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Combatting whiteflies: predatory mites as a novel weapon

Nomikou, M.

Publication date 2003

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Citation for published version (APA): Nomikou, M. (2003). Combatting whiteflies: predatory mites as a novel weapon. IBED, Universiteit van Amsterdam.

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Download date:29 Sep 2021 M.. Nomikou [2003] Combating whiteflies: Predatory mites as a novel weapon

Impactt of alternative food on the dynamics of predatoryy mites, Typhlodromips swirskii, and theirr whitef ly prey

Mariaa Nomikou, Arm Janssen d Maurice W. Sabelis

(BED,(BED, Population Biology, University of Amsterdam, P.O. Box 94084, 1090 CB Amsterdam,Amsterdam, The Netherlands

Thee predatory mite, Typhlodromips swirskii, is a promising candidate forr biological control of the silverleaf whitefly, Bemisia tabaci, a worldwidee pest of agricultural crops. The predator feeds on immature whitefliess and it can develop and reproduce on a diet of B. tabaci. Earlierr population experiments showed that T. swirskii is able to suppresss whitefly populations on single plants in the presence of pollen, ann alternative food source for the predatory mite. To further analyse thee role of pollen, we carried out population experiments with predatoryy mites and whiteflies on single, male-sterile cucumber plants, eitherr provided with pollen or not. In absence of predators, the whiteflyy populations increased exponentially over a period of two months,, whereas their growth was much slower in presence of predators.. The whitefly populations in the treatments with predators reachedd lower numbers on plants with pollen supply. The number of predatorss per plant was higher on plants with pollen, than on pollen- freee plants. Earlier work has shown that the presence of pollen did not affectt predation or oviposition rates of T. swirskii on ample supply of whiteflyy vulnerable prey. Therefore, the positive effect of pollen on whiteflyy control can only arise from its impact on the numerical responsee of the predators to the densities of whiteflies during the predator-preyy interaction.

KeyKey words: Typhlodromips swirskii, Bemisia tabaci, pollen, cucumber, greenhouse,, biological control, predator-prey dynamics

Theoryy predicts that addition of an alternative food source for a predator cann alter predator-prey dynamics (Holt 1977). Within a predator generation, thee addition of alternative food for the predator might result in higher prey numbers,, due to switching or satiation of predators (Holt and Lawton 1994).

97 7 PartPart 2 - Biological control of white fly populations on single plants

Inn the long term, the presence of alternative food can have a negative effect onn the prey by sustaining higher predator numbers than those reached on thee prey alone (Holt and Lawton 1994). Thus, prey equilibrium levels can be reducedd even to extinction. Hence, the use of alternative food for the predatorss in biological control programmes may improve the success of pest controll {Hagen 1986; van Rijn et at. 2002). Wee investigated the effect of alternative food, e.g. pollen, on a novel biologicall control agent for whiteflies in greenhouse crops. The whitefly BemisiaBemisia tabaci (Gennadius) is a worldwide pest that causes significant yield lossess for the growers, especially when outbreaks occur (Oliveira et al. 2001).. Yet, most attempts of biological control for B. tabaci have failed and ongoingg research aims at identifying efficient natural enemies of this pest (Gerlingg et al. 2001). One class of whitefly enemies are phytoseiid predators (Nomikouu et al. 2001). A few phytoseiid species were found in association withh whiteflies, but research on these predator-prey systems has mostly focusedd on feeding trials in the lab (see Nomikou et al. 2001). TyphlodromipsTyphlodromips swirskii (Athias-Henriot) was collected on cotton plants infestedd with whiteflies and it oviposits and develops when feeding on B. tabacitabaci immatures as well as on pollen (Nomikou et al. 2001). The predatory mite,, T. swirskii, was found to suppress whitefly populations on isolated singlee plants {male-sterile cucumber) with a weekly supply of pollen in a greenhousee in the presence of a weekly supply of pollen (Nomikou et al. 2002).. The effect of pollen as an alternative food source for the predator on thee population dynamics may have been two-fold. Either initial predator / preyy ratios might have been sufficiently high due to the presence of pollen andd further addition of pollen was unimportant for the outcome of the predator-preyy interaction, and/or pollen had a significant effect on the predator-preyy dynamics, by keeping predator / prey ratios high during the experiment. . Inn this article, we analyse the effect of pollen on control of whitefly populationss by T. swirskii with population experiments on single cucumber plantss in a greenhouse. In previous experiments, T. swirskii did not show a reducedd predation rate nor a change in the oviposition rate in presence of pollenn and an ample supply of the most vulnerable whitefly stage (crawlers) (Nomikouu et al., submitted). Unless predation and oviposition are affected byy the presence of pollen at lower prey densities, we would therefore not expectt an effect of pollen on the dynamics of the whitefly populations.

