Apolygus Lucorum: Implications for Laboratory Rearing

Bulletin of Entomological Research, Page 1 of 7 doi:10.1017/S0007485318000883 © Cambridge University Press 2018

Host-plant switching promotes the population growth of Apolygus lucorum: implications for laboratory rearing

H.-S. Pan1,2, B. Liu2 and Y.-H. Lu2* 1Scientific Observing and Experimental Station of Crop Pests in Korla, Ministry of Agriculture, Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China: 2State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Abstract

The mirid bug Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae) is a major pest on cotton, fruit trees and other crops in China. A. lucorum adults often switch host plants in the agro-ecosystem, and such host-plant switching may promote more rapid population growth of A. lucorum. Here, we examined the population fitness of A. lucorum on different combinations of two plant foods [fresh maize kernels (Zea mays) and green bean pods (Phaseolus vulgaris)] in the laboratory when reared either individually or in groups. Our results suggested that, compared with A. lucorum nymphs reared on green bean alone, the survival rate, developmental rate, and adult weight significantly increased when they were fed fresh maize kernels for both rearing methods. Both two-plant combinations of foods (i.e., maize as nymphal food then green bean as adult food, and green bean as nymphal food then maize as adult food) generally prolonged adult longevity, improved female fecundity, and higher egg hatching rate compared with maize or green bean as food for both nymphs and adults. The combination of nymphs with maize and adults with green bean showed the highest population growth rate for both individual and group rearing of mirid bugs. Host food switching greatly promoted the population growth of A. lucorum, and suggests a new diet for laboratory rearing of A. lucorum.

Keywords: Miridae, multiple host use, population fitness, mass rearing, Zea mays, Phaseolus vulgaris

(Accepted 30 August 2018)

Introduction adoption of Bt (Bacillus thuringiensis) cotton and the increased planting of fruit trees, population levels of A. lucorum and The mirid bug Apolygus lucorum (Meyer-Dür) is an import- other mirid bugs have greatly increased in China (Lu et al., ant polyphagous pest, broadly distributed in Japan, Russia, 2010a), and A. lucorum has become the dominant pest on Egypt, Algeria, Europe and North America (Miyata, 1994; cotton and many other crops (e.g., alfalfa, Chinese date, Watanabe, 1995; Zhang & Zhao, 1996; Watanabe et al., 1997; grape, apple, pear, peach and tea) (Lu et al., 2010b; Lu & Wu, Lee et al., 2002). It is found in most Chinese provinces except 2012). Hainan and Tibet (Lu & Wu, 2008), and is most common Both nymphs and adults of A. lucorum prefer feeding on in the cotton-planting regions of the Yangtze and Yellow tender plant parts, including leaves, flower buds and fruits Rivers (Lu et al., 2008a). In recent years, with the wide (bolls). Damaged feeding sites cease to develop, while the sur- rounding tissues continued to grow rapidly resulting in ab- scission of flower buds and fruits, and fruit deformation (Lu *Author for correspondence & Wu, 2008). The salivary enzymes of A. lucorum play a greater Phone/Fax: +86 10 62815929 role in causing damage than mechanical injury due to stylet E-mail: [email protected] probing (Zhang et al., 2013). Polygalacturonase (PG) is an

