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A Multiple-Choice Bioassay Approach for Rapid Screening of Key Attractant Volatiles

A Multiple-Choice Bioassay Approach for Rapid Screening of Key Attractant Volatiles Fermentation volatiles attract a wide variety of insects and are used for integrated pest management. However, identification of the key behavior modifying chemicals has often been challenging due to the time consuming nature of thorough behavioral tests and unexpected discrepancies between laboratory and field results. Thus we report on a multiple-choice bioassay approach that may expedite the process of identifying field-worthy attractants in the laboratory. We revisited the four-component key chemical blend (acetic acid, ethanol, acetoin, and methionol) identified from 12 antennally active wine and vinegar chemicals for Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). The identification of this blend took 2 yr of continuous laboratory two-choice assays and then similarly designed field trials. This delay was mainly due to a discrepancy between laboratory and field results that laboratory two-choice assay failed to identify methionol as an attractant component. Using a multiple-choice approach, we compared the co-attractiveness of the 12 potential attractants to an acetic acid plus ethanol mixture, known as the basal attractant for D. suzukii, and found similar results as the previous field trials. Only two compounds, acetoin and, importantly, methionol, increased attraction to a mixture of acetic acid and ethanol, suggesting the identification of the four-component blend could have been expedited. Interestingly, the co-attractiveness of some of the 12 individual compounds, including a key attractant, methionol, appears to change when they were tested under different background odor environments, suggesting that background odor can influence detection of potential attractants. Our findings provide a potentially useful approach to efficiently identify behaviorally bioactive fermentation chemicals. Key words: fermentation volatile, bioassay, background odor, attractant, spotted wing drosophila Fermentation volatiles produced by yeasts and acetic acid bacteria developed based on fermentation bait volatiles and are currently can attract a wide variety of insects and have been extensively used being widely used. Despite the large potential benefits, however, the to manipulate insect pest behavior for integrated pest management, tedious and time-consuming nature of behavioral tests (Turlings including various species of beetles (Nout and Bartelt 1998), flies et al. 2004), the lack of clarity in choosing different behavioral test- (Lee et al. 2012; Landolt et al 2015; Cha et al. 2016b, 2018), moths ing protocols (e.g., subtraction vs. addition approaches; Linn et al. (Yamazaki 1998, Sussenbach and Fiedler 1999, Laaksonen et  al. 1984), and the unexpected discrepancies in behavioral responses 2006, Pettersson and Franzén 2008) and vespid wasps (Dvorak and from laboratory and field experiments ( Knudsen et  al. 2008) have Landolt 2006, Noll and Gomes 2009, De Souza et al. 2011, Landolt often slowed the process of identifying key attractant components et al. 2014a,b). and the development of a synthetic lure. Therefore, a straightfor- The implementation of management program often favors using ward behavioral testing method that can be conducted in a relatively synthetic chemical attractants over bait materials, as a well-char- simple laboratory setting and at the same time generate field-worthy acterized chemical lure composed of essential attractant compo- results would facilitate the development of effective attractant lures. nents may be easier to deploy, longer lasting, and more selective Recently a chemical lure composed of acetic acid, ethanol, ace- than fermentation baits (e.g., Cha et al. 2015). For example, chem- toin and methionol was isolated, identified, optimized and com - ical lures for Vespula spp. (Landolt 1998) and Drosophila suzukii mercialized from a fermentation bait for D.  suzukii (Cha et  al. (Matsumura) (Diptera: Drosophilidae) (Cha et al. 2014) have been 2012, 2014, 2017, 2018), which is more efficient and selective Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. 