Comparative biological parameters of whitefly , Bemisia tabaci ( Genn . ) on fruit bearing vegetable crop plants

Ecology of whitefly Bemisia tabaci Genn., has been studied extensively in the recent past and a varying response was observed on different host plants. The degree of this variation is because of type of host plant combination. The present investigation was conducted to find out the comparative age specific survival, mortality and life table parameters in presence of four major fruit bearing vegetables that is brinjal (Solanum melongena L.), chili (Capsicum annuum L.), tomato (Lycopersicon esculentum Mill.) and okra (Abelmoschus esculentus (L.) Moench), under laboratory conditions (26±3°C, RH: 75±5% and photophase: 14 h). The maximum survival and minimum mortality was observed on brinjal, while chili has been documented with reciprocity. Among the host plants, on which whitefly was reared, brinjal has shown superiority, documenting least mortality and shorter development of immature stages of whitefly. Least generation time (23.67±0.97 days) was observed on brinjal and maximum time was consumed on chili (33.57±1.10 days). Similarly, the highest intrinsic rate of increase (rm) was recorded on brinjal followed by tomato and the smallest rm was observed on chili. A significant difference in net reproductive rate (Ro) was perceptible, being highest on tomato (89.50±2.13 females/female). However; corresponding potential fecundity and maximum mean egg laying was received on brinjal. Fastest doubling time was also recorded on brinjal (8.41±0.02 days) followed by tomato (10.87±0.03 days) while maximum doubling time was witnessed on chili (14.01±0.05 days). The highest annual rate of increase (ARI), 1.27±0.02x10 of individuals per year was found on brinjal and lowest on chili. The host preference of whitefly on the basis of present investigations, can be arranged in the following order brinjal>tomato>okra>chili.

and pulses from 86 botanical families (Salas and Medoza, 1995).Adults and nymphs are damaging stages and generally found resting underside of the leaves.Apart from sap sucking (Khan et al., 2011) and excreting honey dew (Kakimoto et al., 2007), whitefly also transmits more than 115 types of virus (Luan et al., 2011) to the commercial crops among which 90% belong to the Begomovirus genus (Jones, 2003).
A high reproductive rate and protective feeding locations on the host enables them to cause severe damage, also hinders the efficacy of pesticide control.According to Lin et al. (2007), despite major advances having been made in understanding the biology and behavior of B. tabaci and in developing pest-management systems (Gerling and Mayer, 1996;Naranjo, 2001), whitefly still remains a major threat for commercial cultivation and this may be attributed to intensive use of pesticides (Bonato et al., 2007).Characteristic features like high natality rate, broad host range, ability to adapt to new hosts and ability to develop resistance to insecticides etc., are few reasons behind the geographic expansion of whitefly and its importance (Basit et al., 2012).Any pest management program should be based on adequate knowledge on ecological aspects of concerned pest and of factors that is host plants, climatic conditions etc, responsible for change in status of key pest (Southwood, 1978;Bonato et al., 2007).Life parameters have been observed on more than 50 host plants (Naranjo et al., 2010), also in last few decades, a number of studies have been conducted, describing host suitability on various host plants (Carabali et al., 2010;Kakimoto et al., 2007;Bayhan et al., 2006;Samih, 2005;Samih et al., 2003a, b;Tsai and Wang, 1996;Chang-Chi et al., 1995;Bethke et al., 1991;Costa et al., 1991a;Sharaf et al., 1985) but none of the studies have included four vegetables viz., Brinjal (Solanum melongena L.), chili (Capsicum annuum L.), tomato (Lycopersicon esculentum Mill.) and okra (Abelmoschus esculentus (L.) Moench).The present investigation was assigned to investigate the impact of host plants on survival, mortality and life table parameters on major vegetables (brinjal, chili, tomato and okra) in particular.This study intends providing essential gap filling information for devising effective management strategies for whitefly.

