ISJ 12: 179-187, 2015     ISJ 12: 179-187, 2015 ISSN 1824-307X RESEARCH REPORT Antibiosis of tomato, Solanum lycopersicum (Solanaceae) plants to the Asopinae predator Supputius cincticeps (Heteroptera: Pentatomidae) AA de Castro1, W de S Tavares2, J Collatz3, AI de A Pereira4, JE Serrão5, JC Zanuncio6 1Departamento de Entomologia, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais State, Brazil 2Departamento de Fitotecnia, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais State, Brazil 3 Agroscope Institute for Sustainability Sciences ISS, Reckenholzstrasse 191, 8046 Zürich, Switzerland 4Instituto Federal Goiano, Campus Urutaí, 75790-000, Urutaí, Goiás State, Brazil 5Departamento de Biologia Geral, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais State, Brazil 6Departamento de Biologia Animal, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais State, Brazil Accepted July 6, 2015 Abstract Plant feeding can improve development and reproduction of the stink bug Supputius cincticeps (Heteroptera: Pentatomidae), an important biological control agent in South American agro-forestry ecosystems. However, defensive compounds of plants may negatively impact this predator. The development, reproduction and survival of S. cincticeps fed on mealworm, Tenebrio molitor (Coleoptera: Tenebrionidae) pupae with bean (Fabaceae), cotton (Malvaceae), eucalyptus (Myrtaceae), soybean (Fabaceae), or tomato (Solanaceae) leaves were evaluated. Females and males were heavier and the number of nymphs produced per female, the oviposition period and the longevity of females of this predator were higher when fed on eucalyptus, soybean, bean, and cotton than with tomato leaves. Leaves of those plants improved biological parameters of S. cincticeps, while tomato leaves showed antibiosis with lower reproduction and survival of S. cincticeps, probably due to toxic compounds. Key Words: antagonistic association; defense; development; natural enemy; reproduction   Introduction Zoophytophagous stink bugs of the subfamily Asopinae, such as Supputius cincticeps (Heteroptera: Pentatomidae) are considered important biological control agents of numerous pests in South American agro-forestry ecosystems (Zanuncio et al., 2005, 2012, 2014). However, populations of Asopinae predators often only reach significant levels after pest population peaks (Münster-Swendsen and Berryman, 2005; Neves et al., 2009; De Menezes et al., 2013), especially in short cycle crops under conditions of intensive management, such as cotton (Gossypium hirsutum, Malvaceae), soybean (Glycine max, Fabaceae) and tomato (Solanum lycopersicum, Solanaceae) (Vivan et al., 2002; Malaquias et al., 2010; Zanuncio ___________________________________________________________________________ Corresponding author: Wagner de Souza Tavares Departamento de Fitotecnia Universidade Federal de Viçosa 36570-900, Viçosa, Minas Gerais State, Brazil E-mail: wagnermaias@yahoo.com.br et al.,2012). The absence of suitable prey (particularly Lepidoptera) at the early crop stages could partially explain the asynchrony between population dynamics of pests and Asopinae predators (Júnior et al., 2004; Coelho et al., 2009). Furthermore, leaf hairs and plant secondary metabolites can affect the establishment and development not only of pests but also of the Asopinae predators (Holtz et al., 2006). Predatory stink bugs are considered zoophytophagous or phytozoophagous depending on the importance of prey or plant for their development and reproduction (Coll and Guershon, 2002; Lemos et al., 2009a). Plant and animal food sources provide apparently amino acids and other nutrients to predators which cannot be obtained from each of the two food sources alone (Eubanks and Denno, 1999; Freitas et al., 2006). Reproductive