MATERIALSS AND METHODS

Cultures Cultures Cucumberr plants (var. Ventura RZ®, RijkZwaan, De Lier, The Netherlands) weree cultivated in pots (2 I) in a greenhouse compartment ; l:d = 16:8)

98 8 ImpactImpact of pollen on predatory mite - white fly dynamics untill 3 weeks old. Bemisia tabaci strain B (J. Fransen, pers. comm.) was obtainedd from the Research Station for Floriculture in Aalsmeer in March 1995,, where it was cultured on poinsettia. We cultured whiteflies on cucumberr plants in climate boxes ; l:d = 16:8). TyphlodromipsTyphlodromips swirskii was collected in Israel (location Revadim) in 19977 on cotton infested with B. tabaci (Nomikou et at. 2001). It was cultured sincee then on plastic arenas (8x15 cm) placed on a wet sponge in a plastic trayy containing water (see Overmeer 1985). Strips of wet tissue were placed onn the plastic arena along its periphery so that the predators had access to water.. Glue barriers were applied on this tissue to prevent escape and contaminationn with other mite species. A piece of transparent plastic sheet (1-22 cm2) folded in the shape of a tent was placed on each arena and functionedd as a shelter for the mites (Overmeer 1985). A few cotton threads weree put underneath the shelter to serve as oviposition substrate (Overmeer 1985).. Broad bean pollen (Vicia f aba L.) was offered as food for the predatorss by dusting it on the arenas twice per week. The predatory mite culturee was maintained in a climate room , 60% RH). Broadd bean pollen was collected from plants cultivated in a greenhousee compartment at the University of Amsterdam and cattail pollen, TyphaTypha latifolia L, was collected at the University campus. Both types of pollenn were kept in a refrigerator.

ExperimentalExperimental set-up Populationn experiments were carried out in cages in a greenhouse compartmentt at the University of Amsterdam , 60% RH, 16-8h photoperiod).. The cages (0.8 x 0.8 x 1 m) consisted of a metal frame, a plasticc bottom, a Plexiglas® top and three sides with fine mesh gauze (80 (i). AA Plexiglas door covered the fourth side and was closed by strips of magnetic tape.. The cages were placed on 4 tables, each with a tray filled with a 2-3 cmm layer of water. The cages were kept above the water by placing them on bricks.. In this way, a water barrier surrounded the cages, preventing escape andd invasion of mites. Temperature and humidity loggers recorded the conditionss in each cage at 30-minute intervals. Threee cages were placed on each table. A potted cucumber plant of 3 weekss old was placed in each of the cages. Three wooden sticks, (90 cm long)) were stuck in the soil around the young plant and they were tied togetherr near the tip, forming a tent-like frame that supported the plant. Initially,, fertilizer was supplied in capsule form (N:P:K = 15:10:12), but later itt was provided via the irrigation water (N:P:K = 28:14:14). Plants were allowedd to flower and grow lateral stems. Control cages received whiteflies only.. All other cages received predators and whiteflies and we supplied TyphaTypha sp. pollen to half of the plants. The experiment was done from late Octoberr 2001 to January 2002.

