Farmer Baba Alphonse, northern Benin

Sixty-year old farmer Alphonse Ogoule-Okpe of Ogoukpate Village, about 40 km from Porto Novo in northern Bénin, had all but abandoned cassava and maize farming.

Many years ago, insects (mealybug and cassava green mite) and diseases (such as blight) had attacked his cassava crops and “Baba” Alphonse and many like him in his village were hit hard because of the low yields and loss of a food and cash crop. The problem was compounded by the poor soil conditions in the fields.

During a visit to the small village by IITA scientists who distributed planting materials of improved IITA cassava varieties, Baba Alphonse said, “I would be happy if the problem with these insects and diseases will be over. Thanks to IITA, I can plant a new variety that is resistant to the problem pests.”

Unknown to farmer Alphonse, a few kilometers away from his farm was where the predator of the cassava green mite, T. aripo, was first released in Benin by IITA—way back in 1993. That—and his use of the new varieties from IITA would help ensure better cassava harvests for his family and the community.

Variegated grasshopper (Zonocerus variegatus). Photo from Wikimedia commons

When several exotic pests were accidentally introduced into Africa from South America through infected planting materials in the early 1970s, ravaging economically important crops, such as cassava, scientists turned to the origins of the pests to solve the problem.

A lot has been said about the benefits of biological control or biocontrol. It is natural and safe to the environment and humans, and rigorous tests ensure that it is effective only on the target pests.

And almost three decades of research and development at IITA have shown the continuing effectiveness and sustainability of biological control in combination with other approaches for managing insect pests.

These biocontrol practices and technologies provide the subsistence farmers in sub-Saharan Africa with solutions that are sometimes their only safety net.

This issue on biocontrol celebrates the success of solutions to problems in tropical agriculture that IITA and its partners have developed for millions of African farmers.

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Farmer tending cowpea crops in Borno. Photo by IITA

An 81% increase in farmers’ incomes over the past 5 years from improved yields, better access to farm inputs, and social empowerment are the key results of the US$6.33 million PROSAB project in northern Nigeria.

PROSAB is Promoting Sustainable Agriculture in Borno State, a project started in 2004 by IITA with Canadian International Development Agency (CIDA) funding.

In a conference held last September in the state capital of Maiduguri, government officials, farmers, participants, local partners, and other stakeholders said that PROSAB has “helped significantly increase agricultural productivity and build the capacity of thousands of farmers and farmers’ associations in the northern Nigerian state.”

Key project interventions included the introduction of improved crop varieties from IITA, training of farmers on improved agronomic practices, and promotion of gender equality, especially empowerment of women, in agricultural development.

The local government plans to upscale the project to further reduce poverty by promoting greater farmer education on best agricultural practices through the Agricultural Development Program; and encouraging more women to participate in the program.

Amare Tegbaru, PROSAB Manager, says the program has also improved the nutrition of farmers, especially children. “Farmers who adopted improved technologies and management practices experienced increased food availability and improved livelihood. Also, considerable progress has been made in addressing the problems of declining soil fertility and witchweed (Striga hermonthica),” he says.

Last year, in partnership with Google Books, IITA started digitizing and uploading more than 200 publications, which are now available via Google Book Search (GBS). It also uploaded videos in SciVee and YouTube. Now, IITA has accounts with Twitter and Facebook too.

Increasing its online presence is an initiative aimed at “getting the word out” to a wider audience and driving more traffic to the Institute’s Web sites. With these free and popular online services, IITA is potentially tapping into a 300 million-plus combined user-base. Even with just a 1% bite, potentially some 3 million people will get to know more about IITA and what we do.

TGX1835-10e, a rust-resistant soybean. Photo by IITA

Tagged TGx 1835-10E, the variety was bred by scientists at IITA and further developed in collaboration with Nigeria’s National Cereal Research Institute (NCRI).

“The variety is high yielding, averaging 1.6 t/ha grain and 2.2 t/ha fodder in field trials in Nigeria,” says Olumide Shokalu, NCRI pathologist who conducted the trials. It is also early maturing, has good promiscuous nodulation, and resists pod shattering and other prevalent diseases.

“The variety can be used for direct cultivation in tropical Africa or as a source of resistance genes. It was previously released in Uganda through Makerere University, and has already shown excellent performance in trials carried out in Southern Africa, suggesting that it is a well-adapted variety,” says Hailu Tefera, IITA soybean breeder.

