What is ARMYWEB?

ARMYWEB is a web-based resource for the Armyworm Biological Control (ABC) Consortium, a group of researchers and other stakeholders interested in the genetics, ecology and evolution of the African armyworm moth (Spodoptera exempta, Lepidoptera: Noctuidae) and its baculovirus (SpexNPV), and the application of this virus for armyworm biological control.

Members of the Consortium have worked together on a number of related projects since 1996, funded by the Natural Environment Research Council (NERC), the Department for International Development (DFID), US-AID, and other funding bodies.

What is the African armyworm?

The African armyworm moth, Spodoptera exempta is one of the most devastating crop pests in eastern Africa. It is the caterpillar or larval stage that causes such havoc, voraciously feeding on maize, wheat, sorghum, millet, rice and pasture grasses. 

Armyworm have been reported throughout sub-Saharan Africa, however the vast majority of outbreaks occur in the eastern half of the continent, and especially in Tanzania, Kenya and neighbouring countries.

During the long dry season (c. May to September), armyworms occur at very low densities in coastal regions, and other areas where green vegetation is available all year round.

The first outbreaks of the season occur when moths from these low-density populations are concentrated by the convective winds associated with the first rainstorm of the short rains in October-December. These first outbreaks generally occur in identified primary (1⁰) outbreak areas in Tanzania and Kenya. They then spread sequentially across the continent at roughly monthly intervals over a period of 5-8 months, as successive generations of adult moths migrate on the prevailing winds and initiate new high-density larval outbreak cycles (Figure 1).

The most reliable predictor of the annual magnitude of armyworm outbreaks in East Africa is the amount of early-season rainfall: When the rains in November-December are heavy and frequent, relatively few armyworm outbreaks occur throughout the region, whereas when the early-season rains are poor, outbreaks are much more common and widespread (Harvey & Mallya 1995). The exact cause of this relationship has yet to be established.

When armyworms attack the newly sown crop, serious losses result.

The main management tool for armyworm is the application of imported chemical pesticides.

However, recent studies have shown that chemical insecticides are too costly for 70% of smallholder farmers in Tanzania (Njuki et al. 2004), many of whom are women growing cereals that form the most important element in the family food supply for poorer households. 

An alternative method of control for armyworm is a recognised National priority for many of the countries affected. 

What are the alternatives to chemical insecticides?

Whilst the need to control crop pests is well recognised, there is a growing realisation that reliance on chemical insecticides has major limitations. High cost limits the availability of chemical insecticides to poor subsistence farmers, and their use has negative impacts on non-target organisms, including beneficial insects, livestock, wildlife and man, as well as on the environment as a whole.

Consequently, increased effort has been channelled into the development of highly effective alternative control methods, including the use of microbial biopesticides.

These are biological control agents that are natural pathogens of the target pest species, and include entomopathogenic fungi (such as Green Muscle®), bacteria (including Bt) and viruses (including commercially available baculoviruses – NPVs and GVs).

African armyworm baculovirus

African armyworms play host to a highly specific baculovirus: Spodoptera exempta nucleopolyhedrovirus (SpexNPV).

Larvae become infected when they ingest vegetation contaminated with virus occlusion bodies (OBs). The OBs break down in the alkaline conditions of the insect’s mid-gut and the virus replicates within host cells, generating millions of new OBs. Within 3-5 days the larvae die and they exhibit a characteristic inverted-V shape as they hang from vegetation (see photo). Soon, their cuticle ruptures, liberating the OBs on the vegetation where they can infect conspecifics.

1.      SpexNPV is highly host-specific and so does not pose a threat to non-target organisms (Cherry 1992); 
2.         SpexNPV is as effective as currently used chemical insecticides (e.g. Diazanon) when applied using either ground or aerial systems, achieving <90% kill rate (Grzywacz et al. 2007)
3.          Field-based production of SpexNPV in Tanzania is both feasible and affordable, costing approximately US$3 per hectare (Mushobozi et al. 2005)
4.          The proportion of armyworm outbreaks showing signs of overt viral disease at the beginning of the armyworm season is extremely low or zero whereas, in some years at least, it increases to nearly 100% of late-season outbreaks, when many armyworm outbreaks are effectively controlled by the virus
5.          There is a strong positive relationship between larval population density and the prevalence of SpexNPV (Redman 2005), consistent with the hypothesis that the virus is being transmitted horizontally between caterpillars in a density-dependent manner (e.g. Anderson & May 1981)
6.          As larval density and virus prevalence increases, so too does the proportion of viral infections containing two or more virus genotypes (Redman 2005)
7.          Different virus genotypes (‘clones’) differ significantly in their pathogenicity to armyworm and mixed-clone infections were significantly more pathogenic than any single-clone isolate tested (Redman 2005)
8.          SpexNPV is widely prevalent in a “persistent^”, non-pathogenic form that can be vertically-transmitted from parents to offspring (Vilaplana et al. in press) (see Box 1). In a host whose population is both migratory and subject to extreme fluctuations in numbers, the ability of a lethal pathogen to persist in a non-pathogenic form that can be passed vertically to the host’s offspring is key to its survival. This is both interesting and potentially an important characteristic that could be exploited in control, if its activation and persistence mechanism was better understood
9.          Insects receiving a sub-lethal dose of the virus as larvae have an increased level of overt disease in their offspring, passed on to them primarily via trans-ovarial vertical transmission (Vilaplana et al. 2008). 

