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The response of two Bactrocera species (Diptera: Tephritidae) to fruit volatiles
Journal of Asia-Pacific Entomology 22 (2019) 758–765
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Full Length Article
The response of two Bactrocera species (Diptera: Tephritidae) to fruit volatiles
T
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Waqar Jaleela,b, Yurong Heb, , Lihua Lüa a
Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China Key Laboratory of Bio-pesticide Innovation and Application of Guangdong Province, Department of Entomology, College of Agriculture, South China Agricultural University, Guangzhou, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: 3-Carene β-Caryophyllene α-Humulene Bactrocera Olfactometer Female-biased attractant Volatile components
Bactrocera dorsalis and B. correcta are serious pests of agricultural fruit crops. Both species are widely distributed in tropical and subtropical countries, especially in Asia. For integrated management of both Bactrocera species, understanding their olfactory behavior is vital for designing reliable control strategies. In this study, the response of female B. dorsalis and B. correcta adults to three main volatile components of fruits was evaluated using the Ytube olfactometer. Our results showed that at higher concentrations all volatile components, except α-humulene and its combination with β-caryophyllene, attracted significantly more B. dorsalis than the untreated arm. For B. correcta, all the volatile components attracted significantly more females in the treated arm than the untreated arm. However, at 5% and 1% concentration, all the volatile components had similar attraction for B. dorsalis females. In the case of female B. correcta, the percentage of attraction was similar for all the individual volatile chemicals and their respective mixtures at 10% concentration. While, at 5% and 1% concentrations, the percentage of attraction was significantly higher for a mixture of β-caryophyllene and α-humulene than that of individual volatile components and all possible mixture of two and three volatile components. Based on the olfactometer results, this study concluded that 3-carene and the mixture of β-caryophyllene and α-humulene are strong attractants for female flies of B. dorsalis and B. correcta, respectively. This study might be helpful for the bait application against the female adults of B. dorsalis and B. correcta in farms and orchards.
Introduction The genus Bactrocera (Diptera: Tephritidae) contains 500 species, including many severe pests of fruits and vegetables, among them Bactrocera dorsalis (Hendel) and B. correcta (Bezzi) are most economic flies and infesting > 250 hosts (Allwood et al., 1999; Ekesi et al., 2016; Jaleel et al., 2018a, 2018b, 2018c; San Jose et al., 2013), and 90 host plants' families in the world (Allwood et al., 1999; Wee et al., 2018). Both the Bactrocera flies are considered invasive and quarantine fruits pest species because of their polyphagous nature and high dispersal abilities (Liu et al., 2013). The infestation in fruit crops caused by B. dorsalis has been recorded up to 7.5% economic injury level at the time of harvest of carambola (star fruit) (Jiang et al., 2017). The B. correcta (the guava fruit fly) is the 2nd most important pest of fruit crops after B. dorsalis (Tan et al., 2011; Wee et al., 2018; White and Elson-Harris, 1992). And in 2009, the B. correcta was reported in Yuanjiang, Yunnan, China (Liu and Ye, 2009). The B. correcta was recorded as a serious pest of guava and mango fruit in Pakistan, India, Nepal, Myanmar, Thailand,
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Sri Lanka, Vietnam, and China (Liu et al., 2013). The environmentally safe control method of Bactrocera species is the application of phytochemical in farms and orchards, that relies almost exclusively on the attractiveness of the flies to chemical lures (Tan et al., 2014). Females of Bactrocera dorsalis and its sibling species are attracted to the sex pheromone released by conspecific males that have fed on methyl eugenol (ME) leading to significantly improved mating successes (Tan and Nishida, 1996; Shell, 2010). The ME is found in over 450 plant species including Bulbophyllum orchid species that release ME as floral synomone to entice fruit fly pollinators (Tan and Nishida, 2012). Even B. dorsalis males had increased mating success after feeding on the golden shower blossom of Cassia fistula that has very low MEcontent (Shelly, 2000). Jang et al. (2017) have reported the effectiveness of synthetic cucumber lure that increased female-biased sex ratios in trap captures firstly in Taiwanese and then in Hawaiian field trials. Majority of phytochemicals as attractants are specific for specific species of Bactrocera flies (Jang and Light, 1991; Tan et al., 2014). Several control methods have been associated with male Bactrocera flies
Corresponding author. E-mail address: [email protected] (Y. He).
https://doi.org/10.1016/j.aspen.2019.05.011 Received 5 May 2018; Received in revised form 27 May 2019; Accepted 30 May 2019 Available online 31 May 2019 1226-8615/ © 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
Journal of Asia-Pacific Entomology 22 (2019) 758–765
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21 cm
OS
OS
10 cm
W
W
Direction of air flow
A
A
F
F
M
M
21 cm Charcoal Charcoal Insect Entry Hole
Air Inlet
Air Inlet
Fig. 1. Schematic diagram of the Y-tube olfactometer (OS: odor source, W: water for maintaining humidity, AFM: air flow meter, dotted lines represent Teflon hoses).
together with α-humulene in the male pheromone gland of wild B. correcta (Tokushima et al., 2010: Tan et al., 2011, 2014). Chrysopa carnea Stephens was monitored and captured in a trap containing 2 g of β-caryophyllene (Flint et al., 1981). β-Caryophyllene has been tested to attract female flies of C. capitate (Eyles et al., 1999). The α-humulene is the major volatile component in mango and guava fruits. It has been used to capture the Bactrocera flies (Nishimura et al., 1989; Salazar Sandoval et al., 2007; Tamura et al., 2000). 3-Carene is a monoterpene can be extracted from the plant sources (Jayanthi et al., 2012; Sharath et al., 2015). 3-Carene is an important volatile component in the odor of mango that has been used as attractants for female B. dorsalis (Damodaram et al., 2015; Jayanthi et al., 2012). Acanthocinus obliquus (LeConte) and Acmaeops proteus (Kirby) have been trapped by bait containing 3-carene (Costello et al., 2014). Similarly, bark beetle (Tomicus piniperda) is also attracted to the bait containing 3-carene (Schlyter et al., 2000). Behavioral responses of different Bactrocera species to volatiles in the laboratory have been reported using Y-tube assay, which allows screening of plant volatiles in short range and efficient way (Ballhorn and Kautz, 2013; Canale et al., 2015; Giunti et al., 2018; Holtmann, 1962; Teulon et al., 1993). However, there is no detailed information regarding female biased attractants for B. correcta flies were provided elsewhere. Considering the importance female biased attractants, this
(Alagarmalai et al., 2009; Suckling et al., 2016). Previous studies have been conducted to capture the male adults of B. dorsalis, Ceratitis capitata Wiedemann, B. correcta, and Anastrepha flies by the application traps containing ME, trimedlure, β-caryophyllene, and CeraTrap® respectively (Qin et al., 2015; Suckling et al., 2016; Villalobos et al., 2017; Wee et al., 2018; Weems et al., 2001). Female Bactrocera flies search different hosts by using odors that are elicited by fruits. The female flies of B. dorsalis have been captured using host plant odors e.g. fruits, leaves, and twigs (Siderhurst and Jang, 2010). The female flies of B. dorsalis are strongly attracted to ethanol, ethyl acetate, ethyl hexanoate, hexyl acetate, linalyl acetate, ethyl nonate, nonyl acetate, ethyl cinnamate, and (E)-β-farnesene in comparison to male adults, when using olfactometer tests (Siderhurst and Jang, 2006, 2010). However, a female-biased trapping system is assumed to be more effective than mass-trapping of males, because the former reduces fruit damage by preventing oviposition (Jang, 2002; Jang and Light, 1991; Siderhurst and Jang, 2010). Usually, the single volatile is less attractive than the mixture of volatile components, but not the same in all Bactrocera flies (Biasazin et al., 2014; Malo et al., 2012). A major sesquiterpene is β-caryophyllene and present in various ripen fruits as volatile constitute especially in guava fruit (Macleod and de Troconis, 1982). β-Caryophyllene as an attractant has been studied in various insect pests, although detected in relatively large quantities 759
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Statistical analysis
study explains the olfactory response of female B. dorsalis and B. correcta flies to three volatile components, 3-carene, β-caryophyllene, and α-humulene using the Y-tube olfactometer.