“The drought-tolerant maize varieties have mitigated the effects of drought on maize production and farmers are having better incomes,” says Olumide Ibikunle, Research and Development Manager, Premier Seeds. “The seed industry is also better off because demand for maize has actually increased.”

Over the years IITA, CIMMYT, and partners have released several drought-tolerant varieties including Samaz 16, ZM309, and ZM523, in sub-Saharan Africa to cushion the effects of drought on the crop and, ultimately, on farmers and their households.

Researchers and other stakeholders said that developing such varieties will boost maize production, enhancing not only incomes but more importantly food security.

According to Edward Kanju, IITA cassava breeder, 14 types of the crop under research are very promising. Kanju’s team had just harvested an advanced trial of such cassava in Uganda.

This is the fourth year of trials for dual-resistance cassava for the mid-altitudes in Uganda. The trials are being conducted at Mukono, near Kampala, an area regarded as a hot spot for CBSD and CMD. The breeding work started with over 5,000 true seeds of parents with tolerance to CBSD from Tanzania for crossing with IITA varieties that are resistant to CMD.

Farmers have also been involved in the selection process to ensure that the varieties meet their preferences on cooking, taste, texture, and yield. Breeding for dual-resistance cassava is also being conducted in Tanzania and DR Congo.

Close up of Bemisia tabaci adults. Photo by CIAT

Who would think that delicate and exquisite little insects such as whiteflies could pose an ongoing and global challenge to humankind’s need to meet its food requirements?

Whiteflies are one of the top 10 most serious pest threats to agriculture. Although whiteflies, in the taxonomic family Aleyrodidae, are a diverse group of insects of more than 1,200 species, only a few of these are economically important. Among this small group, Bemisia tabaci (Genn.) is by far the most important single species.

B. tabaci was first described from tobacco in Greece, towards the end of the 19th century. Its progress has closely matched developments seen in agriculture in subsequent years, and it now occurs virtually throughout the crop-growing parts of the globe. Its preference for warm weather means that it is particularly prevalent in the tropics, although it has also been able to exploit protected agricultural environments in temperate regions.

Deadly partnerships
If B. tabaci contented itself with doing its own thing and sucking small quantities of sap from the plants that it feeds on, it would probably have fallen under the radar of those whose job it is to protect crops. But it did not. Over time, it evolved a relationship with plant viruses, a relationship that allowed the whitefly to pick up viruses when feeding on plants, harbor them for some time, before introducing them to another plant during feeding, thereby giving rise to a new infection. This enabled the viruses transmitted to expand their ranges as B. tabaci populations grew and spread. These deadly partnerships thus gave rise to plant disease epidemics that had devastating impacts on the crops affected, and on the people growing them.

Large population of B. tabaci adults feeding on the underside of a young cassava leaf. Photo by IITA

B. tabaci transmits many hundreds of virus species, a number that keep rising as more viruses are described and research efforts on the B. tabaci vector are also broadened. The viruses transmitted fall into four virus genera: Begomovirus (family Geminiviridae), Ipomovirus (Potyviridae), Crinivirus, and Carlavirus (Closteroviridae). More than 90% of the more than 100 species transmitted, however, are in the Begomovirus group. One of Africa’s most economically destructive diseases, cassava mosaic disease (CMD), is caused by a group of viruses in the Begomovirus genus. Collectively, these are usually referred to as the cassava mosaic geminiviruses. Evidence also points to B. tabaci being the vector of cassava’s other major expanding disease threat, cassava brown streak disease (CBSD) caused by the Ipomovirus, cassava brown streak virus.

Cassava has always been at the heart of IITA’s research-for-development agenda. Thus, diseases such as CMD and CBSD, and the agents that promote their spread, have long been the focus of research efforts. From its earliest beginnings, IITA was fortunate to receive cassava germplasm, developed in East Africa through the Amani breeding program that most importantly was endowed with resistance to CMD.

It may have been an unfortunate spin-off of the tremendous success of the CMD-resistant varieties, but B. tabaci, the humble vector of the CMGs, received very little research attention before the 1990s. Things were to change abruptly in the mid-1990s, however. It became increasingly clear that unusually large whitefly populations were propelling the expansion of a new, highly virulent form of CMD in Uganda.

