Crop Protection 21 (2002) 113–119

Effect of temperature and host plants on the bionomics of Empoasca decipiens (Homoptera: Cicadellidae) K. Raupacha, C. Borgemeistera,*, M. Hommesb, H.-M. Poehlinga, M. Se! tamoua,c Institute of Plant Diseases and Plant Protection, University of Hannover, Herrenha.user Str. 2, 30419 Hannover, Germany b Federal Biological Research Centre for Agriculture and Forestry, Messeweg 11-12, 38104 Braunschweig, Germany c Texas A&M University, Agricultural Research and Extension Centre, 2415 E. Highway 83, Weslaco, TX 78596-8399, USA a

Received 26 February 2001; received in revised form 23 March 2001; accepted 17 May 2001

Abstract In laboratory experiments, the effect of various temperature regimes on the egg and larval development of Empoasca decipiens Paoli on broad beans were investigated. The shortest egg duration was recorded at 351C. However, the largest number of larvae emerged at 241C. Temperature had a significant effect on the larval development time, with a three-fold longer development time at 151C compared to temperatures X281C. Shortest larval development time was recorded at 301C. The host plant species had a significant effect on the larval development time. At 301C, the shortest development time was recorded on the broad beans (10.2 days) and the longest on aubergines (12.5 days). In a choice experiment, adult E. decipiens significantly preferred older ones compared to younger cucumber plants. In addition, hardly any larvae emerged from younger cucumber plants. These findings are discussed with regard to the increasing pest potential of E. decipiens in European greenhouses. r 2002 Elsevier Science Ltd. All rights reserved. Keywords: Empoasca decipiens; Leafhopper; Greenhouse; Bionomics

1. Introduction Leafhoppers are increasingly becoming serious pests in greenhouses in Europe, i.e., Germany (Schmidt and Rupp, 1997), the Netherlands and the UK (Helyer and Talbaghi, 1994), Bulgaria (Loginova, 1992) and Switzerland (Anonymous, 1998a, b). In most studies, Empoasca decipiens Paoli (Homoptera: Cicadellidae) was identified as the predominant leafhopper species. Its main area of distribution is central and southern Europe, North Africa, the Middle East and central Asia (Ossiannilsson, 1981). In the older reports E. decipiens and Eupteryx atropunctata Goeze (Homoptera: Cicadellidae) were already recorded as the most abundant leafhopper species in field crops in northern Germany (Afscharpour, 1960). However, due to the difficult taxonomy of Empoasca spp. in general, and particularly between the morphologically closely related species E. decipiens and *Corresponding author. Tel.: +49-511-7622641; fax: +49-5117623015. E-mail address: [email protected] (C. Borgemeister).

Empoasca pteridis Curtis (Koblet-Gu. nthardt, 1975; Ossiannilsson, 1981), older field records have to be treated with caution. According to Poos (1932), only male genital preparations assure a precise identification of the different species of Empoasca. Lately, Loukas and Drosopoulos (1992) developed a biochemical method using enzyme electrophoresis for the identification of E. decipiens and Asymmetrasca decedens Paoli (synonymous Empoasca decedens Paoli) (Homoptera: Cicadellidae). Empoasca decipiens has been recorded on a wide variety of crops and non-cultivated plants (Mu. ller, 1956; El-Dessouki and Hosny, 1969; Gu. nthart, 1971; Le Quesne and Payne, 1981). However, in leafhoppers the host plant preference in adults and larvae can vary considerably (DeLong, 1971). For instance, Gu. nthart (1971) failed to establish cultures of E. decipiens on vine, apple, willow trees, sugar beets, Phaseolus beans, and tomatoes. However, Vidano and Arzone (1983) recorded the presence of E. decipiens on vine and Schmidt and Rupp (1997) on tomatoes. In Egypt, E. decipiens and two other leafhopper species are major pests in cotton (El-Dessouki and Hosny, 1969). Moreover,

0261-2194/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 2 6 1 - 2 1 9 4 ( 0 1 ) 0 0 0 7 0 - 9

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Habib et al. (1972) studied the effect of temperature on E. decipiens on broad beans under field conditions in Egypt. However, no detailed laboratory studies on developmental time, thermal thresholds and host plant preferences in E. decipiens have been carried out. Thus, the objectives of this study were to gather basic biological and ecological data on E. decipiens. This information could be extremely valuable for the future development of IPM programmes against E. decipiens.

