EFFECT OF SELECTED INSECTICIDE ON WHITEFLY (Bemisia tabaci) INFESTING BRINJAL PLANTS Publisher: Asian Economic and Social Society ISSN (P): 2304-1455, ISSN (E): 2224-4433 Volume 3 No. 4 April 2013. † Corresponding author Acknowledgements: Authors are grateful to the Tobacco Research Board of Zimbabwe who sponsored this study. The Biology of the Red and Green Morphs of the Tobacco Aphid, Myzus Persicae Nicotianae (Blackman) on Flue-Cured Tobacco Masukwedza Rhoda (Plant Health Services Department, Kutsaga Research Station, Tobacco Research Board, Harare, Zimbabwe) Mazarura Upenyu † and Chinwada Peter (University of Zimbabwe, Crop Science Department, Mt. Pleasant, Harare, Zimbabwe) Dimbi Susan (Plant Health Services Department, Kutsaga Research Station, Tobacco Research Board, Harare, Zimbabwe) Citation: Masukwedza Rhoda, Mazarura Upenyu, Chinwada Peter and Dimbi Susan (2013) “The Biology of the Red and Green Morphs of the Tobacco Aphid, Myzus Persicae Nicotianae (Blackman) on Flue-Cured Tobacco”, Asian Journal of Agriculture and Rural Development, Vol. 3, No. 4, pp. 205-214. The Biology of the Red and Green ... 205 Author(s) Masukwedza Rhoda Plant Health Services Department, Kutsaga Research Station, Tobacco Research Board, Harare, Zimbabwe Mazarura Upenyu and Chinwada Peter University of Zimbabwe, Crop Science Department, Mt. Pleasant, Harare, Zimbabwe Dimbi Susan Plant Health Services Department, Kutsaga Research Station, Tobacco Research Board, Harare, Zimbabwe The Biology of the Red and Green Morphs of the Tobacco Aphid, Myzus Persicae Nicotianae (Blackman) on Flue-Cured Tobacco Abstract The tobacco aphid, Myzus persicae nicotianae is an economically important pest of tobacco. Damage is through direct injury by sucking sap of infested plants as well as reduction of the quality of the leaf by leaving honey-dew which encourages the subsequent growth of sooty-mould. In addition to this, aphids also transmit economically important virus diseases such as the bushy-top virus, the alfalfa mosaic virus and the potato virus-Y. Before 2002, the main colour form of the tobacco aphid in Zimbabwe was green. However, during the 2003/2004 tobacco season, concerns were raised where red forms of the tobacco aphid were observed to be more prevalent than the green form. During the 2004/2005 tobacco season, green forms of the tobacco aphid could only be found with difficulty. In intensive research spanning three years, the days to adulthood, days to 1 st nymph, nymphs/day, longevity, fecundity and survival of the red morph were compared to that of the green aphid. Across all years, days to adulthood were the same for the two forms. The red morph produced more nymphs/day than the green morph. Longevity was similar but fecundity was 1½ to 2 times higher for the red morph than the green aphid. The red morph survived longer than the green aphid. These parameters combined to give the red morph of the tobacco aphid a greater reproductive potential and rate of population increase over the green morph thereby partly explaining the sudden increase in this pest in the recent past. Keywords: Aphid, Red morph, Green morph, Flue-cured tobacco Introduction The green peach aphid, Myzus persicae persicae (Sulzer) (Hemiptera: Aphididae) has a world-wide distribution and is an important vector of plant viruses, spreading diseases among many crops (Blackman & Eastop 2000). It is assumed to be of Asian origin because its primary host, peach (Prunus persica L.), on which sexual reproduction occurs, originated in Asia (Blackman & Eastop 2007). Myzus persicae persicae is known to develop populations specifically adapted to certain host plants (Margaritopoulos et al., 2000). The tobacco (Nicotiana tabacum L. (Solanaceae)) adapted form is considered to be a distinct subspecies and is known as the tobacco aphid, M. persicae nicotianae (Blackman) (Margaritopoulos et al., 2000). This aphid exhibits morphometric (Blackman 1987; Blackman & Eastop 2007; Margaritopoulos et al. 2000) and genetic differences with respect to M. p. persicae (Blackman & Spence 1992; Margaritopoulos et al., 1998; Margaritopoulos et al., 2007). Relative preference for tobacco by M. p. nicotianae has been demonstrated experimentally (Margaritopoulos et al., 