The difference between the two treatments was analyzed by Chisquared (χ2) test in SPSS Statistics 15.0 (SPSS Inc., Chicago, IL, USA) with the expected value (α = 0.05). Non-responder females were not included in statistical analysis. Female flies of Bactrocera species response to treatments (at each concentration), summarized as the percentage of female flies of Bactrocera species attracted into the treated arm (the number of Bactrocera flies attracted in the treated arm divided by the total number Bactrocera species flies in both treated and untreated arm). There were seven treatments as (1) 3-carene, (2) β-caryophyllene, (3) α-humulene (4) 3-carene + β-caryophyllene, (5) 3-carene + α-humulene, (6) βcaryophyllene + α-humulene (7) 3-carene + β-caryophyllene + αhumulene. The difference among 7 treatments at each dose was analyzed separately by using the Kruskal-Wallis one-way ANOVA, at P < .05, allpairwise comparisons test of the homogenous group in SPSS Statistics 15.0 (SPSS Inc., Chicago, IL, USA).
Materials and methods Insect The population of both species e.g. B. dorsalis and B. correcta was reared in the controlled room (25 ± 2 °C, 60–65% relative humidity, and a photoperiod of L:D 14:10 h) at the College of Agriculture, South China Agricultural University, Guangzhou, China. The temperature was controlled by the air-conditioner (Gree Electric Appliances, Inc. of Zhuhai, Zhuhai, China) and the humidity was maintained by the humidifier. Adult flies were reared in cages (30 × 30 × 30 cm) by providing water-soaked cotton wool in a box (12 × 6.8 × 7 cm), powdered yeast and sugar (2:1) in a petri-dish (6 × 1.5 cm). Larvae were reared on semi-artificial diet described by Jaleel et al. (2018a, 2018b, 2018c). Gravid female adults of B. dorsalis and B. correcta (15–18 days old) were used for all behavioral assays.
Results Olfactometer bioassay Effect of volatile components to the response of B. dorsalis and B. correcta The behavioral responses of female adults of B. dorsalis and B. correcta to the volatile components were observed in a Y-tube olfactometer. The Y-shaped glass tube olfactometer with entry arm of 16 cm and two side arms of 21.00 cm, each 2.5 cm in diameter. Activated charcoal-filtered and humidified air were pumped inside the olfactometer arms. The airflow was set to 0.5 l min−1 and passed through Teflon tubes that were joined to each arm. The Y-tube was placed inside a box of white fabric, to avoid the visual distraction of the flies (Fig. 1). Volatile components e.g. 3-carene (90%), β-caryophyllene (≥ 80%, FCC, FG), and α-humulene (≥ 96.0% (GC) were purchased from Alfa Aesar, Beijing, China. Structural formulae are in Fig. 2. Seven treatments were made (1) 3-carene, (2) β-caryophyllene, (3) α-humulene (4) 3-carene + β-caryophyllene, (5) 3-carene + α-humulene, (6) β-caryophyllene + α-humulene (7) 3-carene + β-caryophyllene + α-humulene. Three different concentrations e.g. 10%, 5%, and 1% (v/v) were prepared in acetone (75%) for each treatment. Mixture of volatile compounds are prepared in ratios of 1:1 (v/v) and 1:1:1 (v/v/v) for a mixture of two and three chemicals, respectively. Each treatment in one arm was compared to control arm that contained only acetone. For this experiment, 100 μl of each solution of treatment was applied to a piece of filter paper (2.0 × 0.5 cm) and placed on a small glass holder at the air entrance of the Y-tube. A total of 80 flies of each species were selected and used per treatment. Bactrocera flies that did not move within 15 min were considered as non-responders. After the test of 5 flies, the Y-tube or odor sources were switched to avoid contamination by Bactrocera flies or test odor. Tubes were washed with 95% alcohol and placed in an oven at 250 °C for 30 min. Experiment proceeded on with new odor sources, clean tubes and female Bactrocera flies. Each female Bactrocera fly was used only once. Each experiment was replicated eight times.
All three factors, Bactrocera species, volatile components, concentrations, and the interactions between Bactrocera species and volatile components had significantly influenced the response. While the remaining all possible interactions e.g. interactions between (1) Bactrocera species and concentrations, (2) volatile components and concentration, and as well as interaction among Bactrocera species, volatile components, concentrations had no significant effects in the response to the volatile components (Table 1). The response of female B. dorsalis and B. correcta to 3-carene The 10% concentration of 3-carene was more attractive for the female flies of B. dorsalis in the treated arm than the untreated arm of Ytube olfactometer (χ2 = 15.78, P < .001) (Fig. 3A). While at 5% and 1% concentrations of 3-carene had no significant difference in B. dorsalis females' response between treated and untreated arms (Fig. 3A). More B. correcta females were attracted to the odor of 3-carene at 10% concentration (χ2 = 8.39, P = .004) than in the untreated arm. There was no significant effect of 3-carene at 5% and 1% concentrations to the response of female B. correcta flies between the treated arm and untreated arm (Fig. 3B). The response of female B. dorsalis and B. correcta to β-caryophyllene The female flies of B. dorsalis remarkably attracted more to arm contained β-caryophyllene (10%) than the untreated arm of the Yshaped glass tube (χ2 = 6.25, P = .012) (Fig. 4A). There was no significant attraction for the female flies of B. dorsalis at 5% and 1% Table 1 Three-factors ANOVA statistics for analyzing the % response of female B. dorsalis and B. correcta adults to volatile components.