2. Material and methods 2.1. Mass rearing All experiments were conducted with an E. decipiens strain collected in 1997 on the island of Reichenau in southern Germany and since then maintained in the laboratories of the Federal Biological Research Centre for Agriculture and Forestry (BBA) in Braunschweig, Germany. The leafhoppers were mass reared on broad bean plants (Vicia faba L., cv. ‘Witkiem Major’) at 20711C, a 16 : 8 (L:D) photoperiod, and relative humidity (rh) ranging 50-85% in large Plexiglas cages (50
50
60 cm3). 2.2. Test insects Only insects with a uniform age structure were used in the experiments. For Experiments I and II, non-infested plants were introduced for 24 h in the mass rearing cages. Thereafter, the plants were removed, all adults and larvae were gently brushed off, and subsequently plants were kept individually. Empoasca decipiens females lay their eggs into the plant tissue (Mu. ller, 1956) and the eggs are visually difficult to detect (Poos, 1932). Thus the initial egg density could not be recorded. For experiments with 1st instars, plants were examined daily for the emergence of larvae. Subsequently, newly emerged larvae were transferred to individual leaves kept in specific experimental units (see next section). The experiments were conducted one after another, depending on the availability of insects and temperaturecontrolled chambers. 2.3. Experiment I: effect of temperature on the development time of eggs Adult leafhoppers were given the opportunity to oviposit on non-infested plants by introducing these plants for 24 h into the mass rearing cages. Thereafter, plants were removed and all leafhoppers, i.e., adults and larvae, were gently brushed off, using a fine camel brush. Experiments were conducted in temperature-controlled chambers, and the following temperature regimes were tested: 151C, 201C, 241C, 281C, 301C, 32.51C, 351C, and

371C. In all treatments, rh was in the range of 7075% and the experiments were conducted at a 16 : 8 (L : D) photoperiod. Emergence of larvae was recorded daily and the number of larvae counted. The egg development time was calculated according to the following formula: Ed ¼ Sðni
xi Þ=Sni ; with Ed the time from oviposition to emergence of 1st instars (in days), xi the development time (in days) and ni the number of larvae. Six to ten plants were used for each temperature treatment. One plant per temperature regime was exposed to the mass-rearing cage per day, such that data of each treatment were collected over time. 2.4. Experiment II: effect of temperature on the development time of larvae The same temperature regimes as in Experiment I were tested, and all trials were carried out in temperature-controlled chambers. Two different experimental set-ups were used: For 151C, 201C, and 241C, leafhoppers were kept in Petri dishes (+9 cm). The base of the Petri dishes was filled with a 2 mm thick layer of water agar (20 g Bacto-agar in 1 l of water). Ascorbic acid (10 mg/100 ml of water agar) was added to prevent fungal infections. In each Petri dish, a young broad bean leaf was placed on two wooden place holders, which enabled leafhopper larvae to feed on the lower side of the leaf, the preferred feeding site of leafhoppers (DeLong, 1971). After introducing the test larvae, the Petri dishes were sealed with parafilm, and the top cover of the Petri dish was finely perforated with a pin to allow aeration. Leaves were changed weekly; however, when leaves were heavily damaged by leafhoppers they were changed earlier. This set-up was modified for temperatures X281C, because the increasing condensation caused the water agar to dissolve. Hence, larvae which dropped off from the leaves sometimes got stuck in the sticky agar and died. Thus for 281C, 301C, 32.51C, 351C, 37.51C, and 401C a different method was used: Leafhoppers were kept in small transparent plastic cups of 4.5 cm height and a diameter of 3.5 cm. The cover of the cups was also finely perforated to allow aeration also. One broad bean leaf was placed upright in each cup. Leaves were changed weekly, but heavily damaged leaves were immediately replaced with new ones. Elevated air humidity in the cups or Petri dishes posed no major problems for the development of E. decipiens. Leafhoppers, in general, live on the underside of leaves, especially under conditions of high relative humidity (DeLong, 1971). Only freshly emerged 1st instars, as indicated by the red colour of their eyes (El-Kady et al., 1974), were used. L1 were obtained by keeping noninfested plants for 24 h in the E. decipiens mass rearing cages. Thereafter, plants were removed from the rearing

