African Crop Science Journal African Crop Science Society ISSN: 1021-9730 EISSN: 2072-6589 Vol. 7, Num. 4, 1999, pp. 511-522

African Crop Science Journal, Vol. 7. No. 4,  pp. 511-522, 1999                                                              

Effects of Cassava mosaic virus disease on the growth and yield of cassava - some highlights from Makerere experiments

D.S.O. OSIRU, W.S. SSERUBOMBWE, P. SSERUWAGI, M. THRESH¹ and  G.W. OTIM-NAPE²
Department of Crop Science, Makerere University, P.O. Box 7062, Kampala, Uganda
¹Natural Resources Institute, University of Greenwich, Chatham Maritime, Kent. ME4 4TB, U.K.
²Namulonge Agricultural and Animal Production Research Institute, P.O. Box 7084, Kampala, Uganda

Code number: CS99042

ABSTRACT

A series of experiments is described in which the effects of cassava mosaic disease (CMD) on the growth and yield of cassava were evaluated. Four cassava varieties of differing resistance/susceptibility were used. These were Ebwanatereka (Susceptible local), Nase 2 (Moderately resistant/improved), SS4 and Migyera (Resistant/improved). The results showed significant differences between varieties and their mixtures both in the incidence and the amount of disease that developed. Ebwanatereka had the highest CMD incidence while SS4 had the lowest. Varietal mixtures consistently and significantly decreased the incidence of CMD and the population of adult whiteflies compared to their corresponding pure stand treatments. Stage of infection significantly affected the yield of the susceptible variety, Ebwanatereka. The earlier the infection, the greater was the effect of CMD. However, the stage of infection did not appear important in the resistant varieties. Compensation occurred in all varieties although significantly more compensation was achieved in Ebwanatereka. The health status of the immediate neighbours significantly influenced the losses sustained. Application of NPK fertiliser significantly increased the incidence of CMD in Nase 2 and Migyera compared with the unfertilised treatments. However, little difference was apparent in Ebwanatereka which became almost totally infected in all treatments. Adult whitefly populations were increased significantly by the application of NPK in Nase 2 and Ebwanatereka, whereas no effect was observed in Migyera. The implications of these findings in the epidemiology and management of CMD and the scope for future research are discussed.

Key Words: Bemisia tabaci, CMD, leaf area index, Uganda

RÉSUMÉ

Des séries d’essais sont décrites dans lesquels les effets de la maladie de la mosaïque du manioc sur la croissance et le rendement du manioc ont été évaluées. Quatre varietés de manioc de résistance/sensibilité variée ont été utilisées. Elles étaient Ebwanatereka (local sensible), Nase 2 (Modérément résistante/ améliorée), SS4 et Migyera (résistantes et améliorées). Les résultats ont montré des différences significatives entre les variétés et leurs mélanges dans la fréquence et la quantité de la maladie développée. Ebwanatereka a eu l’incidence la plus faible. Les mélanges variétaux ont consistement et significativement réduit l’incidence de CMD et  la population de mouches blanches adultes  comparés aux traitements correspendant en position pure. Le stade d’ infection a significativement affecté le rendement de la variété sensible Ebwanatereka. Cependant le stade d’infection n’a pas apparu important chez les variétés résistantes. La compensation s’est produite chez toutes les varietés bien qu’elle a été significativement plus considérable chez Ebwanatereka. L’état de santé des plantes avoisinates immédiates a influencé des  pertes encourues. L’ application d’engrais NPK a augmenté l’incidence de CMD chez Nase 2 et Migyera comparée aux traitements non-fertilizés. Cependant, une petite différence a été apparente chez Ebwanatereka qui est devenue presque totallement infectée dans tous les traitements. Les populations adultes de mouches blanches ont été augmentées par l’application de NPK chez Nase 2 et Ebwanatereka. Les implications de ces résultats dans l’épidemiologies de  la gestion de CMD et les perspectives futures de recherche sont discutées. Plus l’infection était précoce, plus important était l’effet de CMD.

