survival of bemisia tabaci adults under different climatic conditions

EntomologiaExpertmentalis etApplicata 80: 511-519, 1996. 511 �9 1996KluwerAcademicPublishers. PrintedinBelgium.

Survival of Bemisia tabaci adults under different climatic conditions

M. J. Ber l inge r l, N i n a L e h m a n n - S i g u r a j & R. A. J. Taylor 2 I Entomology Laboratory, ARO, Gilat Regional Experiment Station, Mobile Post Negev 85-280, Israel 2Entomology Department, Ohio Agricultural Research and Development Center, Wooster, OH 44 691, USA

Accepted. January 23, 1996

Key words." sweet potato whitefly, temperature, relative humidity, migration and dispersal, virus transmission, Homoptera, Aleyrodidae

Abstract

The ability of the sweet potato whitefly, Bemisia tabaci Gennad., to survive a range of environmental conditions was investigated in the laboratory. The range of temperature and humidity investigated corresponds to the normal climatic range during B. tabaci's summer migration in Israel. Adult whiteflies confined to small test cages were exposed to combinations of temperature (25, 30, 35, and 41 ~ and relative humidity (20, 50, 80, and 100%) for periods of 2, 4, or 6 h.

A logistic regression model describing the four-dimensional surface defining percent survival as a function of time, temperature, and humidity was developed. Using stepwise regression to exclude non-significant terms, the linear predictor included temperature, and the products of temperature and time, and humidity and time. The model accounted for 75% of the variance. A reparameterization of the fitted regression model suggests that survival potential is conditioned by temperature conditions prevailing during the previous 10 h.

Whitefly survival after 2 h exposure ranged from ~ 90% survival at 25 ~ and 100% RH, to <2% survival at 41 ~ and 20% r.h.. No whiteflies survived more than 2 h exposure at these latter extremes of temperature and humidity. Survival rates decreased slightly after experimental whiteflies were kept in a cage with food a further 20 h at 25 + 2 ~ 55 + 5% r.h. Investigations of the effects of hunger and virus infection, showed that both increased mortality.

Introduction

The sweet potato (also called the tobacco or cotton) whitefly, Bemisia tabaci Gennad. vectors viral pathogens of several crops (Duffus, 1987). In Israel and neighboring countries it is the sole vector of toma- to yellow leaf curl virus (TYLCV) that is the principal limiting factor of autumn and winter greenhouse toma- to production. B. tabaci can be found year round on crops and wild hosts throughout the Eastern Mediter- ranean.

In Israel, B. tabaci numbers increase through the spring and summer, reaching a peak in September followed by a decline through to December (Avidov, 1956; Gerling & Horowitz, 1983; Horowitz, 1986; Berlinger et al., 1988). Population monitoring by yellow sticky traps over a ten year period shows a major

peak in aerial density occurring in September. How- ever, large increases in temperature and declines in humidity result in dramatic declines in yellow trap catches. For example, the day to day variation during September 1986 was much smaller than the decline from the 20-23 September which correlates perfectly with the fall in humidity and rise in temperature during the 'Chamsin' which peaked on 23 September 1986 (Figure 1). In this month, as at other times, B. tabaci flight activity is seen provided the maximum daily temperature <35 ~ and the relative humidity >50%. The drying capacity of the atmosphere imposes severe limitations on the survival of all flying insects. Thus. although it is not certain, it seems highly probable that the normal early morning flight was inhibited during the Chamsin extremes of temperature and humidity.

512

2 5 0

2 0 0

1 5 0

1 0 0

5 0

f i I I t I I I I [ i I I f 1 I I f I l i I I 1 1 I I I I

0 5 1 0 1 5 2 0 2 5 3 0

,,-.4

8 0

6 0

4 0

2 0

0

4 0

3 5 o

~D

3 0 , ~

2 5 ~

I i i I I I I f I I i r i t I I I t r I i r f I I i I i i 2 0

0 5 1 0 1 5 9 ' 0 9 ' 5 3 0

September 1986 -*- Re la t ive Humid i ty ":'- Maximtun T e m p e r a t u r e

Ftgure 1. Bemtsla tabaci za'e caught on yellow sticky traps throughout their dispersal season provided the daily maximum shade temperature <35 ~ and relative humidity is >50%. But, on 'Chamsin' days, when humidity <30% and temperature >35 ~ the number of trapped whiteflies decreases dramatically, as occurred on 23 September 1986.