K. Raupach et al. / Crop Protection 21 (2002) 113–119

cages and all leafhoppers, i.e., adults and larvae, were gently brushed off. Depending on the availability of L1 and since E. decipiens are found at a wide range of density on plants, 5–10 1st instar larvae were initially introduced into each experimental unit per set-up. When the larvae moulted to L3, no more than six larvae were kept per experimental unit. Also, because of the high larval survival rate (>95%), the superfluous L3 were then transferred to additional units whenever the initial larval density exceeded six per given unit. In the Petri dish experiments, 7–12 experimental units and in the plastic cup experiments 5–10 experimental units per temperature treatment were used, respectively. The experimental units were observed daily until adult emergence and the total development time per individual larva in each set-up was recorded. An additional experiment was conducted at 301C to compare the two experimental set-ups. For the statistical analyses, every larva was considered as one unit. 2.5. Experiment III: effect of host plants on the development time of larvae The total development times of larvae were compared on five different host plants, i.e., tomatoes (Lycopersicon lycopersicum (L.) Karst. ex Farw., cv. ‘Sparta’), cucumber (Cucumis sativus L., cv. ‘Tyria’), sweet pepper (Capsicum annuum L., cv. ‘Mazurka’), aubergines (Solanum melongena L., cv. ‘Mastoma’) and broad beans (Vicia faba L., cv. ‘Witkiem Major’) as control. According to Koblet-G.unthardt (1975), broad beans are good host plants for rearing E. decipiens. Moreover, infestations of tomatoes, cucumber, sweet pepper, and aubergines by E. decipiens have been frequently observed in greenhouses in Germany (Schmidt and Rupp, 1997). All plants were reared in a greenhouse at ca. 241C. Broad beans were directly sowed into small plastic pots (+10 cm), whereas the other plants were first kept in nursery beds and later transferred to similar plastic pots. A commercial growing substrate (Klasman Tonsubstrat, Kultursubstrat I) was used, and except for broad beans the plants were fed once a week, using a standard vegetable fertiliser, i.e. 100 ml per plant of 0.5% Flory 4 (PLANTA D.ungemittel GmbH, Regenstauf, Germany) and 1% calcium nitrate. Because of the completely different growth patterns of the host plant species, experimental plants were of varying ages. Broad bean and cucumber plants were approximately four weeks old, whereas aubergine, sweet pepper and tomato plants were approximately ten weeks old. In broad beans, older leaves were used. Due to their size, younger leaves were used in sweet pepper and cucumber. In preliminary experiments, E. decipiens larvae did not develop on the pubescent younger leaves of aubergines and tomatoes. Therefore older tomato and aubergine leaves were used in the experiments. All trials were conducted in temperature-controlled chambers at 301C