2005; Troncoso et al., 2005), suggesting that its capacity to detoxify and thus overcome allelochemicals from tobacco plants has been key during specialization (Cabrera-Brandt et al., 2010). The tobacco aphid causes significant losses on tobacco directly by feeding and honeydew deposition and indirectly by contamination and as a vector of a wide range of viruses (Dixon, Asian Journal of Agriculture and Rural Development, 3(4): 205-214 206 1998). In Zimbabwe and other tropical regions, M. p. nicotianae has an anholocyclic lifecycle (not capable of producing sexual morphs or not producing viable eggs) and overwinters as active stages on crops and weeds such as Nicandra spp. Both winged and wingless forms can each produce about 80 offspring in a lifetime. Embryonic development begins before the mother’s birth, in the body of the grandmother, whose food intake sustains three generations of about 6 000 individuals. This peculiar reproduction, together with a short life involves the telescoping of generations, providing high rates of population increase (Blair, 1990). Colour variation among individuals of the green peach aphid is common and appears to be interclonal and sympatric in occurrence (Takada, 1981; Miyazaki, 1987). Two distinct colour forms are produced namely the green- yellow and red morphs. Although the benefit of colour dimorphism in M. persicae nicotianae is not clearly understood, the red morph is thought to able to absorb solar radiation and warm itself better than the green form (Markukula and Rautapaa, 1967). The colouration of aphids may reflect genetic differences (Muller, 1985, 1982) or be the result of environmental influences. Colour differences may be correlated with certain biological and ecological features, such as host specificity (Honek, 1982; Weber, 1985), insecticide resistance (Abdel-Aal, 1992), reproductive performance (Araya et al., 1996) and resistance to aphid parasitoids (Tomiuk and Wohrmann, 1980;). At times body colour serves as an indicator of a certain biotype or subspecies (Muller, 1985). Before 2002, the main colour form of the tobacco aphid in Zimbabwe was green. However, during the 2003/04 tobacco season, red forms of the aphid were observed to be more prevalent than the green ones at Kutsaga Research Station, Zimbabwe. During the 2004/05 season, green forms could not be found and where they were found, constituted small numbers. Elsewhere in the world, the red form of the tobacco aphid had been observed as far back as 1985 in North Carolina, U.S.A. (Harlow & Lampert, 1990) and appeared to be a more serious pest than the green form. The occurrence and subsequent dominance of the red form of M. p. nicotianae has brought about the need for a study of its biology as this is an important tool for the development of effective control strategies. The objective of this study therefore, was to compare the fecundity, longevity and survival of the red and green forms of the tobacco aphid M. p. nicotianae on flue-cured tobacco in Zimbabwe. Materials and Methods Aphid Culture The aphid culture was collected from the most commonly grown variety of flue-cured tobacco, Kutsaga Rootknot 26 (K RK26), grown at Kutsaga Research Station. This culture was reared and maintained on K RK26 in the greenhouse until ready for use. Determination of Aphid Fecundity, Longevity and Survival From the greenhouse culture, 45 apterous adults of each morph were collected, marked with nail varnish and placed on 80 mm diameter flue-cured tobacco leaf discs. After reproducing for one day, 100 one-day-old nymphs from each morph were collected with a fine brush and placed in marked individual Petri-dishes (9.1 cm in diameter, 1.2 cm deep) containing moistened filter paper and one 30 mm leaf disc. Containers were kept in a constant temperature room at 24 °C with 16:8 (Day/Night) h photoperiod. Leaf discs were replaced three times a week (Lampert & Dennis 1987). Colonies were observed on alternate days until the first nymph was produced, then daily thereafter. On each observation, the instar of each aphid as evidenced by exuviae and their condition was recorded. Offspring present were counted and removed. From this data, days to adulthood, days to first nymph, longevity, mean nymphs per day and total nymphs per aphid and survival were calculated for both the red and green morph. The experiment was a factorial laid out in 4 randomised complete blocks with time (3 years) and aphid colour (Red and Green) as the main effects replicated 30 times. In addition a Life Table analysis was also performed. ANOVA was done on the data using Genstat Version 11. The Biology of the Red and Green ... 