Pandora Delphacis (Entomophthorales

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Pandora delphacis (Entomophthorales: Entomophthoraceae) infection aﬀects the fecundity and population dynamics of Myzus persicae (Homoptera: Aphididae) at varying regimes of temperature and relative humidity in the laboratory

Jun-Huan Xu and Ming-Guang Feng*

Research Institute of Microbiology, College of Life Science, Zhejiang University, Hangzhou 310029, PR China

Received 7 December 2001; accepted 11 March 2002

Abstract

Apterae of the green peach aphid, Myzus persicae, on detached cabbage leaves were exposed to a Pandora delphacis conidial shower (112 conidia/mm2) and were then observed for reproduction and mycosis development at different temperatures (10–30 °C) and relative humidities (74–100% RH). Based on daily counts of nymphs and adults (living and mycosed) at each regime, the fecundity of apterae exposed to P. delphacis was greatly reduced with the net reproductive rate (R0) and the innate capacity for increase (rm) declining at all temperature and humidity regimes compared to those of unexposed aphids. Moreover, the rm estimates for batches of exposed aphids were significantly different among the temperature regimes, being parabolically related to temperature, with the largest rm being obtained at 20–25 °C. However, there was no significant effect of RH on rm. During a 30-day period of observation, the development of P. delphacis mycosis greatly suppressed the increase of aphid populations relative to the control and the fungus played a more important role in the control of aphids at the regimes of 20–30 °C and P 95% RH than at the others. The cumulative mortality caused by P. delphacis was P 80% at all humidity regimes at 30 °C and at 74%, 95%, and 100% RH at 25 °C. However, the mortality was <50% at 10, 15, and 20 °C for all humidity regimes, except for 100% RH. The results suggest that P. delphacis has the potential as a useful fungal agent for control of aphids. Ó 2002 Elsevier Science (USA). All rights reserved.

Keywords: Pandora delphacis; Myzus persicae; Fecundity; Temperature; Relative humidity; Microbial control

1. Introduction been identified as potential microbial control agents of aphid pests (Feng, 1997; Feng et al., 1998). The green peach aphid, Myzus persicae Sulzer, is Pandora delphacis (Hori) Humber is an important globally an economically important pest, infesting more pathogen of plant and leafhoppers (Feng et al., 1996; than 40 families of plants (Blackman and Eastop, 1984). Melissa and James, 1987). This fungus has not been In China, this pest species mainly infests cruciferous found causing an epizootic in aphid populations under crops along the middle and lower reaches of the field conditions though its infectivity to an aphid host Changjiang River (Liu, 1991). There are several en- was first observed on Aphis gossypii Glover in a labo- tomophthoralean fungi including Pandora and Zooph- ratory bioassay (Shimazu, 1977). Xu and Feng (2000, thora species that play an important role in natural 2001a,b) showed that P. delphacis can kill M. persicae control of aphid populations (Feng et al., 1991). In more rapidly than P. neoaphidis (Remandiere and southern China, entomophthoralean fungi frequently Hennebert) Humber, a well-known aphid pathogen. cause epizootics in M. persicae populations and have This stimulated our interest in the effect of P. delphacis on M. persicae fecundity. Previous reports demonstrate that the development, survival, and reproduction of * Corresponding author. Fax: +86-571-86971129. M. persicae are influenced by various factors such as E-mail address: [email protected] (M.-G. Feng). temperature, parasitoids, and pathogens, which ultimately