946 Downloaded from https://academic.oup.com/ee/article/47/4/946/4970129 by DeepDyve user on 13 July 2022 Environmental Entomology, 2018, Vol. 47, No. 4 947 than the original material of a wine plus vinegar mixture (Cha Here, we report on a simple laboratory multiple-choice assay et al. 2013, 2015). However, the lure development was slow, tak- approach that uses a mixture of acetic acid and ethanol as a basal ing more than 2 yr of continuous laboratory two-choice assays attractant and tests co-attractiveness of all of the individual EAD- and field-trapping experiments in multiple locations, even after active compounds separately but concurrently. The new assay was 12 candidate attractant chemicals were determined using gas conducted by revisiting the 12 EAD-active wine and vinegar chem- chromatography-electroantennographic detection (GC-EAD). One icals involved in the development of the four-component chem- of the major reasons behind the delay was discrepancies in behav- ical lure for D.  suzukii. In the multiple-choice assay, all of the 12 ioral testing results between laboratory choice assays (Cha et  al. EAD-active compounds were available to SWD to respond to in 2012) and field trapping experiments ( Cha et al. 2014; summarized the headspace inside the cage, but released from separate individ- in Table  1). The co-attractiveness (Meagher and Landolt 2008, ual traps with acetic acid and ethanol as a basal attractant. This Landolt et al. 2014a,b) of some of the 12 EAD-active compounds laboratory assay allowed us to quickly predict which compounds to a mixture of acetic acid and ethanol were different in laboratory would be co-attractive with acetic acid plus ethanol for SWD in and field, resulting in different blend compositions that resulted the field, which was essential to achieve the same level of attraction in different attractiveness in the field. The discrepancy could have from D. suzukii to the original benchmarking mixture of wine and been due to the differences in background odor available in two- vinegar. choice laboratory assays versus field trapping experiments ( Cha et al. 2014). As the 12 EAD-active compounds were ubiquitous fer- mentation volatiles, field sites may have had a mixture of these 12 Materials and Methods compounds and even other volatile compounds in the background, Insects released from various materials including fermenting SWD host For multiple-choice bioassays, a colony of SWD was maintained at fruits, while in laboratory only the chemicals tested in a specific the New York State Agricultural Experiment Station, Geneva, New two-choice assay were present as the background. York. Flies were reared at 21.5 ± 0.9°C, 23.7 ± 0.1 % RH, 16:8 (L:D) The two major fermentation volatiles, acetic acid and ethanol, h on standard cornmeal diet (1 liter distilled water, 40  g sucrose, have been shown to be involved in insect attraction to fermentation 25 g cornmeal [Quaker Oats Co., Chicago, IL], 9 g agar [No. 7060, sources as individual compounds or as a mixture. In some cases, Bioserve, Flemington, NJ], 14  g torula yeast [No. 1720, Bioserve], a mixture of acetic acid and ethanol was sufficiently attractive to 3 ml glacial acetic acid [Amresco, Solon, OH], 0.6 g methyl paraben explain such attraction, while in other cases additional fermenta- [No 7685, Bioserve], and 6.7 ml ethanol). tion volatiles in addition to acetic acid and ethanol were necessary. For example, a mixture of acetic acid and ethanol was as attractive Chemicals as the original material of yeast-sugar fermenting solution for an avian parasitic fly, Philornis downsii (Cha et al. 2016) or as a wine For this study, we used the 12 EAD-active chemicals (Table  1) plus vinegar bait for false stable flies ( Landolt et al. 2015). In con- that were previously identified from a Merlot wine and a rice trast, in other insects such as D. suzukii, although ethanol and acetic vinegar mixture (Cha et  al. 2012). Ethyl butyrate (99%, CAS acid were essential for the attraction, additional fermentation vola- No. 105-54-4), 3-hydroxybutan-2-one (acetoin) (≥96%, CAS tiles were necessary to achieve the similar level of attraction to the No. 513-86-0), 3-methylbutyl acetate (isoamyl acetate) (98%, original fermentation material (Landolt et al. 2012b). In particular, CAS No. 123-92-2), 2-methylbutyl acetate (99%, CAS