and biological characteristics of predators can be positively affected by plant feeding (Eubanks and Denno, 2000; Robinson et al., 2008; Paleari, 2013), but plant secondary compounds can 179   mailto:wagnermaias@yahoo.com.br     Table 1 Effect of feeding of different plants and Tenebrio molitor pupae on the duration (mean ± standard error) (days) of different nymphal stages of Supputius cincticeps Treatments Instar Bean Cotton Eucalyptus Soybean Tomato I 4.00 ± 0.00 a 4.00 ± 0.00 a 4.00 ± 0.00 a 4.00 ± 0.00 a 4.00 ± 0.00 a II 4.94 ± 0.22 b 5.34 ± 0.16 a 3.40 ± 0.12 c 4.79 ± 0.14 b 5.49 ± 0.17 a III 4.27 ± 0.17 b 5.10 ± 0.17 a 3.93 ± 0.08 b 4.10 ± 0.10 b 4.87 ± 0.12 a IV 4.53 ± 0.09 a 4.72 ± 0.09 a 4.70 ± 0.13 a 4.19 ± 0.12 a 4.91 ± 0.58 a V 6.35 ± 0.09 a 6.82 ± 0.16 a 6.39 ± 0.11 a 6.19 ± 0.15 a 6.77 ± 0.74 a Total 24.09 ± 0.30 b 25.98 ± 0.34 a 22.43 ± 0.22 b 23.26 ± 0.35 b 26.05 ± 1.28 a Ns = Not significant; Means (± standard error) followed by the same letter in a row are not significantly different by the Scott-Knott’s test at 5 %. Number of insects = 375. also have negative effects on natural enemies (De Clercq et al., 2000; Holtz et al., 2010). Phytophagy is commonly beneficial to Asopinae predators (Holtz et al., 2009; Lemos et al., 2009b; Malaquias et al., 2010), mainly during prey shortages (Perdikis et al., 2007; Holtz et al., 2009, 2010) or during periods of low nutritional prey (Vivan et al., 2003; Lemos et al., 2009b), and it has been shown to reduce cannibalism (Laycock et al., 2006; Leon-Beck and Coll, 2007; Frank et al., 2010). The zoophytophagous predator S. cincticeps occurs on bean (Phaseolus vulgaris, Fabaceae), cotton and soybean crops in Brazil (Zanuncio et al., 2003, 2012; de Castro et al., 2013a) preying mainly on species of Diptera, Coleoptera, Hemiptera, and Lepidoptera (Zanuncio et al., 2005; Lemos et al., 2009b; da Silva et al., 2012). Presence of this stink bug can reduce insecticide sprays (Zanuncio et al., 1998, 2003; Tavares et al., 2009) and it seems to be compatible with certain products (Zanuncio et al., 2013; de Castro et al., 2013a; Malaquias et al., 2014). Development and reproduction parameters of S. cincticeps are highest when fed on a diet composed of both, plant and prey, although negative effects have been observed when feeding on certain plant species (Zanuncio et al., 2004, 2005; Lemos et al., 2009b). Therefore, this study aimed to investigate the effects of different food plants on S. cincticeps by comparing biological aspects of the predator when fed on mealworm, Tenebrio molitor (Coleoptera: Tenebrionidae) pupae combined with bean, cotton, eucalyptus (Eucalyptus cloeziana, Myrtaceae), soybean, or tomato leaves. Material and Methods Seeds Seeds of bean variety majestoso, eucalyptus, soybean variety UFV 16, and tomato variety Santa Clara were obtained from the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil and those of cotton variety BRS aroeira from the germplasm bank of the Brazilian Agricultural Research Corporation (EMBRAPA Algodão) in Campina Grande, Paraíba State, Brazil. Plant species were chosen due to their economic importance for grain, fruit, wood production, and their numerous potential pest species, mainly caterpillars, which can be preyed by S. cincticeps (Zanuncio et al., 2004; Lemos et al., 2009b). Plants were grown in 500 mL plastic pots with a mixture of soil and humus from earthworms, Eisenia fetida (Haplotaxida: Lumbricidae) and Eudrilus eugeniae (Haplotaxida: Eudrilidae) in 4:1 ratio. Plants were cultivated in a greenhouse, watered as needed and pests controlled manually. No chemical fertilizers were applied. Supputius cincticeps Nymphs of S. cincticeps were obtained from the mass rearing of the Laboratory of Biological Control of Insects (LCBI) of