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important group of salivary enzymes in A. lucorum, among towel (Lu et al., 2008b). We then used a pesticide residue de- which two PG genes (PG3-4 and PG3-5) are highly expressed tector (RP-420, Sykam Scientific instrument co., LTD, Beijing, (Zhang et al., 2015). Both play key roles in the injury caused by China) to detect any residual pesticides, and only used A. lucorum nymphs and adults on host plants (Zhang et al., residue-free pods (each divided into 3 cm length) for the trials. 2017). These injuries greatly reduce the yield and quality of Sweet maize cobs were also purchased from a local supermar- cotton, causing serious economic loss of 20–30% during ket, but because of the limited use of pesticides on maize dur- years of high infestation (Lu & Wu, 2011), and also greatly re- ing its later growth stages, we just removed the bract and duce the yield and quality of several fruits (Li et al., 2012). filament from them. The previous detection showed that Apolygus lucorum can feed on more than 200 species of host maize kernels were residue-free. Then, we used either maize plants (Jiang et al., 2015;Panet al., 2015). Its adults have a great kernels or slices (groups of kernels from slices along the cob, flight and dispersal capacities (Lu et al., 2007; Song et al., 2012; 2 cm thickness) in the experiments. Fu et al., 2014), and they often switch food plants in the local agro-ecosystem (Pan et al., 2013). One study found that female Individual rearing A. lucorum adults significantly preferred to feed and lay more eggs on flowering individuals of three plant species To compare the performance of A. lucorum nymphs be- (Gossypium hirsutum L., Impatiens balsamina L. and Ricinus com- tween maize and green bean, newly emerged (i.e., first instar) munis L.), and their offspring performed significantly better on nymphs from the laboratory colony were individually placed these plants in flower (Dong et al., 2013). Moreover, Wang et al. into glass vials (3 cm high, 3 cm diam.) covered with a nylon (2017) developed a molecular gut-content analysis for A. lucor- screen (120 mesh). Each glass vial contained one sweet maize um, which demonstrated the frequent movement of A. lucorum kernel or one 3-cm green bean pod for food and a curled strip adults among host plants [i.e., cotton and Vigna radiata (L.) of paper (5 cm × 1 cm) to increase the activity space of nymphs Wilczek.]. Host-plant switching has been found to improve (Lu et al., 2008b). Experiments were conducted at 25 °C in en- the population growth of a number of phytophagous insect vironmental growth chambers (RXZ-500C, Ningbo Jiangnan pests (Bernays et al., 1992, 1994; Modder & Tamu, 1996; Instrument Factory, Ningbo, China) with a photoperiod of Hägele & Rowell-Rahier, 1999). For example, the fecundity 14:10 h (L:D) and 65% RH. Plant foods were changed daily. and host adaptability of adults of the whitefly Bemisia tabaci Nymphal development and mortality were recorded daily (Gennadius) significantly increased after being transferred until nymphs molted to adults or died. The female ratio and from the less-preferred host (pepper, Capsicum annuum L.) to weight of emerging adults were also determined. The trial the preferred host (tomato, Lycopersicon esculentum Mill.) was replicated four times for each plant food, and 28–30 (Zhou et al., 2011). Furthermore, the aphid Myzus persicae nymphs were assayed for each replicate. Moreover, we reared (Sulzer) fed on tobacco showed a higher reproductive capacity 800 