Fig. 2. Structures of three volatile components.
Indexes
Factors
df
F
P
Response
a b c a*b a*c b*c a*b*c
1294 6294 2294 6294 2294 12,294 12,294
25.11 2.85 88.14 10.65 2.81 1.73 0.54
< 0.001 0.010 < 0.001 < 0.001 0.061 0.060 0.890
a: Bactrocera species; b: volatile components; c; concentrations. 760
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Fig. 3. Attraction of B. dorsalis (A) and B. correcta (B) female flies to 3-carene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Fig. 5. Attraction of B. dorsalis (A) and B. correcta (B) female flies to α-humulene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
(A)
concentrations of β-caryophyllene between the treated and untreated arm (Fig. 4A). The 10% (χ2 = 6.25, P = .005) and 5% (χ2 = 6.25, P = .027) concentration of β-caryophyllene had remarkably attracts the female responders of B. correcta in treated arm as compare to their respective untreated arm (Fig. 4B). The response of female B. dorsalis and B. correcta to α-humulene There were no significant effects of α-humulene at all concentrations (10%, 5%, and 1%) to the female adults of B. dorsalis between the treated and untreated arm (Fig. 5A). While, the 10% concentration of αhumulene had the higher attraction of female B. correcta flies in the treated arm than the untreated arm of Y-shaped glass tube (χ2 = 8.23, P = .004) (Fig. 5B).
**
(B)
The response of female B. dorsalis and B. correcta to the mixture of 3carene + β-caryophyllene The female adults of B. dorsalis were remarkably attracted to the arm that contained the mixture of 3-carene + β-caryophyllene at 10% concentration (χ2 = 9.94, P = .002) than untreated arm (Fig. 6A). Similarly, the female adults of B. correcta had shown a strong preference to the arm that contained the mixture of 3-carene + β-caryophyllene at 10% concentration (χ2 = 5.88, P = .015) than untreated arm (Fig. 6B).
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The response of female B. dorsalis and B. correcta to the mixture of 3carene + α-humulene At 10% concentration, the female adults of B. dorsalis were remarkably more attracted to treated arm containing the mixture of 3carene + α-humulene (χ2 = 4.44, P = .035) than untreated arm (Fig. 7A). Similar trend was observed in female adults of B. correcta to the mixture of 3-carene + α-humulene at 10% concentration
Fig. 4. Attraction of B. dorsalis (A) and B. correcta (B) female flies to β-caryophyllene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
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(A)
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Fig. 6. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of 3-carene + β-caryophyllene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Fig. 7. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of 3-carene + α-humulene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
(χ2 = 5.40, P = .020) (Fig. 7B).
P < .001) (Fig. 10A). In the case of B. correcta, percentage attraction of females was similar at 10% concentration of individual component of 3-carene, βcaryophyllene and α-humulene and mixture of two (3-carene + βcaryophyllene, 3-carene + α-humulene, β-caryophyllene + α-humulene) and three volatiles components (3-carene + β-caryophyllene + α-humulene) (Fig. 10B).
The response of female B. dorsalis and B. correcta to the mixture of βcaryophyllene + α-humulene The mixture of β-caryophyllene + α-humulene at all concentrations had no significant attraction for female flies of B. dorsalis between the treated and untreated arm of Y-shaped tube (Fig. 8A). While, the mixture of β-caryophyllene + α-humulene at all concentrations e.g. 10% (χ2 = 11.52, P = .001), 5% (χ2 = 11.21, P = .001), and 1% (χ2 = 5.58, P = .018) had significantly higher attraction for female adults of B. correcta in the treated arm than untreated arm (Fig. 8B).
Comparative effect of volatile components and their mixtures at 5% to female flies of B. dorsalis and B. correcta Attraction (%) of female B. dorsalis was not influenced at 5% doses of all volatile and their combination (F6,49 = 8.02, P = .327) (Fig.11A). While, the attraction (%) of female B. correcta was remarkably higher at 5% concentration of mixture containing β-caryophyllene and α-humulene than those of other three volatile components, all mixtures of two and three volatile components (F2,15 = 3.62, P = .004) (Fig. 11B).
The response of female B. dorsalis and B. correcta to the mixture of 3carene + β-caryophyllene + α-humulene The mixture of three components e.g. 10% of 3-carene + β-caryophyllene + α-humulene had significantly attracted more female adults of B. dorsalis than untreated (χ2 = 7.66, P = .006) (Fig. 9A). The female adults of B. correcta were remarkably attracted to the 10% (χ2 = 6.91, P = .009) and 5% (χ2 = 4.91, P = .015) concentrations of 3-carene + β-caryophyllene + α-humulene (Fig. 9B).
Comparative effect of volatile components and their mixtures at 1% to female flies of B. dorsalis and B. correcta
Comparative effect of volatile components and their mixtures at 10% to female flies of B. dorsalis and B. correcta
The attraction (%) of female B. dorsalis was not influenced at 1% doses of all volatile and their combinations (F6,49 = 8.02, P = .245) (Fig. 12A). While, the attraction (%) of female B. correcta was remarkably higher at 1% concentration of mixture containing β-caryophyllene and α-humulene than individual components, all other mixtures of two and three volatile components) (F2,15 = 4.26, P = .002) (Fig. 12B).
The response (%) or attraction (%) of female B. dorsalis adults was remarkably higher to the 3-carene at 10% concentration than those of two other volatile components (β-caryophyllene and α-humulene) and mixture of two (3-carene + β-caryophyllene, 3-carene + α-humulene, β-caryophyllene + α-humulene), and mixture of three volatiles components (3-carene + β-caryophyllene + α-humulene) (F6,49 = 8.02, 762
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Fig. 9. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of 3-carene + β-caryophyllene + α-humulene in Y-tube olfactometer. The χ2test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Fig. 8. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of β-caryophyllene + α-humulene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Discussion
(A)
Attraction (%)
Previous studies have been concluded that Y-tube olfactometer is better to measure the short distance location of female adults of moths and fruit flies in comparison to other methods (Calatayud et al., 2014; Biasazin et al., 2018). Because, the orientation is a more discriminant in Y-tube olfactometer (Piñero and Dorn, 2007; Giunti et al., 2018). The ideal bait for Bactrocera flies' management programs would be (1) available naturally, and (2) highly specific attractive to the target species. Damodaram et al. (2015) have used the circular Perspex fourarm olfactometer and evaluated the effect of salicylic acid, the salicylic acid is responsible to induced tolerance in mango fruit that reduced oviposition of female B. dorsalis (Damodaram et al., 2015; Jayanthi et al., 2012). In this study, response (attraction) of both species to three volatile components and their mixtures was dose-dependent. 3-Carene is a strong attractant for female B. dorsalis (Jayanthi et al., 2014). This is corroborated by the work of Damodaram et al. (2015), in which mangoes treated with salicylic acid were not preferred by B. dorsalis females when compared with untreated mangoes. GC/MS analysis showed that the treated mangoes did not emit 3-carene. In this study, 3-carene was a more specific and stronger attractant for female flies of B. dorsalis than other two volatile components and their all possible mixture. Wee et al. (2018) have reported that β-caryophyllene (CAR) was more effective attractant against male adults of B. correcta. However, ‘there is no published record for attractant against female adults of B. correcta. In laboratory bioassays, the attractiveness of βcaryophyllene (CAR) and ME have shown that male B. correcta responded strongly to CAR at newly adults’ stage be compared to ME. The CAR male lure is more effective than ME for male adults of B. correcta, while field study has reported B. dorsalis male adults also attracted to CAR (Wee et al., 2018). In this study, female flies of B. correcta was more attracted to the mixtures of β-caryophyllene and α-humulene.