99 9 PartPart 2 - Biological control of white flypopulations on single plants

InitialInitial conditions and pollen supply Sincee an earlier population experiment on cucumber plants with B. tabaci andd 7. swirskii showed successful control in presence of Typha sp. pollen (Nomikouu et at. 2002), we chose similar initial conditions. At the start of the presentt experiment, twenty adult whiteflies (10 females and 10 males) were introducedd to each of the 12 plants. Three days later, each plant was suppliedd with predators, 48 females and 120 juveniles and males (as estimatedd from the initial conditions of the previous experiment) on the 3rd lowestt leaf of all plants, using a fine brush. One day later, the number of adultt female predators was always lower than 40. To recreate equal initial conditionss we added females from the cultures to achieve an initial number off 40 on all plants. The predators released were obtained from cultures startedd two weeks earlier with 24, 8-10 days old females supplied with 25-30 mgg of pollen as the only food source. After a week, we added an extra 24 femaless and again 25-30 mg of pollen to these cultures to obtain a populationn structure similar to that of earlier population experiments. Onee day after predator release, half of the plants were supplied with 25-300 mg of Typha sp. pollen in plastic vials (19 mm diameter and 15 mm high)) suspended from the base of the 3rd leaf stem by means of a piece of electricityy wire that was inserted in 2 holes at opposite sides near the vial rim.. We placed empty vials at corresponding leaf stems on the pollen-free plants.. Every week, plants that received pollen were supplied with 25-30 mg off fresh pollen in a new vial that was suspended two leaves higher than the previouss vial. This quantity of pollen is sufficient to sustain a population of phytoseiidss in laboratory cultures (M. Nomikou, pers. obs.). Moreover, the qualityy of Typha sp. pollen remains good for a week (Y.M. van Houten, unpublishedd data). Vials with pollen were removed from the plant after 3 weekss and checked for predators, with a binocular microscope. Predators weree transferred back to the leaf that was closest to the vial. Hence, plants providedd with pollen carried one vial in the first week, two vials in the secondd week, and never more than 3 vials during the subsequent experimentall period. Ass a control, we followed the dynamics of whitefly populations without predatorss on 6 cucumber plants. Due to limited greenhouse space and limitedd number of available cages, we started this control right after the firstt cages in the predator treatment became available due to the destructivee method of sampling (see below). Plants were handled as above, andd whiteflies were released as above. Moreover, plastic vials were attached too the same leaves as above, but they were not provided with pollen, thus makingg the control best comparable with the predator treatment without pollenn supply. Whiteflies are phloem plant feeders and it has not been observedd (M. Nomikou, pers. obs.) nor reported that they can utilise pollen ass food source.

100 0 ImpactImpact of pollen on predatory mite - white fly dynamics

RecordingRecording the population dynamics Adultt whiteflies were counted while removing them from all leaves of a plantt with an aspirator. Subsequently, these leaves were detached from the plantt and adult female predatory mites were counted by visual inspection of thee detached leaf. Finally, four leaf discs (15 mm diameter each) were punchedd from each detached leaf, two from the left and two from the right leaff sections, defined by two adjacent veins at each side that were nearest too the main vein. These discs were stored in a closed plastic vial (3 cm diameter,, ca. A cm high) filled with 70% alcohol and they were inspected laterr under a binocular microscope, to count the number of immature whitefliess distinguishing 4 classes: (1) eggs, (2) crawlers and second instars, (3)) third instars and (4) pupae. The first count was done the 37th-39th day (wee counted 2 plants per day, 6 plants in total) and the second the 58th-59th dayy (we counted 3 plants per day, 6 plants in total) after whitefly release. Onn the control plants, adult whitefly populations (not the immatures!) weree counted on 3 plants, 38th-39th day after release (on the two and one plantss respectively) and on only one plant 59 days after release, whereas the numberss on the remaining two plants were determined in terms of order of magnitudee (100, 1000 or 10.000) for logistic reasons.