The September flight peak occurs nearly simultaneously throughout Israel, including areas lacking any known host plants (Berlinger & Taylor, unpubl.). This led Berlinger & Dahan (1986) to conclude that the late summer flight is dispersive, with significant numbers travelling distances of 20 km. Support for their con- clusion comes from several sources.

�9 Marked B. tabac i have been recovered within a week 7 km from their release point (Cohen et al.,

1986). �9 Large numbers of B. tabac i were trapped on the roof

of a 45 m high building in Beer Sheva (Berlinger & Dahan, 1986); at this height, well above their boundary layer (LR Taylor, 1958, 1960a, 1974), the whiteflies were almost certainly migrating (Johnson, 1957; LR Taylor, 1960b).

�9 B. tabaci have been trapped in several locations in the Arava desert >20 km away from any known host plant (Berlinger & Bar nir, 1989).

Whiteflies are weak fliers, classified along with aphids and leafhoppers, as aeroplancton (Johnson, 1969). Migratory flight, as opposed to local appetitive flight, is above the boundary layer and is maintained by upward flight with horizontal movement provided by air currents. Like aphids and leafhoppers, whiteflies probably have control over when and for how long they are airborne, but the direction of flight is determined exclusively by the wind (Johnson, 1969).

Many Homopterans have a crepuscular flight habit, the actual time of flight resulting from the relative values of temperature and light thresholds (e.g. leafhoppers, RAJ Taylor, 1985; RAJ Taylor et al., 1993). How-

ever, unlike most leafhoppers and aphids, B. tabaci is not truly crepuscular, as it lacks an afternoon or evening flight (Byrne & Bellows, 1991; Blackmer & Byrne, 1993a, 1993b). The morning flight presumably occurs as soon as the temperature is high enough for flight muscles to function efficiently, but well before the heat of the day when atmospheric turbulence is maximal. Early morning flight thus permits local redistribution of the population with reduced risk of long distance dispersal which would result from takeoff later in the day. Flights by B. tabaci over distances of several kilo- meters do occur and are appropriately called migratory (RAJ Taylor, 1985; LR Taylor, 1989). In any dispersal episode, most individuals travel only a short distance, but a small density-dependent proportion make large displacements (RAJ Taylor, 1978, 1981, 1985). In B. tabaci the majority of adults making early morn- mg short appetitive flights remain close to their take- off point, but some climb, or are blown through their boundary layer and make flights lasting several hours. For these individuals the limits to displacement are set by the wind speed, their flight endurance (fuel, moisture), and their thresholds (temperature, relative humidity, light, hunger) for closing their wings and settling.

For all airborne insects moisture loss is a potential hazard, but insects flying in mid- to late summer over Israel are subject to extreme drying conditions. Day- time temperatures in August-September, when sam- pling indicates peak migration, are typically in the range 30-40 ~ with humidities sometimes as low as 20-25%. Thus, desiccation is a serious risk for all insects airborne during the day, and constitutes a major factor setting the upper limit to the duration of flight.

In this paper we examine the ability of adult sweet potato whiteflies to survive over the range of atmospheric temperature and relative humidity conditions prevailing when trap catches in Israel indicate they are migrating. A series of experiments were conducted to gauge the survival prospects of migrating cotton whiteflies in mid-summer in Israel. The effects of five factors on survival were examined in laboratory experiments: temperature; relative humidity; duration of exposure to drying conditions; availability of food; virus infection status.

Materials and methods

Whiteflies were cage-reared on potted three to four leaf cotton seedlings (cultivar Acala S J2) in a

513

65 x 55 x 56 cm rearing cage kept in a glasshouse under natural light conditions at 2 5 • ~ and 60 • 5% r.h.. To inhibit spider mite attack, the plants were dipped in a 0.1% chlorobenzilan solution the day before a whitefly colony was started. To ensure that our whitefly cultures are as similar as possible to wild whiteflies, the cultures are started afresh each autumn from adults collected in commercial cotton fields.