86 J.-H. Xu, M.-G. Feng / Biological Control 25 (2002) 85–91 affect the fecundity of aphids (Liu, 1991; Liu et al., ball of sterile cotton saturated with Hoagland–Snyder 1999). However, little is known about the degree to nutrient solution (Adams and van Emden, 1972). Leaves which P. delphacis, and other entomophthoralean fungi, so treated could support aphids for about 30 days. affect the fecundity of aphids, despite numerous reports on the collapse of aphid populations caused by fungal 2.3. Exposure of aphids to conidial showers diseases in the field (e.g., Feng et al., 1991; Pickering et al., 1989). Such information may help us predict the Detached leaves with 7-day-old nymphs/adults were ability of a fungal pathogen to suppress the growth of placed in 150-mm petri dishes lined with moistened filter aphid population. In this study, we assessed the innate paper. A sporulating mycelial mat was inverted 5 cm capacity for increase and the dynamics of experimental above the dish containing aphids on one or two leaves. M. persicae populations exposed to P. delphacis at dif- The aphids were exposed to a shower of conidia dis- ferent regimes of temperature and relative humidity charged from the mycelial mat for 1 h by rotating the (RH) to evaluate its potential for control of aphids in inverted dish 90° every 15 min. One 20-mm glass cov- the field. erslip was placed at the center of each aphid dish to collect discharged conidia. After exposure, the conidial concentrations that the aphids received were determined 2. Materials and methods using counts of conidia from five fields of the coverslip (0.785 mm2/field) under a microscope at 200 magnifi- 2.1. Preparation of inocula cation. The exposure resulted in a concentration of 112 22:8 conidia/mm2, which resulted in high M. per- An isolate of P. delphacis, F98401, was derived from a sicae mortality (Xu and Feng, 2000). cadaver of the white-backed planthopper, Sogatella fur- cifera Horvath, on rice plants in Hangzhou, Zhejiang 2.4. Arrangement of treatments Province in October 1998. It was maintained on SEMA (80% Sabouraud’s dextrose agar, 11.5% fresh milk, and Groups of three apterae after exposure were placed 8.5% egg yolk in 1 L of distilled water) at 10 °C and a onto a detached leaf where they were allowed to freely photoperiod of 12L:12D and subcultured every 3 months. produce progeny for initiation of a new colony for the Preparation of P. delphacis inocula (Feng et al., 1998; Xu development of P. delphacis infection. Each treatment and Feng, 2000) was initiated by growing the isolate on consisted of eight replicates of 3-apterae colony and the SEMA at 25 °C for 7 days. The resulting fungal colony aphid colony was maintained at one of the 25 different was macerated with a needle and was inoculated into a temperature and RH combinations on detached leaves in 100-ml flask containing 30-ml Sabouraud’s dextrose meshed petri dishes. Unexposed aphids were included as broth [SDB: 1% peptone, 1% yeast extract, and 4% glu- controls. Live and dead aphids (including progeny) were cose plus 20 lg/ml PSN (penicillin, streptomycin, and recorded daily for 30 days. RH was controlled using an neomycin) antibiotic mixture (Gibco BRL, Grand Island, air pump, three rubber tube-collected containers, and a NY)]. The liquid culture was shaken in the dark at Plexiglas experimental chamber placed in a growth in- 28 1 °C for 24 h (150 rpm) and then was poured into a cubator that controlled light and temperature, as de- 200-ml flask containing 80 ml SDB for another 48 h at the scribed by Feng et al. (1999a). The RH was controlled same regime. Subsequently, the liquid culture was poured using glycerin solutions that yielded 74%, 85%, 90%, in 10-ml aliquots onto 90-mm petri dishes containing 2% 95%, and 100% RH at concentrations of 59.8%, 40.0%, agar only. Excessive liquid medium was removed using 31.4%, 18.8%, and 0%, respectively, in the Plexiglas sterile filter paper and mycelial mats on the dishes were chamber, regardless of temperature (Doberski, 1981). ready for use when the fungus uniformly sporulated. 2.5. Data analysis 2.2. Source of aphids The counts of aphids (including living and dead An experimental population of M. persicae was es- adults and progeny) in each replicate of the treatments tablished from field-collected aphids and maintained on were made daily. The cumulative mortality was calcu- cabbage plants, Brassica olerracea L. (cv. Jingfeng 1), at lated by dividing the total aphid counts (including living 20 °C and a photoperiod of 12L:12D. Three healthy and dead aphids) by the cumulative dead ones. The apterae were selected from the population and were al- parameters R0 (net reproductive rate), T (generation lowed to produce nymphs on detached cabbage leaves for time), rm (innate capacity for increase), and k (finite rate 2 days before removing them and leaving the nymphs on of increase) were estimated by the following equations the leaves. For longer maintenance, the petiole of each based on the life tables (Liu, 1991): leaf was treated with 1000 ppm a-naphthyl-acetic-acid to X initiate adventitious roots before being wrapped with a R0 ¼ lxmx; ð1Þ ______中国科技论文在线 www.paper.edu.cn