Cohort establishment and assessment of survival and mortality
Seedlings of tomato, chili and brinjal were transplanted while okra was sown in thermo-coal pots of 9 cm in top diameter, 6 cm in bottom diameter, with 7 cm in height under laboratory conditions (temperature 26±3°C, RH: 75±5% and photophase: 14 h) at Department of Protection, Faculty of Agricultural Sciences, Aligarh Muslim University, India and kept screened to avoid further whitefly infestation.The leaves having pupae of B. tabaci were collected from from the brinjal crop grown at experimental fields of Department of Plant Protection, Aligarh Muslim University.Ten pairs of adult whitefly emerged from the collected pupae were released in confined plastic vials on undersurface of leaves to obtain fresh eggs.These vials were provided with two square shape ventilation windows at either ventral sides, one at bottom and second one at neck opposite to that of bottom and a fine meshed cloth was pasted as screen on the windows (Plate 1).After 24 h of confined exposure, eggs were selected for the further studies on development and survival.Two eggs from each exposed leaf were selected and marked with black permanent and nontoxic marker and such leaves containing those of eggs were tagged at petiole region to facilitate the infestation identity while rest of the eggs were discarded.The whole amount of such tagged plants used under the study were screened with fine meshed white cotton cloth to avoid further infestation of whitefly, mites or ants if there were any.This ensured that every leaf chosen remained with a specific number of eggs, all of which had been marked.A single leaf was used per plant and 100 eggs were marked on 100 plants to give a cohort of 200 eggs.Settled first-instar nymphs were identified and marked on separate leaves by making a circle.The leaves and nymphs were marked using the same procedure as above.These first instars were identified by their translucent color, small size, and characteristic ovoid shape.Marked nymphs were revisited after 1 h to ensure that they had settled.Any nymph that had crawled out of the circle was replaced by marking new one on another leaf of a new plant.All cohorts in each plot were established on the same day, and were marked between 07:00 and 10:00 h of the same day.

Effect of host plants on whitefly life parameters
Newly emerged male and female B. tabaci were paired and each couple was released in plastic vials described above and attached on undersurface of leaves of the respective new food plants.Female fertility life tables constituting parameters viz., female fecundity, pre-oviposition, oviposition and post-oviposition periods etc, were constructed based on Birch (1948) and Southwood (1978).For adults, the survival rate from birth to age x (I x ) and fecundity (m x ) were calculated according to Birch (1948).The data obtained were further used to analyze the intrinsic rate of increase (r m , females per female per day), the net reproductive rate (R 0 , females per female per generation), finite rate of increase (λ, individuals per females per day), the mean generation time (T, In (R 0 )/r m ), and the doubling time (DT, day) were estimated using dedicated software.

Data analysis
The below given assumptions were used for the documentation of age specific life-table .x = age of the insect in days; lx = number of individuals that survived at the beginning of each age interval x; d x = number of individuals that died during the age interval x; 100q x = per cent mortality, computed through the following equation: 100qx = [d x / l x ] x 100; e x = expectation of life or mean life remaining for individuals of age x; Life expectation was calculated using the equation:e To obtain e x , two other parameters L x and T x were also computed as below: L x = the number of individuals alive between age x and x+1 and calculated by the equation: L x = l x +1 (x+1)/2 T x = the total number of individuals of x age units beyond the age x and obtained by the equation: T x = l x + (l x + 1) + (l x + 2)………….+l w Plate 1. Plate plastic vials used to rear adults under leaflets of different host plants in this study.
Where, l w = the last age interval.
The following parameters were also computed for female fertility table:

Net reproductive or replacement rate (R o )
Net reproductive or replacement rate (R o ) is known as the "carrying capacity" of the average insect under defined set of abiotic conditions.The information on the multiplication rate of a population in one generation is obtained from the following equation:

Mean length of generation (T)
Mean length of generation (T) is denoted as the mean period between the birth of the parent and the birth of their offspring.
This period is an evaluated approximate value since the progeny is produced over a period of time and not at a definite time.The calculation was made through the method opined by Dubin and Lotka (1925).