Mots Clés: Bemisia tabaci, CMD, indice de la surface foliaire, Ouganda

Introduction

Cassava (Manihot esculenta Crantz) is a major staple crop and one of the major sources of food energy for more than 200 million people in the tropics (Hahn et al., 1980). However, the productivity of cassava is extremely low particularly in Africa where the yield in tonnes per hectare is 19% below the world average and 35% below the yields in South America. There are many reasons for this unsatisfactory situation. One is that the greater proportion of cassava is grown in marginal climatic conditions on poor land, at a late stage in the crop rotation without artificial or organic fertilisers. Another is that many farmers continue to use the local unproductive, disease and pest susceptible varieties often grown at unsatisfactory plant spacing and population densities.  A third reason, and probably the most important, is that there are several important pests and diseases which seriously decrease the growth and yield of cassava. The most important pests are the cassava mealybug (Phenococcus manihoti) and the green mites (Mononychellus tanajoa).

Cassava mosaic disease (CMD) is by far the most important disease of cassava in Africa and the Indian subcontinent. The disease is caused by any of the whitefly-borne cassava mosaic viruses in the family Geminiviridae when present alone or in combination (Thresh et al., 1998). There is abundant evidence that CMD greatly reduces the growth and yield of cassava particularly of  local unimproved varieties (Thresh et al., 1997). In Uganda, CMD has in recent years caused considerable losses in cassava yield and has had devastating effects on the food security situation in the country.

Results of several recent surveys indicate large differences within and between plantings in the incidence and severity of CMD, even in the same locality (Thresh et al., 1997). Much of the variation is associated with the varieties used, which differ considerably in their response to infection. An important feature of cassava production in Africa is that many different varieties are grown in the same field and in many cases these are usually interplanted with a wide range of other crop species (Nweke, 1994). Further, although serious epidemics of CMD have occurred in many parts of Uganda (Otim-Nape et al., 1997) the damage caused has been particularly severe in those areas which depend on one or only a few varieties grown in monoculture compared with those where many varieties were grown in mixtures.

The implication of this is that varietal mixtures and intercrops are likely to influence the spread of CMD and infestation by the whitefly vector (Bemisia tabaci). However, published information to confirm this supposition is lacking largely because previous epidemiological studies have been carried out exclusively with stands of single varieties grown in monoculture. The results of the surveys also indicate that most of the severely affected districts of Uganda (northern Luwero, Tororo, Pallisa, Kumi, Lira and Apac) are generally characterised by poor, low fertility soils (Otim-Nape and Ingoot, 1987). It was therefore generally believed that the low fertility status of the soil may be partly responsible for the prevalence and severity of CMD in these areas.

The objective of the Makerere University experiments were therefore to determine the effects of CMD on growth and yield and the possible compensation effects in mixed stands. An additional objective was to determine the influence of soil fertility status on epidemics of CMD  and yield of cassava.

Experimental Procedure

Experimental site. All experiments were carried out at Namulonge Agricultural and Animal Production Research Institute (NAARI). NAARI is located 27 km north of Kampala in the humid “Lake Victoria Crescent” region. The area is characterised by a bimodal rainfall pattern with peaks in April/May in the first season and October/November in the second season. The mean annual rainfall is 1270 mm and temperatures are moderate with maxima occasionally exceeding 31ºC while the minima does  not fall below 17ºC. The location was selected to represent a high CMV-spread area as categorised by the Uganda National Cassava Programme to ensure that natural infection occurred.

Experimental treatments and design. Two sets of experiments were carried out. In the first, three field experiments were conducted using four varieties of differing resistance/susceptibility,  namely; Ebwanatereka (Ugandan local), SS4 (Ugandan improved), Nase 2 (TMS 30337) and Migyera (TMS 30572). Ebwanatereka is highly susceptible, Nase 2 is moderately resistant, whereas SS4 and Migyera are highly resistant. One of the experiments examined the progress of CMD infection in single varieties (pure stands) and in varietal mixtures. In this trial, treatments consisted of each of the four varieties grown alone and as a random mixture in equal proportions. The treatments were examined in a Randomised Complete Block Design with four replications. Materials for planting were obtained from symptomless plants at NAARI and from nearby farmers fields. The experiment was planted in May 1996 and October 1996.