The experiments were conducted in test-cages whose construction was described by Berlinger (1973). The cages are comprised of two glass tubes each 2.5 cm in diameter by 10 cm long. The upper tube, the 'whitefly-chamber', was joined to the lower compartment with Parafilm| The two chambers were separat- ed by a piece of porous polypropylene sheet (Agryl | Sodoca SA, France) to exclude the whiteflies from the lower compartment, but allow air exchange. Humid- ity was controlled by placing a known concentration of NaOH, adjusted for temperature (Madge, 1961), in the lower compartment to one third of its capacity (Berlinger, 1973). To produce an almost saturated atmosphere (~, 100% r.h.) distilled water was used. The r.h. actually achieved in the whitefly-chamber was verified by cobalt thiocyanate paper (Solomon, 1957). The upper opening of the whitefly-cage was plugged by a piston, which could be moved up and down to regu- late the volume of the whitefly-chamber and minimize the humidity gradient from the lower chamber. Dur- ing the experiment the piston was placed so as to leave ,~ 10 mm head space in the whitefly-chamber. The test- cages were kept at constant temperature in illuminated growth chambers, and except as noted, were without food or free water.

Fifteen to 20 post-teneral B. tabaci (males and females) were collected from the rearing cages with an aspirator and immediately placed in test-cages; conse- quently, they were known to be virus-free. The experiments were initiated during the morning, and because B. tabaci feeds predominantly at night, the subjects were assumed to have recently fed. In most experiments ten replicates were used for each combination of factors. Whiteflies were scored immediately upon removal from the whitefly-chamber as either living or dead. After scoring, the whiteflies were transferred by aspirator to a growth chamber at 25 4-2 ~ and 55 • 5%, and provided with a cotton seedling. After an additional ~ 20 h they were again scored as living or dead.

Effect of exposure time, temperature, and humidity on survival. The effects of temperature and humidity on

514

B. tabaci survival were examined under sixteen combinations of temperature (25, 30, 35, and 41 ~ + 2 ~ and humidity (20, 50, 80, 4- 2%, and 100%). Ten test- cages each containing 15-20 whiteflies were placed in an illuminated growth chamber set to one of the four temperatures. Three trials were performed such that whiteflies were exposed to each temperature-humidity combination for 2, 4, or 6 h.

Effect of feeding on survival. To test the influence of feeding on survival, whiteflies were kept in test-cages with and without food. The experimental procedure was as described above, except for the inclusion of a fresh cotton leaf for food in one treatment. Survival was scored after 2, 4, and 6 h at one combination of temperature and humidity (25 + 2 ~ and 55 4- 5%).

Effect of TYLCV-status on survival. The effect of viral infection on B. tabaci survival was tested by exposing viruliferous and virus-free B. tabaci to one temperature (30 4- 2 ~ and two humidities (50 + 2 ~ and 100%). Whiteflies were caught in the rearing cages and transferred to cages containing either TYLCV-infected or virus-free tomato plants. After permitting them to feed for 48 h, i.e., sufficient time to inoculate those on the TYLCV-infected plants (Cohen & Nitzany, 1966), the whiteflies were transferred to the test-cages. Survival was scored after 4 h.

Statistical analysis. A preliminary analysis of the four- dimensional response surface (survival, temperature, humidity, and time) was performed using the generalized linear modelling program, GLIM (Baker & Nelder, 1978). Prior knowledge suggested non-linear decreases in survival with time (t) and temperatures (T), and a non-linear incraese in survival with relative humidity (R). In addition, interactions between time, temperature, and relative humidity seemed plausible. The shape of the survival curves suggested a dosage- response curve:

P = Prob (survival) - Sz

- F( /h) (1) Nr

where N, is the number of whiteflies in the ith experimental unit, S, is the number surviving, # is the linear predictor, and F is the dosage-response relationship. In generalized linear modelling, equation 1 is rear- ranged so that a transformation of p is equated to the linear predictor. Three transformations, or link functions, which differ somewhat in shape and have differ-

ent biological interpretations, are commonly applied to dosage-response data:

logit: # = log{p/(1 - p)}

probit: # = NPI - 1 (p)

complementary loglog: # = log {-log(1 - p)} Where NPI(.) is the normal probability integral,

or cumulative response curve. All three link functions were used to fit a multiple regression model as the linear predictor. The preliminary regression model included all three terms and the four interactions:

# = b o + b l . t + b 2 . T + b 3 . H + b 4 . t . T + (3)

+b5 �9 t . H + b6 �9 T . H + b7 �9 t �9 T . H

where t, is the time, T~ is the temperature, H, is the relative humidity, and bo, bl, b2, b3, b4, b5, b6, and b7 are the regression coefficients. The intercept, b0, is the mortality factor common to all treatments, the background mortality including death due directly or indirectly to handling. The best fitting link function was selected on the basis of goodness of fit measured by minimum X 2. The terms in the linear predictor were reduced by eliminating non-significant interactions using the procedure of stepwise multiple regression.