DataData analysis Temperaturee conditions during the experiment varied over time, but did not differr among the cages (Table 1). The average temperature was around 25 C (rangee 18 . However, humidity conditions varied both over time and amongg the cages. Even though the positions of each of the two treatments weree randomised and the control experiments were carried out in cages formerlyy occupied by either of the two treatments, there appeared to be a systematicc gradient in humidity: ca. 50% in the control experiments, ca. 60% inn the predator treatment without pollen and ca. 65% in the treatment with predatorss and pollen (Table 1). This can be explained by different environmentall conditions that occurred in the compartment during the periodss that we conducted the control and the treatments (relative humidity onn average during days 0-35: treatments 59.3%, control 48.7%). We, therefore,, included humidity as a covariate in the analysis. Twoo statistical analyses were applied. First, an ANCOVA was carried outt on the log-transformed total number of adult whiteflies per plant with timee and treatment (control, predators only, predators plus pollen) as independentt variables and relative humidity as a covariate. Note that the ANCOVAA with time as a factor is appropriate because other dependent variabless (the other whitefly stages and predators) were not or could not be measuredd in the control experiment, and because our population estimates weree obtained by destructive sampling, thus making them independent. Second,, a MANCOVA with time and presence or absence of pollen as factors

101 1 PartPart 2 - Biological control of white fly populations on single plants

Tablee 1 Average and standard deviation of temperature and relative humidity in the threee control cages (whiteflies only), in the three cages with whiteflies and predatorss and in the cages with whiteflies, predators and pollen. Because sampling off whitefly and predator populations was destructive, the measurements after 38 andd 59 days, as well as of the whiteflies only pertain to different periods.

Whitefliess only Whitefliess and predators Whiteflies,, predators and pollen n 1stt Count 2nd Count 1stt Count 2nd Count 1stt Count 2nd Count Temperaturee ) 25.99 2 25.0 0 4 24.8 1 24.9 1.5 24.7 3 25.11 9 25.4 1 24.6 5 25.0 5 24.5 1.3 25.2 4 25.11 9 25.3 0 24.9 3 24.7 3 25.2 1.5 24.4 1 Relativee Humidity (%) 43.66 4 61.1 4 57.0 i 8.0 57.6 12.8 70.2 12.0 63.1 12.5 42.00 3 52.1 3 71.0 6 60.6 + 12.4 64.5 10.8 65.2 12.4 53.11 6 54.9 5 55.4 5 65.5 12.5 65.4 0 63.5 12.9

andd relative humidity as covariate was performed on the following log- transformed,, dependent variables: numbers per total leaf area punched fromm a plant of (1) vulnerable, early whitefly stages {eggs, crawlers and secondd instars together) and (2) invulnerable, late whitefly stages (third instarss and pupae together), as well as the total per-plant number of (3) invulnerable,, adult whiteflies and (4) adult female predators. Planned comparisonss were made for the whitefly populations between the control andd the two predator treatments (with and without pollen) on each sampling datee in order to test the effect of predators on B. tabaci. Further, planned comparisonss with data from the predator treatments were made for each dependentt variable to test (a) the effect of pollen (comparisons between presencee and absence of pollen on each sampling date) and (b) the effect of timee (comparisons within pollen and no-pollen treatments between 1st and 2ndd sampling date). The critical a values were corrected according to the Dunn-Sidakk method (Sokal and Rohlf 1995).

Tablee 2 Analysis of covariance for log-transformed numbers of whiteflies in the 3 treatmentss (with predators and pollen, with predators and without pollen, and withoutt predators and pollen on the first and second sampling day with relative humidityy as a covariate.