No. 624- acetic acid + ethanol was more attractive than either chemical alone 41-9), 3-methylsulfanylpropan-1-ol (methionol) (≥98%, CAS (Landolt et al. 2012a) but less attractive than a mixture of wine and No. 505-10-2), ethyl (2E,4E)-hexa-2,4-dienoate (ethyl sorbate) vinegar that contained the same amount of acetic acid and ethanol, (≥97%, CAS No. 2396-84-1), and 2-phenylethanol (≥99%, CAS suggesting that SWD are responding to some other wine and vinegar No. 60-12-8) were purchased from Sigma-Aldrich (St. Louis, chemicals (Landolt et al. 2012b). MO). Ethyl 2-hydroxypropionate (ethyl lactate) (>97%, CAS No. Table 1. Comparison of co-attractiveness of D. suzukii candidate attractants with acetic acid (AA) and ethanol (EtOH) in 1) a laboratory two- choice experiment (AA + EtOH vs. AA + EtOH + one of the candidate attractant; Cha et al. 2012), 2) a field ‘add-on’ test (AA + EtOH vs. AA + EtOH + one of the candidate attractants; Cha et al. 2014), and 3) multiple-choice assay conducted in this study Candidate co-attractant (SWD antennally active yeast chemicals) Laboratory two-choice test Field add-on test Multi-choice test 3-hydroxy butan-2-one (acetoin)* Positive Positive Positive 3-methylsulfanylpropan-1-ol (methionol)* Neutral Positive Positive Ethyl 2-hydroxypropionate (Ethyl lactate) Negative Positive Neutral 2-methylbutyl acetate Negative Neutral Negative Ethyl (2E,4E)-hexa-2,4-dienoate (Ethyl sorbate) Negative Neutral Neutral 3-methylbutyl 2-hydroxypropionate (Isoamyl lactate) Neutral Negative Neutral Ethyl 3-hydroxybutyrate (Grape butyrate) Neutral Neutral Neutral 2-phenylethanol Neutral Neutral Neutral Diethyl butanedioate (Diethyl succinate) Neutral Neutral Neutral Ethyl butyrate Negative Negative Negative 1-hexanol Negative Negative Negative 3-methylbutyl acetate (Isoamyl acetate) Negative Negative Negative Positive indicates that the compound added attractiveness to AA + EtOH (P < 0.05), negative decreased the attractiveness (P < 0.05), and neutral had no effect (P > 0.05) based on Tukey-Kramer tests (Cha et al. 2012, 2014 and Fig 1). *(bold) indicates two key chemicals in the four-component essential blend (acetic acid, ethanol, acetoin and methionol). Downloaded from https://academic.oup.com/ee/article/47/4/946/4970129 by DeepDyve user on 13 July 2022 948 Environmental Entomology, 2018, Vol. 47, No. 4 97-64-3), 3-methylbutyl 2-hydroxypropionate (isoamyl lactate) Results (>98%, CAS No. 19329-89-6), and diethyl butanedioate (diethyl The results from the laboratory multiple-choice test showed that succinate) (>99%, CAS No. 123-25-1) were purchased from TCI two compounds, acetoin and methionol, were co-attractive with a America (Morris, Portland, OR). Ethyl 3-hydroxybutyrate (grape mixture of acetic acid and ethanol (basal attractant), significantly butyrate) (99%, CAS No. 5405-41-4) was purchased from Arcos increasing the number of D.  suzukii trapped by 4.5- and 2.6-fold, Organics (New Jersey). Ethanol (200 proof, CAS No. 64-47-5), respectively, compared to the control traps baited with the mixture acetic acid (99.8%, CAS No. 64-19-7), and 1-hexanol (>95%, of acetic acid and ethanol (F  = 37.81, P < 0.0001; Fig. 1). 12,48 CAS No. 111-27-3) were purchased from Pharmco (Brookfield, In each experiment listed in Table  1, an EAD-active compound CT), Fisher Scientific (Pittsburgh, PA, USA), and J.  T. Baker was indicated ‘positive’ (i.e., co-attractive) when adding the com- (Philipsburg, NJ), respectively. pound to the mixture of 1.6% acetic acid and 7.2% ethanol resulted in a significant increase in D.  suzukii trap catches (P  <  0.05; Cha Multiple-Choice Assay et al. 2012, 2014 and Fig. 1) compared to the acetic acid and etha- The multiple choice assay (N  =  5) was conducted with an arena nol mixture, ‘neutral’ when adding the compound did not influence design using a dome cage (60  cm W × 60  cm L × 60  cm H; trap catches (P > 0.05; Cha et al. 2012, 2014 and Fig. 1), and ‘nega- BugDorm-2120 Insect tent; shop.bugdorm.com). Within each arena, tive’ (i.e., antagonistic) when the compound significantly decreased 13 traps were positioned in a circle (20 cm diameter) at equal dis- D. suzukii trap catches (P < 0.05; Cha et al. 2012, 2014 and Fig. 1). tance with each trap 9.7 cm apart along the circumference. We used Co-attractiveness of