newly emerged nymphs individually on maize cobs or when transferred to radish (Zhu et al., 2012). Lygus lineolaris green beans according to the same procedure as above for (Palisot de Beauvois) showed different rates of reproduction the following adult trials. on different hosts, suggesting that host switching can consid- To measure the effects of maize or green bean on the lon- erably increase the population growth and survival of species gevity and fecundity of adult bugs, we tested four plant (Stewart & Gaylor, 1994). food combinations: (1) MM, in which both nymphs and adults Lu et al.(2008b) developed a method to rear the nymphs fed on maize; (2) MG, in which nymphs fed on maize and and adults of A. lucorum using only fresh green bean pods. adults switched to feed on green bean; (3) GM, in which Maize is one of the preferred host plants of A. lucorum, and nymphs fed on green bean and adults switched to feed on maize cobs have generally low pesticide residues and are an- maize; and (4) GG in which both nymphs and adults fed on nually available in the market. Hence, we examined the popu- green bean. Newly emerged adults that had fed on either lation fitness of A. lucorum nymphs and adults on one or two maize or green beans were separately paired, and each pair kinds of plant foods [fresh maize kernels (Zea mays L.) and was placed in a glass vial (3 cm high, 3 cm diam.) covered green bean pods (Phaseolus vulgaris L.)] by bugs reared either with a nylon screen (120 mesh). Either one sweet maize kernel individually or in groups. The results of this study would con- or one 3-cm green bean pod was provided as both food and tribute to the development of improved rearing techniques for oviposition substrate, and a 5 cm × 1 cm paper strip was A. lucorum. added to increase the activity space of adults. Experiments were conducted in environmental growth chambers at 25 °C with a photoperiod of 14:10 h (L:D) and 65% RH. Plant Materials and methods foods were changed daily and then inspected for eggs. Adult mortality and fecundity (i.e., the number of eggs laid Insects and plants by a female) were recorded daily. The trial was replicated A laboratory colony of A. lucorum was established with four times for each plant food combination, and a total of 20 500–800 nymphs and adults collected from cotton fields at mated pairs were assayed for each replicate. the Langfang Experimental Station (39.53°N, 116.70°E) of the In addition, we also evaluated the influence of nymphal Chinese Academy of Agricultural Sciences in Hebei Province, and adult food sources on the hatching rate of A. lucorum China. The colony was reared on green bean pods and supplied eggs, which was done by using filter paper as oviposition sub- with a cotton ball soaked with a 10% sucrose solution, as strate to eliminate the influence of plant materials on the hatch- described by Lu et al.(2008b). Insects were held at 25–28°C, ing rate (Chen et al., 2012). For each of four plant food 60–70% RH and a 14:10 h L:D photoperiod. combinations (MM, MG, GM and GG), newly-emerged adults Fresh pods of green bean purchased from a local market that had fed on maize or green beans were separately paired in were soaked for 10 min in 0.5% NaClO, wiped down to re- a glass vial, with a total of 20 pairs for each plant food combin- move any residual pesticides from their surface, and then ation, and the rearing methods and environmental conditions rinsed several more times in water before being dried with a were the same as above mentioned. During peak oviposition