Sourcee of variation df f Meann square F F P P Treatment t 2 2 1.605 5 51.890 0 4.11 x 10"7 Time e 1 1 3.482 2 112.550 0 2.55 x106 Treatmentt x Time 2 2 0.393 3 12.718 8 0.001 1 Relativee humidity 1 1 0.011 1 0.365 5 0.558 8 Error r 11 1 0.031 1 Total l 17 7

102 2 ImpactImpact of pol/en on predatory mite - whitefly dynamics

Patternss of the vertical distribution of adult whiteflies and their vulnerablee immature stages on the plants (at day 59) were analysed with a XX22 test, under the null hypothesis that the fraction of leaves inhabited by preyy in each stratum equals the fraction of leaves inhabited by prey on the entiree plant. The first 6 leaves were not included in the analysis because theyy were either old or dead at the end of the experiment, thus harbouring littlee or no whiteflies and predators. Leaves 7-12 were the leaves that were highestt above soil level, while leaves 13-18 were positioned on the part of thee plant that was suspended downward from the tip of the frame supportingg the plant and were thus closer to the soil level. These leaves carriedd the vials that were either empty or provided with pollen. All other leavess of the main stem and all lateral leaves were lumped together, as a thirdd and last group. The same type of analysis was done with respect to predators,, to test whether their distribution over the three groups of leaves deviatedd from the expectation based on the fraction of leaves per group.

RESULTS S

Overr the 59 days of the experiment, adult whitefly populations per plant in thee predator treatments increased on average 2-fold in presence of pollen, 15-foldd in absence of pollen, but more than 250-fold in the controls (Figure 1).. The average numbers of T. swirskii per plant increased 5-fold in presence off pollen and 2-fold in absence of pollen (Figure 2). An ANCOVA with numberss of adult whiteflies per plant as the dependent variable showed a significantt effect of the treaments, a significant effect of time as well as a significantt effect of the interaction between time and treatment, but there wass no significant effect of relative humidity as covariate (Table 2). A MANCOVA,, with numbers of vulnerable, invulnerable immatures and invulnerablee adults of the whiteflies and the number of adult female predatorss as dependent variables, showed a significant effect of pollen supplyy (Wilks' Lambda(4,4) = 0.097, P = 0.026) and a significant effect of time (Wilks'' LambdaHi4) = 0.066, P = 0.012). The interaction between pollen availabilityy and time was not significant (Wilks' Lambda(4,4, = 0.215, PP = 0.118), indicating that the effect of pollen did not vary through time. Thee relative humidity as covariate was not significant for any of the dependentt variables (df = 1, P > 0.468). Plannedd comparisons showed that the adult whitefly populations in the controlss differed from those in the predator treatments on the two sample dayss (whiteflies alone vs. whiteflies with predators on plants with and withoutt pollen; 1st sampling day, P = 7.6 x 10'4; 2nd sampling day, P = 4.6 x 108).. The adult whitefly populations in the two predator treatments with andd without pollen differed significantly, but only in the last of the two samplee days (Table 3). It can be concluded that the addition of predators

103 3 PartPart 2 - Biological control of whitefly populations on single plants

andd pollen led to the most severe suppression of the adult whitefly population. .

30 0 timee (days)

Figuree 1 Population dynamics of adult B. tabaci (closed circles: with predators and pollen;; open circles: with predators no pollen; asterisks: no predators, no pollen). Dataa shown are means +1 SD.

withh pollen -A- without pollen

22

o o

10 0 20 0 30 0 40 0 50 0 60 0 timee (days)

Figuree 2 Population dynamics of adult female T. swirskii on plants with whiteflies (closedd circles: with pollen; open circles: without pollen). Data shown are means +1 SD. .

104 4 ImpactImpact of pollen on predatory mite - white fly dynamics

Tablee 3 Planned comparisons of the effect of pollen on populations of B. tabaci and T.T. swirski on isolated cucumber plants. Significant differences after correcting the a withh Dunn-Sidak method, are highlighted in gray.