Studying the pandemic
IITA initiated a wide-ranging research program with the dual aims of enhancing scientific understanding of the deadly virus-vector combination as well as working with national partners to manage the pandemic.

The genetics and epidemiology of CMGs associated with the pandemic were extensively documented over the decade following the initial explosion of interest. Although less research attention was focused on the whitefly vector, a number of important advances were made in understanding the nature and role of B. tabaci. Perhaps most significantly, it was demonstrated that superabundance of B. tabaci was a key factor driving the pandemic’s so-called ”front”, and, furthermore, that the front could be pushed forwards by up to 100 km/year in this way. Although whiteflies are weak fliers, single B. tabaci individuals have been shown elsewhere to fly for up to 7 km, assisted by the wind, and given a generation time of slightly less than one month, it is easy to see how such a long distance spread could be achieved.

Superabundant B. tabaci and the CMD pandemic (Yellow shaded area is the approximate region affected by the CMD pandemic by 2009. Arrows indicate the direction of pandemic expansion. White explosions indicate areas in which B. tabaci superabundance has been most prominent, together with associated physical damage to cassava crops.). by IITA

Extensive and regular disease surveys conducted by IITA and its NARS partners from 1997 up to the present have helped build up a comprehensive picture of the pandemic’s expansion into 11 countries of East and Central Africa and the interrelationships with vector populations. Moreover, these data have been used to provide risk assessments of future patterns of spread which have supported disease management initiatives.

Superabundant B. tabaci populations are typically 100-fold greater than those outside the pandemic zone. As well as delivering a sharply increased level of virus transmission, these cause physical damage to cassava plants. Experimental studies conducted at IITA-Uganda showed that yield losses from whitefly damage alone can be as much as 50%, and that these losses are particularly severe for some of the recent releases of CMD-resistant varieties. A gray-black sooty mold covering the lower leaves that develops on the sugary excreta produced by whitefly nymphs is a characteristic symptom of heavy whitefly infestation. These symptoms have been observed in various parts of East and Central Africa, and always occur in areas affected by the CMD pandemic.

Research priority
The obvious research question that has been thrown up from these sets of circumstances is: ”what causes superabundance in B. tabaci?” There are two principal hypotheses. One suggests that superabundance is a result of the spread of a novel ‘fitter’ B. tabaci biotype, and the second, that superabundance is the consequence of a synergistic interaction between B. tabaci and CMD-infected cassava plants.

To examine the first hypothesis, IITA has been working with the University of Arizona, USA, to develop molecular markers to allow discrimination between cassava-colonizing B. tabaci populations. The earliest work made use of sequence portions of the cytochrome oxidase 1 gene of mitochondrial DNA (mtCO1). MtC01 sequences were obtained from whiteflies collected along transects straddling the pandemic ”front” in Uganda. Analysis of sequence homologies showed that there were two major genotype clusters, and that one of these, the so-called “invader” was strongly associated with the pandemic-affected zone. Subsequent collections made after the pandemic had covered the whole of the cassava-growing area of Uganda, however, provided an apparently contradictory outcome, as the ”invader” genotype cluster appeared only infrequently. This is not altogether surprising, however, as B. tabaci cassava biotypes from different countries, and even different continents, have been shown to be able to interbreed successfully.

Finding novel solutions
Current efforts are therefore focusing on developing microsatellite markers that provide a much wider coverage of the B. tabaci genome and will make it more likely that we can discriminate between putative superabundant and normal B. tabaci biotypes. To investigate the intrinsic biological characteristics of different cassava B. tabaci populations, their associated genetics and the biology of offspring produced through inter- and intra-population mating, core funds are currently being used to run a PhD program in Tanzania. This study will also be used to examine the hypothesis of B. tabaci-CMD infected cassava synergism. Preliminary results from cage trials conducted at NRI using a single variety have shown increased B. tabaci abundance on CMD-infected plants, when compared with uninfected material.

Chlorosis on shoot tip and sooty mold on lower leaves caused by heavy B. tabaci infestation. Photo by IITA

The idea that diseased cassava makes for a better food source for B. tabaci has parallels in studies conducted with B. tabaci on other host plants, where virus infection has led to increased whitefly populations. In the cassava system there are some contradictions, however. It is significant that the greatest abundances of B. tabaci in pandemic-affected areas are actually observed on CMD-free resistant varieties. Further research is clearly required before a clear-cut explanation can be given for the superabundance enigma.

