James Legg, firstname.lastname@example.org
Who would think that delicate and exquisite little insects such as whiteflies could pose an ongoing and global challenge to humankindâ€™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.
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.
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 Africaâ€™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 cassavaâ€™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 IITAâ€™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 pandemicâ€™s so-called â€frontâ€, 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.
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 pandemicâ€™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.
The obvious research question that has been thrown up from these sets of circumstances is: â€what causes superabundance in B. tabaci?â€ There are two principal hypotheses. One suggests that superabundance is a result of the spread of a novel â€˜fitterâ€™ 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 â€frontâ€ in Uganda. Analysis of sequence homologies showed that there were two major genotype clusters, and that one of these, the so-called â€œinvaderâ€ 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 â€invaderâ€ 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.
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 periodâ€”from 1999 to 2008â€”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-IPMâ€™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.
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.