Meann square (df = 1,7) Effect t Error r F F P P Afterr 38 days Whiteflyy stage Vulnerablee immatures 0.171 1 0.082 2 2.083 3 0.192 2 Invulnerablee immatures 0.001 1 0.044 4 0.034 4 0.858 8 Adults s 0.179 9 0.044 4 4.047 7 0.084 4 Femalee predators 0.534 4 0.031 1 17.280 0 0.004 4

Afterr 59 days Whiteflyy stage Vulnerablee immatures 1.627 7 0.082 2 19.793 3 0.003 3 Invulnerablee immatures 0.792 2 0.0436 6 18.136 6 0.004 4 Adults s 1.511 1 0.044 4 34.147 7 6.4x10" " Femalee predators 0.359 9 0.031 1 11.621 1 0.011 1

2000 -, r r4 0 0 E33 with pollen [ [ without pollen 160 0 i i

O) ) o>120 0

Q Q 22 80

.. T T T L L I I II ' ' eggs s earlyy instars

Vulnerablee immatures * Invulnerablee immatures'

Figuree 3 Number of whitefly immatures on a surface of 7.07 cm2 of all leaves, on plantss with pollen (gray bars) and on plants without pollen (white bars) after 59 days.. Data shown are means + 1 SE. Asterisk indicates significant differences within vulnerablee and invulnerable whitefly stages between plants with or without pollen (P<0.05). .

105 5 PartPart 2 - Biological control of white flypopulations on single plants

Tablee 4 Planned comparisons of the effect of time on B. tabaci and T. swirskii populationss on isolated cucumber plants with and without pollen. Significant differencess after correcting the a with the Dunn-Sidak method, are highlighted in gray. .

Meann square (df = 1,7) Effect t Error r F F P P Withoutt polle n n Whiteff ly stage Vulnerablee immatures 2.919 9 0.082 2 35.513 3 5.66 x 10 4 Invulnerablee immatures 1.777 7 0.044 4 40.708 8 3.77 x10 4 Adults s 1.379 9 0.044 4 31.162 2 8.33 x 10'* Femalee predators 0.022 2 0.031 1 0.707 7 0.428 8

With hpolle n n Whiteff ly stage Vulnerablee immatures 0.696 6 0.082 2 8.461 1 0.023 3 Invulnerablee immatures 0.202 2 0.044 4 4.627 7 0.069 9 Adults s 0.137 7 0.044 4 3.097 7 0.122 2 Femalee predators 0.002 2 0.031 1 0.067 7 0.804 4

Att the first sampling day (38 days after the first whitefly release), the differencess in numbers of vulnerable and invulnerable immature whitefly stages,, were not significant between plants with or without pollen (Table 3). However,, at the second sampling day (59 days since first whitefly release), thee numbers of all whitefly stages were significantly lower on plants suppliedd with pollen than on plants without pollen (Table 3, Figure 1, 3). In betweenn the two sampling days, there was a significant increase of the vulnerablee whitefly stages on pollen-free and pollen-supplied plants with predators,, but there was only a significant increase in the invulnerable stagess on plants without pollen (Table 4, Figure 1). Thus, the increase in vulnerablee stages was not followed by an increase in invulnerable stages on plantss with pollen and predators. Thee numbers of predators were significantly higher in plants with pollenn than in plants without pollen on the two sampling days (Table 3, Figuree 2). The numbers of T. swirskii found on the second sampling day were nott significantly different from those on the first sampling day, both in the treatmentt with and without pollen (Table 4, Figure 2). Analysiss of the vertical distribution of adult B. tabaci within plants at thee end of the experiment (day 59) showed that significantly more whiteflies weree found on the group of leaves highest above the soil (i.e. top leaves; Tablee 5). On pollen-free plants, higher numbers of vulnerable immature whiteflyy stages were found on the top leaves than on other leaves. This did nott occur on plants with pollen (Table 5). On plants without pollen, female