With whitefly numbers at record levels, and physical damage exacerbating the already grave problems posed by CMD, it has been increasingly recognized that effective measures for whitefly control need to be identified. Two main options appeared to offer greatest potential: resistance and biocontrol. Pesticides, although widely used in northern commercial agricultural systems, are easily dismissed for use on cassava in SSA, because of the extreme cost and the environmental hazard that they pose.

Is biocontrol the answer?
IITA had great success in its classical biological control programs for managing cassava mealybug and cassava green mite. Why not do a similar thing for whiteflies? Sadly, B. tabaci poses a greater challenge since it is considered to be African in origin, and therefore should already be benefiting from the presence of indigenous natural enemies. Significant work was nevertheless undertaken at IITA-Uganda to characterize the natural enemies of B. tabaci on cassava and to investigate the potential for augmentation.

A combination of surveys, life table studies, mortality measurements, and behavioral assessments conducted over a 10-year period—from 1999 to 2008—revealed that although natural enemies accounted for significant mortality in B. tabaci populations, under normal circumstances this was not sufficient to keep B. tabaci populations at levels below those causing significant economic damage.

To change this balance, it was concluded that complementary B. tabaci control measures would be required, such as the introduction of climate-matched exotic B. tabaci parasitoids or the use of cassava varieties either less favorable to whiteflies or more favorable to parasitoids. Although no attempt has yet been made to introduce exotic B. tabaci parasitoids to East Africa, a significant amount of effort has been made to enhance whitefly resistance in cassava germplasm. IITA partnered with CIAT, NRI, and NARO (Uganda), under the SP-IPM’s Tropical Whitefly Project, to pioneer efforts to introduce to East Africa strong sources of whitefly resistance developed in Latin America by CIAT (albeit to different whitefly species).

The NARO team have had some success in identifying Latin American germplasm that appears to have partial resistance to African B. tabaci, but the challenge still remains to combine these sources of resistance with the other key traits that are required by cassava in the East African farming environment. To achieve this, whitefly resistance markers will need to be built in to marker-assisted selection approaches. Much untapped potential may yet exist, however, in African germplasm, and beyond that, within wild relatives. These are important areas of future research.

Women bringing cassava to market. Photo by IITA

Need more studies on whitefly
The recent upsurge in the importance of CBSV in the Great Lakes region of East/Central Africa poses yet more challenges to the cassava research community. Although published reports identify B. tabaci as the vector, researchers remain divided on the accuracy of this claim. As such, IITA, working closely with NRI, is actively addressing this question systematically, by combining field epidemiological studies with cage-based transmission experiments, both of which are being facilitated by newly improved virus diagnostic techniques.

Preliminary results seem to support the earlier claim that B. tabaci is the vector, as the level of CBSV infection in whitefly-protected experimental plots was approximately half that in whitefly-infested plots. These preliminary data will need to be confirmed by repeat trial plantings and cage trial results before any more definitive outcome can be claimed.

Whiteflies have been recognized as an important threat to cassava production for more than a century, but at the outset of the 21st century, that threat appears to be greater than ever. It appears likely that B. tabaci is driving a dual pandemic of CMD and CBSD through the cassava-growing heartlands of Africa.

Recognition of the importance of the twin threats to cassava is at an all-time high, with record levels of funding available to tackle them. By contrast, the role of the vector in the cassava crisis has received much less recognition. This fact will need to be addressed by IITA and its partners in developing future cassava-oriented R4D projects and programs.

Bactrocera invadens adults on a mango

Biocontrol has been around for over 2000 years. The most ancient example of biocontrol use recorded was that of Chinese and Southeast Asian fruit growers, who used weaver ants to protect their citrus crops. Farmers in Asia continue to practice this until today.

Weaver ants (one colony of Oecophylla = several nests) live on trees and defend their territories using chemicals or “pheromones” that they leave on leaves, branches, and fruit. Pheromones are chemicals secreted by insects that strongly influence, in the case of ants, the behavior of others of the same species. The release of these pheromones, which is a form of nonverbal communication, can effectively recruit ants to new food sources or trigger warnings as a protection against intruders.

There are two Oecophylla (Hymenoptera Formicidae) species in the world—the Asian species, Oecophylla smaragdina Fabricius, and the African species, O. longinoda Latreille.