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and 7075% rh. Experiments were conducted in small plastic cups containing one leaf of the respective test plant (for details see Experiment II). Depending on the availability of L1, initially 5–10 1st instar larvae were introduced into each experimental unit. When the larvae moulted to L3, no more than seven larvae were kept per experimental unit. In experimental units where the initial larval density exceeded seven, the superfluous L3 were then transferred to additional units. Per host plant species 10–14 experimental units were used. The leaves and the leafhoppers were inspected daily and the total development time until adult emergence was recorded. Leaves were changed weekly, but heavily damaged leaves were replaced immediately. 2.6. Experiment IV: host plant age preference of adult leafhoppers In a choice experiment, adult leafhoppers were offered three and five weeks old cucumber plants (cv. ‘Tyria’). Three week old plants were approximately 10 cm in height, whereas five weeks old plants were ca. 30 cm in height. Adult leafhoppers were offered two plants of different ages, each plant placed in opposite corners of a cage (50
50
60 cm3). In the middle of the cage, i.e., at equal distance to the two test plants, four adult leafhopper couples were released from a Petri dish. Test insects had previously been collected as 5th instar larvae from the mass rearing cages and were subsequently kept at 241C on broad bean plants until their final moult. At the time of the experiment, the leafhoppers were adults of 7–10 days. Starting one day after the release, the position of the E. decipiens adults on the two plants was recorded daily for a total observation period of seven days. Thereafter, all adults were removed and plants remained in the cage for another three weeks. Since first instar E. decipiens do not leave their host plants (Poos and Wheeler, 1943), the two plants were kept in the same cage. However, care was taken that the plants did not touch each other. Plants were inspected daily for newly emerged larvae, which were counted and then removed. The experiment was conducted in a temperature-controlled chamber at 241C and 7075% rh and repeated five times. 2.7. Statistical analysis Data on development time (Experiments I, II and III) were analysed using ANOVA, and mean comparisons were performed using a multiple t-test with Bonferroni probability adjustment procedure (SAS, 1992). In Experiment I, the egg development time depending on the temperature, in Experiment II, the larval development time depending on the temperature and in Experiment III, the larval development time depending on the host plant were analysed. The egg development

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time in Experiment I was subjected to a two-way ANOVA with time and temperature as factors. For Experiment II, a t-test was initially run to compare the effect of the two experimental set-ups on larval development time at 301C. Since no significant effects of set-up were observed (see results), data from the two set-ups were pooled for analysis. Larval development time was subjected to a three-way ANOVA with temperature, time of conduct of the experiment and initial larval density used as factors. In Experiment III, homogeneity of variance for data of the different experimental set-up was tested (Zar, 1974) and the two experimental set-ups were compared at 301C using a ttest. Since the variances were homogenous and no significant differences were observed between the two set-ups, data from all temperatures were pooled before analysis. For the host plant age preference behaviour (Experiment IV), the presence of the E. decipiens adults on young and old cucumber plants was compared using a Chi-square test. Number of hatched larvae on both types of plants was compared using a t-test with Bonferroni probability adjustment (SAS, 1992). In all the analyses, the significance level was set at a ¼ 0:05:

3. Results 3.1. Experiment I Since a series of experiments were conducted with time, the test plants used for a given temperature were treated as repetitions. The significant effect of test plants on the developmental time (F ¼ 7276:36; P ¼ 0:0001; df ¼ 15) showed that the experimental conditions were not uniform. However, the effect of temperature on the duration of egg development was highly significant (Table 1) with shortest egg duration recorded at 351C. By far the largest number of larvae emerged at 241C, and combined with the relatively short egg development period indicated that this temperature may provide optimum conditions for egg development. At 37.51C and 401C no larvae emerged (Table 1). 3.2. Experiment II No significant differences between the two experimental set-ups were found at 301C (t ¼ 0:467; n ¼ 82; P ¼ 0:642). Therefore, the data of the two experimental set-ups were combined in a unique analysis. Although the time of conduct of the experiment was significant (F ¼ 3273:05; df ¼ 6; P ¼ 0:0001), indicating a nonuniformity of the experimental units, temperature had a significant effect on the larval development time, with a three-fold longer development time recorded at the lowest temperature (Table 2). Shortest larval development

Table 1 The influence of temperature on the mean time of egg duration in E. decipiens on broad bean plants Temperature Mean duration Total no. No. of Mean no. of (1C) (days) of of emerged test emerged larvae egg stage larvae plants per plant (7SE) 15 20 24 28 30 32.5 35 37.5 40

28.2970.09aa 14.8870.04b 11.1170.02c 8.7070.05d 8.4570.03e 8.4070.05e 8.1970.08e Fb Fb

154 294 1260 300 381 147 36 F F

8 8 10 6 9 9 10 F F

19.3 36.8 126.0 50.0 42.3 16.3 3.6 F F

a Means per column followed by different letters are significantly different (t-test with Bonferroni probability adjustment, Po0:05). b No larvae emerged.