106 6 ImpactImpact of pollen on predatory -- mitewhitefly dynamics

Tablee 5 Differences in the distribution of adult whiteflies, adult female predators andd vulnerable immature whitefly stages (eggs, crawlers and 2nd instars) between thee top leaves (7th-12th leaf), the leaves carrying a vial (13th-18th leaf) and the rest of thee leaves (all leaves > 18) on plants with and without pollen after 59 days. Each columnn represents data from each plant; Different symbols ab,c indicate significant 2 differencee (x , P< 0.01) from the expected numbers calculated under the H0 that thee distributions of predator and prey are homogeneous on the plant.

POLLEN N NOO POLLEN Topp leaves

JJ 1 1 1 1 1- top p 12» » 20» » 50» » 244» » 369» » 273» »

vials s 3ab b 0" " 9» » 35" " 37* * 67" "

rest t 28b b X" " 83" " 114' ' 348" " 268' '

top p 44» » 60» » 29» » 16» » 19» » 22» »

vials s 39» » 42" " 22» » b b 5" " 7" "

rest t 204" " 160" " 46" " 29" " 22" " 50" "

top p 2» » 0" " 3» » 86» » 40» » 30» » vials s 0» » 0» » 3» » 0 0 11» » 16" " 12" " rest t 10» » 7» » 26» » 115» » 133" " 108" "

predatorss aggregated significantly more on the top leaves than on other partss of the plant. On plants with pollen, female predators were also found too aggregate but they were now relatively abundant on the top leaves as welll as on the leaves where the pollen was supplied (i.e. leaf 13-18, Table 5). .

DISCUSSION N

Whiteflyy numbers increased exponentially in the absence of predatory mites. Afterr 59 days, whitefly populations in the presence of T. swirskii were suppressedd to levels more than 40-fold lower than in the controls. The additionn of pollen to plants with predators also led to a more than 8-fold reductionn of the whitefly populations. Populations of T. swirskii reached

107 7 PartPart 2 - Biological control of white fly populations on single plants

higherr numbers on plants with pollen. These plants, however, had lower preyy availability than the pollen-free plants. Hence, the higher growth rates off predatory mites in presence of pollen must be due to higher oviposition, developmentt and /or survival rates of predators on a diet of whiteflies and pollen. . Predatorss mainly consume B. tabaci eggs and crawlers and they hardly killl later immature stages and adults (Nomikou et al., submitted). In laboratoryy tests with ample supply of crawlers, the addition of pollen neitherr altered predation rate nor increased predator's oviposition rate (Nomikouu et al., submitted). Hence, we conclude that whitefly prey was a limitingg factor for predator oviposition on plants with and without pollen duringg an extensive period of the population experiment. However, T. swirskiiswirskii could have higher reproduction on plants with pollen due to the presencee of this supplementary food. Alternatively and complementary to thee effect of pollen on predator reproduction, a mixed diet e.g. whiteflies andd pollen might have a positive effect on the survival and/or developmentall rate of predators. Data on longevity of these phytoseiids on whiteflyy prey has not been collected and thus we can not conclude anything concerningg the adult survival. The juvenile survival and the developmental periodd of T. swirskii were found to be similar on a diet of pollen and on a diett of ample supply of whitefly immatures (Nomikou et al. 2001; Nomikou etet al., in prep). This suggests that development of predators could also be enhancedd by pollen, when prey availability is limited. The dietary effect of pollenn on predators is further supported by the fact that the predators aggregatedd on leaves carrying a vial only if the vials contained pollen. Anotherr consistent pattern that emerged from our analysis is the aggregationn of adult whiteflies and female predators in the top stratum of alll plants. Since immature whiteflies stay on their natal leaf (Byrne and Bellowss 1991), we expect the immatures to be aggregated there as well. Indeed,, this pattern was found on pollen-free plants, but not on plants providedd with pollen. This may arise from increased predation on the plants withh pollen. Usingg a detailed population model, van Rijn et al. (2002) showed that iff pollen supply is concentrated on a few leaves, it promotes thrips control byy predatory mites. This is because thrips can also utilise pollen, but not if thee pollen sites are occupied by their predators. This requires that predatory mitess do not stay put on the pollen sites, but also roam around to feed on thripss elsewhere on the plant. It is striking to find that the impact of the predatoryy mites on the thrips population in van Rijn et al. (2002) and on the whiteflyy population in our study is more pronounced in presence of pollen, whereass the predatory mites tend to aggregate on leaves near pollen. This suggestss that the local supply of pollen on the plant does not arrest the predatoryy mites to such an extent that they fail to find and feed on prey in otherr strata on the plant. How predatory mites allocate foraging time to leavess close to pollen vials vs. leaves with prey and no pollen, requires