207 Life Tables were used to describe the biology of the morphs according to Price, 1984 and Birch 1948 using the following parameters: x = Age of the insect in days lx = Number of aphids alive at age x, out of 100 dx = Number of deaths in the interval (x,x+1), out of 100, computed as lx – lx+1 qx = probability of dying at age x. Also known as age specific risk of death, computed by dx / lx 100qx = Mortality rate at the age interval x and calculated using the formula dx /lx x 100 Lx = The number of aphids alive between age x and x+1, computed by: (lx + lx+1 )/2, out of 100 Tx = The total number of living aphids at age x and beyond computed as Tx = Lx + Lx + 1 +Lx+2 + …+ Lx + n Finally, the average amount of time yet to be lived by members surviving to particular age/life expectancy: ex = Tx/lx Life expectancy, which is the mean number of age categories remaining until death for individuals surviving to the beginning of age category . Mx= The average number of offspring produced by an individual in age category x while in that age category.. Ro = ∑ . Net Reproductive Rate represents the average lifetime number of offspring produced by an individual of maximum lifespan Results Days to adulthood There was no interaction between year and colour, (Table 1) although the general trend was that the days to adulthood decreased from year 1 to year 3 (Table 1). No significant differences (P> 0.05) between the two forms were observed in the days taken to reach adulthood over the three year period (Table 1). However, significant differences were observed from the first to the third year where both forms took a significantly shorter time (P < 0.001) to reach adulthood (Table 1). Although the red morph tended to have a shorter time to adulthood, this was not significantly (P > 0.05) shorter than for the green morph (Table 1). Days to 1 st Nymph, Nymphs per Day and Total Number of Nymphs There was no interaction between year and colour for days to 1 st nymph, nymphs per day and total number of nymphs but consistently for 3 years the red morph, took a significantly shorter time (P < 0.001) to produce its first offspring, produced a significantly greater number (P < 0.001) of total nymphs (Table 1) and nymphs per day (Table 2) than the green morph. Table 1: Days to Adulthood & to First Nymph, Fecundity, Nymphs per Morph, Longevity and Survival for the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae Year Colour Days to adulthood Days to first nymph Total nymphs/aphid (Fecundity) 1 Red 8.64 8.36 63.10 1 Green 9.39 10.22 40.10 2 Red 7.00 6.57 107.12 2 Green 7.18 8.17 63.40 3 Red 6.84 5.80 99.47 3 Green 7.23 7.92 50.90 Year * Colour: F-Probability 0.66 0.69 0.33 L.S.D 0.87 0.85 17.38 Asian Journal of Agriculture and Rural Development, 3(4): 205-214 208 Colour Red 7.46 6.89 90.97 Green 7.89 8.73 52.21 F-Probability 0.10 <0.001 <0.001 L.S.D 0.51 0.50 14.35 Year Days to adulthood Days to first nymph Fecundity Red Green Red Green Red Green 8.64 9.39 8.36 10.22 63.10 40.10 7.00 7.18 6.57 8.17 107.13 63.39 6.84 7.23 5.80 7.92 99.47 50.90 F- Probability <0.001 <0.001 <0.001 <0.001 0.002 0.18 L.S.D 0.85 0.90 0.88 0.84 24.54 24.95 Table 2: Nymphs / day, Longevity and Survival for the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae Year Colour Nymphs/Day Survival Longevity 1 Red 70.00 57.92 25.43 1 Green 46.70 50.57 22.13 2 Red 117.50 66.91 23.30 2 Green 79.20 56.58 22.50 3 Red 120.20 66.90 20.77 3 Green 87.50 56.38 18.67 Year * Colour: F-Probability 0.903 0.92 0.79 L.S.D 47.10 8.62 50.9 Colour Red 100.20 63.60 23.17 Green 69.30 54.30 21.10 F-Probability 0.028 0.01 0.17 L.S.D 27.54 7.11 2.94 Year Nymphs/Day Survival Longevity Red Green Red Green Red Green 1 2.76 2.29 57.95 50.57 25.43 22.13 2 5.34 4.20 66.91 56.58 23.30 22.50 3 5.54 4.71 66.90 56.38 20.77 18.67 F- Probability 0.025 0.021 0.30 0.47 0.12 0.34 L.S.D 