Table 2 The influence of temperature on the mean larval development time in Empoasca decipiens on leaves of broad beans Temperature (1C)

Mean time (7SE) for larval development (days)

No. of experimental unitsa

Total no. of emerged adults

15 20 24 28 30 32.5 35 37.5 40

36.970.24ab 18.870.15b 14.870.12c 11.770.24d 10.270.15e 10.570.12e 10.870.14e Fc Fc

8 12 7 6 10 6 8 5 5

38 56 34 21 48 33 25 F F

a

For L3 and older larvae. Means per column followed by different letters are significantly different (t-test with Bonferroni probability adjustment, Po0:05). c All larvae died within 24 h. b

time was recorded at 301C. As in the previous experiment on egg development, no larval development was observed at 37.51C and 401C. Overall, the initial density had no significant effect on larval development. However, considering each temperature separately, significant effects of larval density on development times were recorded at 201C (F ¼ 6:53; df ¼ 5; P ¼ 0:0001) and at 351C (F ¼ 4:58; df ¼ 3; P ¼ 0:013). The developmental period is prolonged in both the cases when larval density increases, suggesting the existence of competition for feeding sites. The number of emerged adults was not related to the different temperature regimes but reflects the varying initial larval densities in the respective experimental units at the beginning of the experiment. This suggests that temperature had no significant effect on larval survival of E. decipiens.

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Fig. 1. Development time (mean7SE) of Empoasca decipiens on leaves of different host plants at 301C. Total number of emerging adult leafhoppers on broad beans=48, cucumbers=40, sweet pepper=54, tomatoes=55, and aubergines=27. Bars with different letters are significantly different at Po0:05:

3.3. Experiment III For all host plant species, significant effects of the experimental units on the larval development time were observed (F ¼ 13:87; df ¼ 9; P ¼ 0:0001). The larval development time, ranging from 10.2 days in broad beans to 12.5 days in aubergines, varied significantly with host plant species (Fig. 1). 3.4. Experiment IV On all the observation dates, older cucumber plants were significantly preferred by adult E. decipiens for oviposition, compared to younger cucumber plants (Fig. 2). Moreover, in only one case the emerged larvae were recorded from younger cucumber plants (Table 3).

Fig. 2. Mean number (7SE) of Empoasca decipiens adults per observation date on three (‘young’) and five (‘old’) weeks old cucumber plants. Leafhopper numbers significantly differed between ‘young’ and ‘old’ cucumber plants for every observation date.

4. Discussion The egg development time in E. decipiens was strongly influenced by temperature. Although we observed the shortest development time at X281C, the data on total number of larvae emerging strongly suggest that optimum egg development for E. decipiens is around 241C. However, no data on egg mortality was recorded, as E. decipiens females lay their eggs in the plant tissue (Mu. ller, 1956), and they are visually difficult to detect (Poos, 1932; Scho. pke, 1996). Yet the high variability in the total number of emerged larvae in the different temperature treatments indicate high egg mortality at temperatures below and above 241C, respectively. For a given temperature that was tested, all plants were kept in

the same cage. Although it was impossible to record leafhopper densities in the mass rearing cage, in the course of the experiments initial density of the adults there remained very stable. No detailed laboratory study on the bionomics of E. decipiens as affected by various temperature regimes has been carried out. In a field study in Egypt, Habib et al. (1972) recorded a slightly shorter egg development in E. decipiens on broad beans. However, for the range between 201C and 241C our findings correspond with laboratory data of E. vitis (Go. the) (Homoptera: Cicadellidae) (Cerutti et al., 1990), a closely related leafhopper species and polyphagous pest of vine, sugar beets, cotton, tea and various

