Antibiosis of Tomato, Solanum Lycopersicum (Solanaceae) Plants to the Asopinae Predator Supputius Cincticeps (Heteroptera: Pentatomidae)

Antibiosis of Tomato, Solanum Lycopersicum (Solanaceae) Plants to the Asopinae Predator Supputius Cincticeps (Heteroptera: Pentatomidae)

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 et al.,2012). The absence of suitable prey Asopinae, such as Supputius cincticeps (particularly Lepidoptera) at the early crop stages (Heteroptera: Pentatomidae) are considered could partially explain the asynchrony between important biological control agents of numerous population dynamics of pests and Asopinae pests in South American agro-forestry ecosystems predators (Júnior et al., 2004; Coelho et al., 2009). (Zanuncio et al., 2005, 2012, 2014). However, Furthermore, leaf hairs and plant secondary populations of Asopinae predators often only reach metabolites can affect the establishment and significant levels after pest population peaks development not only of pests but also of the (Münster-Swendsen and Berryman, 2005; Neves et Asopinae predators (Holtz et al., 2006). al., 2009; De Menezes et al., 2013), especially in Predatory stink bugs are considered short cycle crops under conditions of intensive zoophytophagous or phytozoophagous depending management, such as cotton (Gossypium hirsutum, on the importance of prey or plant for their Malvaceae), soybean (Glycine max, Fabaceae) development and reproduction (Coll and Guershon, and tomato (Solanum lycopersicum, Solanaceae) 2002; Lemos et al., 2009a). Plant and animal food (Vivan et al., 2002; Malaquias et al., 2010; Zanuncio sources provide apparently amino acids and other ___________________________________________________________________________ nutrients to predators which cannot be obtained from each of the two food sources alone (Eubanks Corresponding author: Wagner de Souza Tavares and Denno, 1999; Freitas et al., 2006). Departamento de Fitotecnia Reproductive and biological characteristics of Universidade Federal de Viçosa predators can be positively affected by plant feeding 36570-900, Viçosa, Minas Gerais State, Brazil (Eubanks and Denno, 2000; Robinson et al., 2008; E-mail: [email protected] Paleari, 2013), but plant secondary compounds can 179 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 Clara were obtained from the Federal University of Clercq et al., 2000; Holtz et al., 2010). Phytophagy Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil is commonly beneficial to Asopinae predators (Holtz and those of cotton variety BRS aroeira from the et al., 2009; Lemos et al., 2009b; Malaquias et al., germplasm bank of the Brazilian Agricultural 2010), mainly during prey shortages (Perdikis et al., Research Corporation (EMBRAPA Algodão) in 2007; Holtz et al., 2009, 2010) or during periods of Campina Grande, Paraíba State, Brazil. Plant low nutritional prey (Vivan et al., 2003; Lemos et al., species were chosen due to their economic 2009b), and it has been shown to reduce importance for grain, fruit, wood production, and cannibalism (Laycock et al., 2006; Leon-Beck and their numerous potential pest species, mainly Coll, 2007; Frank et al., 2010). caterpillars, which can be preyed by S. cincticeps The zoophytophagous predator S. cincticeps (Zanuncio et al., 2004; Lemos et al., 2009b). Plants occurs on bean (Phaseolus vulgaris, Fabaceae), were grown in 500 mL plastic pots with a mixture of cotton and soybean crops in Brazil (Zanuncio et al., soil and humus from earthworms, Eisenia fetida 2003, 2012; de Castro et al., 2013a) preying mainly (Haplotaxida: Lumbricidae) and Eudrilus eugeniae on species of Diptera, Coleoptera, Hemiptera, and (Haplotaxida: Eudrilidae) in 4:1 ratio. Plants were Lepidoptera (Zanuncio et al., 2005; Lemos et al., cultivated in a greenhouse, watered as needed and 2009b; da Silva et al., 2012). Presence of this stink pests controlled manually. No chemical fertilizers bug can reduce insecticide sprays (Zanuncio et al., were applied. 1998, 2003; Tavares et al., 2009) and it seems to be compatible with certain products (Zanuncio et al., Supputius cincticeps 2013; de Castro et al., 2013a; Malaquias et al., Nymphs of S. cincticeps were obtained from the 2014). Development and reproduction parameters mass rearing of the Laboratory of Biological Control of S. cincticeps are highest when fed on a diet of Insects (LCBI) of the Institute of Biotechnology composed of both, plant and prey, although Applied to Agriculture (BIOAGRO) at the UFV. negative effects have been observed when feeding on certain plant species (Zanuncio et al., 2004, Experiments 2005; Lemos et al., 2009b). All experiments were conducted at 25 ± 2 °C, Therefore, this study aimed to investigate the 60 ± 10 % relative humidity and a 12:12 light:dark effects of different food plants on S. cincticeps by photoperiod in a Biochemical Oxygen Demand comparing biological aspects of the predator when (BOD). Seventy-five early second instar nymphs of fed on mealworm, Tenebrio molitor (Coleoptera: S. cincticeps were transferred to 15 plastic pots Tenebrionidae) pupae combined with bean, cotton, (500 mL) (five nymphs per pot) per treatment. Two eucalyptus (Eucalyptus cloeziana, Myrtaceae), pupae of T. molitor were introduced per pot three to soybean, or tomato leaves. four times a week. Two cylindrical tubes (2.5 mL), one with distilled water and one with leaves of Material and Methods different plants, were inserted in the pots through the cover. Plants were replaced after loss of Seeds turgidity. Nymphs were fed on one of the following Seeds of bean variety majestoso, eucalyptus, diets: T1 (bean leaves + T. molitor + water), T2 soybean variety UFV 16, and tomato variety Santa (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 + Statistics T. molitor + water), and T5 (tomato leaves + T. The experimental design was completely molitor + water). Adults of S. cincticeps were sexed randomized (CRD). The data were submitted to by the appearance of the external genitalia (De univariate variance analysis (ANOVA) and the Castro et al., 2013b) and weighed after emergence means compared with the Scott-Knott post hoc test (< 24 h). Duration (days) and survival per instar (%) at 5 % probability using the software SAS version and of the total nymph stage (%), weight of fifth 9.0 (Statistical Analysis System, 2002) (Supplier: instar nymphs (mg) and of male and female adults UFV). Homogeneity of variance and normality of (mg) were recorded. Three days after emergence, errors were checked using Q-Q plots (Wilk and adults of S. cincticeps were mated placing each one Gnanadesikan, 1968) and data were transformed couple into one plastic container (twenty pairs per when necessary. treatment) (Zanuncio et al., 2004). Couples of S. cincticeps received water daily and two T. molitor Results pupae three to four times a week. Adults were fed on the same combinations of T. molitor as prey and Supputius cincticeps fed on a mealworm pupae plant species as nymphs. Males of S. cincticeps, diet supplemented with leaf material of different which died during the experiment, were replaced by plant species showed marked difference in their life others of similar age and reared with the same history parameters according to the plant species.

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