2.26 1.81 13.36 10.14 4.46 5.71 Longevity and Survival There was no interaction between year and colour but the red morph survived for a significantly longer time (P < 0.001) than the green morph while longevity was the same for the morphs (Table 2). Over the three years no significant year differences (P> 0.001) were observed in survival or longevity for each morph (Table 2). Life Tables Figures 1to 3 show the age-specific fecundity of the red and the green morph of the tobacco aphid Myzus nicotianae from 2008 to 2010. The number of nymphs produced by the red morph reached two peaks on day 9 and 16 whilst that of that of the green morph reached peaks on day 12 and 20 for 2008 (Fig 1). The first peak for both morps was always smaller than that of the second. In 2009 the red morph peaked at age 17 while the green morph peaked 3 days later (Fig 2) while in 2010 The Biology of the Red and Green ... 209 thered morph peaked at 18 days and the green morph at 22 days (Fig 3). The general trend was that the red morph began to reproduce earlier than the green morph and reached peak reproduction earlier than the green morph (Fig 1, 2,3). Figures 4-6 show the age-specific survival of the red and green morphs of the tobacco aphid Myzus nicotianae. From 2008 to 2010 the red morph consistently had higher survival than the green morph up to about day 25. Survival curves for both morphs fell similarly with time. Fig 1: Age-specific Fecundity (mx) of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae in 2008 Fig 2: Age-specific Fecundity (mx) of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae in 2009 0 2 4 6 8 10 12 14 16 18 20 22 24 1 4 7 10 13 16 19 22 25 28 31 34 37 40 43 A g e- sp ec if ic f ec u n d it y (m x ) Age in days Red Green 0 2 4 6 8 10 12 14 16 18 1 4 7 10 13 16 19 22 25 28 31 34 Red Green Age in days A g e- sp ec if ic fe cu n d it y( m x) Asian Journal of Agriculture and Rural Development, 3(4): 205-214 210 Fig 3: Age-specific Fecundity (mx) of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae in 2010 Fig 4: Age-specific Survivorship (lx) of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae in 2008 Fig 5: Age-specific Survivorship (lx) of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae in 2009 0 5 10 15 20 1 4 7 10 13 16 19 22 25 28 31 34 Red Green Age in days A g e- sp ec if ic fe cu n d it y( m x) 0 10 20 30 40 50 60 70 80 90 100 1 4 7 10 13 16 19 22 25 28 31 34 37 40 43 46 A g e- sp ec if ic s u rv iv al (l x ) Age in days Red Green 0 10 20 30 40 50 60 70 80 90 100 1 4 7 10 13 16 19 22 25 28 31 34 Red Green Aphid age in days A ge -s p ec if ic s u rv iv al ( lx ) The Biology of the Red and Green ... 211 Fig 6: Age-specific Survivorship (lx) of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae in 2010 Analysis of the life table of green and red morphs of the tobacco aphid showed that the red morph consistently had a higher net reproductive rate (RO) over the three year study than the green morph. However, for both morphs net reproductive rate increased between 2008 and 2010 (Table 3). The intrinsic rate (rm) of increase was also higher for the red morph than the green and results of the mean generation time (Tc) showed that the red morph had a shorter mean generation time than the green morph (Table 3). Table 3: Life-table Parameters of the Red and Green Morphs of the Tobacco Aphid, Myzus nicotianae Year Parameters Red morph Green morph 2008 Ro 95.73 63.57 rm 0.349 0.256 Tc 13.06 16.19 2009 Ro 129.3 87.40 rm 0.355 0.276 Tc 13.71 16.21 2010 Ro 128.73 88.00 rm 0.353 0.262 Tc 13.76 17.09 R0 = net reproductive rate, rm = intrinsic rate of increase, Tc = mean generation time Discussion Understanding the biology of an insect is crucial in the development of an effective integrated pest management programme. A shorter period to adulthood would make an insect more competitive, since this could mean a shorter life cycle. However, in this respect the red morph only tended to develop in a shorter period than the green morph, suggesting that this did not give the red morph any related advantage over the green morph. However, the period to 1 st nymph (to reproductive age) was shorter for the red morph than the green morph. This was also shown by the higher net reproductive