The two comparison experiments were analyzed using the logit-transformed survival proportions (equation 2a). In the comparison of the survival of fed versus unfed whiteflies, the linear predictor included time as a covariate as before, and feeding status as an indicator variate. In the comparison of viruliferous and virus- free whiteflies, humidity and virus status were the factors in the predictor equation. Differences between treatments in both experiments were determined by analysis of variance.

Results

In the response-surface experiment whitefly survival decreased with time and temperature, and increased with humidity (Figure 2). Mortality increased somewhat during the 20 h recovery period, suggesting that some whiteflies were mortally injured by the test conditions, even though they were alive at the end of the experimental period.

The preliminary analysis using GLIM (Table 1) resulted in the selection of the logit link function, and a reduced regression equation consisting of temperature and two products:

(2a)

(2b)

(2c)

515

2 Hours

00 , " ' , ~ r 40 11 loO

2 / 50 80 ~b~-~

25 30 / / - 40 ,,~ "b~"

4 Hours

,oo ,/~

ooi', > I" e~ 40 ,

/ 20 '~ 8O

35

"r ~'Ut" e 45

6 Hours

6O

4O tO ~

T 35

~"~ttUre 45

Figure 2 Survival surfaces for Bemlsta tabaci exposed to a range of temperature an humidity conditions for a) 2 h, b) 4 h, and c) 6 h The fitted surfaces are logistic regressions (equation 4)

Table l Results of the preliminary analysis of the survival of Bemlsla tabaci exposed to a range of temperature and humidity conditions for different time periods: Deviance x 2 obtained with different link functions

Link function Full model (eqn. 3) Reduced model (eqn. 4)

Total 31,150 31,150

Comp log-log 10,500 10,640

Probit 8,637 8,644

Loglt 8,554 5,573

# = bo + bl �9 T + t . (b2 �9 T + b3 �9 H ) (4)

The best fitting transformation or link function, the logit, is derived from the logistic equation. It can be interpreted as follows: the probability of dying due to heat increases as the rate of heat accumulation increases. When the rate of accumulation exceeds a certain value, the insect dies. Thus, it is the amount of heat required to kill an individual that varies between individuals. The probit model, on the other hand, assumes that each individual is programmed with a fixed temperature value for mortality, that this critical temperature is normally distributed in the population, and that death results when it is exceeded.

Effect of exposure time, temperature, and humidity on survival. Whitefly survival decreased from ~ 90% to <2% as a result of increasing the exposure time from 2 to 6 h, increasing the temperature from 25 to 41 ~ and decreasing humidity from 100 to 20%. As long as the exposure time did not exceed 2 h and the temperature was <35 ~ or the temperature was >25 ~ for exposure periods up to 6 h, at least 66% of the whitefly population survived. However, the survival rates decreased rapidly when exposure time was increased to 4 and 6 h, and temperatures _>30 ~ regardless of the humidity. When the temperature was as high as 41 ~ >85% of the whiteflies died after only 2 h, even when the air was saturated (humidity + 100%), and no whiteflies survived this temperature at any humidity for 4 h.

The results of the statistical analysis show that whitefly survival was affected most by temperature and somewhat less by exposure time and humidity (Tables 1 & 2). Surprisingly, the effects of temperature and humidity appear to be almost independent, their compound effect, with and without time, accounting for <0.1% of the variance. There are, however, interactions between time and both temperature and humidity, supporting the hypothesis that the effect of drying conditions is cumulative.

Effect of feeding on survival. The survival of unfed whiteflies was less than the control which was provided with food (65% vs. 85%). The lack of food caused an additional mortality, which increased with exposure time, and was calculated to be 17% after 2 h, 21% after 4 h, and 27% after 6 h. Analysis of variance showed that the whitefly survival was significantly higher with than without food (F],5=36, a<0.001; Table 3). As

516

Table 2. Improvement of fit w~th the addition of terms to the linear predictor using the logit link function

Residual Improvement of fit Adding model term' df Deviance x 2 x 2 F-ratio

Grand mean 450 31150 - - Temperature 449 13310 17840 601.8"** Time.temperature 448 10770 2540 105.7"** Time-humidity 447 8574 2196 114.5"** Time 446 8573 1 0.1 N/S Temperature.humidity 445 8572 1 0.1 N/S Temperature.humidity time 444 8566 6 0.3 N/S Humidity 443 8554 12 0 6 N/S

**% a<0.001; N/S, not significant (a>0.25)

i~arameter estimates of the fitted model (equation 4) describing the mortality of Bemisia tabact exposed to a range of temperature and humidity conditions for different time periods

Pmameter Estimates Std. error

bo Intercept 8 3000 0.08330 bl Temperature -0.2082 0 00244 B2 Time.temperature - 0 0204 0.00033 b2 Time.humidity 0.0064 0 00010

with the previous experiment, mortality did not change significantly over time, however the significant inter- action between time and feeding confirms what one would expect, that feeding both postpones death and reduces the death rate.