Box 1. Persistent, covert virus infections

Most viruses are transmitted in a density-dependent fashion and so rely on interactions between hosts for transmission and persistence. This becomes a problem in low density populations due to a shortage of new hosts to infect. Consequently, viruses have evolved a number of mechanisms to ensure persistence in the face of low or variable host densities. For the insect viruses, these include long-term survival in the environment, alternative hosts and vertical transmission.

While it has long been thought that horizontal transmission and persistence in the environment (outside of the host) are the main means of baculovirus survival, it is becoming increasingly evident that many species harbour ‘covert’ infections that are passed from adults to their offspring. Our understanding of this process, even in a group as widely employed as insecticides as the baculoviruses, is poor and we have little idea of how covert infections contribute to the maintenance of virus populations in the field.

There are two types of covert virus infection; ‘persistent’ infections and ‘latent’ infections. They are distinguished by the degree to which virus-encoded gene products are expressed and whether or not infectious virus particles are present.

Persistent virus infections are characterised by a constant low-level production of virus particles within an infected cell.  These infections represent a balance between the host and the virus, which may be maintained through the interaction of the cells and the virus alone, interaction with the host immune system, the production of defective interfering virus, or a combination of all three.  Persistent virus infections still express the full range of viral genes, although this expression may be down-regulated.

In a latent virus infection, the viral genome, and possibly some virus-encoded products, are present, but infectious virus particles are not formed.  Latent virus infections involve a shut-down in viral gene transcription with only those genes involved in maintaining the latent state being expressed.  Latent infections do not represent a dead-end for the virus as, with an appropriate triggering stimulus, the infection can revert to a fully reproductive overt infection.

For the majority of these ‘covert’ infections in insects, it has yet to be determined whether they represent persistent or latent infections, but clearly their prevalence indicates that they may play an important role in the survival and persistence of the virus in host populations.

The ultimate goal of the African Armyworm Baculovirus Project is to further our understanding of the natural interaction between an insect host, the African armyworm (Spodoptera exempta), and its virus (SpexNPV), with a view to determining the impact of the virus on its host’s outbreak dynamics and how this might ultimately be manipulated in a novel, Africa-wide strategic control system (Box 2).

The project has the following specific objectives:

1.        To determine the spatial and temporal pattern of natural virus epizootics.

2.        To examine seasonal and spatial trends in the degree of genetic and phenotypic variation in the virus.

3.        To determine whether the prevalence of “persistent” SpexNPV infections in field populations varies within and/or between seasons and whether this mirrors the pattern of overt virus epizootics

4.      To determine the tissue specificity of “persistent” viruses, the factors that might trigger them to become lethal and the effect of sub-lethal infection on overt disease in the next generation.

5.        To determine which environmental factors predict the spatio-temporal variation in armyworm outbreaks and viral prevalence.

Box 2. Strategic control of armyworm using SpexNPV

Strategic control defined:

Conventionally, armyworm control is implemented when the caterpillars are feeding on food crops, with the aim of reducing losses. However, there is the potential for an alternative strategy for reducing armyworm impact: “strategic control”.

With this strategy, the pest is controlled in primary outbreak areas early in the armyworm season, regardless of which host plant it is feeding on, with the aim of preventing these infestations from acting as source populations for future pest outbreaks at the same sites or elsewhere (Rose et al. 2000).

Strategic control is longer-term and indirect, and is particularly appealing for migratory pest species because it can help to limit the geographical spread of the pest, so allowing resources for control to be better focussed.