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Table 3 Total number of emerged Empoasca decipiens larvae on older, i.e., five weeks at the onset of the experiment, and younger, i.e., three weeks at the onset of the experiment, cucumber plants Replicate

Total no. of larvae on older plants

Total no. of larvae on younger plants

1 2 3 4 5

20 42 6 28 30

0 0 0 3 0

solanacaeous crops (Mu. ller, 1956). Likewise, larval development time of E. decipiens on broad beans was significantly influenced by temperature. As in the experiments on egg developmental time, shortest development time for larvae was recorded at temperatures X281C, supporting the hypothesis that E. decipiens most likely originates from southern Europe, North Africa, and/or the Middle East and central Asia (Ossiannilsson, 1981). Moreover, our laboratory results corroborate field observations on E. decipiens development on broad beans in Egypt (Habib et al., 1972). Host plant species had a significant effect on the larval development time in E. decipiens. The shortest development time was recorded on broad beans, supporting earlier findings of Koblet-Gu. nthardt (1975) on the superior quality of broad beans as host plants for E. decipiens. However, another reason for the shortest development time recorded on broad beans could be the fact that our leafhopper strain was mass reared on V. faba. The significantly longest larval development time was observed on aubergines. The lower leaf side of aubergines is very pubescent, affecting the mobility of herbivores. For instance, the white fly Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) prefers non-hairy to hairy aubergine varieties (Mohanty et al., 1996). Moreover, only on aubergines we observed E. decipiens larvae frequently feeding on the upper sides of the leaves. In general, leafhopper larvae prefer the lower side for feeding (DeLong, 1971). Hosny and ElDessouki (1968) observed reduced infestations by leafhoppers on pubescent compared to glabrous cotton varieties. Broad bean and sweet pepper leaves are not pubescent, and the tested cucumber variety ‘Tyria’ is only moderately pubescent. The significantly longer larval development time on tomatoes compared to broad beans, sweet pepper and cucumber was most likely also due to the pubescent nature of the leaf surface. Moreover, tomatoes posses hairy glands on leaves and stems, possibly affecting the feeding of E. decipiens larvae. In addition, tomato plants contain the alkaloid tomatine, toxic for many herbivores, e.g. the polyphagous noctuid Helicoverpa zea Boddie

(Lepidoptera: Noctuidae) (Stamp et al., 1996). In a field study, Habib et al. (1972) observed a prolonged larval development time in E. decipiens on tomatoes compared to broad beans. In cucumbers, adult E. decipiens significantly preferred older to younger plants. Moreover, hardly any larval development was recorded on young cucumber plants. These results suggest, that in addition to the host plant species, the age of the host plant determines selection in E. decipiens. In the field, Empoasca spp. preferentially feed on older cotton plants (Hosny and El-Dessouki, 1968). In E. vitis the physiological conditions of the host plant, in particular the high content of soluble N-compounds in older plants, largely determine the host plant selection of this polyphagous leafhopper species (Nuorteva, 1952). Our laboratory data indicate that E. decipiens can develop well at temperatures common in central European greenhouses. Moreover, economically important vegetable crops like cucumbers and sweet pepper are excellent host plants for this leafhopper species. The recent spectacular outbreaks of E. decipiens in southern Germany (Schmidt and Rupp, 1997) and in the UK and the Netherlands (Helyer and Talbaghi, 1994) clearly highlight the pest potential of the leafhopper. In the ongoing studies, we are trying to develop an integrated pest management strategy, focussing particularly on biological control.

Acknowledgements The authors would like to thank Sabine Schamlott for technical assistance during the course of the experiments, and Mathias Otto and Patrick Helling for their helpful comments on earlier versions of the manuscript.

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