The second experiment assessed the influence of stage of CMD infection on cassava growth and yield. The same four varieties were used and the treatments consisted of plants raised from healthy cuttings and diseased cuttings of each variety. The experiment was carried out in a Randomised Complete Block Design and replicated four times. A third experiment assessed the influence of the CMD health status of the neighbouring plants on cassava growth and yield. Only three of the four varieties were used, namely, Ebwanatereka, Nase 2 and Migyera. Plants with typical symptoms of CMD (Hahn et al., 1980) and symptomless plants were selected to provide disease and healthy cuttings,  respectively. Three infection levels were established to include;  100% representing treatments in which all plants were raised from infected cuttings; 0% representing treatments in which all plants were raised from healthy cuttings and 50% representing treatments in which plants were raised from equal proportions of diseased and healthy cuttings. The 50% treatment was achieved by planting healthy and diseased cuttings alternately in the rows. The resulting stand combinations were; infected plants surrounded by infected neighbours (ddd); infected plants surrounded by healthy neighbours (hdh); healthy plants surrounded by diseased neighbours (dhd) and healthy plants surrounded by healthy neighbours (hhh). The treatments were examined in a Randomised Complete Block Design replicated four times.

The second set of experiments assessed the influence of NPK fertilisers on the growth and yield of CMD affected cassava plants. Treatments consisted of three cassava varieties namely; Migyera (TMS 30572), Nase 2 (TMS 30337) and the local cultivar, Ebwanatereka. These were grown with and without NPK fertiliser in a split plot arrangement in which the varieties were assigned to main plots and fertilisers were in the subplots replicated four times. The fertilisers, 250:250:250 kg ha^-1 NPK with active ingredients (a.i) N (46%), P2O5 (19%) and KCl (60%) were used to provide nitrogen (N), phosphorus (P) and potassium (K), respectively, in equal proportions. All the experiments were planted in May 1996 and October 1996.

Experimental measurements.  Data on CMD incidence and severity were collected monthly from 1 month after planting (MAP) to 8 MAP. CMD incidence was assessed as the percentage of plants with symptoms while the severity was based  on the scale of 1-5 where; 1= absence of the disease and 5= very severe symptoms (Hahn et al., 1980). Whitefly populations were determined by counting the number of adults on the four top -most expanded apical leaves of representative shoots as described by Otim-Nape et al. (1994). Leaf area indices (LAI) were determined monthly beginning at 2 MAP using a LAI -2000 plant canopy analyser (LI-COR, Lincoln, USA).

Results and Discussion

Significant differences were observed in the incidence of CMD among varieties. Ebwanatereka was the most susceptible variety to CMD and had a significantly higher incidence while SS4 had the lowest incidence compared to that recorded in Nase 2 and Migyera (Fig. 1). The highest CMD severity scores were also recorded on Ebwanatereka, which had negative and significant relationship with tuber yield. Thus in sensitive varieties, CMD limits growth and yield of cassava by the amount proportional to the degree of damage as indicated by the severity of symptoms. This is, however, not  the case with resistant varieties (Nase 2 and Migyera), possibly due to internal competition effects between the aerial parts and roots following infection.  There may also be localisation of the virus, leading to compensation effects by the healthy tissues. The results also indicate that CMD limits cassava production by limiting growth and yield through reduction in leaf area, plant height, leaf weight, stem weight, plantable cuttings and the number and weight of tuberous roots. These results are consistent with those reported earlier by Pascalet (1932), Beck and Chant  (1958), and Ayanru and Sharma (1982), who provided an histological insight into the effects of CMV. Similar results have also been reported by Dubern (1976) and Fauquet et al. (1987). The practical implication of this is that in areas of low CMD spread and low incidence, the combined effects of competition and compensation will result in self-elimination of diseased materials. This is because farmers in such areas would select stronger and healthy plants as source of planting materials and,  consequently, the overall incidence would decline with time.