Intrinsic rate of increase (r)
Intrinsic rate of increase (r) is defined as the instantaneous rate of increase of a population in a unit time under a set of ecological condition (Birch, 1948).A rough and accurate estimate of the intrinsic rate of increase (r) can be calculated by using the following equation: (i) r = [Loge R o ] / T (for rough estimation) (ii) e -rx .I x m x = 1 (for accurate estimation) Where 'R o ' represents net reproductive rate and 'T' represents mean length of generation.

Finite rate of increase (λ)
Finite rate of increase (λ) provides the information about the frequency of the population multiplication in a unit of time (Birch, 1948).
λ = e r (8) Taking loge on both sides we get log e λ = loge e r , where, λ =Antilog e e r

Potential fecundity (Pf)
Potential fecundity (Pf) is the total number of eggs laid by an average female in her life span.This was obtained by adding up the age-specific fecundity column.Pf = ∑ m x

Doubling time (DT)
Doubling Time (DT) is defined as the time required for the population to double and is calculated as follows:

Annual rate of increase (ARI)
Annual rate of increase (ARI) can be calculated from the intrinsic rate of increase (r), finite rate of increase (λ), doubling time (DT), or the net reproductive rate (R o ) assuming that the rate of increase was constant throughout the year.program (La Rossa and Kahn, 2003).The data on variation in number of both sexes emerging, duration of different life parameters on different host crops were subjected to analysis of variance (ANOVA) by the program "MINITAB version 11" unless stated otherwise.Tukey's HSD test was used to compare r m and other life table parameters on different vegetable crops.

Age specific survival, expectation of life and mortality
With the advancement of age, the age specific survival was found to turn down gradually (Figure 1).Mortality pattern was observed to be fluctuating on all the host crops whereas the maximum mortality was observed at egg, 1 st larval and at pupal stage (Figure 1).It is revealed from the current findings that it took maximum period (43 days) to complete a single generation on tomato followed by chili (41 days) with the least on brinjal (33 days) (Figure 1).On the other hand the, maximum life was expected at egg stage was 25.56 days on chili Followed by 18.31 days on brinjal.The life expectation dropped down as life advanced in case of brinjal and chili but it was found to increase a bit on tomato and okra (Figure 1).
The pre-oviposition period of B. tabaci is defined as the period between adult emergence and egg deposition.A short period of varying pre-oviposition period was also recorded in this study (f-72.56,p-0.00, df-3, 12), being maximum on tomato (1.45±0.55days) and the minimum on chili (0.75±0.25 days) (Table 1).Adult longevity varied significantly on all the host plants (f-66.76,p-0.00, df-3, 12) and females had longer longevity than males on all host plants.The longest duration of male adult life (15.42±0.28days) and female life (1946±0.43days) was observed on tomato while shortest duration for male (1030±0.34days) and female (12.00±0.40days) was recorded on okra (Table 1).

Development and survivorship of immature stages
An identical and highest span of 1 st instar larval life was recorded on chili (4.36±0.10days) and okra (4.36±0.15days) (f-78.56,p-0.00, df-3, 12) (Table 2) whereas the maximum mortality at 1 st instar larval stage occurred on okra (10.30%) followed by brinjal (12%) with least on chili (3.71%).However, in 2 nd instar larval stage, there was no mortality on chili (Figure 2).During 2 nd instar, okra documented least mortality (3.28%) but the development at same stage was also found to be maximum (4.74±0.13days) on okra (f-566.08,p-0.00, df-3, 12).The 3 rd instar larval stage registered longest span of time on tomato (5.74±0.16days) and lowest period on brinjal (2.78±0.13days) (f-1850.51,p-0.00, df-3, 12) and the highest mortality at 3 rd stage was found on tomato (8.34%) (Figure 2).Among the entire host plants, on which whitefly was reared, brinjal has shown superiority producing least mortality and shorter development for immature stages of whitefly (Table 2) which indicate the suitability of brinjal as a host for immature development of whitefly.The pupal stage exhibited maximum development period on chili (7.21±0.12days) and minimum on tomato (3.26±0.39days) (f-3688.94,p-0.00, df-3, 12), the concerned mortality was also observed to be highest on chili (5.8%) and lowest on tomato (1.82 %).The overall development of immature whitefly on all the host plants exhibited a significant difference except on tomato and okra (f-136.34,p-0.00, df-3, 12) and was found to be delayed most on chili (28.89±0.87days) whereas the least period of development was recorded on brinjal (19.31±0.34days) (Table 2).In the present findings, the development rate, survival and fecundity were significantly different on each host plants.