seven EAD-active compounds (acetoin, grape an aluminum foil-covered 100-ml glass beaker with a cut centrifuge butyrate, 2-phenylethanol, diethyl succinate, ethyl butyrate, 1-hex- vial (0.7 cm diameter) inserted in the foil for SWD entry, as a trap anol, and isoamyl acetate) did not change over three different tests (Cha et al. 2012). All 13 traps had 20 ml 1.6% acetic acid + 7.2% (Table  1). However, co-attractiveness of the other five compounds ethanol with soap as a basal attractant and drowning solution. One changed among different tests. For example, the co-attractiveness of of the traps served as a control and the remaining 12 traps had one methionol and ethyl sorbate was changed from positive and neutral, of the 12 EAD-active compounds added to the control blend, loaded respectively, when they were tested in field experiments or in mul - as described in Cha et al. (2012) and released from 1.5-ml vial with tiple-choice assays, to neutral and negative, respectively, when they 3-mm hole with a piece of cotton. A  cotton ball (3  cm diameter) were tested in a two-choice assay, suggesting a potential role of back- soaked with distilled water was placed in the center of arena to pro- ground odor on the behavioral implication of a chemical compound. vide water to SWD. Adult flies (160–235, roughly 1:1 male: female ratio, 7–10-d-old) Discussion were released in each arena. Choice assays started at 1:00 p.m. each day (21.5 ± 0.9°C, 23.7 ± 0.1% RH, 16:8 [L:D] h). The number of Acetoin and methionol, along with acetic acid and ethanol, are key flies inside treatment and control traps was counted after 20 h. attractant components for D.  suzukii. Previously these chemicals were discovered after 2 yr of extensive laboratory and field trapping Statistical Analysis experiments. However, based on the results from this study, the same A randomized complete block design was used. Trap catches were outcome could have been achieved with 1 wk of laboratory experi- analyzed with block as a random factor and different odor sources ments. The main problem was that the laboratory two-choice assay as a fixed factor using Proc Mixed ( SAS Institute 2009). Fly catch used in Cha et al. (2012) failed to recognize methionol as an attract- data were square-root transformed to improve normality and ive blend component for D. suzukii. This resulted in the formulation homoscedasticity (Zar 1984). The means were compared using the of a sub-optimally attractive blend that was not statistically different Tukey-Kramer test (SAS Institute 2009). but numerically inferior to the target mixture of wine and vinegar in Fig. 1. Mean (±SEM) numbers of Drosophila suzukii flies captured in traps baited with a control (a mixture of 1.6% acetic acid and 7.2% ethanol; AA + EtOH) and 12 different ‘add-on’ blends (AA + EtOH + one of the EAD-active compounds listed in Table  1). AT: Acetoin, EL: Ethyl lactate, IAA: Isoamyl acetate, MBA: 2-methylbutyl acetate, GB: Grape butyrate, PE: 2-phenylethanol, EB: Ethyl butyrate, HX: 1-hexanol; MT: Methionol, IAL: Isoamyl lactate, ES: Ethyl sorbate, DS: Diethyl succinate. Different letters on bars indicate significant differences by Tukey-Kramer tests at P < 0.05. Statistical tests were based on square-root- transformed data. Means from untransformed data are shown. Downloaded from https://academic.oup.com/ee/article/47/4/946/4970129 by DeepDyve user on 13 July 2022 Environmental Entomology, 2018, Vol. 47, No. 4 949 the field ( Cha et al. 2012). Methionol was identified as an attractant cases, including pheromone and host plant attraction, insects typi- component and added to the blend later based on a field repetition cally do not respond to single compounds). However, we expect it of a similar experiment (Cha et al. 2014). Although the exact olfac- will be relatively successful for insects that respond to fermenta- tory mechanisms underlying our finding are still not clear, it appears tion baits as well as other baits like decomposing plant or animal evident that the background odor available to D. suzukii can mod- material where the same principal would apply. For example, this ulate the attractiveness of some potential attractant compounds, approach may be useful to identify attractants for insects respond- an important aspect to consider during the