Effect o f TYLCV-status on survival. The survival of virus-free B. tabaci was higher than that of viruliferous whiteflies (72% vs. 58%). Both virus-free and viruliferous whiteflies survived better at higher humidities (78% vs. 70% survival at 100% r.h.) than at low humidities (66'survival at 50% r.h.). Analysis of variance showed that the difference in survival between viruliferous and virus-free whiteflies was highly significant (F2,36 = 12.6, a<0.001) indicating that the sus- ceptibility to drying was increased by virus infection. Partitioning the sums of squares into position and slope revealed differences in position only (Table 4), suggesting that viruliferous whiteflies start to die at higher humidities, but that the mortality increases with declin- ing humidity at the same rate for viruliferous and virus- free individuals.

Discussion

We have attempted here to assay the survival prospects ofB. tabaci under temperature and humidity conditions similar to those prevailing during summer in Israel. However, it cannot be inferred that the results are survival estimates of sedentary whiteflies under similar conditions of temperature and humidity in the field, because plant leaves change the microclimate consid- erably. However, our results probably do define the limits to survival ofB. tabaci not protected by a plant's microhabitat.

Nor can our results be translated directly into estimates of migration survival. Instead, the results show relative differences in survival under different atmospheric conditions. Our results suggest that survival under extreme atmospheric conditions is minimal. Any whiteflies taking off under such conditions are unlikely to survive long, thus limiting the dispersal distance (although this does not rule out quite long distance migration by a series of short, daily flights). Survival rates above 66% were observed in the laboratory at all humidity levels whenever the exposure time was 2 h, and temperature <35 ~ When the temperature was <25 ~ the whiteflies survived for as long as 6 h. More than 66% survived temperatures of 30 - 35 ~ for up to 6 h provided the humidity was sufficiently high. How- ever, ~ 2% of whiteflies survived 6 h at 20% r.h., or 2 h at 41 ~ at 20% r.h., non survived >2 h at 41 ~ or >4 h at 35 ~ when the humidity was 20%. These conditions define the limits of whitefly survival, thus, one can expect whiteflies to survive on a normal summer day of 32 ~ and 50% r.h. for at least 6 h without food or the protection conferred by a plant's microhabitat. Under the experimental conditions, the whiteflies were deprived of not only food and free moisture, but also the microclimate of host plant leaves, which no doubt ameliorates the extreme atmospheric conditions of hot-dry Chamsin days.

Climatic conditions which limit the dispersal potential and distance travelled by virus vectors are of great importance in the study of virus epidemiology. The effects of various combinations of temperature, humidity, and time, that were tested in these experiments, represent the range of prevailing climatic conditions to which B. tabaci are likely to be exposed during migration. The shade temperatures, during the time of B. tabaci dispersal are usually between 25-35 ~ with 41 ~ on a few exceptional days. Humidity is typically 50-80% with extremely low humidity values _<20% prevailing on exceptionally hot days in spring

Table 3. Influence of food on the survival of Bemisia tabaci adults, after exposure to 2 5 ~ and 55% humidity. Analysis of

variance

Residual Improvement of fit

Adding model term' df Deviance x 2 x 2 F-ratio

Grand mean 59 99.47 - -

Time 58 98.89 0.58 0.67 N/S

Food 57 52.86 46 03 52 86"**

Time.food 56 48.76 4.10 471 *

�9 **, a<0.001; *, a<0 05, N/S, not significant (a<0.25)

Estimates of survival probability due to the lack of food

Exposure % Surviving % Mortality due to

time (h) with food without food lack of food

2 86 t 71 4 17.1

4 78.0 61.7 20.9

6 88.4 64 3 27.3

Analys~s of Vmlance of the effect of feeding on survival

and autumn. It is unclear whether whiteflies take-off during a Chamsin, because hardly any flight activity has been recorded either by direct observations or by trapping.