(B)
Volatile components and their combinations Fig. 10. Attraction (%) of (A) B. dorsalis (B) B. correcta to the 10% concentration of different volatile components. A: 3-carene, B: β-caryophyllene, C: αhumulene, A + B: 3-carene + β-caryophyllene, A + C: 3-carene + α-humulene, B + C: β-caryophyllene + α-humulene, A + B + C: 3-carene + β-caryophyllene + α-humulene. Different letters above each bar indicate significant differences in volatile treatments by Kruskal-Wallis one-way ANOVA, at P < .05, all-pairwise comparisons test of homogenous group.
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Attraction (%)
(A)
Both β-caryophyllene and α-humulene were detected in large quantities in the pheromone gland of some wild male adults of B. correcta (Tokushima et al., 2010; Tan et al., 2014). Liquid protein hydrolysatebased (torula yeast/borax slurry) has a strong attraction to catch both male and female adults of Zeugodacus cucurbitae (Coquillett) (Shelly and Manoukis, 2018). While B. dorsalis female adults gave a more positive response to 3-carene. In another study, 3-carene, 1-octen-3-ol, ethyl tiglate, and γ-octalactone have been reported as attractants for B. dorsalis females (Jayanthi et al., 2014). Female Bactrocera flies search different hosts by using odors that are elicited by host fruits. Most of volatile components from different hosts are specific to females in each Bactrocera species (Jayanthi et al., 2014). In most cases, a single volatile component is less attractive than blend or mixture of volatile components to Bactrocera flies (Biasazin et al., 2014; Malo et al., 2012), but not the same in all Bactrocera species (Biasazin et al., 2014; Malo et al., 2012). Jayanthi et al. (2014) have reported that 3-carene is more attractive and highly specific to female flies of B. dorsalis. Similarly, in this study, the mixture of volatile components was less attractive than a single volatile component e.g. 3carene. The mixture of linalool, β-caryophyllene, α-humulene, and αfarnesene are good attractant for female cabbage root fly (Kergunteuil et al., 2015). The female flies of B. tryoni were more attracted to the mixtures of ethyl acetate, ethyl butyrate, and ethyl propionate (Cunningham et al., 2016). Female flies of D. suzukii had shown strong attraction toward the mixture of acetic acid, ethanol, acetoin, and methional instead of individual volatile components (Cha et al., 2014). This suggests that wild males are ingesting, via pharmacophagy, the chemicals from natural plant sources. A field test showed that a mixture (1:1) of β-caryophyllene and α-humulene did captured B. correcta males, although in significantly smaller numbers than in traps baited with ME. However, Wee et al. (2018) showed field traps baited with βcaryophyllene captured only B. correcta in numbers much higher than those baited with ME. It is interesting to note that in both the field tests, not a single female of B correcta was captured. The (E)-2-hexenal is more attractive for female B. oleae than α-pinene, farnesene, xylene, and (Z)-9-tricosene as well as their mixtures (Malheiro et al., 2015). The mixture of limonene, myrcene, and α-humulene had been found strong attractant for the female flies of A. obliqua (Tosta et al., 2015). Similarly, in this study the mixture of β-caryophyllene and α-humulene are strong attractants for female adults of B. correcta. Based on the olfactometer experiments, this study concluded that all volatile components had significantly attracted female flies of B. dorsalis except α-humulene and its combination with β-caryophyllene. While all volatile components had significantly attracted the female flies of B. correcta. This study provides the initial basis for future studies related to usage of the attractants in field application for control of these Bactrocera pest species. Additionally, further chemo-ecological studies pertaining to the inter-relationship between the two Bactrocera species and their respective parasitoids are warranted to ascertain the roles of the semiochemicals in the natural ecosystems.
(B)
Volatile components and their combinations Fig. 11. Attraction (%) of (A) B. dorsalis (B) B. correcta to the 5% concentration of different volatile components. A: 3-carene, B: β-caryophyllene, C: α-humulene, A + B: 3-carene + β-caryophyllene, A + C: 3-carene + α-humulene, B + C: β-caryophyllene + α-humulene, A + B + C: 3-carene + β-caryophyllene + α-humulene. Different letters above each bar indicate significant differences in volatile treatments by Kruskal-Wallis one-way ANOVA, at P < .05, all-pairwise comparisons test of homogenous group.
Attraction (%)
(A)
(B)
Acknowledgment This research was supported by The National Science and Technology Pillar Program of China (2015BAD08B02). The National Key R and D Program of China (2017YFC1200600), Innovation Team of Modern Agricultural Industry Technology System of Guangdong Province (2018LM1078), and National Science and Technology Pillar Program during the Twelfth Five-year Plan Period (2015BAD08B02).
Volatile components and their combinations Fig. 12. Attraction (%) of (A) B. dorsalis (B) B. correcta to the 1% concentration of different volatile components. A: 3-carene, B: β-caryophyllene, C: α-humulene, A + B: 3-carene + β-caryophyllene, A + C: 3-carene + α-humulene, B + C: β-caryophyllene + α-humulene, A + B + C: 3-carene + β-caryophyllene + α-humulene. Different letters above each bar indicate significant differences in volatile treatments by Kruskal-Wallis one-way ANOVA, at P < .05, all-pairwise comparisons test of homogenous group.