the Institute of Biotechnology Applied to Agriculture (BIOAGRO) at the UFV. Experiments All experiments were conducted at 25 ± 2 °C, 60 ± 10 % relative humidity and a 12:12 light:dark photoperiod in a Biochemical Oxygen Demand (BOD). Seventy-five early second instar nymphs of S. cincticeps were transferred to 15 plastic pots (500 mL) (five nymphs per pot) per treatment. Two pupae of T. molitor were introduced per pot three to four times a week. Two cylindrical tubes (2.5 mL), one with distilled water and one with leaves of different plants, were inserted in the pots through the cover. Plants were replaced after loss of turgidity. Nymphs were fed on one of the following diets: T1 (bean leaves + T. molitor + water), T2 (cotton leaves + T. molitor + water), T3 (eucalyptus 180       Fig. 1 Effect of feeding of different plants and Tenebrio molitor pupae on the weight (mg) of fifth instar nymphs and adults of Supputius cincticeps. Bars with the same letters do not differ significantly by the Scott-Knott’s test at 5 %. Comparison was made within the same developmental stage feeding on different plants. Number of insects = 210. leaves + T. molitor + water), T4 (soybean leaves + T. molitor + water), and T5 (tomato leaves + T. molitor + water). Adults of S. cincticeps were sexed by the appearance of the external genitalia (De Castro et al., 2013b) and weighed after emergence (< 24 h). Duration (days) and survival per instar (%) and of the total nymph stage (%), weight of fifth instar nymphs (mg) and of male and female adults (mg) were recorded. Three days after emergence, adults of S. cincticeps were mated placing each one couple into one plastic container (twenty pairs per treatment) (Zanuncio et al., 2004). Couples of S. cincticeps received water daily and two T. molitor pupae three to four times a week. Adults were fed on the same combinations of T. molitor as prey and plant species as nymphs. Males of S. cincticeps, which died during the experiment, were replaced by others of similar age and reared with the same conditions and treatments. Egg masses of S. cincticeps were collected daily and placed in Petri dishes with a moistened cotton ball and the nymphs counted 48 h after hatching. The number of eggs and nymphs per female and egg mass, respectively, and of egg masses; period of pre-oviposition, oviposition and post-oviposition, and of incubation (days); female longevity (days), and egg viability (%) of S. cincticeps were measured. Statistics The experimental design was completely randomized (CRD). The data were submitted to univariate variance analysis (ANOVA) and the means compared with the Scott-Knott post hoc test at 5 % probability using the software SAS version 9.0 (Statistical Analysis System, 2002) (Supplier: UFV). Homogeneity of variance and normality of errors were checked using Q-Q plots (Wilk and Gnanadesikan, 1968) and data were transformed when necessary. Results Supputius cincticeps fed on a mealworm pupae diet supplemented with leaf material of different plant species showed marked difference in their life history parameters according to the plant species. The duration of the total S. cincticeps nymph stage was significantly influenced by the plant food source (Table 1). It was shorter with eucalyptus, soybean or bean leaves than with cotton or tomato leaves (Table 1). Duration of the first, fourth and fifth nymph instars were unaffected by the diet, whereas the second instar was significantly shorter on eucalyptus leaves compared to the other plant food sources (Table 1). The third instar was significantly 181       Table 2 Effect of feeding of different plants and Tenebrio molitor pupae on the survival (mean ± standard error) (days) of different nymphal stages of Supputius cincticeps Treatments Instar Bean