Whiteflies, when trapped at a distance of more than a few dozen meters from their host plants, represent the dispersing fraction of the population flying in search of new hosts (Cohen et al., 1974). There is a significant correlation between the number of these trapped B. tabaci and the incidence of TYLCV-infected plants (Berlinger et al., 1988). This correlation indicates the importance of whitefly dispersal in the epidemiology of TYLCV (Berlinger et al., 1988). If dispersal is over short distances only, control of B. tabaci on local non-crop hosts or phytosanitation could be effective in reducing TYLCV incidence in crops. Sample data suggest that dispersal occurs simultaneously through-

Table 4 Survtval of viruliferous and virus-free whltettles after 4 exposure to 30 ~ and 50 or 100% r.h. AnalysLs of variance

Residual Improvement of fit

Adding model term' df Deviance x 2 x 2 F-ratio

Gland mean 39 97.04 -

Huml&ty 38 55.56 41 45 35.99 ***

Position 37 42.79 12 77 11.09 **

Parallehsm 36 41.46 1 33 1 15 N/S

~*, a<0 001, **, a<0.005; N/S, not stgmficant (a<0 25)

517

out Israel provided temperature <33 ~ and humidity >35%. This is important for management of TYLCV because the dispersal distance of viruliferous whiteflies arriving in newly planted fields or greenhouses can influence the success of control strategies. Carry- ing TYLCV significantly reduces B. tabaci's ability to survive. The whiteflies used in the virus test did not have food available during the test, thus an indirect effect via the host plant seems unlikely. Because bear- ing TYLCV caused a significant increase in the death rate of the whiteflies, we infer that dispersal by viruliferous whiteflies may be shorter than healthy whiteflies. TYLCV is a semi-persistent geminivirus not reproduc- ing in the vector. Thus, its effect differs from some persistent infections which can increase the survival prospects of their vectors (e.g., corn stunt spiroplasma- infected Dalbulus maidis; Ebbert & Nault, 1994).

Survival of a few whiteflies under extreme experimental conditions for a short time suggests that B. tabaci may be able to fly over short distances even in extreme weather conditions; a distance of a few kilo- meters, perhaps. B. tabaci feed mainly at night and fly principally during the morning (M. J. Berlinger, unpubl.; Byrne & von Bretzel, 1987; Blackmer & Byrne, 1993a), and like aphids (Halgren & Taylor, 1968; Dry & Taylor, 1970) they fly only within a certain range of temperatures (Blackmer & Byrne, 1993b). The lack of insects in the air on hot dry days could be due to either the death of those that do attempt flight, or the inhibition of flight. At the moment we have no information on the humidity- and temperature-flight thresholds, however, it seems more likely that the low trap catches are due to reduced activity. Relative humidity is known to restrict other activities, even for whiteflies on plants that can obtain moisture through feeding. Oviposition, for example, ceases altogether at relative humidities <60% although survival is not affected (Avidov, 1956). Intuitively, we might expect that the effect of drying conditions is a cumulative process so that insects' exposure to a low humidity and/or high temperatures for a long period would elicit a higher mortality than exposure to the same conditions for a shorter period. With relative humidity this was the observed effect. The product of humidity and time accounted for more variance than the sum of the pair (15% vs. 8%), confirming that the ability of B. tabaci to survive short exposures to low humidity is much greater than the ability to survive similar periods of high temperature. However, the data show that there is a direct effect of temperature in addition to the compound effect of temperature and time. Over the course

518

of the 2-6 h experiments, no direct effect of time was observed; no significant time-(age- )dependent mortality occurred.

The highly significant direct effect of temperature on survival is surprising, for it suggests an immedi- ate response to temperature, in addition to the expect- ed cumulative response represented by the product of time and temperature. However, rearranging equation 4 offers an alternative explanation:

# = bo + b2' T - (t + to) + b3 �9 H . t (5)

where to = bl/b2 ( ~ 10) is a relocation parameter. We interpret to as a historical factor, that defines the effect of the conditions prevailing over the previous 10 h. The experiments all started, by definition, at t=0. But, at t= - I0 it was night and the insects were still on plants in the rearing chamber at ~ 25 ~ The experimental temperature conditions alone do not define the survival of whiteflies. Instead, survival at the experimental temperature is modified by a factor which depends on the prior experience: in this case, the experience was ~ 25 ~ for 10 h. The value of to will vary with rearing temperature: to will be minimum for the most benign temperatures, and maximum for temperature extremes. If this is the correct interpretation of the relocation parameter under laboratory conditions, then temperature-dependent survival in the field will also depend on prior temperatures.