J.-H. Xu, M.-G. Feng / Biological Control 25 (2002) 85–91 87

ln R than those produced by exposed aphids (day 3, r ¼ 0 ; ð2Þ m T t ¼ 3:51; df ¼ 49; P < 0:01; day 7, t ¼ 6:33; df ¼ 49; P P < 0:01). This was conspicuous at 25 and 30 °Conday l m x 3, or 20 and 25 °C on day 7 (Fig. 1). The mean number T ¼ x x ; ð3Þ R0 of progenies produced by the exposed aphids differed significantly among the regimes of temperature (day 3, X1 rmx F ¼ 85:37; df1 ¼ 4; P < 0:01; day 7, F ¼ 48:96; df1 ¼ 4; e lxmx ¼ 1: ð4Þ x¼0 P < 0:01) and humidity (day 3, F ¼ 9:60; df2 ¼ 5; P < 0:01; day 7, F ¼ 21:52; df2 ¼ 5; P < 0:01) based on The aphid counts (live and dead) and cumulative the analysis of variance. Reproduction was greatest at mortality in the controls were averaged from all humidity 25 and 30 °C on day 3 after exposure and at 20 and 25 °C regimes at a given temperature. The analysis of variance on day 7. On the other hand, more progenies were for aphid counts was conducted using the software of produced by aphids at 74–90% RH on day 7 after ex- DPS data processing system (Tang and Feng, 1997). posure than at P 95% RH (Fig. 1). Apparently, mod- erate humidity and temperature (20–25 °C) conditions were most conducive to producing progeny, whereas the 3. Results combinations of high humidity and high or low temperature were less favorable. 3.1. Effect on fecundity and innate capacity for increase Estimates of the net reproduction rate (R0) and innate capacity for increase (rm)ofM. persicae exposed to The apterae exposed to conidial showers were ob- P. delphacis are given in Table 1. Both R0 (t ¼ 7:02; df ¼ served producing nymphs during the incubation period 24; P < 0:01) and rm (t ¼ 4:13; df ¼ 24; P < 0:01) were for P. delphacis (Xu and Feng, 2000). Progenies pro- significantly lower in the colonies of the exposed aphids duced by aphids in the control were significantly more than the unexposed ones, especially at 15–25 °C. In

Table 1 The estimates of net reproduction rate (R0) and innate capacity for increase (rm) for M. persicae exposed to P. delphacis at various temperatures and RH

RH Temp R0 rm (%) (°C) Treated CK Treated CK 74 10 56.3 61.2 0.1 0.1 15 18.2 45.7 0.2 0.2 20 24.0 29.7 0.3 0.3 25 5.9 17.3 0.3 0.4 30 1.1 18.7 0.0 0.3

85 10 30.7 37.7 0.1 0.1 15 16.7 32.7 0.2 0.2 20 17.2 47.4 0.2 0.3 25 8.8 22.3 0.3 0.3 30 2.4 11.4 0.1 0.4

90 10 23.8 39.5 0.1 0.1 15 13.1 22.3 0.1 0.2 20 21.7 30.0 0.3 0.3 25 12.9 22.1 0.3 0.3 30 1.8 15.4 0.1 0.3 95 10 29.0 30.4 0.1 0.1 15 14.2 18.9 0.1 0.2 20 15.5 28.0 0.2 0.3 25 10.9 39.7 0.3 0.5 30 0.1 13.7 <0 0.3 100 10 15.3 54.3 0.1 0.1 15 14.4 14.2 0.1 0.1 20 14.6 28.3 0.2 0.3 Fig. 1. Reproduction of M. persicae apterae at diﬀerent regimes of 25 4.4 16.7 0.3 0.4 temperature and RH after exposure to P. delphacis conidial shower at 30 )0.4 5.4 0.3 3 (A) and 7 days (B) post-treatment. ______中国科技论文在线 www.paper.edu.cn

88 J.-H. Xu, M.-G. Feng / Biological Control 25 (2002) 85–91 addition, the rm estimates were significantly different exposed aphids were significantly smaller than those for among temperatures tested for both exposed the unexposed aphids at 15 °C(t ¼ 3:83; df ¼ 4; P < (F ¼ 85:77; df ¼ 4; P < 0:01) and unexposed aphids 0:05), 20 °C(t ¼ 6:08; df ¼ 4; P < 0:01), 25 °C(t ¼ 3:54; (F ¼ 106:94; df ¼ 4; P < 0:01), showing a parabolic df ¼ 4; P < 0:05), and 30 °C(t ¼ 6:52; df ¼ 4; P < 0:01), curve with a peak at 25 °C. However, no significant effect respectively, but little difference was detected at 10 °C of humidity on the rm was detected in either exposed (t ¼ 1:37; df ¼ 4; P ¼ 0:24). However, there was no sig- (F ¼ 0:74; df ¼ 4; P ¼ 0:58) or unexposed aphids nificant difference in rm value between the exposed and (F ¼ 0:79; df ¼ 4; P ¼ 0:57). unexposed aphids at 74% (t ¼ 1:84; df ¼ 4; P ¼ 0:16), Although the R0 estimates for exposed aphids were 85% (t ¼ 2:14; df ¼ 4; P ¼ 0:12), 95% (t ¼ 2:039; df ¼ 4; consistently lower than those for unexposed aphids at all P ¼ 0:13), and 100% RH (t ¼ 1:91; df ¼ 4; P ¼ 0:15). temperature regimes, the rm values were significantly Significant differences in rm value occurred only at 90% lower only at higher temperatures. The rm values for the RH (t ¼ 3:87; df ¼ 4; P < 0:05). These results indicate

Fig. 2. The dynamics of M. persicae populations contaminated with P. delphacis at diﬀerent regimes of temperature and RH. The observations for control at diﬀerent RH regimes were pooled at each given temperature. ______中国科技论文在线 www.paper.edu.cn