Life table parameters
A definite pivotal age was also observed during the course of oviposition (Figure 3).The longest egg laying duration of 19 days was observed on tomato followed by 14 days on brinjal whereas an identical mortality period of 12 days each was recorded on chili and okra (Figure 3).A significant difference (f-1726.48,df-3, 12, p-0.00) in net reproductive rate (R o ) was perceptible on all the host plants, being highest on tomato (89.50±2.13females/female), nevertheless, corresponding potential fecundity was received on brinjal (Table 3).The maximum mean egg laying was also recorded on brinjal.A fractional difference (f-406.48, p-0.00, df-3, 12) was observed in intrinsic rate of increase (r m ) (Table 3).It was found maximum on brinjal (0.190±0.002 females/ female/ day) followed by tomato (0.147±0.007 females/ female/ day).The smallest r m was observed on chili (0.114±0.004 females/ female/ day) pointing a poor performance of whitefly on chili (Table 3).There was a significant difference on mean generation time (T c ) on different host plants (f-573.01,p-0.00, df-3, 12) (Table 3).Whitefly documented least generation time (23.67±0.97days) on brinjal and maximum time was consumed on chili (33.57±1.10days) (Table 3).

Age specific survival, expectation and mortality
Host plant species differ greatly in expressions of their suitability as food source and shelter for specific insects with regard to survival and reproductive rates of an insect (Lin and Ren, 2005).Varying responses of B. tabaci in terms of life attributes was observed when exposed to different host plants (Qui et al., 2003;Lin et al., 2003).In the present investigation, a gradual decrease was observed in age-specific survival (Figure 1).A fluctuating trend of mortality was observed on all the host and egg, 1 st instar larval and pupal stages were found to be most susceptible.
In eggs, there is an arrangement of tube like structure called as stalk which helps the egg to get attached with leaf surface (Lloyd, 1922).This acts as a source of water transport from the tissues to the eggs (Paulson and Beardsley, 1985;Buckner et al., 2002).This mortality may be attributed to egg hatch failure due to certain reasons like problem of improper solute uptake through egg stalk (Iida, 2009;Kakimoto et al., 2007), and egg might have taken up certain chemicals through stalk depending upon host plant that might have spoiled the eggs (Iida, 2009).
The shortest life of whitefly was observed on brinjal and the longest on tomato (Figure 1).Similar findings were also reported by Tasai and Wang (1996) while, the early mortality at first instar stage, could be attributed to the longer time required for crawlers to settle down on host plants (Lin and Ren, 2004;Tsai and Wang, 1996).
According to Van Lenteren and Noldus (1990), the host plant preference in Trialeurodes vaporariorum (Westwood) was directly related to biological performance on the plant.Elevated rate of reproduction, low transience rate and shorter development time of insects on a particular host points toward greater suitability of a host plant (Costa et al., 1991, a, b;Coudriet et al., 1985;Awmack and Leather, 2002;Hasan and Ansari, 2011).The gradual decreasing expectation of life was noticed as maximum on chili in the present investigation (Figure 1).Samih et al. (2003) recorded a gradual decreasing life expectation of whitefly on chili which is in agreement with the present findings.The egg survival was observed maximum on brinjal with least on chili (Table 1) which is in complete agreement with the results of Sharaf et al. (1985).Development of eggs laid by females on each host plant was found varying and the highest mortality of eggs was observed on okra (30%) and the least on brinjal (12%) (Figure 2).Hatching period was greatest on tomato.However, a significant variation was recorded among all the host plants (Table 2).Adult life of whitefly varied significantly among the host plants and females' life was observed more than males on all host plants.Host plants were found influencing the sex ratio significantly (Bonato et al., 2007).The superior sex ratio was witnessed on brinjal (Table 1) among all the host plants as was reported by Sharaf et al. (1985), contrary to Fekrat and Shishehbor (2004) who reported a significant role of temperature in the case of sex ratio.