stage (10–15 day-old adults) (Dong et al., 2012), we replaced all Results plant foods in the vials with four layers of wrinkled moist filter Individual rearing paper as an oviposition substrate at 20:00 pm, because >90% eggs were laid at night (Dong et al., 2012). After 12 h, the Compared with mirid bugs reared on green bean, the sur- eggs laid in filter paper were counted under microscope, vival rate of A. lucorum nymphs reared on maize was signifi- and about 100 eggs were transferred with the filter paper cantly higher (χ2 = 6.65, df =1,P = 0.0099), the developmental into a petri dish and held at 25 °C, 65% RH and a 14:10 h L: duration was shorter (t = 4.31, df =6, P = 0.0050), and adult D photoperiod to hatch, as described by Chen et al.(2012). weight was greater (t = 9.35, df =6,P < 0.0001) (table 1). In con- Four batches of eggs were assayed for each plant food combin- trast, female ratio [Female/(Female + Male)] was not signifi- ation. Egg hatch was recorded daily and each newly emerged cantly different when bugs reared on maize vs. green bean nymph was removed. (t = 1.06, df =6,P = 0.3311) (table 1). For adults, male longevity of A. lucorum on the plant food combination GM was significantly higher than on MM Group rearing (F = 3.95, df = 3, 12, P = 0.0358) (table 2), while female longevity on plant food combinations MG and GG was significantly We repeated the above experiment using a group rearing greater than on MM or GM (F = 43.87, df = 3, 12, P < 0.0001) process, in which 100 newly emerged nymphs were placed (table 2). Meanwhile, female fecundity on plant food combin- into rearing container and held at 25–28 °C, 60–70% RH and ation GM and GG was higher than on MM and MG (F = 17.49, a 14:10 h L:D photoperiod. The lid of the container was cov- df = 3, 12, P < 0.0001) (table 2). In addition, the hatch rate of ered with a nylon screen (120 mesh) for ventilation, and A. lucorum eggs on MG was significantly higher than on the some curled paper strips (5 cm × 1 cm) were added to increase other three plant food combinations (F = 33.90, df = 3, 12, the activity space of nymphs. Either four sweet maize slices or P < 0.0001) (table 2). The population growth rate of A. lucorum four green bean pods were provided as food, and plant foods on plant food combination MG was significantly higher than were changed daily. We used four containers for each plant on GG, but was similar to that on MM or GM (F = 3.90, df =3, food to examine nymphal survival and development, female 12, P = 0.0371) (fig. 1); meanwhile a significant difference in ratio and adult weight. Moreover, we reared 1200 newly the population growth rate was found between GM and GG emerged nymphs in groups on maize cobs or green beans ac- (t = 3.03, df =6, P = 0.0232), but no significant difference was cording to the same procedure as above for the next adult found between MM and MG (P > 0.05) (fig. 1). trials. From these containers, newly emerged adults fed on maize or green bean were separately paired (30 pairs per rearing container) and were provided with either four maize slices or four green bean pods as food and oviposition substrate, and some 5 cm × 1 cm paper strips were added to increase the activity Group rearing space of adults. Four plant food combinations (MM, MG, Under conditions of group rearing, the survival rate of A. GM and GG) were tested, and plant foods were changed lucorum nymphs was also significantly higher when they fed daily and inspected for eggs. Adult mortality and fecundity on maize than on green bean (χ2 = 3.47, df =1, P = 0.0134) were recorded daily, and the trial was replicated four times (table 1), and the weight of adults fed on maize was likewise for each plant food combination. higher than on green bean (t = 8.23, df =6,P = 0.0002), whereas At the same time, the eggs were also collected from each no significant difference was found in developmental duration plant food combination (MM, MG, GM and GG) using and female ratio when insects reared on maize vs. green beans wrinkled moist filter paper, and egg hatch was recorded (all P > 0.05) (table 1). daily using the same method as described above in the experi- Male longevity of A. lucorum adults on plant food com- ment of individual rearing. bination MM was significantly shorter than on MG, GM or GG (F = 37.05, df = 3, 12, P < 0.0001), and there were no significant differences among the last three mentioned plant food Statistical analysis combinations (P > 0.05) (table 2). Female longevity on plant Nymphal survival rates and female adult ratio [Female/ food combination MG was significantly greater compared (Female + Male)] for A. lucorum offspring were compared be- with other plant food combinations (F = 24.27, df = 3, 12, tween maize and green bean using a χ2 goodness-of-fit test P < 0.0001) (table 2), while female fecundity on plant food (PROC FREQ), and percentage data were arcsine transformed combinations MG and GM was higher than on MM or GG before analysis. Paired t tests (PROC TTEST) were employed (F = 47.13, df = 3, 12, P < 0.0001), and there was no significant to compare the developmental duration of nymphs, adult difference between MG and GM (P > 0.05) (table 2). weight, female and male longevity, female fecundity [log10(n Moreover, the hatching rates of A. lucorum eggs on three + 1)-transformed] and hatch rate of A. lucorum eggs between plant food combinations (MM, MG, and GM) were significant- maize and green bean reared either individually or in a group. ly higher than on GG (F = 73.13, df = 3, 12, P < 0.0001), and Among the four plant food diets (MM, MG, GM and GG), dif- there were no significant differences among MM, MG, and ferences in female and male longevity, female fecundity [log10- GM (table 2). Meanwhile, the population growth rate of A. lu- (n + 1)-transformed], hatch rate of eggs, and population corum on plant food combination MG was higher than on the growth rate (i.e., nymphal survival rate×female adult ratio×fe- other three plant food combinations, and those of GM were male fecundity×egg hatching rate) of A. lucorum were further significantly higher than GG (F = 14.77, df = 3, 12, P = 0.0002) analyzed using one-way ANOVA (PROC ANOVA) followed (fig. 1). In addition, there were significant differences between by Tukey’s HSD. All statistical analyses were performed MM and MG (t = 3.14, df =6,P = 0.0201), and between GM and using SAS 9.13 software (SAS Institute, 2005). GG (t = 6.26, df =6,P = 0.0008) (fig. 1).