African armyworm strategic control

African armyworm moths are highly migratory and can fly 100 km or more per night over several consecutive days (Rose et al. 2000). Their movements are largely governed by the seasonal progression of the inter-tropical convergence zone (ITCZ).

Thus, armyworm outbreaks in southern and central Tanzania act as “source” populations for moths that will migrate to northern Tanzania and Kenya. The offspring of these moths will ultimately migrate further northwards towards countries such as Sudan, Ethiopia, Somalia and Yemen; they also move southwards towards South Africa.

So, by controlling early-season outbreaks over large areas of central/southern Tanzania, it may be possible to prevent subsequent outbreaks from occurring in other parts of Tanzania and the rest of Africa later in the season.

Strategic control using chemical insecticides

Whilst strategic control of armyworm appears to be both desirable and economically feasible (Cheke & Tucker 1995), there are a number of problems associated with implementing this policy using conventional insecticides.

First, it is undesirable to inundate the environment with large amounts of toxic chemicals that could provide a health risk to humans and their livestock, as well as to beneficial non-target insects and wildlife.

Second, it is unlikely that enough of the key outbreaks could be controlled using conventional insecticides, due to restrictions associated with spraying chemicals in National Parks and other sensitive wildlife areas, as well as the high costs of chemical insecticides.

However, neither of these problems is associated with armyworm control using NPV, due to the benign nature of the product and its relatively low cost (around US$3 per hectare for field-produced virus).

Strategic control using baculovirus

SpexNPV also has a number of potential benefits not offered by conventional chemical insecticides.

In particular, unlike chemical insecticides, the virus is self-replicating.  This means that it not only kills the caterpillars targeted during the control operation, but also produces new virus OBs which then become available to infect new hosts several days later (‘secondary cycling’).

In addition, moths that are sub-lethally infected as larvae appear capable of passing on lethal infections to their offspring, via vertical transmission of the virus through the ova (Vilaplana et al. in press).

So, not only does SpexNPV result in effective control of armyworms in situ, but it may also provide a mechanism for controlling future outbreaks at the same site or elsewhere, as the virus migrates from outbreak to outbreak with sub-lethally infected moths.

Moreover, it potentially points to a novel approach to biological control by deliberately applying sub-lethal doses of virus to early-season outbreaks, with the aim of generating sub-lethal infections in adult moths that could disseminate virus to distant outbreaks where virus epidemics might be triggered.

Importantly, using field-based techniques, we estimate that SpexNPV could be manufactured for something in the region of US$3 per hectare, compared with around US$10 per hectare for many chemical insecticides.

Although a large-scale, strategic approach to pest management poses many logistical challenges, especially in Africa, there are a number of examples were an area-wide approach to pest control has proved extremely successful and highly cost-effective, including screwworm eradication in North Africa (e.g. Lindquist et al. 1992) and cassava mealybug control in West Africa (e.g. Neuenschwander 2001)

For enquiries about the African Armyworm Baculovirus Project, email Dr Ken Wilson (ken.wilson@lancaster.ac.uk) or one of the other project partners.

Consortium Partners

•          Dr Ken Wilson (Lancaster University, UK)
•          David Grzywacz (University of Greenwich, UK)
•          Wilfred Mushobozi (EcoAgriConsult Ltd, Tanzania)
•          Prof Jenny Cory (Simon Fraser University, Canada)
•          Prof Seif Madoffe (Sokoine University of Agriculture, Tanzania)
•          Gaspar Mallya (Pest Control Sevices, Ministry of Agriculture, Tanzania)
•          Dr Alan Shirras (Lancaster University, UK)

Project Researchers

•       Dr Rob Graham (Lancaster University, UK)
•       Yamini Tummala (Lancaster University, UK)
•       Phil Nott (Lancaster University, UK)

Armyworm in the news

For latest armyworm news, click on the News page

Key Armyworm publications:

• Armyworm biological control leaflet (2008)
• DFID “Perspectives on armyworm biological control” article (2006)
• “Pathways Out of Poverty” – Aspects of Applied Biology #75 (2005)
• Field trials of armyworm SpexNPV – Crop Protection #27 (2008) 
• Vertical transmission of SpexNPV virus in armyworms – Oecologia (2008)
• Armyworm migration in East Africa – Journal of Animal Ecology (1993)
• Density-dependent armyworm NPV transmission – Proceedings B (1998)

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References:

Anderson, R.M. and R.M. May (1981) The population dynamics of microparasites and their invertebrate hosts. Phil. Trans. Roy. Soc. Lond. B. 291: 451-524.