The experiments also showed that varietal mixtures have the capacity to reduce the progress of CMD. Consistently low incidence and lower populations of adult whiteflies were recorded in Ebwanatereka grown in mixtures than when it was gown alone (Figs. 1 and 2). The effect was attributed to differences in the food resource concentration, improved efficacy of natural enemies and moderated micro-climatic conditions associated with varietal mixtures. The results suggest that resistant varieties provide protection to susceptible varieties through a reduction of intra-plot spread (Janzen, 1973; Gould et al., 1994; Nault et al., 1995). In varietal mixtures,  infection of the susceptible variety is delayed and occurs predominantly later  in the season when its effects on growth and yield are minimal (Sserubombwe, 1998). From Figure 3 , it is evident that intermediate and late-infected plants of Ebwanatereka (the susceptible variety) in varietal mixtures out-yielded their counterparts in monoculture. The early-infected plants were most seriously affected. This scenario is not altogether surprising since there is more competition by the vigorous resistant plants in the mixtures and the early-infected plants are exposed to strong competitive effects for longer periods than both the intermediate and late-infected plants. Such effects are less pronounced in monocultures where competition between plants is largely the same, as much of the infection occurs early (Sserubombwe, 1998).

The important practical implication of these results is that in situations where farmers grow susceptible varieties alongside the resistant improved varieties being introduced ( very common practice in Uganda) varietal mixtures provide an important means of minimising the spread of CMD. This also explains in part why there is usually a high incidence of CMD in areas where farmers rely on one variety grown in pure stands compared to areas which are characterised  by varietal mixtures. The effect is likely to be even greater in mixtures involving cassava and other crop species as evident from the findings of Fargette et al. (1988). The effects of crop mixtures (intercropping) was not, however, examined in the present study. This, therefore, forms an important area for future research attention.

Compensation and competition effects occurred in partly CMD infected stands of all varieties. However, these effects were more pronounced in the susceptible variety, Ebwanatereka (Fig. 4). Yield of diseased plants surrounded by healthy neighbours (hdh) decreased much more than in situations where diseased plants were surrounded by diseased neighbours (ddd). In contrast, the yield of healthy plants surrounded by diseased plants (dhd) was significantly higher than the yield of healthy plants surrounded by healthy plants (hhh). Similar results were reported earlier (Otim-Nape et al., 1997). This effect is likely to be due to the fact that in sensitive varieties, the competition gradient is high as a result of marked impairment of growth by the high level of CMD infection. By contrast in the resistant varieties which retain much of their competitiveness even when infected by CMV. The implication of the compensation and competition effects, however, is that the yield losses of plants in mixed stands of infected and uninfected plants is usually lower than expected. Similar observations have been made by Byabakama et al. (1999).

The results of these experiments have also shown that the stage at which CMD infection occurs is important in determining yield loss, particularly in susceptible varieties. The earlier the infection, the greater is the decrease in yield (Fig. 5). The drastic effects of CMD in sensitive varieties has been attributed to the rapid trans-location of the causal virus, which multiplies rapidly to reach high concentration in most parts of the plant (Sserubombwe, 1998). These results are largely in agreement with previous findings (Hahn et al., 1980; Fauquet et al., 1987) and account for the detrimental effects reported on tuberous root initiation and bulking. The early stages of crop growth are particularly vulnerable to the effects of the virus as they are critical for the physiological processes that influence yield (Pascalet, 1932; Beck and Chant, 1958). Comparatively, in resistant varieties the stage of infection does not appear to be important. Resistant varieties appear to restrict the movement and multiplication of the virus, and there is no clear effect on yield (Sserubombwe, 1998). In many cases reversion (absence of disease symptoms) may occur. In the present experiments, reversion was observed in both Migyera and Nase 2, but not in the highly susceptible variety, Ebwana-tereka.

Application of NPK fertilisers significantly increased CMD incidence in Migyera and Nase 2 (Seruwagi, 1998).  In the highly susceptible variety, Ebwanatereka, there was no significant difference between the fertilised and unfertilised treatments (Fig. 6). The disease incidence was almost  total high in both the fertilised and the unfertilised treatments. It would appear that in Ebwanatereka, the effect of fertiliser was not apparent because disease saturation occurred early in both the unfertilised and the fertilised treatments.