Table 1. Survival rate and developmental duration of Apolygus lucorum nymphs reared either individually or in groups on maize and green bean.

Nymph Adult Rearing methods Plant foods Survival rate (%) Developmental duration (d) Weight (mg) Female ratio (%) Individually Maize 89.45 ± 1.67 * 13.62 ± 0.04 4.48 ± 0.06 * 51.47 ± 1.16 ns Green bean 76.84 ± 2.14 14.24 ± 0.14 * 3.51 ± 0.08 48.86 ± 2.18 In groups Maize 75.75 ± 6.05 * 11.71 ± 0.11 3.66 ± 0.07 * 52.05 ± 0.72 ns Green bean 53.75 ± 1.93 11.84 ± 0.09 ns 3.01 ± 0.03 47.55 ± 4.85

Note: There were 115 nymphs and 112 nymphs reared individually on maize and green bean respectively, and 400 nymphs reared in groups on both maize and green bean. Data are presented as means ± SE. Asterisk (*) in the same column indicates that there is a significant difference between maize and green bean reared either individually or in groups (P < 0.05), and ns means no significant difference between them (P > 0.05).

Table 2. Longevity and female fecundity of Apolygus lucorum adults reared either individually or in groups on maize and green bean.

Adult Egg Rearing Nymphal Male longevity Female longevity Fecundity (eggs per methods foods Adult foods (d) (d) female) Hatching rate (%) Individually Maize Maize 29.25 ± 2.18 b 23.55 ± 0.49 c 89.77 ± 3.59 b 71.67 ± 2.81 (403) b Green bean 34.28 ± 0.91 ab 32.73 ± 0.62 a 96.13 ± 9.53 b 86.52 ± 2.94 (401) a Green bean Maize 36.15 ± 0.76 a 29.49 ± 0.69 b 152.44 ± 7.99 a 65.40 ± 3.71 (407) b Green bean 33.12 ± 1.57 ab 32.46 ± 0.75 a 128.41 ± 5.29 a 43.94 ± 2.58 (439) c In groups Maize Maize 12.95 ± 0.63 b 19.76 ± 0.57 c 44.61 ± 2.11 b 82.25 ± 1.03 (389) a Green bean 18.77 ± 0.09 a 25.61 ± 0.54 a 87.41 ± 2.87 a 78.87 ± 1.33 (391) a Green bean Maize 20.49 ± 0.68 a 23.13 ± 0.48 b 81.51 ± 3.16 a 79.95 ± 1.19 (498) a Green bean 19.98 ± 0.67 a 23.10 ± 0.31 b 50.46 ± 4.10 b 55.97 ± 2.00 (389) b

Note: There were 80 pairs and 120 pairs of adults reared either individually or in groups on maize and green bean, respectively. The data in the brackets ‘()’ indicate the number of tested eggs for each plant food combination. Data are presented as means ± SE. Means in the same column followed by different letters are significantly different among four plant food combinations reared either individually or in groups (Tukey’s HSD, P < 0.05).

Fig. 1. Population growth rate of Apolygus lucorum both individually and group reared on maize and green bean. MM means that both nymphs and adults fed on maize; MG means that nymphs fed on maize and adults switched to feed on green bean; GM indicates that nymphs fed on green bean and adults switched to feed on maize; GG means that both nymphs and adults fed on green bean. Means (± SE) followed by different letters denotes significant differences among four plant food combinations (Tukey’s HSD, P < 0.05). Asterisk (*) indicates that there is a significant difference between maize and green bean when nymphs fed on the same plant food (Paired t tests, P < 0.05), and ns means no significant difference between them (Paired t tests, P > 0.05).

Discussion been successfully reared on this plant food for the last 10 years (Lu et al., 2008b, 2009). In this study, we found that Lygus bugs have usually been reared on green bean pods in fresh kernels of sweet maize were better for the rearing of A. the laboratory (Beards & Leigh, 1960; Wilson, 1973), and in lucorum nymphs and that the survival rate of A. lucorum China, mirid bugs (A. lucorum and Adelphocoris spp.) have nymphs was significantly higher when they fed on maize