No recovery from the experimental conditions was noticed after the additional 20 h of favorable conditions. This could be the consequence of an irreversible change to the cuticle following a period of exposure to high temperatures (Chapman, 1982). However, the residual effect of temperature on survival suggested by equation 5 would have the same effect if short term physiological acclimation modifies the upper lethal temperature as suggested by Maynard Smith (1957). In practice this means that the probability of whiteflies recovering after landing on a suitable host plant with its improved micro-climatic conditions declines with the duration of exposure to adverse atmospheric conditions during flight. Conversely, if conditions were such as to reduce the value of to, this could extend the period that flying whiteflies could survive adverse atmospheric conditions. All other things being equal, to will be at its minimum early in the morning. Thus, it would be most advantageous for whiteflies to fly only in the morning, as soon as the temperature is high enough for flight muscles to finction efficiently. Considering the

significantly lower survival potential under the Cham- sin conditions, it is probable that there is an upper temperature threshold for flight which inhibits take-off on such mornings.

Recently-fed post-teneral adults were used in the experiments as models for morning flyers which are potential dispersers. Because hunger reduces B. tabaci's ability to survive drying conditions by 17% to 27% and free moisture is unavailable while flying, the time since the last meal is an important arbiter of survival during migration. The harmful effect of starvation means that even at rather common climatic conditions, e.g. 25-28 ~ and 50-60% r.h., the time available for dispersal flight, and therefore the dispersal distance, is limited. Furthermore, although feeding can prevent death due to desiccation, its ability to promote recovery after prolonged exposure to drying conditions appears limited. Thus, the number of individuals remaining airborne for more than a few hours in summer is probably quite low, and the incidence of very long duration and distance (> 100 km) migratory flights, such as some aphids (Berry & Taylor, 1968) and leafhoppers (RAJ Taylor & Reling, 1986; RAJ Taylor, 1989) engage in, must be very rare.

Acknowledgments

We wish to thank Dr R. K. Lindquist for his critical review of the manuscript and a number of helpful sug- gestions. This research was supported by grant No. 1- 589-83 from the United States-Israeli Binational Agri- cultural Research and Development Fund (BARD). Contribution from the Agricultural Research Organi- zation, The Volcani Center, Bet Dagan, Israel. Number 1561-E, 1995 Series.

References

Avidov, Z., 1956. Bionomics of whitefly (Bemisia tabaci Gennad.) in Israel. Ktavim 7: 25~-1.

Baker, R. & J. Nelder, 1978. GLIM Reference Manual. National Algorithms Group, Oxford.

Berlinger, M. J., 1973. Effect of relative humidity and temperature on the survival of Clausenia josefi (Hymenoptera: Encyrtidae) Entomologia Experimentalis et Applicata 16: 373-379.

Berlinger, M. J. & L. Bar Nlr, 1989. A population growth model for Bemtsta tabaci. Phytoparasitica 17: 228-229.

Berlinger, M. J. & R. Dahan, 1986. Flight Patterns ofBemtsta tabact, a vector of plant viruses. International Conference on Tropical Entomology, Nairobi, Kenya.

Berhnger, M. J., R. Dahan & S. Cohen, 1988. Phenology of the tobacco whitefly, Bemisia tabaci, in glasshouse tomatoes in Israel. Phytoparasitica 12:2-3

Berry, R. E. & L. R. Taylor, 1968 High-altitude migration of aphids in maritime and continental climates Journal of Animal Ecology 37' 713-722.

Blackmer, J L. & D. N. Byrne, 1993a. Flight behawour of Bemisia tabaci in a vertical flight chamber: effect of time of day, sex, age and host quality Physiological Entomology 18' 223-232.

Blackmer, J L & D. N. Byrne, 1993b Environmental and physiological factors influencing phototactic flight by Bemtsia tabact. Physiological Entomology 18:336-342

Byrne, D. N. & T S Bellows, 1991. Whitefly biology Annual Review of Entomology 36' 431~-57.

Byrne, D N & P K von Bretzel, 1987. Similarity in flight activity rhythms in coexisting species of Aleyrodidae, Bemista tabact and Trtaleurodes abutihmea Entomologla Experimentalis et Apph- cata 43.215-219,

Chapman, R. F., 1982 The Insects, third edition. Harvard University Press, Cambridge, M~ss 919 pp

Cohen, S & F E. Nitzany, 1966. Transmission and host range of the tomato yellow leaf curl virus Phytoparasitica. 56:1127-1131.