Cotton Eucalyptus Soybean Tomato II 85.33 ± 3.63 a 86.67 ± 5.11 a 93.33 ± 3.19 a 92.00 ± 3.27 a 66.67 ± 5.40 b III 80.00 ± 3.38 a 78.67 ± 4.56 a 88.00 ± 4.28 a 86.67 ± 5.04 a 62.67 ± 4.31 b IV 73.33 ± 4.22 a 68.00 ± 5.79 a 82.66 ± 5.11 a 82.67 ± 5.12 a 51.33 ± 4.87 b V 70.67 ± 3.84 a 65.33 ± 6.01 a 80.00 ± 5.16 a 76.00 ± 5.59 a 44.67 ± 4.24 b Total 70.66 ± 3.83 a 65.33 ± 6.00 a 82.67 ± 4.31 a 76.00 ± 5.58 a 44.66 ± 4.23 b Means (± standard error) followed by the same letter in a row are not significantly different by the Scott-Knott’s test at 5 %. prolonged with cotton or tomato leaves as food source (Table 1). Weight of S. cincticeps was also significantly affected by the plant species fed (Fig. 1). Fifth instar nymphs were significantly lighter when fed with tomato leaves, compared to all other plants. This effect was visible in both sexes (Fig. 1). Overall survival of S. cincticeps nymphs, as well as stage-specific survival of second, third, fourth, and fifth instar nymphs was influenced by the plant species fed (Table 2). Survival was significantly higher with eucalyptus, soybean, bean, or cotton than with tomato leaves (Table 2). The longevity of S. cincticeps females was significantly longer with eucalyptus, soybean, bean, and cotton leaves than with tomato leaves (Table 3). While the total number of eggs per female and egg mass and the number of egg masses were similar among treatments (Fig. 2), the pre-oviposition period of S. cincticeps was significantly longer with tomato leaves and the oviposition period significantly shorter. The post-oviposition period was similar between treatments (Table 3). The number of emerging nymphs per egg mass was significantly higher with eucalyptus or cotton leaves than with soybean, bean or tomato leaves (Table 3). Egg viability of S. cincticeps was significantly lower with tomato leaves and higher with eucalyptus leaves, while the incubation period was similar between treatments (Table 3). The number of surviving nymphs per female was significantly higher with eucalyptus, soybean, bean, or cotton leaves than with tomato leaves (Table 3). Discussion In the present study we could show that almost all life history characteristics of S. cincticeps were negatively affected when they were fed with tomato leaves, and some parameters were also inferior when the nymphs fed on cotton leaves compared to the other plant food sources. These differences could result from differences in food accessibility, the content of secondary plant defense compounds and/or differences in nutritional quality of these plants (Júnior et al., 2004; Holtz et al., 2009; Malaquias et al., 2010). Morphological and chemical properties of plants may influence their attractiveness for herbivores as well as the biological characteristics of herbivores (Agrawal, 2000; Hagenbucher et al., 2013; Eaton and Karban, 2014) and Asopinae predators (Hilker and Meiners, 2002; Degenhardt et al., 2003). While Asopinae predators often benefit from additional plant feeding by enhanced growth and reproduction (Holtz et al., 2009; Lemos et al., 2009b; Malaquias et al., 2010), morphological characteristics, e.g., trichomes and chemical characteristics, such as secondary plant compounds, may have negative effects on the predator. Thereby influences on the life cycle may vary among plant species, as well as among stink bug species feeding on the same plant (Júnior et al., 2004; Lemos et al., 2009b; Malaquias et al., 2010). Similar studies have reported shortened durations of the nymph stage and higher fecundity of P. nigrispinus fed on cotton or whiteweed, Ageratum conyzoides (Asteraceae) without prey (Júnior et al., 2004); fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) on cotton cultivars (de Jesus et al., 2014), and cotton