subsequent surveys over time in the mid to western parts of the country are therefore expected to produce more natural parasitoids.

The highest parasitism, ranging between 6.38-10.71% was recorded for C. luteum. The parasitism levels of 2.56-3.45, 2.86, 2.17 and 2.35 for the other four natural parasitoids Chelonus sp., C. sonorensis, Exorista sp. and Cotesia sp., respectively were relatively very low (Table 2). The relatively high parasitism exhibited by C. luteum compared to the rest of the collected natural parasitoids in the field coupled with a wide distribution in Ghana, of this natural parasitoid makes it a promising candidate for the management of S. frugiperda in Ghana.

The most widely distributed natural parasitoid was the Coccygidium luteum Brullé (Fig. 1 and Table 2). The C. luteum has recently been reported to be associated with S. frugiperda in Ethiopia, Sisay et al.15 as well as in Ghana and Benin23 with high parasitism level and a significant reduction in S. frugiperda population.

Table 1:Identified natural parasitoids of fall armyworm

Table 2:Levels of fall armyworm parasitization by natural parasitoids in the field

Coccygidium spp. have been found to attack several Spodoptera species including S. frugiperda, S. exigua, S. exempta and S. litura in several countries from West to Southern Africa16 and India as well as parts of Middle East24.

The generally low parasitism levels of S. frugiperda by the recorded natural parasitoids could be due to the excessive use of broad-spectrum insecticides in surveyed areas (Table 2). While some farmers indicated they have not yet sprayed their farms at the time of sampling, the majority had at least once applied insecticides prior to the collection of specimens although farms that had not been sprayed for at least 3 weeks were purposively selected. A survey reported by Groote et al.3, who indicated that there is widespread and high use of broad-spectrum insecticides in all maize growing areas in Ghana. Repeated field trials without application of insecticides in the hot spots are expected to record higher parasitism levels among all the parasitoids identified in this study.

Chelonus sp. and Cotesia sp. are two other Braconid parasitoids that were found attacking S. frugiperda in this study. Although their distribution and parasitism levels were limited in the studied areas, particularly Chelonus sp., they are known to be effective generalist parasitoids of agricultural importance. Cotesia sesamiae (Cameron) has been known to parasitize noctuid stemborers in Africa with the capability of expanding its host range25,26.

Another important parasitoid in our collection worth considering is Campoletis sonorensis though its distribution was not widespread in this survey. C. sonorensis have been identified as a major parasitoid of S. frugiperda in Mexico12,26 where both maize and the pest originated. Another species from the Genus have also been recorded in India, where the pest recently invaded18,27. High parasitism level (30-35%) of Campoletis on S. frugiperda were recorded by Barreto-Barriga et al.12 in Mexico but the 3% by C. chlordideae recorded by Sharanabasappa et al.24 in India was very low, probably due to the limited area surveyed by the latter. The importance of Campoletis in the suppression of S. frugiperda is the evidence suggesting that it is attracted to the plant of its host even if the host is present or absent19. Adoption of good management practices in maize fields will inadvertently help the colonization of this natural parasitoid.

Exorista sp. is the only parasitoid of the order Diptera recorded in the current survey and was found in only one location in the middle belt. The parasitism level was low and similar to the other natural parasitoids, except C. luteum. Sissay et al.15 observed Palexorista zonata (Curran) (Diptera: Tachinidae) to attack S. frugiperda with appreciable parasitism levels in Kenya and Ethiopia but not in Tanzania.

Predators: A number of predators were also observed attacking S. frugiperda on infested maize. They included coccinellids (Harmonia octomaculata [F.] and Coccinellastrans versalis [F.]) (Coleoptera: Coccinellidae), earwigs Forficula sp., wasps, a wide range of spiders and the millipede eating ants Plectoctena sp.

Sharanabasappa et al.24 suggested H. octomaculata and C. transversalis and Forficula sp. might be of great importance against early larval instars of S. frugiperda in India. This is because high numbers of these predators, which are known to prey on eggs and larvae of lepidopterans, were encountered in maize fields infested with S. frugiperda.

According to Schatz et al.28 workers of Plectoctena minor, mainly prey on millipedes but have the tendency to prey on other soft-bodied arthropods, including termites and larvae of beetles. Late instar S. frugiperda larvae that drop to the ground ostensibly to pupate were preyed upon in fields where Plectoctena sp. was abundant. All these predators are critical to the management of F. frugiperda. The actual impact of these predators in suppressing S. frugiperda needs to be assessed further.

CONCLUSION

Some indigenous parasitoids of lepidopterans have been identified to attack the invasive S. frugiperda in Ghana. It can be concluded that the dominant parasitoids are from the Hymenoptera family, particularly the order Braconidae. The most predominant parasitoid recorded in this survey with great potential for the management of the S. frugiperda is the Coccygidium luteum Brullé followed by Campoletis sonorensis Cameron. The parasitism levels of C. luteum amidst heavy insecticide usage were highly appreciable. Further on-field insecticide exclusion studies at different ecological zones need to be undertaken before meaningful integrated pest management strategies involving the natural enemies can be developed.

SIGNIFICANCE STATEMENT

This study discovered five indigenous natural parasitoids and some predators that can be beneficial for the management of the new invasive pest, fall armyworm in Ghana. This study will help researchers to uncover the critical areas of natural enemy dynamics that many researchers were not able to explore. Thus a new theory on the spate of how natural enemies adapt to new pests may be arrived at.

ACKNOWLEDGMENT

The authors are thankful to Dr. Lakpo Koku Agboyi. CABI, Accra and Dr. Maxwell Billah, University of Ghana, Legon for identifying the specimen. We are also grateful to our able technicians Gilbert Agyeman and Paul Adjei for the laboratory work and Mr. Alexander Owusu Ansah of CSIR-Soil Research Institute for the cartographic work. This research was funded by Alliance for a Green Revolution in Africa (AGRA: Grant number 2017 GH006) while funds for the publication was provided by Korea-Africa Food and Agriculture Cooperation Initiative (KAFACI).

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