Cohen, S , M J Berlinger, N. Lehmann-Sigura, J. Keren, I. Harpaz & R Ben Joseph, 1986. The epidemiology of a whitefly-borne virus in Israel Workshop on the Epidemiology of Plant Virus Diseases 6-8 August 1986, Orlando, Florida (Abstract)

Cohen, S , V. Melamed-Madjar & J. Hamem, 1974 Prevention of the spread of tomato yellow leaf curl virus transmitted by Bemtsta taba~t (Gennadms) (Homoptera, Aleyrodidae) in Israel Bulletin of Entomological Research 64: 193-197.

Dry, W W & L R Taylor, 1970 Light and temperature thresholds for take-off by aphids. Journal of Ammal Ecology 39: 493-504.

Duffus, J E., 1987 Whitefly transmission of plant viruses Current Topics in Vector Research 4' 73-91.

Ebbert, M. A & L R. Nault, 1994. Improved overwintering ability in Dalbulus maidzs (Homoptera: Cicadellidae) vectors infected with Sptroplasma kunkehi (Mycoplasmatales: Spiroplasmat- aceae). Environmental Entomology 23:634-644

Gerliug, D & R Horowitz, 1983. Yellow traps for evaluating the population levels and dispersal patterns of Bemtsta tabacl (Homoptera, Aleyro&dae) Annals of the Entomological Society of America 77 753-759

Halgren, L A & L R Taylor, 1968 Factors affecting flight respons- es of ahenicolae of Aplus ['abae Scop. and Schtzaphts grammum Rondani (Homoptera. Aphididae) Journal of Animal Ecology 37 583-593

519

Horowltz, A. R., 1986. Population dynamics of Bemtsta tabact (Gennadius) with special emphasis on cotton fields. Agriculture Ecosystems and Environment 17: 37-47.

Johnson, C. G., 1957. The distribution of insects in the air and the empirical relation of density to height Journal of Ammal Ecology 26. 479494.

Johnson, C. G., 1969. Migration and Dispersal of Insects by Fhght Methuen, London. 763 pp.

Madge, S. D., 1961. The control of relatwe humidity with aqueous solutions of sodium hydroxide. Entomologia Experimentahs et Applicata 4 143-147

Maynard Smith, J., 1957. Temperature tolerance and acclimatization In Drosophila vubobscura Journal of Experimental Biology 34 85-96.

Solomon, M E, 1957. estimation of humidity with cobalt thlo- cyanate papers and permmlent colour standmds Bulletin of Ento- mological Research 48 489-506

Taylor, L. R., 1958. Aphid dispersal and diurnal periodicity. Pro- ceedmgs of the Lmnean Society of London 169' 67-73.

Taylor, L. R., 1960a. The distribution of insects at low levels in the air Journal of Animal Ecology 29' 45-63

Taylor, L. R., 1960b. Mortality and viability of insect migrants high in the air. Nature 189:732-735

Taylor, L. R., 1974. Insect migration, flight periodicity, and the boundary layer. Journal of Animal Ecology 43 225-238

Taylor, L. R., 1989. The four kinds of migration. In: W. Dantha- narayana (ed), Insect Flight Dispersal and Migration. Springer Verlag, Berlin, pp. 265-280.

Taylor, R. A. J., 1978. The relationship between density and distance of dispersmg insects Ecological Entomology 3: 63-70.

Taylor, R. A. J., 1981. A family of regression equations describing density distribution of dispersing organisms. Nature 286:53-55

Taylor, R. A. J., 1985. Migratory behavior in the Auchenorryncha. In. L. R. Nault, & J. G. Rodriguez (eds.), The Leafhoppers and Planthoppers John Wiley & Sons, New York, pp 259-288.

Taylor, R. A. J., 1989. Potato leafhopper migration the mystery of the return migration. Miscellaneous Papers of the Entomological Society of America 72 42-52.

Taylor, R. A J & D. Rehng, 1986. The preferred wind direction of long-distance leafhopper (Empoas~ a ['abae) migrants and its relevance to the return migration of small insects Journal of Animal Ecology 55:1103-1114

Taylor, R. A. J., L. R. Nault & W. E. Styer, 1993 Fhght activity of three leafhoppers of the genus Dalbuluv (Homoptera. Auchenor- ryncha) obtained from free flight in the laboratory Annals of the Entomological Society of America 96: 655-667.

survival of bemisia tabaci adults under different climatic conditions

Documents