rate and intrinsic rate of increase of the red morph. This would thus give the red morph a distinct advantage over the green morph in terms of capacity to quickly colonize a habitat. This could be one of the contributing factors to the success of the red morph as this may give the red aphids an advantage of early colony establishment. The present study agrees with findings by Goundoudaki et al. (2003) who indicated a shorter developmental time in the red morph of the tobacco aphid relative to the green morph. Araya et al. (1996) also showed that the pink English grain aphid, Sitobion 0 20 40 60 80 100 1 4 7 10 13 16 19 22 25 28 31 34 Red Green Aphid age in days A g e- sp ec if ic su rv iv al ( lx ) Asian Journal of Agriculture and Rural Development, 3(4): 205-214 212 avenae had a shorter reproductive period compared to the green form. Not only did the red morph reach reproductive age earlier, but it also produced more nymphs per day giving it advantage over the green morph. However, longevity was comparable to that of the green morph, giving it no distinct advantage over the green morph. Higher longevity could mean an organism would produce more offspring in its lifetime and thus making it more competitive. Goundoudaki et al. (2003), however, showed a significantly higher longevity in the red morph relative to the green morph. Age- specific fecundity showed that the red morph reached its peak reproduction time earlier than the green morph and consistently had a higher survival than the green morph. In the present study, the red morph tended to have a greater longevity consistently but this was not significantly higher than for the green morph, perhaps showing that this “new” morph is still adapting to its new environment. That the fecundity of the red morph was 1½ to 2 times higher than that of the green morph suggests that it would out-compete the green morph. This coupled with a greater survival implies greater competitive advantage and may explain the predominance of the red morph, particularly in warm temperatures. Reed & Semtner (1991) showed that the red morph could develop, reproduce and survive better than the green morph at 25 °C or higher, confirming earlier findings by Lampert & Dennis (1987). Summary Polyphenism, the production of two or more alternative phenotypes by a single genotype, is a characteristic feature of aphids (Dixon, 1998). Aphids exhibit a wide range of phenotypic plasticity characteristics, whereby the same genotype can respond to different environments by producing alternate phenotypes in a way that maximizes its fitness (Halkett et al. 2006). The predominance of the red morph in Zimbabwe is a new phenomenon in the country but the success of the red morph has been a worldwide experience (Blackman 1987; McPherson and Bass, 1990). This success could be linked to its ability to survive, reproduce and develop faster than the green morph (Reed & Semtner, 1991; Lampert & Dennis, 1987). Our work agrees with these findings and we postulate that the red morph will be a “new” menace in the region. This red morph has been conclusively associated with insecticide resistance (Blackman, 1987; Harlow & Lampert, 1990; McPherson & Bass, 1990). Conclusions and Recommendations The parameters studied in this study show that the red morph has competitive advantage in terms of days to 1 st nymph, number of nymphs/day, fecundity and survival. These factors suggest that the increases in populations observed over the short period may be partly explained by these advantages. This study would therefore be useful in obtaining data for later use in the development of population models of tobacco aphids and development of integrated pest management strategies. In addition, we recommend more judicious use of insecticides and a need for a holistic approach to aphid control, utilizing perhaps natural enemies and insecticides not harmful to such enemies. More work is required to establish which of the pesticides available in the region the pest has already developed resistance to. Lastly, we recommend work in the area of biological control in order to augment insecticide usage. References Abdel-Aal, Y. A. I., Lampert, E. P., Roe, R. 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