Conflict of interests This manuscript has no conflict and has not been published or presented elsewhere in part or in entirety and is not under consideration by another journal. 764
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guava fruit fly, Bactrocera correcta, in mainland China. J. Pest. Sci. 86, 449–458. Macleod, A.J., de Troconis, N.G., 1982. Volatile flavour components of guava. Phytochem 21, 1339–1342. Malheiro, R., Ortiz, A., Casal, S., Baptista, P., Pereira, J.A., 2015. Electrophysiological response of Bactcera oleae (Rossi) (Diptera: Tephritidae) adults to olive leaves essential oils from different cultivars and olive tree volatiles. Ind. Crop. Prod. 77, 81–88. Malo, E.A., Gallegos Torres, I., Toledo, J., Valle Mora, J., Rojas, J.C., 2012. Attraction of the West Indian fruit fly to mango fruit volatiles. Entomol. Exp. Appl. 142, 45–52. Nishimura, O., Yamaguchi, K., Mihara, S., Shibamoto, T., 1989. Volatile constituents of guava fruits (Psidium guajava L.) and canned puree. J. Agri. Food Chem. 37, 139–142. Piñero, J.C., Dorn, S., 2007. Synergism between aromatic compounds and green leaf volatiles derived from the host plant underlies female attraction in the oriental fruit moth. Entomol. Exp. 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Full Length Article
The response of two Bactrocera species (Diptera: Tephritidae) to fruit volatiles
T
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Waqar Jaleela,b, Yurong Heb, , Lihua Lüa a
Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China Key Laboratory of Bio-pesticide Innovation and Application of Guangdong Province, Department of Entomology, College of Agriculture, South China Agricultural University, Guangzhou, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: 3-Carene β-Caryophyllene α-Humulene Bactrocera Olfactometer Female-biased attractant Volatile components
Bactrocera dorsalis and B. correcta are serious pests of agricultural fruit crops. Both species are widely distributed in tropical and subtropical countries, especially in Asia. For integrated management of both Bactrocera species, understanding their olfactory behavior is vital for designing reliable control strategies. In this study, the response of female B. dorsalis and B. correcta adults to three main volatile components of fruits was evaluated using the Ytube olfactometer. Our results showed that at higher concentrations all volatile components, except α-humulene and its combination with β-caryophyllene, attracted significantly more B. dorsalis than the untreated arm. For B. correcta, all the volatile components attracted significantly more females in the treated arm than the untreated arm. However, at 5% and 1% concentration, all the volatile components had similar attraction for B. dorsalis females. In the case of female B. correcta, the percentage of attraction was similar for all the individual volatile chemicals and their respective mixtures at 10% concentration. While, at 5% and 1% concentrations, the percentage of attraction was significantly higher for a mixture of β-caryophyllene and α-humulene than that of individual volatile components and all possible mixture of two and three volatile components. Based on the olfactometer results, this study concluded that 3-carene and the mixture of β-caryophyllene and α-humulene are strong attractants for female flies of B. dorsalis and B. correcta, respectively. This study might be helpful for the bait application against the female adults of B. dorsalis and B. correcta in farms and orchards.
Introduction The genus Bactrocera (Diptera: Tephritidae) contains 500 species, including many severe pests of fruits and vegetables, among them Bactrocera dorsalis (Hendel) and B. correcta (Bezzi) are most economic flies and infesting > 250 hosts (Allwood et al., 1999; Ekesi et al., 2016; Jaleel et al., 2018a, 2018b, 2018c; San Jose et al., 2013), and 90 host plants' families in the world (Allwood et al., 1999; Wee et al., 2018). Both the Bactrocera flies are considered invasive and quarantine fruits pest species because of their polyphagous nature and high dispersal abilities (Liu et al., 2013). The infestation in fruit crops caused by B. dorsalis has been recorded up to 7.5% economic injury level at the time of harvest of carambola (star fruit) (Jiang et al., 2017). The B. correcta (the guava fruit fly) is the 2nd most important pest of fruit crops after B. dorsalis (Tan et al., 2011; Wee et al., 2018; White and Elson-Harris, 1992). And in 2009, the B. correcta was reported in Yuanjiang, Yunnan, China (Liu and Ye, 2009). The B. correcta was recorded as a serious pest of guava and mango fruit in Pakistan, India, Nepal, Myanmar, Thailand,
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Sri Lanka, Vietnam, and China (Liu et al., 2013). The environmentally safe control method of Bactrocera species is the application of phytochemical in farms and orchards, that relies almost exclusively on the attractiveness of the flies to chemical lures (Tan et al., 2014). Females of Bactrocera dorsalis and its sibling species are attracted to the sex pheromone released by conspecific males that have fed on methyl eugenol (ME) leading to significantly improved mating successes (Tan and Nishida, 1996; Shell, 2010). The ME is found in over 450 plant species including Bulbophyllum orchid species that release ME as floral synomone to entice fruit fly pollinators (Tan and Nishida, 2012). Even B. dorsalis males had increased mating success after feeding on the golden shower blossom of Cassia fistula that has very low MEcontent (Shelly, 2000). Jang et al. (2017) have reported the effectiveness of synthetic cucumber lure that increased female-biased sex ratios in trap captures firstly in Taiwanese and then in Hawaiian field trials. Majority of phytochemicals as attractants are specific for specific species of Bactrocera flies (Jang and Light, 1991; Tan et al., 2014). Several control methods have been associated with male Bactrocera flies
Corresponding author. E-mail address: [email protected] (Y. He).
https://doi.org/10.1016/j.aspen.2019.05.011 Received 5 May 2018; Received in revised form 27 May 2019; Accepted 30 May 2019 Available online 31 May 2019 1226-8615/ © 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
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21 cm
OS
OS
10 cm
W
W
Direction of air flow
A
A
F
F
M
M
21 cm Charcoal Charcoal Insect Entry Hole
Air Inlet
Air Inlet
Fig. 1. Schematic diagram of the Y-tube olfactometer (OS: odor source, W: water for maintaining humidity, AFM: air flow meter, dotted lines represent Teflon hoses).