leafworm, Alabama argillacea (Lepidoptera: Noctuidae) with cotton or fennel, Foeniculum vulgare (Apiaceae) (Malaquias et al., 2014). However, the longer duration of the second and third instar, and of the total nymph stage as well as reduced longevity of S. cincticeps with cotton or tomato leaves in our study suggest negative effects, as were found for the longer duration of the nymph stage of Brontocoris tabidus (Heteroptera: Pentatomidade) with cotton (Coelho et al., 2009; Torres et al., 2010). Like tomato plants, cotton 182       Table 3 Effect of feeding of different plants and Tenebrio molitor pupae on the reproductive parameters and longevity of Supputius cincticeps Treatments Reproductive parameters Bean Cotton Eucalyptus Soybean Tomato Number of eggs/female 157.11 ± 20.03 a 125.76 ± 20.77 a 163.28 ± 18.94 a 165.73 ± 25.25 a 121.67 ± 18.05 a Number of nymphs/female 120.38 ± 16.02 a 101.28 ± 17.42 a 142.00 ± 17.36 a 125.80 ± 21.64 a 59.78 ± 8.23 b Pre-oviposition period (days) 8.81 ± 0.38 b 8.72 ± 0.51 b 9.39 ± 0.16 b 8.07 ± 0.73 b 10.78 ± 0.79 a Oviposition period (days) 31.81 ± 3.44 a 25.36 ± 2.76 a 29.83 ± 3.17 a 28.00 ± 3.92 a 17.11 ± 2.25 b Post-oviposition (days) 4.12 ± 0.68 a 3.80 ± 0.73 a 2.22 ± 0.42 a 5.47 ± 1.23 a 3.78 ± 0.62 a Longevity (days) 45.42 ± 3.49 a 37.40 ± 3.12 a 43.50 ± 2.98 a 41.53 ± 4.18 a 28.22 ± 2.01 b Egg viability (%) 74.11 ± 3.25 b 77.64 ± 2.25 b 86.06 ± 1.45 a 72.48 ± 3.57 b 53.30 ± 3.74 c Incubation period (days) 5.91 ± 0.04 a 5.84 ± 0.07 a 5.81 ± 0.03 a 5.85 ± 0.08 a 5.85 ± 0.07 a Number of eggs/egg mass 10.55 ± 0.49 a 11.30 ± 0.72 a 11.49 ± 0.46 a 11.95 ± 0.79 a 11.81 ± 0.64 a Number of nymphs/egg mass 7.24 ± 0.55 b 8.97 ± 0.71 a 9.89 ± 0.44 a 7.83 ± 0.78 b 6.67 ± 0.52 b Number of egg masses 14.69 ± 1.74 a 11.04 ± 1.66 a 14.28 ± 1.57 a 14.13 ± 2.01 a 10.89 ± 1.70 a Means (± standard error) followed by the same letter in a row are not significantly different by the Scott-Knott’s test at 5 %. Twenty couples per treatment. contains secondary plant metabolites, e.g., the terpenoid gossypol that is active against leaf feeding insects (Hagenbucher et al., 2013). Supputius cincticeps is a generalist predator that may utilize prey and leaf material of different plants species (Lemos et al., 2009b) and thus it might not be adapted to metabolize tomato and cotton plant allelochemicals very efficiently. In contrast to generalist species that often possess enzymes to metabolize a broad range of defense substances to certain extend (Krieger et al., 1971; Li et al., 2004), specialist herbivores are able to detoxify the specific defense substances from their few host plants highly efficiently (Mao et al., 2006; Lampert et al., 2011). Effects of plant feeding on life-history characteristics of predators can be negative, as with tomato plants, for S. cincticeps or in the case of Podisus maculiventris (Heteroptera: Pentatomidade) where feeding on a vegetable diet (bean) negatively affected the development, weight gain and growth of nymphs compared to individuals fed only on T. molitor pupae (Crum et al., 1998; Weiser and Stamp, 1998). However plant feeding can also have positive effects on S. cincticeps, when nymph stages are shortened, lifetime prolonged and reproduction is enhanced (Zanuncio et al., 2004, 2012). Shortened nymph stages of S. cincticeps would allow this predator to reach adulthood and reproduce faster (Zanuncio et al., 2004, 2005; Holtz et al., 2006). Adult weight, mainly of females may indicate the reproductive success of predatory stink bugs, with heavier ones presenting greater longevity and reproduction (Legaspi and Legaspi, 2005; Oliveira et al., 2005; Lemos et al., 2009b). Likewise the lower weight of S. cincticeps females with tomato leaves resulted also in reduced longevity, oviposition