The influence of soil fertility on the incidence and effects of CMD on growth and yield seem unclear. In some recent surveys in Uganda, the high incidence of CMD and its drastic effects on yield was thought to be associated with the low soil fertility in the affected areas  (Thresh et al., 1994; Otim-Nape, 1995). However, the results of the present experiments are clearly in disagreement with these observations, but are consistent with other previous findings (Arraudeau, 1987; Raffailac et al., 1988 ). In related studies on other viral diseases, Bawden (1960) found that the virus content per unit area of leaf and the amount of leaf tissue affected increased with the amount of nitrogen applied. These findings are also corroborated by the strong and positive relationship established between the population of adult whiteflies and leaf area in the present experiments. The results therefore suggest that plant vigour plays a very important role in the colonisation of the plant by whiteflies. The behaviour of whiteflies is such that they colonise vigorous plants containing higher concentration of nutrients and having a large leaf area for oviposition (Adipala et al., 1998; Byabakama et al., 1997, 1999).

These experiments showed increases in tuberous root yield with the application of fertiliser to the resistant varieties but no response to NPK fertiliser was achieved with Ebwanatereka (Fig. 7). The results suggest that resistance together with the application of fertiliser enhance yield loss reduction in cassava due to CMD. However, because of the likely increase in CMD incidence due to NPK fertiliser application, greater response to NPK application will be achieved with healthy than with CMD-affected plants of a resistant variety.

Conclusions

A number of conclusions emerge from these experiments. The first and probably the most important is that the effects of CMD are greater in susceptible than in resistant varieties. Susceptible varieties, as exemplified by Ebwanatereka, show high incidence, high systemicity and high virus concentration. Varietal resistance is therefore a key tool in the management of CMD. Secondly, the experiments have shown that varietal mixtures greatly reduce the progress of CMD, even in high CMD spread areas. The important implication of this is that in situations where farmers grow susceptible varieties alongside the resistant ones being introduced, varietal mixtures may provide an important means of control of CMD. The results obtained in these experiments partly explain the higher incidence and more severe effects of CMD in some parts of Uganda which grow few and mainly susceptible varieties or where monoculture is practised. Thirdly, the stage of CMD infection plays an important role in determining yield in susceptible varieties but does not seem important in resistant varieties owing to the phenomena of recovery and reversion. Fourthly, compensation effects are much more important in the sensitive varieties. This effect makes the yield losses of mixed stands of infected and uninfected plants usually lower than would be expected. The final conclusion is that enhanced soil fertility increases the susceptibility of cassava plants to CMD infection.

Acknowledgements

This study was funded by the Rockefeller Foundation. The assistance of the staff of the Department of Crop Science, Makerere University, and Namulonge Agricultural and Animal Production Research Institute is acknowledged.

References

Adipala, E., Byabakama, B.A., Ogenga-Latigo, M.W. and Otim-Nape, G.W. 1998.  Effect of planting date and varietal resistance on the development of cassava mosaic virus disease in Uganda. African Plant Protection  4:71-79.

Arraudeau, M. 1987. African cassava mosaic disease and its control. In: Proceedings of the International seminar: African Cassava Disease and its control. Fargette, D., Fauquet, C. and Thouvenel, J-C. (Eds.), pp. 20-25, CTA-ORSTOM. Yamoussoukro, Côte d’Ivoire. 4-8 May 1987.

Ayanru, D.K. and Sharma, V.C. 1982. Effects of cassava mosaic disease on certain leaf parameters of field-grown cassava clones. Phytopathology 72:1057-1059.

Bawden, F.C. 1960. The multiplication of viruses. In: Plant Pathology. Volume II.  Horsfall, J.G. and Diamond, A.E. (Eds.). Academic Press, New York and London 3:71-116

Beck, B.D.A. and Chant, S.R. 1958. A preliminary investigation on the effect of mosaic virus on Manihot utilissima Pohl. in Nigeria. Tropical Agriculture (Trinidad) 35:59-64.

Byabakama, B.A., Adipala, E.,  Ogenga-Latigo, M.W. and Otim-Nape, G.W. 1997. The resistance of improved cassava varieties to African cassava mosaic disease in Uganda. African Journal of Plant Protection   7:45-57.

Byabakama, B.A., Adipala, E.,  Ogenga-Latigo, M.W. and Otim-Nape, G.W. 1999. The  effect of amount and disposition of inoculum on cassava mosaic virus disease development and tuberous root yield of cassava. African Plant Protection 5:21-29.