together with α-humulene in the male pheromone gland of wild B. correcta (Tokushima et al., 2010: Tan et al., 2011, 2014). Chrysopa carnea Stephens was monitored and captured in a trap containing 2 g of β-caryophyllene (Flint et al., 1981). β-Caryophyllene has been tested to attract female flies of C. capitate (Eyles et al., 1999). The α-humulene is the major volatile component in mango and guava fruits. It has been used to capture the Bactrocera flies (Nishimura et al., 1989; Salazar Sandoval et al., 2007; Tamura et al., 2000). 3-Carene is a monoterpene can be extracted from the plant sources (Jayanthi et al., 2012; Sharath et al., 2015). 3-Carene is an important volatile component in the odor of mango that has been used as attractants for female B. dorsalis (Damodaram et al., 2015; Jayanthi et al., 2012). Acanthocinus obliquus (LeConte) and Acmaeops proteus (Kirby) have been trapped by bait containing 3-carene (Costello et al., 2014). Similarly, bark beetle (Tomicus piniperda) is also attracted to the bait containing 3-carene (Schlyter et al., 2000). Behavioral responses of different Bactrocera species to volatiles in the laboratory have been reported using Y-tube assay, which allows screening of plant volatiles in short range and efficient way (Ballhorn and Kautz, 2013; Canale et al., 2015; Giunti et al., 2018; Holtmann, 1962; Teulon et al., 1993). However, there is no detailed information regarding female biased attractants for B. correcta flies were provided elsewhere. Considering the importance female biased attractants, this
(Alagarmalai et al., 2009; Suckling et al., 2016). Previous studies have been conducted to capture the male adults of B. dorsalis, Ceratitis capitata Wiedemann, B. correcta, and Anastrepha flies by the application traps containing ME, trimedlure, β-caryophyllene, and CeraTrap® respectively (Qin et al., 2015; Suckling et al., 2016; Villalobos et al., 2017; Wee et al., 2018; Weems et al., 2001). Female Bactrocera flies search different hosts by using odors that are elicited by fruits. The female flies of B. dorsalis have been captured using host plant odors e.g. fruits, leaves, and twigs (Siderhurst and Jang, 2010). The female flies of B. dorsalis are strongly attracted to ethanol, ethyl acetate, ethyl hexanoate, hexyl acetate, linalyl acetate, ethyl nonate, nonyl acetate, ethyl cinnamate, and (E)-β-farnesene in comparison to male adults, when using olfactometer tests (Siderhurst and Jang, 2006, 2010). However, a female-biased trapping system is assumed to be more effective than mass-trapping of males, because the former reduces fruit damage by preventing oviposition (Jang, 2002; Jang and Light, 1991; Siderhurst and Jang, 2010). Usually, the single volatile is less attractive than the mixture of volatile components, but not the same in all Bactrocera flies (Biasazin et al., 2014; Malo et al., 2012). A major sesquiterpene is β-caryophyllene and present in various ripen fruits as volatile constitute especially in guava fruit (Macleod and de Troconis, 1982). β-Caryophyllene as an attractant has been studied in various insect pests, although detected in relatively large quantities 759
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Statistical analysis
study explains the olfactory response of female B. dorsalis and B. correcta flies to three volatile components, 3-carene, β-caryophyllene, and α-humulene using the Y-tube olfactometer.
The difference between the two treatments was analyzed by Chisquared (χ2) test in SPSS Statistics 15.0 (SPSS Inc., Chicago, IL, USA) with the expected value (α = 0.05). Non-responder females were not included in statistical analysis. Female flies of Bactrocera species response to treatments (at each concentration), summarized as the percentage of female flies of Bactrocera species attracted into the treated arm (the number of Bactrocera flies attracted in the treated arm divided by the total number Bactrocera species flies in both treated and untreated arm). There were seven treatments as (1) 3-carene, (2) β-caryophyllene, (3) α-humulene (4) 3-carene + β-caryophyllene, (5) 3-carene + α-humulene, (6) βcaryophyllene + α-humulene (7) 3-carene + β-caryophyllene + αhumulene. The difference among 7 treatments at each dose was analyzed separately by using the Kruskal-Wallis one-way ANOVA, at P < .05, allpairwise comparisons test of the homogenous group in SPSS Statistics 15.0 (SPSS Inc., Chicago, IL, USA).
Materials and methods Insect The population of both species e.g. B. dorsalis and B. correcta was reared in the controlled room (25 ± 2 °C, 60–65% relative humidity, and a photoperiod of L:D 14:10 h) at the College of Agriculture, South China Agricultural University, Guangzhou, China. The temperature was controlled by the air-conditioner (Gree Electric Appliances, Inc. of Zhuhai, Zhuhai, China) and the humidity was maintained by the humidifier. Adult flies were reared in cages (30 × 30 × 30 cm) by providing water-soaked cotton wool in a box (12 × 6.8 × 7 cm), powdered yeast and sugar (2:1) in a petri-dish (6 × 1.5 cm). Larvae were reared on semi-artificial diet described by Jaleel et al. (2018a, 2018b, 2018c). Gravid female adults of B. dorsalis and B. correcta (15–18 days old) were used for all behavioral assays.
Results Olfactometer bioassay Effect of volatile components to the response of B. dorsalis and B. correcta The behavioral responses of female adults of B. dorsalis and B. correcta to the volatile components were observed in a Y-tube olfactometer. The Y-shaped glass tube olfactometer with entry arm of 16 cm and two side arms of 21.00 cm, each 2.5 cm in diameter. Activated charcoal-filtered and humidified air were pumped inside the olfactometer arms. The airflow was set to 0.5 l min−1 and passed through Teflon tubes that were joined to each arm. The Y-tube was placed inside a box of white fabric, to avoid the visual distraction of the flies (Fig. 1). Volatile components e.g. 3-carene (90%), β-caryophyllene (≥ 80%, FCC, FG), and α-humulene (≥ 96.0% (GC) were purchased from Alfa Aesar, Beijing, China. Structural formulae are in Fig. 2. Seven treatments were made (1) 3-carene, (2) β-caryophyllene, (3) α-humulene (4) 3-carene + β-caryophyllene, (5) 3-carene + α-humulene, (6) β-caryophyllene + α-humulene (7) 3-carene + β-caryophyllene + α-humulene. Three different concentrations e.g. 10%, 5%, and 1% (v/v) were prepared in acetone (75%) for each treatment. Mixture of volatile compounds are prepared in ratios of 1:1 (v/v) and 1:1:1 (v/v/v) for a mixture of two and three chemicals, respectively. Each treatment in one arm was compared to control arm that contained only acetone. For this experiment, 100 μl of each solution of treatment was applied to a piece of filter paper (2.0 × 0.5 cm) and placed on a small glass holder at the air entrance of the Y-tube. A total of 80 flies of each species were selected and used per treatment. Bactrocera flies that did not move within 15 min were considered as non-responders. After the test of 5 flies, the Y-tube or odor sources were switched to avoid contamination by Bactrocera flies or test odor. Tubes were washed with 95% alcohol and placed in an oven at 250 °C for 30 min. Experiment proceeded on with new odor sources, clean tubes and female Bactrocera flies. Each female Bactrocera fly was used only once. Each experiment was replicated eight times.
All three factors, Bactrocera species, volatile components, concentrations, and the interactions between Bactrocera species and volatile components had significantly influenced the response. While the remaining all possible interactions e.g. interactions between (1) Bactrocera species and concentrations, (2) volatile components and concentration, and as well as interaction among Bactrocera species, volatile components, concentrations had no significant effects in the response to the volatile components (Table 1). The response of female B. dorsalis and B. correcta to 3-carene The 10% concentration of 3-carene was more attractive for the female flies of B. dorsalis in the treated arm than the untreated arm of Ytube olfactometer (χ2 = 15.78, P < .001) (Fig. 3A). While at 5% and 1% concentrations of 3-carene had no significant difference in B. dorsalis females' response between treated and untreated arms (Fig. 3A). More B. correcta females were attracted to the odor of 3-carene at 10% concentration (χ2 = 8.39, P = .004) than in the untreated arm. There was no significant effect of 3-carene at 5% and 1% concentrations to the response of female B. correcta flies between the treated arm and untreated arm (Fig. 3B). The response of female B. dorsalis and B. correcta to β-caryophyllene The female flies of B. dorsalis remarkably attracted more to arm contained β-caryophyllene (10%) than the untreated arm of the Yshaped glass tube (χ2 = 6.25, P = .012) (Fig. 4A). There was no significant attraction for the female flies of B. dorsalis at 5% and 1% Table 1 Three-factors ANOVA statistics for analyzing the % response of female B. dorsalis and B. correcta adults to volatile components.