108 8 ImpactImpact of pollen on predatory mite - white fly dynamics

furtherr study and it can elucidate the mechanism underlying the reduction off whitefly populations.

ACKNOWLEDGEMENTS S

Wee thank Paul van Rijn for advice. Ludek Tikovsky and Harold Lemereis were mostt helpful in arranging greenhouse space and RijkZwaan B.V., De Lier providedd cucumber seeds. Erik van Gool, Sara Magalhaes and Marta Montserratt are thanked for discissions. The manuscript was improved by J.C.. van Lenteren and J. Fransen. The research was funded as project ABI. 41655 by the Technology Foundation STW to MN and AJ.

REFERENCES S

Byrne,, D.N. and Bellows, T.S. 1991. Whitefly biology. Annu. Rev. Entomol. 36: 431- 457. . Gerling,, D., Alomar, 0. and Arno, J. 2001. Biological control of Bemisia tabaci using predatorss and parasitoids. Crop Protection 20: 779-799. Hagen,, K.S. 1986. Ecosystem analysis: Plant cultivars (HPR), entomophagous species andd food supplements. In: Interaction of plant resistance and parasitoids and predatorss of insects, D.J. Boethel and R.D. Eikenbarry (eds). John Wiley and Sons,, New York, USA. pp. 151-197 Holt,, R.D. 1977. Predation, apparent competition and the structure of prey communities.. Theor. Pop. Biol. 12: 197-229. Holt,, R.D. and Lawton, J.H. 1994. The ecological consequences of shared natural enemies.. Annu. Rev. Ecol. Syst. 25: 495-520. Nomikou,, M., Janssen, A., Schraag, R. and Sabelis, M.W. 2001. Phytoseiid predators ass potential biological control agents for Bemisia tabaci. Exp. Appl. Acarol. 25:: 271-291. Nomikou,, M., Janssen, A., Schraag, R. and Sabelis, M.W. 2002. Phytoseiid predators suppresss populations of Bemisia tabaci on cucumber plants with alternative food.. Exp. Appl. Acarol. (in press). Nomikou,, M., Janssen, A., Schraag, R. and Sabelis, M.W. Vulnerability of immature stagess of Bemisia tabaci to phytoseiid predators, consequences for oviposition andd influence of alternative food, (submitted). Oliveira,, M.R.V., Henneberry, T.J. and Anderson, P. 2001. History, current status, andd collaborative research projects for Bemisia tabaci. Crop Protection 20: 709-723. . Overmeer,, W.P.J. 1985. Rearing and handling. In: Spider Mites, Their Biology, Naturall Enemies and Control, Vol. 1b, W. Helle and M.W. Sabelis (eds), pp. 162-170.. Elsevier, Amsterdam. Sokal,, R.R. and Rohlf, F.J. 1995. Biometry (3rd ed). Freeman, New York, vann Rijn, P.C.J., van Houten, Y.M. and Sabelis, M.W. 2002. How plants benefit from providingg food to predators even when it is also edible to herbivores. Ecology 83:: 2664-2679.

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