Dubern, J. 1976. Impact of African mosaic on the growth and yield of cassava. In: Proceedings of the international seminar: African cassava mosaic disease and its control. Yamoussoukro, Côte d’Ivoire. 4-8 May 1987. Fargette, D., Fauquet, C. and Thouvenel, J-C. (Eds.), pp. 20-25. CTA-ORSTOM.

Fargette, D., Fauquet, C. and Thouvenel, J-C. 1988. Yield losses induced by African cassava mosaic virus in relation to the mode and date of infection. Tropical Pest Management 34: 89-91.

Fauquet, C., Fargette, D. and Thouvenel, J-C. 1987. The resistance of cassava to African cassava mosaic. In: Proceedings of the International Seminar: African Cassava Mosaic Disease and its control, Yamou-ssoukro, Cote d’Ivoire. 4-8 May 1987. Fargette, D., Fauquet, C. and Thouvenel, J.C. (Eds.), pp. 183-188. CTA-ORSTOM.

Gould, F., Follet, P., Nault, B. and Kennedy, G.G. 1994. Resistance management strategies for transgenic potato plants. In: Advances in potato pest biology and management. Zehneder, G., Jansson, R.K., Powelson, M.L. and Raman, K.V. (Eds.), pp. 257-277. APS Press, St. Paul, MN. 

Hahn, S.K., Terry, E.R. and Leuschner, K. 1980.  Breeding cassava for resistance to cassava mosaic disease. Euphytica 29:673-683.

Janzen, D.H. 1973. Host plants as Islands. II. Competition in evolutionary and conte-mporary time. American Naturalist 107:786-790

Nault, B.A., Follet, P.A., Gould, F. and  Kennedy, G.G.  1995. Assessing compensation for insect damage in mixed plantings of resistant and susceptible potatoes. American Potato Journal 72:157-176.

Nweke, F.I. 1994. Farm level practices relevant to cassava plant protection. African Crop Science Journal 2:563-582.

Otim-Nape, G.W. and Ingoot, D. 1987. The effect of spacing, time of planting and number of shoots on the incidence and severity of the African cassava mosaic disease (ACMD). In: Proceedings of the Third Triennial Symposium of the International Society of Tropical Toot Crops - Africa  branch. Terry, E.R., Akoroda, M.O. and Arene, O.B. (Eds.), pp. 105-108. IITA, Nigeria. 

Otim-Nape, G.W., Shaw, M.W. and Thresh, J.M. 1994. The effects of cassava mosaic geminivirus on growth and yield of cassava in Uganda. Tropical Science 34:43-54.

Otim-Nape, G.W., Thresh, J.M.  and Shaw, M.W. 1997. The effect of cassava mosaic virus disease on yield and compensation in mixed stands of healthy and infected cassava. Annals of Applied Biology 130: 503-521.

Pascalet, M. 1932. La mosaique ou lepredu manioc. Agronomie Coloniale 21:117-131.

Raffaillac, J.P. and Nedelec, G. 1988. Component du manioc (Manihot esculenta Crantz, variety CB) pour differenties densities de plantation. Premiers Resultats: Rapport. ORSTOM. 15pp.

Sserubombwe, W.S. 1998. Progress of cassava mosaic virus disease (CMD) and its effects on growth and yield of four cassava varieties. Msc. Thesis, Makerere University, Kampala. 185 pp.

Sseruwagi, P. 1998. Influence of NPK fertiliser on disease spread, growth and yield of cassava mosaic disease affected plants. MSc. Thesis, Makerere University, Kampala. 103pp.

Thresh, J.M., Fargette, D. and Otim-Nape, G.W. 1994. Effects of African cassava mosaic geminivirus on yield of cassava. Tropical Science 34:26-42.

Thresh, J.M., Otim-Nape, G.W., Legg, J.P. and Fargette, D. 1997. African cassava mosaic virus disease: the magnitude of the problem. African Journal of Root and Tuber Crops 2: 11-17.

Thresh, J.M., Otim-Nape, G.W., Thankappan, M. and Muniyappa, V. 1998. The mosaic diseases of cassava in Africa and India caused by whitefly-borne geminiviruses. Review of Plant Pathology 77: 823-833.

©1999, African Crop Science Society

The following images related to this document are available:

Photo images