Fig. 2. Structures of three volatile components.
Indexes
Factors
df
F
P
Response
a b c a*b a*c b*c a*b*c
1294 6294 2294 6294 2294 12,294 12,294
25.11 2.85 88.14 10.65 2.81 1.73 0.54
< 0.001 0.010 < 0.001 < 0.001 0.061 0.060 0.890
a: Bactrocera species; b: volatile components; c; concentrations. 760
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***
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Fig. 3. Attraction of B. dorsalis (A) and B. correcta (B) female flies to 3-carene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Fig. 5. Attraction of B. dorsalis (A) and B. correcta (B) female flies to α-humulene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
(A)
concentrations of β-caryophyllene between the treated and untreated arm (Fig. 4A). The 10% (χ2 = 6.25, P = .005) and 5% (χ2 = 6.25, P = .027) concentration of β-caryophyllene had remarkably attracts the female responders of B. correcta in treated arm as compare to their respective untreated arm (Fig. 4B). The response of female B. dorsalis and B. correcta to α-humulene There were no significant effects of α-humulene at all concentrations (10%, 5%, and 1%) to the female adults of B. dorsalis between the treated and untreated arm (Fig. 5A). While, the 10% concentration of αhumulene had the higher attraction of female B. correcta flies in the treated arm than the untreated arm of Y-shaped glass tube (χ2 = 8.23, P = .004) (Fig. 5B).
**
(B)
The response of female B. dorsalis and B. correcta to the mixture of 3carene + β-caryophyllene The female adults of B. dorsalis were remarkably attracted to the arm that contained the mixture of 3-carene + β-caryophyllene at 10% concentration (χ2 = 9.94, P = .002) than untreated arm (Fig. 6A). Similarly, the female adults of B. correcta had shown a strong preference to the arm that contained the mixture of 3-carene + β-caryophyllene at 10% concentration (χ2 = 5.88, P = .015) than untreated arm (Fig. 6B).
**
**
The response of female B. dorsalis and B. correcta to the mixture of 3carene + α-humulene At 10% concentration, the female adults of B. dorsalis were remarkably more attracted to treated arm containing the mixture of 3carene + α-humulene (χ2 = 4.44, P = .035) than untreated arm (Fig. 7A). Similar trend was observed in female adults of B. correcta to the mixture of 3-carene + α-humulene at 10% concentration
Fig. 4. Attraction of B. dorsalis (A) and B. correcta (B) female flies to β-caryophyllene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
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(A)
(A)
**
**
(B)
(B)
**
**
Fig. 6. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of 3-carene + β-caryophyllene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Fig. 7. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of 3-carene + α-humulene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
(χ2 = 5.40, P = .020) (Fig. 7B).
P < .001) (Fig. 10A). In the case of B. correcta, percentage attraction of females was similar at 10% concentration of individual component of 3-carene, βcaryophyllene and α-humulene and mixture of two (3-carene + βcaryophyllene, 3-carene + α-humulene, β-caryophyllene + α-humulene) and three volatiles components (3-carene + β-caryophyllene + α-humulene) (Fig. 10B).
The response of female B. dorsalis and B. correcta to the mixture of βcaryophyllene + α-humulene The mixture of β-caryophyllene + α-humulene at all concentrations had no significant attraction for female flies of B. dorsalis between the treated and untreated arm of Y-shaped tube (Fig. 8A). While, the mixture of β-caryophyllene + α-humulene at all concentrations e.g. 10% (χ2 = 11.52, P = .001), 5% (χ2 = 11.21, P = .001), and 1% (χ2 = 5.58, P = .018) had significantly higher attraction for female adults of B. correcta in the treated arm than untreated arm (Fig. 8B).
Comparative effect of volatile components and their mixtures at 5% to female flies of B. dorsalis and B. correcta Attraction (%) of female B. dorsalis was not influenced at 5% doses of all volatile and their combination (F6,49 = 8.02, P = .327) (Fig.11A). While, the attraction (%) of female B. correcta was remarkably higher at 5% concentration of mixture containing β-caryophyllene and α-humulene than those of other three volatile components, all mixtures of two and three volatile components (F2,15 = 3.62, P = .004) (Fig. 11B).
The response of female B. dorsalis and B. correcta to the mixture of 3carene + β-caryophyllene + α-humulene The mixture of three components e.g. 10% of 3-carene + β-caryophyllene + α-humulene had significantly attracted more female adults of B. dorsalis than untreated (χ2 = 7.66, P = .006) (Fig. 9A). The female adults of B. correcta were remarkably attracted to the 10% (χ2 = 6.91, P = .009) and 5% (χ2 = 4.91, P = .015) concentrations of 3-carene + β-caryophyllene + α-humulene (Fig. 9B).
Comparative effect of volatile components and their mixtures at 1% to female flies of B. dorsalis and B. correcta
Comparative effect of volatile components and their mixtures at 10% to female flies of B. dorsalis and B. correcta
The attraction (%) of female B. dorsalis was not influenced at 1% doses of all volatile and their combinations (F6,49 = 8.02, P = .245) (Fig. 12A). While, the attraction (%) of female B. correcta was remarkably higher at 1% concentration of mixture containing β-caryophyllene and α-humulene than individual components, all other mixtures of two and three volatile components) (F2,15 = 4.26, P = .002) (Fig. 12B).
The response (%) or attraction (%) of female B. dorsalis adults was remarkably higher to the 3-carene at 10% concentration than those of two other volatile components (β-caryophyllene and α-humulene) and mixture of two (3-carene + β-caryophyllene, 3-carene + α-humulene, β-caryophyllene + α-humulene), and mixture of three volatiles components (3-carene + β-caryophyllene + α-humulene) (F6,49 = 8.02, 762
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(A)
**
(B)
(B)
**
***
**
**
**
Fig. 9. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of 3-carene + β-caryophyllene + α-humulene in Y-tube olfactometer. The χ2test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Fig. 8. Attraction of B. dorsalis (A) and B. correcta (B) female flies to the mixture of β-caryophyllene + α-humulene in Y-tube olfactometer. The χ2-test was used to compare the difference between treated and untreated arm for each concentration of volatile components (***: P < .001, **: P < .01, n = 80).
