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Terpenoids Dominate the Bouquet of Volatile Organic Compounds

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Terpenoids Dominate the Bouquet of Volatile Organic Compounds Arthropod-Plant Interactions (2018) 12:123–131 DOI 10.1007/s11829-017-9560-2 ORIGINAL PAPER Terpenoids dominate the bouquet of volatile organic compounds produced by Passiflora edulis in response to herbivory by Heliconius erato phyllis (Lepidoptera: Nymphalidae) Eliane de O. Borges1,2 · Camila B. C. Martins1 · Rodolfo R. da Silva1 · Paulo H. G. Zarbin1,2 Received: 16 January 2017 / Accepted: 19 August 2017 / Published online: 4 September 2017 © Springer Science+Business Media B.V. 2017 Abstract In response to injury, plants produce volatile plants displayed a peak of emission of (E)-β-ocimene after organic compounds (VOCs) that usually differ depending 72 h, which distinguished them from HB plants. MD plants on the type of damage they have suffered (e.g., mechanical showed a general increase of VOCs versus undamaged damage, herbivory, and oviposition). The objectives of this control plants. Furthermore, it has been suggested that (E)- study were to identify and compare the bouquet of volatiles β-ocimene may be sequestered by larvae of H. erato phyllis emitted by passion vine plants (Passiflora edulis) after as a component of the odoriferous bouquet of the abdom- injury caused by mechanical damage (MD), herbivory inal scent glands present in adult males, which play a role (HB), and oviposition (OV) by the lepidopteran, Heliconius in sexual communication. erato phyllis. Following injury, extracts of plant emissions were collected from each treatment every 24 h for three Keywords Butterfly · (E)-β-ocimene · Homoterpenes · days and were analyzed by GC and GC/MS. Results show Passion vine · Plant–insect interaction · Terpenes · TMTT that plants emitted 12 volatiles before and after damage, namely terpenoids, ketones, and aldehydes. Although no significant differences were detected between the three Introduction treatments individually, if the entire bouquet of volatiles is analyzed, samples collected at 24 h were different from Volatile organic compounds (VOCs) produced by plants in samples collected at 48 and 72 h. However, terpenoid response to herbivory may attract the enemies of herbivore emission increased significantly in HB plants after 24 h. insects (Arimura et al. 2009; Pinto-Zevallos et al. 2013) HB plants emitted approximately 6300, 50, 46, 11, 6, and and may activate responses in conspecific plants and other 3.6 times more (3E,7E)-4,8,12-trimethyl-1,3,7,11-tride- organisms, for example, attracting or repelling lepidopteran catetraene, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), females for oviposition (De Moraes et al. 2001; Zakir et al. (E)-β-ocimene, (Z)-β-farnesene, (E)-β-caryophyllene, and 2013). In plants, oviposition by herbivorous insects pro- farnesane, respectively, compared to control plants. OV motes the emission of volatile signals, the formation of necrotic tissues, and the production of ovicidal substances (Hilker and Meiners 2006). In the literature, various studies investigate the production of VOCs by plants following Handling Editor: Anna-Karin Borg-Karlson. herbivory and/or oviposition by lepidopterans (Pare´ and & Paulo H. G. Zarbin Tumlinson 1999; Fatouros et al. 2012; Zakir et al. 2013; [email protected] Horas et al. 2014; Hatano et al. 2015). Many plants are able 1 to discriminate between the damage caused by herbivorous Laborato´rio de Semioquı´micos, Departamento de Quı´mica, insects or mechanical damage by recognizing chemical Universidade Federal do Parana´ (UFPR), CP 19081, Curitiba, PR 81531–990, Brazil elicitors present in the oral secretions of herbivores, and by assessing the quantity and quality of tissue damaged, along 2 Departamento de Zoologia, Programa de Po´s-graduac¸a˜oem Entomologia, Universidade Federal do Parana´ (UFPR), with the pattern, frequency, and the period of feeding by CP 19020, Curitiba, PR 81531-980, Brazil herbivores (Wu and Baldwin 2009). 123 124 E. de O. Borges et al. Passiflora edulis Sims, 1818 (Malpighiales, Passiflo- their production methodology and the lineages involved are raceae) produces the yellow passion fruit and is the host unknown. plant of several species of Nymphalidae butterflies, known Volatile Collection Headspace collections were per- as passion vine butterflies (Brown and Mielke 1972; formed using glass chambers (11.5 9 35 cm), inside a Bianchi and Moreira 2005), which are common herbivores room with controlled temperature and humidity conditions of passion fruit plantations in Brazil (Rossetto et al. 1974). (24 ± 2 °C, 12 L: 12 D, 58 ± 2%). Samples were collected Heliconius erato phyllis (Fabricius 1775) (Lepidoptera: using a humidified and charcoal-filtered airflow at Nymphalidae) uses passion vines for oviposition and as a 0.5 L min−1 per chamber. VOCs were collected on glass larval food plant (Benson et al. 1976). Furthermore, studies columns containing 20 mg of the polymer HayeSep Q 80– suggested that Heliconiinae butterflies and its host plants 100 mesh (Althech, Lokeren, Belgium), and eluted with have