period, number of nymphs produced per female and egg mass, and egg viability of this predator. In contrast, these parameters were enhanced with eucalyptus, soybean, bean, and cotton leaves, suggesting a positive effect of these plants, as found for the reproduction of P. nigrispinus with eucalyptus (Holtz et al., 2009, 2011; Torres et al., 2010). The favorable effect on development and reproduction of S. cincticeps was similar to other Asopinae fed on plant diets (Holtz et al., 2009, 2011; Lemos et al., 2009a). As secondary plant defense compounds tomato plants contain chlorogenic acid (the ester of caffeic acid and (-) -quinic acid) and tomatine, a glycoalkaloid (Lambert, 2007; Inbar and Gerling, 2008; Tian et al., 2012) that can inhibit acetylcholinesterase and thus interrupt the transmission of nerve impulses (Friedman, 2002). 183       Fig. 2 Effect of feeding of different plants and Tenebrio molitor pupae on the number of eggs and nymphs produced per week and survival of Supputius cincticeps. Bars representing same letters do not differ significantly by the Scott-Knott’s test at 5 %. Comparison was made within the same developmental stage feeding on different plants. Nymphs of P. maculiventris and P. nigrispinus that were reared with prey (Lepidoptera) fed on chlorogenic acid, gossypol and tomatine of tomato plants developed slower and had other negative effects on development and reproduction (Traugott and Stamp, 1997; Kaplan and Thaler, 2010; Evangelista et al., 2011). Plant secretions (enzymes) and trichomes may interfere with searching behavior of natural enemies and thus reduce their foraging efficiency (Gruenhagen and Perring, 2001; Bjorkman and Ahrne, 2005; Rodriguez-Lopes et al., 2011). Cotton trichomes inhibited searching behavior of natural enemies (mainly Hymenoptera) on insect-herbivores (Hagenbucher et al., 2013). Especially glandular trichomes that excrete enzymes such as gossypol can be a major problem for herbivores and beneficials alike (Evangelista et al., 2011). The glandular trichomes of the tomato variety Heinz, for example, excrete exudates and other substances that stuck to the legs of P. maculiventris nymphs, which hamper its movement and feeding (De Clercq et al., 2000; Lambert, 2007; Kaplan and Thaler, 2010). To assess directly whether the presence of trichomes has interfered with food accessibility for S. cincticeps behavioral bioassays would have been necessary. 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Biol. 144: 357- 361, 2004. 187   http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Zanuncio%20JC&ut=000222254100012&pos=1 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Zanuncio%20JC&ut=000222254100012&pos=1 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Lacerda%20MC&ut=000222254100012&pos=2 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Junior%20JSZ&ut=000222254100012&pos=3 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Zanuncio%20TV&ut=000222254100012&pos=4 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Zanuncio%20TV&ut=000222254100012&pos=4 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Da%20Silva%20AMC&ut=000222254100012&pos=5 http://apps.isiknowledge.com/DaisyOneClickSearch.do?product=WOS&search_mode=DaisyOneClickSearch&db_id=&SID=4E5jmoE17ijGhGg2bHJ&name=Espindula%20MC&ut=000222254100012&pos=6 The experimental design was completely randomized (CRD). The data were submitted to univariate variance analysis (ANOVA) and the means compared with the Scott-Knott post hoc test at 5 % probability using the software SAS version 9.0 (Statistical Analysis System, 2002) (Supplier: UFV). Homogeneity of variance and normality of errors were checked using Q-Q plots (Wilk and Gnanadesikan, 1968) and data were transformed when necessary. References