Benton TG, Plaistow SJ & Coulson TN (2006) Complex population dynamics and complex causation: devils, details and demography.  Proc. Roy. Soc. Lond. B. 273: 1173-1181.

Burden JP, Possee, RD, Sait SM, King LA & Hails RS (2006) Phenotypic and genotypic characterisation of persistent baculovirus populations of the cabbage moth (Mamestra brassicae) within the British Isles. Archives of Virology 151: 635-649.

Cheke RA & Tucker MN (1995) An evaluation of the potential economic returns from the strategic control approach to the management of African armyworm Spodoptera exempta populations in East Africa. Crop Protection 12: 91-103.

Cherry, A. J. (1992). Cross-infectivity of Spodoptera exempta nuclear polyhedrosis virus (SeNPV) and the infectivity of foreign viruses in S. exempta. Project Technical Report. Project A0047 Natural Resources Institute. Chatham UK. pp6

Coulson T, Catchpole EA, Albon SD, Morgan BJT, Pemberton JM, Clutton-Brock TH, Crawley MJ & Grenfell BT (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science 292: 1528-1531.

Day RK, Haggis MJ, Odiyo PO, Mallya G, Norton GA & Mumford JD (1996) WormBase: A data management and information system for forecasting Spodoptera exempta (Lepidoptera: Noctuidae) in eastern Africa. J. Econ. Entomol. 89: 1-10.

Grzywacz D, Mushobozi W, Parnell M, Jolliffe F & Wilson K (in press) The evaluation of Spodoptera exempta nucleopolyhedrovirus (SpexNPV) for the field control of African armyworm (Spodoptera exempta) in Tanzania. Crop Protection.

Harvey AW & Mallya GA (1995) Predicting the severity of Spodoptera exempta (Lepidoptera: Noctuidae) outbreak seasons in Tanzania. Bull. Ent. Res. 85: 479-487;

Hodgson DJ, Hitchman RB, Vanbergen AJ, Hails RS, Possee RD & Cory JS (2004) Host ecology determines the relative fitness of virus genotypes in mixed-genotype nucleopolyhedrovirus infections. J. Evol. Biol., 17: 1018-1025.

Ibrahim KM, Yassin Y & Elguzouli A (2004) Polymerase chain reaction primers for polymorphic microsatellite loci in the African armyworm, Spodoptera exempta (Lepidoptera: Noctuidae). Molecular Ecology Notes 4: 653-655.

Lee KP, Cory JS, Wilson K, Raubenheimer D & Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. Roy. Soc. B., 273: 823-829.

Leirs H, Stenseth NC, Nichols JD, Hines JE, Verhagen R & Verheyen W (1997) Stochastic seasonality and nonlinear density-dependent factors regulate population size in an African rodent. Nature 389: 176-180.

Lindquist DA, Abusowa M & Hall MJR (1992) The New World screwworm fly in Libya – a review of its introduction and eradication. Medical & Veterinary Entomology 6: 2-8.

Mushobozi WL, Grzywacz D, Musebe R, Kimani M & Wilson K (2005) New approaches to improve the livelihoods of poor farmers and pastoralists in Tanzania through monitoring and control of African armyworm, Spodoptera exempta. Aspects of Appl. Biol. 75: 37-35.

Neuenschwander P (2001) Biological control of the cassava mealybug in Africa: a review. Biological Control 21: 214-229.

Njuki J, Mushobozi W & Day R (2004) Improving armyworm forecasting and control in Tanzania: a socio-economic survey. CABI Africa Regional Centre Nairobi 39. pp49.

Parnell, M., Grzywacz, D., Jones, K, A,. Brown, M., Oduor, G. & Ong’aro, J. (2002) The strain variation and virulence of granulovirus of diamond back moth (Plutella xylostella Linnaeus, Lep., Yponomeutidae) isolated in Kenya.  J. Invert. Pathol. 79: 192-196.

Redman EM (2005) Baculovirus Diversity and its Effect on Virulence. PhD Thesis, University of Stirling.

Rose DJW, Dewhurst CF & Page WW (2000) The African Armyworm Handbook: The Status, Biology, Ecology, Epidemiology and Management of Spodoptera exempta (Lepidoptera: Noctuidae). Natural Resources Institute, Greenwich.

Vilaplana L, Wilson K, Redman EM & Cory JS (2009) Pathogen persistence in migratory insects: high levels of vertically-transmitted virus infection in field populations of the African armyworm. Evolutionary Ecology 22pp. DOI: 10.1007/s10682-009-9296-2.