J.-H. Xu, M.-G. Feng / Biological Control 25 (2002) 85–91 89 that the fecundity of M. persicae was largely reduced by populations increased very slowly at 10–15 °C. At 20– P. delphacis infection, especially at higher temperatures. 30 °C, however, the populations increased rapidly in the first few days. The rate for the decrease of the popula- 3.2. Population dynamics tions after the peak level depended on both temperature and humidity. Rapid decrease occurred at the regimes of Aphid colonies contaminated with P. delphacis were high temperature and high humidity. significantly smaller than those of the controls The cumulative mortality estimates for the aphid col- (t ¼ 9:70; df ¼ 1339; P < 0:01) (Fig. 2). Moreover, the onies contaminated with P. delphacis were significantly size of the contaminated colonies varied significantly greater (t ¼ 19:99; df ¼ 1339; P < 0:01) than those for among the temperatures (F ¼ 1415:59; df ¼ 4; P <0:01), the uncontaminated colonies (Fig. 3). In the contami- RH (F ¼ 168:44; df ¼ 4; P < 0:01), and their combina- nated colonies, the mortality attributed to P. delphacis tions (interaction, F ¼ 74:08; df ¼ 16; P < 0:01). The infection, in most cases, tended to increase as the

Fig. 3. The cumulative mortality in M. persicae colonies after being contaminated with P. delphacis at diﬀerent regimes of temperature and RH. The observations for control at diﬀerent RH regimes were pooled at each given temperature. ______中国科技论文在线 www.paper.edu.cn

90 J.-H. Xu, M.-G. Feng / Biological Control 25 (2002) 85–91 temperature and humidity increased within the ranges of Russian wheat aphid Diuraphis noxia Kurdyumov 15–30 °C and 74–100% RH tested. In the last few days of (Wang and Knudsen, 1993), and M. persicae (Liu et al., the experiment, the cumulative mortality increased sig- 1999). However, the reduction of the fecundity of M. nificantly at 25 and 30 °C relative to 10 and 15 °C. persicae and rm by B. bassiana was much less than that by P. delphacis in our study. There are several reasons that may explain this phenomenon. Liu et al. (1999) 4. Discussion reported that more virulent B. bassiana strains had a greater effect on the fecundity and rm of aphids than less Fecundity is an important parameter for insect pop- virulent strains. P. delphacis invades aphids very fast. It ulations and is usually influenced by a variety of factors, penetrates into the aphid cuticle within 4–6 h and causes including temperature (Liu, 1991; Wyatt and Brown, a peak mortality 3–4 days after inoculation compared 1977), pesticides (Rumpf et al., 1998), food quality with P. neoaphidis that has a peak mortality occurring (Nagata et al., 1998; Spieles and Horn, 1998), and par- 4–5 days after inoculation (Feng et al., 1999b; Xu and asitoids (Liu, 1990). Temperature also affects insect de- Feng, 2000) and B. bassiana that has a peak mortality of velopmental rate, life span, and survivorship, and 5–6 days after inoculation (Feng et al., 1996). Addi- fecundity (Liu, 1991; Wyatt and Brown, 1977). tionally, P. delphacis forms protoplasts or hyphal bodies Liu (1991) reported that the effect of temperature on in the host hemocoel and kills its hosts by exhausting the the innate capacity for increase of M. persicae was a host nutrition, enhancing its effect on aphid fecundity parabolic response curve, with maximum rm occurring and rm. The reduced rm for M. persicae in this study may at 20–22 °C, similar to the results obtained in the present be attributed to the rapid invasion of P. delphacis. Thus, study. However, the effect of temperature on the rm of this fungal pathogen can be considered as a potential M. persicae contaminated with P. delphacis did not microbial control agent for M. persicae. show the same type of response. The optimal temperatures for P. delphacis growth in vitro and for M. persicae development are 20–25 C (Xu and Feng, 1998) and 20– ° Acknowledgments 22 °C (Liu, 1991), respectively. At 20–25 °C, the aphid propagates rapidly, but the fungus also grows fast and This work was supported by the ‘Cheung Kong infects aphids quickly. As a result, the fecundity of the Scholars Programme,’ the National Natural Science aphids infected by P. delphacis was reduced compared to Foundation of China (Grant Nos. 30070514 and the uncontaminated aphid population. The r values m 30070025), and the Ministry of Science and Technology and population growth differed greatly between the of China (G2000016208-04). We thank the anonymous contaminated and uncontaminated colonies at optimal reviewers for their critical comments and grammatical temperatures than at other temperatures (Table 1). For suggestions on the earlier draft of this paper. instance, the rm estimates for the aphids exposed to P. delphacis were significantly lower than those for the controls at 20–25 °C, whereas no significant difference occurred at 10 °C. 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