than on green beans, both individually and in groups. Maize Saraiva, 1993; Velasco & Walter, 1993; Pinto & Panizzi, cobs possess the advantage of having low pesticide residues, 1994). Our study suggests that feeding sweet maize to A. lucor- being enclosed in the bract. In our present study, both maize um nymphs and then feeding adults with green bean had the kernels and green bean pods were changed by the same time best outcome. interval (i.e., daily) to avoid the potential effect of rearing prac- Using the rearing method described by Lu et al.(2008b), tice. But in fact of mass laboratory rearing, green bean pods mirid bugs (inc. A. lucorum) were successfully reared on must be changed every 2 days (Lu et al., 2008b), and maize green bean pods in the laboratory, with an egg hatch rate of cobs need only be changed every 7 days (Personal observa- 80%. During the course of these experiments, we found that tion). This greatly reduces the workload, as well as potential maize kernels will dry out in 3–5 days, which severely reduced injury and disturbance to mirid bugs. Female A. lucorum the hatch rate of A. lucorum eggs. Since fresh plant tissues eas- adults have been found to lay more eggs on flowering plants, ily lose water, the type of oviposition substrate (such as cotton, and their offspring performed significantly better on them alfalfa, soybean, cowpea, and kidney bean) significantly af- (Dong et al., 2013), likely because the sugar content (e.g., su- fects egg hatching rate of mirid bugs (Fu et al., 2008; Guo crose) was significantly higher in flowers than in new foliage et al., 2008). To eliminate the impact of plant materials on of host plants. We found sweet maize can enhance survival egg hatching rate, we chose instead to use four layers of and development of A. lucorum nymphs over green bean, pos- wrinkled moist filter paper as an oviposition substrate to sibly because of the high content of sugars contained in sweet evaluate the influence of plant foods of nymphs and adults maize kernels. on the hatching rate of A. lucorum eggs. Chen et al.(2012) In our study, female longevity of A. lucorum adults and egg also used wet filter papers to attract mirid bugs (A. lucorum hatch rate significantly increased if adults switched to feed on and Adelphocoris suturalis) for oviposition and had an egg green bean after being reared on maize as nymphs, and such hatching rate above 80%. food switching was also associated with that prolonged fe- Life tables are one of the most useful tools in the study of male and male longevity, improved female fecundity and insect population dynamics and play an important role in bio- population growth rate compared with individuals where logical and ecological research (Gao & Yang, 2015). When es- both nymphs and adults fed on maize. Likewise, bugs, tablishing these tables, it is important to distinguish the results where green bean was the nymphal food and maize, was the between the individual and group rearing (Guo et al., 2008; adult food showed significantly increased female fecundity, Feng et al., 2012). In our study, the population growth rate of egg hatching rate and population growth rate compared group-reared A. lucorum on the plant food combinations MG with those of where both nymphs and adults fed on a green and GM were significantly higher compared with those on bean. These findings suggested that switching food plants MM and GG, respectively, but there were no significant differ- from nymphs to adults can improve the survival and popula- ences between MG and MM, or GM and GG when individu- tion growth of A. lucorum, a pattern common for other mirid ally reared. In general, group rearing is closer to laboratory bugs (Womack & Schuster, 1987; Panizzi, 1997; Esquivel & rearing, and as such provides important information about Mowery, 2007; Esquivel & Esquivel, 2009). For example, rear- conditions suitable for mass rearing of A. lucorum in the ing nymphs on green bean pods and then switching the laboratory. newly-emerged adults to pods of Crotalaria lanceolata, In conclusion, we demonstrated that host food switching Desmodium tortuosum or Sesbania vesicaria, or mature seeds of promotes population fitness of A. lucorum, and our study Glycine max or Arachis hypogaea, improved the longevity and shows the value of a new food combination (i.e., maize as reproductive performance of Nezara viridula (L.) adults nymphal food and green bean as adult food) for mass rearing (Panizzi & Slansky, 1991), while the reproductive performance of A. lucorum in the laboratory. and percentage gain in adult weight of N. viridula were better for those whose food was switched from radish to soybean from nymph to adulthood, as compared with those solely fed on radish (Panizzi & Saraiva, 1993). Under field condi- Acknowledgements tions, host-plant switching of mirid bug adults is common as This study was financially supported by the National bugs search for the most suitable plant foods for themselves Key Research and Development Program of China and their offspring (Wheeler, 2001; Geng et al., 2012; Dong (2017YFD0201900), the Special Fund for China Agriculture et al., 2013). Research System (CARS-15-19), the National Natural Science In this study, the population growth rate of A. lucorum Funds of China (No. 31501645, 31621064). reared both individually and as a group, on the plant food combination, MG (maize as nymphal food and green bean as adult food) was significantly increased compared with References those on GG (green bean as foods of both nymph and adult). Such food changing from nymphs to adults has been found to Beards, G.W. & Leigh, T.F. (1960) A laboratory rearing method have varied effects on a number of phytophagous insects for Lygus hesperus Knight. 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