Life table parameters
To compare the whitefly population, significance of life table parameter was highlighted by Wang and Tsai (1996).The longest egg laying duration was observed on tomato followed by brinjal (Figure 3).A significant difference in net reproductive rate (R o ) was perceptible being the highest on tomato.However, corresponding potential fecundity was received on brinjal (Table 3).This difference in net reproductive rate may be attributed to different host plants (Islam and Shunxiang, 2007;Bonato et al., 2007) or the varying environmental conditions (Lin and Ren, 2004).However the maximum egg laying was received on brinjal contrary to the results of Tsai and Wang (1996).Omondi et al. (2005) has opined the oviposition as a good indicator of host acceptance in choice assays.A clear difference in intrinsic rate of increase (r m ) was apparent in our study and was observed to be highest on brinjal (Table 3).It was found maximum on brinjal followed by tomato (Table 3).Kakimoto et al. (2007) has also reported superior rate of natural increase on brinjal as compared to tomato and other host plants.There was a significant difference on mean generation time (Tc) on different host plants (Table 3).Whitefly performed well on brinjal by documenting least time and maximum time was consumed on chili (Table 3).On the other hand, whitefly doubled its population fastest on brinjal pursued by tomato while maximum doubling time was witnessed on chili (Table 3).The highest annual rate of increase (ARI) individuals per year was found on brinjal and lowest on chili (Table 3).

Development and survivorship of immature stages
The literature on biology and ecology from recent past reveals that the development of immature Bemisia tabaci is dependent on type of whitefly population or biotype (Muniz and Nombela, 2001;Bonato et al., 2007) or host plants (Zalom et al., 1995;Tsai and Wang, 1996;Muniz and Nombela, 1997;Nava-Camberos et al., 2001;Lin and Ren, 2004;Bonato et al., 2007).The instar duration of B. tabaci was differently affected by the various hosts during nymphal development (Campos et al., 2003;Bonato et al., 2007).Among the entire host plants, on which whitefly was reared, brinjal has shown superiority by documenting least mortality and shorter development time for immature stages of whitefly (Table 2) which indicates the suitability of brinjal as a host for immature development of whitefly (Awmack and Leather, 2002;Hasan and Ansari, 2011).Sharaf et al. (1985) has also revealed the superiority of brinjal over other host plants for immature B. tabaci.Tsai and Wang (1996) observed that the survival of immature stage of B. argentifolii was more on brinjal than tomato and whitefly took less time for development from egg to adult on brinjal than tomato.Nymphal survival was found contrary to the findings of Campos et al. (2003).In present findings, the development rate, survival and fecundity were significantly different on each host plants and the results are contrary to the findings of Samih (2005) and are in agreement with those of Camberos et al. (2001).

Conclusion
The whitefly, when reared on four major fruit vegetables (brinjal, chili, okra and tomato) showed high fondness of brinjal by documenting maximum survival, minimum mortality, shorter generation time, highest potential fecundity and intrinsic rate of increase whereas chili was inferior most among all the host plants.It can be concluded from the above investigations and discussion that brinjal can serve most preferred host.Therefore an avoidance of continuous cultivation of brinjal in areas having in vogue cultivation of the above mentioned major fruit vegetables.

Table 2 .
Life parameters (mean ± SEM) of Bemisia tabaci on different vegetable hosts.