Their successful application as an endemic natural enemy is rising in tropical countries. New research started exploring the mechanisms underlying ant protection of plants against arthropods. Apart from direct control mechanisms, including the predation on or deterrence of insect pests during direct encounters, indirect mechanisms have recently been discovered involving the detection of the territories of enemy ants.

Researchers have demonstrated that the Asian Oecophylla species can deter insect herbivores or plant eaters through info-chemical action. A laboratory test showed that a beetle which this ant preys on was more reluctant to feed on leaves sampled within ant territories than on leaves sampled outside.

In Africa, O. longinoda is being used as a biocontrol agent against agricultural pests. This species defends chemically marked territories at both levels, the intraspecific (within species) and interspecific (between species). Due to their pronounced territoriality, permanent surveillance (all year round, day and night), and very efficient recruitment, O. longinoda respond quickly to any increase in prey numbers.

Nest of O. longinoda on a mango tree

The use of O. longinoda colonies is suitable for perennial cropping systems in sub-Saharan Africa because they are efficient against fruit fly pests, one of the widespread threats, constantly present in tropical agricultural systems.

Two fruit fly (Diptera Tephritidae) species—Bactrocera invadens Drew Tsuruta & White and Ceratitis cosyra (Walker), were found to be the most important species in terms of fly abundance and fruit damage in Bénin during the 2005 and 2006 seasons. The first is an exotic species from Asia, only recently recorded in West Africa, where it has become a huge threat in main fruit crops, such as mango (Mangifera indica) and citrus. The second species is indigenous.

To control fruit flies, growers sometimes resort to pesticides that are registered for cotton production. This control method is not convenient or effective at all.

Because of the economic importance of fruit flies and the lack of appropriate control methods especially in SSA, research efforts on alternative fruit fly control strategies have received greater attention, including the use of endemic biological control agents.

Making more efficient use of natural means of pest control can greatly benefit planters.

At the beginning of 2008, a Regional Control Program of Mango Fruit Flies called “West African Fruit Fly Initiative” (WAFFI) was launched in West Africa by IITA-CIRAD, with World Bank funding. The program was based in IITA-Bénin. Seven West African countries took part in 2008, and another eight in 2009. A part of the WAFFI research focused mostly on the behavior of economically significant fruit flies and their control with biological control agents, such as weaver ants.

In Bénin, we studied the behavior of fruit flies in both laboratory and field tests over several months. These experiments revealed the fundamental role of info-chemicals of ants in repelling females of two fruit fly species during their oviposition or egg-laying period in mango. Interactions were studied on mango between two frugivorous or fruit-eating fly species (B. invadens and C. cosyra) and the African weaver ant (O. longinoda).

Predation of fruit fly larva third larval instar by weaver ants

Results showed that: (1) female flies are strongly attracted to the mango fruit at ripening stages for egg laying; (2) without previous passage of ants on the fruit, the oviposition of tephritids (flies) is very important in mango; (3) once weaver ants have “patrolled” on mango fruit, female oviposition is significantly reduced; (4) C. cosyra seemed twice as sensitive as B. invadens about landing on treated fruit vs. untreated fruit; (5) similar results were found for the time spent on mango fruit; (6) ant-treated fruit had six times less damage from B. invadens and four times less damage from C. cosyra than untreated fruits; (7) B. invadens had significantly more pupae per kilogram fruit than C. cosyra in ant-free mango fruit, whereas no significant difference in ant-treated fruit was detected between the native C. cosyra and the exotic B. invadens.

The presence of weaver ants in mango trees reduced the damage caused by the fruit fly family Tephritidae through predation of adult fruit flies (rare), predation of third-stage larvae (quite frequent) and, especially, the effect of pheromones left by the ants on the fruit so that flies are repelled and are discouraged from egg-laying. Weaver ant presence resulted in a marked reduction in fruit damage.

The influence of info-chemicals from predators such as ants on the foraging behavior of fruit insects and more generally on pests could have crucial consequences for future observations and applications on host selection and consequently in host protection against these pests.

Practical information about the use of weaver ants in fruit fly pest control should be made available to all those involved in the fruit industry at every level, particularly local official producers, pickers, and rural advisors.

This work is also a good example of collaboration among IITA, Africa Rice, and CIRAD on a very important issue about high-value products in West Africa.

References
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