Discussion
(A)
Attraction (%)
Previous studies have been concluded that Y-tube olfactometer is better to measure the short distance location of female adults of moths and fruit flies in comparison to other methods (Calatayud et al., 2014; Biasazin et al., 2018). Because, the orientation is a more discriminant in Y-tube olfactometer (Piñero and Dorn, 2007; Giunti et al., 2018). The ideal bait for Bactrocera flies' management programs would be (1) available naturally, and (2) highly specific attractive to the target species. Damodaram et al. (2015) have used the circular Perspex fourarm olfactometer and evaluated the effect of salicylic acid, the salicylic acid is responsible to induced tolerance in mango fruit that reduced oviposition of female B. dorsalis (Damodaram et al., 2015; Jayanthi et al., 2012). In this study, response (attraction) of both species to three volatile components and their mixtures was dose-dependent. 3-Carene is a strong attractant for female B. dorsalis (Jayanthi et al., 2014). This is corroborated by the work of Damodaram et al. (2015), in which mangoes treated with salicylic acid were not preferred by B. dorsalis females when compared with untreated mangoes. GC/MS analysis showed that the treated mangoes did not emit 3-carene. In this study, 3-carene was a more specific and stronger attractant for female flies of B. dorsalis than other two volatile components and their all possible mixture. Wee et al. (2018) have reported that β-caryophyllene (CAR) was more effective attractant against male adults of B. correcta. However, ‘there is no published record for attractant against female adults of B. correcta. In laboratory bioassays, the attractiveness of βcaryophyllene (CAR) and ME have shown that male B. correcta responded strongly to CAR at newly adults’ stage be compared to ME. The CAR male lure is more effective than ME for male adults of B. correcta, while field study has reported B. dorsalis male adults also attracted to CAR (Wee et al., 2018). In this study, female flies of B. correcta was more attracted to the mixtures of β-caryophyllene and α-humulene.
(B)
Volatile components and their combinations Fig. 10. Attraction (%) of (A) B. dorsalis (B) B. correcta to the 10% concentration of different volatile components. A: 3-carene, B: β-caryophyllene, C: αhumulene, A + B: 3-carene + β-caryophyllene, A + C: 3-carene + α-humulene, B + C: β-caryophyllene + α-humulene, A + B + C: 3-carene + β-caryophyllene + α-humulene. Different letters above each bar indicate significant differences in volatile treatments by Kruskal-Wallis one-way ANOVA, at P < .05, all-pairwise comparisons test of homogenous group.
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Attraction (%)
(A)
Both β-caryophyllene and α-humulene were detected in large quantities in the pheromone gland of some wild male adults of B. correcta (Tokushima et al., 2010; Tan et al., 2014). Liquid protein hydrolysatebased (torula yeast/borax slurry) has a strong attraction to catch both male and female adults of Zeugodacus cucurbitae (Coquillett) (Shelly and Manoukis, 2018). While B. dorsalis female adults gave a more positive response to 3-carene. In another study, 3-carene, 1-octen-3-ol, ethyl tiglate, and γ-octalactone have been reported as attractants for B. dorsalis females (Jayanthi et al., 2014). Female Bactrocera flies search different hosts by using odors that are elicited by host fruits. Most of volatile components from different hosts are specific to females in each Bactrocera species (Jayanthi et al., 2014). In most cases, a single volatile component is less attractive than blend or mixture of volatile components to Bactrocera flies (Biasazin et al., 2014; Malo et al., 2012), but not the same in all Bactrocera species (Biasazin et al., 2014; Malo et al., 2012). Jayanthi et al. (2014) have reported that 3-carene is more attractive and highly specific to female flies of B. dorsalis. Similarly, in this study, the mixture of volatile components was less attractive than a single volatile component e.g. 3carene. The mixture of linalool, β-caryophyllene, α-humulene, and αfarnesene are good attractant for female cabbage root fly (Kergunteuil et al., 2015). The female flies of B. tryoni were more attracted to the mixtures of ethyl acetate, ethyl butyrate, and ethyl propionate (Cunningham et al., 2016). Female flies of D. suzukii had shown strong attraction toward the mixture of acetic acid, ethanol, acetoin, and methional instead of individual volatile components (Cha et al., 2014). This suggests that wild males are ingesting, via pharmacophagy, the chemicals from natural plant sources. A field test showed that a mixture (1:1) of β-caryophyllene and α-humulene did captured B. correcta males, although in significantly smaller numbers than in traps baited with ME. However, Wee et al. (2018) showed field traps baited with βcaryophyllene captured only B. correcta in numbers much higher than those baited with ME. It is interesting to note that in both the field tests, not a single female of B correcta was captured. The (E)-2-hexenal is more attractive for female B. oleae than α-pinene, farnesene, xylene, and (Z)-9-tricosene as well as their mixtures (Malheiro et al., 2015). The mixture of limonene, myrcene, and α-humulene had been found strong attractant for the female flies of A. obliqua (Tosta et al., 2015). Similarly, in this study the mixture of β-caryophyllene and α-humulene are strong attractants for female adults of B. correcta. Based on the olfactometer experiments, this study concluded that all volatile components had significantly attracted female flies of B. dorsalis except α-humulene and its combination with β-caryophyllene. While all volatile components had significantly attracted the female flies of B. correcta. This study provides the initial basis for future studies related to usage of the attractants in field application for control of these Bactrocera pest species. Additionally, further chemo-ecological studies pertaining to the inter-relationship between the two Bactrocera species and their respective parasitoids are warranted to ascertain the roles of the semiochemicals in the natural ecosystems.
(B)
Volatile components and their combinations Fig. 11. Attraction (%) of (A) B. dorsalis (B) B. correcta to the 5% concentration of different volatile components. A: 3-carene, B: β-caryophyllene, C: α-humulene, A + B: 3-carene + β-caryophyllene, A + C: 3-carene + α-humulene, B + C: β-caryophyllene + α-humulene, A + B + C: 3-carene + β-caryophyllene + α-humulene. Different letters above each bar indicate significant differences in volatile treatments by Kruskal-Wallis one-way ANOVA, at P < .05, all-pairwise comparisons test of homogenous group.
Attraction (%)
(A)
(B)
Acknowledgment This research was supported by The National Science and Technology Pillar Program of China (2015BAD08B02). The National Key R and D Program of China (2017YFC1200600), Innovation Team of Modern Agricultural Industry Technology System of Guangdong Province (2018LM1078), and National Science and Technology Pillar Program during the Twelfth Five-year Plan Period (2015BAD08B02).
Volatile components and their combinations Fig. 12. Attraction (%) of (A) B. dorsalis (B) B. correcta to the 1% concentration of different volatile components. A: 3-carene, B: β-caryophyllene, C: α-humulene, A + B: 3-carene + β-caryophyllene, A + C: 3-carene + α-humulene, B + C: β-caryophyllene + α-humulene, A + B + C: 3-carene + β-caryophyllene + α-humulene. Different letters above each bar indicate significant differences in volatile treatments by Kruskal-Wallis one-way ANOVA, at P < .05, all-pairwise comparisons test of homogenous group.
Conflict of interests This manuscript has no conflict and has not been published or presented elsewhere in part or in entirety and is not under consideration by another journal. 764
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