coevolved. Evidence suggests that development of 240 μL of double-distilled HPLC-grade hexane (Zarbin plant defenses have affected diversification of both passion et al. 1999). An internal standard (IS) of heptadecane (C17: fruits and Heliconiinae butterflies (Smiley 1985a; Ehrlich 150 or 750 ng) was added to the final extract. Then, the and Raven 1964). Strategies used by passion vine plants final IS concentration was calculated and the extract was include structural modifications, which can discourage or quantified based on the IS peak area. For the purpose of prevent oviposition (Willlians and Gilbert 1981; Gilbert quantification accuracy, only peaks greater than 30 ng were 1982, 1991), perforate larvae (Gilbert 1971) and attract considered for the analyses. ants as predators (e.g., extrafloral nectaries) (Gilbert 1975; Passiflora edulis seedlings (five months of age and 10 Smiley 1985b). Also, induced responses to herbivory by leaves) were subjected to mechanical damage with a cir- Heliconiinae include the production of toxic and repellent cular pasta cutter (3 marked leaves), or to herbivory (10 compounds (Spencer 1988; Benson et al. 1976). Some of larvae), or to oviposition (five mated females that laid a the Heliconiinae responses to overcome plant defenses are mean of 20 eggs) by H. erato phyllis for 24 h or were used the preference to oviposit in the apex of tendrils avoiding as control plants. For the experiments, twelve plants were ant predation, the ability of larvae to coat trichomes with used once for each treatment. Treated plants were always silk to avoid cuticle perforation, and vision and memory compared to control plants. Mated females were identified abilities, which can help butterflies find and select host by the characteristic odor of the abdominal scent gland. plants (Benson et al. 1976). Headspace collections were performed at 24, 48, and 72 h Until now, induced defenses of Passiflora spp. have not after treatments for 24 h. been investigated concerning volatile emission or the Seedlings of each treatment were maintained in separate discrimination of different types of herbivore damage. For rooms to avoid plant-plant communication. Twelve repli- this reason, we aimed to compare the responses of P. cates were conducted of each experimental set. Each edulis to different injuries by identifying and quantifying experimental set contained four plants, three of them the VOCs emitted by treated plants (mechanical damage, treated (mechanical damage, herbivory, and oviposition) herbivory, and oviposition by H. erato phyllis) and control and one control, totaling 144 samples [12 replicates 9 4 plants. treatments = 48; 48 9 3 (24, 48, and 72 h) = 144]. Col- lections began at the same time each day until the end of the experiment. Extracts were stored at −20 °C until further Methodology analysis. VOCs were compared between treatments using gas chromatography (GC) and using combined gas chro- Rearing of Heliconius erato phyllis and cultivation of matography and mass spectrometry (GC–MS). Passiflora edulis seedlings Adults butterflies were collected Analytical Procedures Extracts were analyzed by com- in a native forest inside the Centro Polite´cnico, Universi- bined gas chromatography and mass spectrometry (GC– dade Federal do Parana´, in Curitiba, Parana´, Brazil. For the MS) on a Shimadzu QP 2010 Plus. The GC and GC/MS rearing and the manipulation of adults an insectary coated were equipped with a RTX-5 column (30 m 9 0.25 mm i. with Sombrite ®, which allows passage of 30% of direct d., 0.25 mm film thickness; Restek, Bellefonte, PA, USA). sunlight, was used as a semi-natural environment. Inside Injections of 1 μL were performed in the splitless mode, the insectary, pots with P. edulis; P. actinia Hooker, 1943; with an injector temperature of 250 °C. The column oven Impatiens walleriana Hook; Lantana camara Linnaeus, temperature was held at 50 °C for 1 min, increased to 250 ° 1753; and containers with artificial diet (Borges et al. 2010) Cat7°C min−1, and held for 10 min. Helium was the were used as oviposition and feeding substrate, respec- carrier gas at a linear velocity of 36.3 cm s−1. The same tively. Passiflora edulis individual seeds (Isla Pak®) were parameters were used for all analyses. cultivated inside plastic bags (15 cm 9 25 cm) containing Identification of Compounds VOCs were identified by untreated soil in a greenhouse. As seeds were purchased, Kovats indices (KI) and mass spectra comparisons with the 123 Terpenoids dominate the bouquet of volatile organic compounds produced by Passiflora edulis… 125 literature (Adams 2007; El-Sayed 2016), and by co-injec- variation (Fig. 3a). ANOVA showed that volatiles inter- tions with commercially available standards. 5-hydroxi-4- acted with treatment and time (Pillai trace = 0.041, octanone, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), far- F 6 = 2.261, P ≤ 0.5*), with treatment alone (Pillai nesene, and (3E,7E)-4,8,12-trimethyl-1,3,7,11- trace = 0.019, F 3 = 3.407, P ≤ 0.05*), and with time tridecatetraene (TMTT) were tentatively identified. Non- (Pillai trace = 4.73e-06, F 2 = 13.557, P ≤ 0.001*).
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