process of identifying ing to protein baits with basal attractants such as chemicals con- behavior modifying chemicals. The key to the success of our multi- taining ammonia (e.g., ammonium acetate, ammonium carbonate, ple-choice approach is to first determine a basal attractant that other ammonium bicarbonate, etc; Epsky et  al. 2004, Yee et  al. 2005). potential attractants are co-attractive to. For a fermentation bait, This type of interference from background odors may be more acetic acid, ethanol or the mixture are likely candidates for the basal common when ubiquitous volatiles from plants, microbes, or food attractant (Landolt et al. 2015, Cha et al. 2016). are involved in the attraction, compared to pheromone attraction, Comparing the co-attractiveness of multiple compounds simul- which may be chemically more distinctive and less influenced by a taneously but released individually from multiple point sources is background odor. a novel approach to directly identify key components of behavior modifying chemicals. In this study, acetoin and methionol were co-attractive to acetic acid plus ethanol mixture and this comprised Acknowledgments the same four-component blend that was developed previously from We thank Gabrielle Brind’Amour and Shinyoung Park for maintaining the extensive trapping experiments (Cha et al. 2012, 2014) and further insect colony and technical assistance and two anonymous reviewers for improved by optimizing proportionality of the blend components insightful comments. This research was supported in part by funding from the (Cha et al. 2017). While there have been several studies employing Washington Tree Fruit Research Commission, Cornell University’s New York State Agricultural Experiment Station federal formula funds, project 2015- multiple-choice assays to facilitate screening of attractants, these 16-180, New York State Agriculture and Markets (C0011GG) and National studies generally compared attractiveness of different mixtures or Institute of Food and Agriculture (2016-0228-08). extracts and involved elaborate special multi-arm glass olfactometer, such as four- (Vet et al. 1983), six- (Turlings et al. 2004), and eight- arm olfactometers (Liu and Şengonca 1994, Abraham et al. 2015). References Cited Our design may be more flexible, as it does not require a specialized Abraham, J., A. Zhang, S. Angeli, S. Abubeker, C. Michel, Y. Feng, and olfactometer and thus is not as limited in terms of the number of C.  Rodriguez-Saona. 2015. Behavioral and antennal responses of co-attractants that can be tested together. 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A Multiple-Choice Bioassay Approach for Rapid Screening of Key Attractant Volatiles

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Oxford University Press
Copyright
Copyright © 2022 Entomological Society of America
ISSN
0046-225X
eISSN
1938-2936
DOI
10.1093/ee/nvy054
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Abstract

Fermentation volatiles attract a wide variety of insects and are used for integrated pest management. However, identification of the key behavior modifying chemicals has often been challenging due to the time consuming nature of thorough behavioral tests and unexpected discrepancies between laboratory and field results. Thus we report on a multiple-choice bioassay approach that may expedite the process of identifying field-worthy attractants in the laboratory. We revisited the four-component key chemical blend (acetic acid, ethanol, acetoin, and methionol) identified from 12 antennally active wine and vinegar chemicals for Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). The identification of this blend took 2 yr of continuous laboratory two-choice assays and then similarly designed field trials. This delay was mainly due to a discrepancy between laboratory and field results that laboratory two-choice assay failed to identify methionol as an attractant component. Using a multiple-choice approach, we compared the co-attractiveness of the 12 potential attractants to an acetic acid plus ethanol mixture, known as the basal attractant for D. suzukii, and found similar results as the previous field trials. Only two compounds, acetoin and, importantly, methionol, increased attraction to a mixture of acetic acid and ethanol, suggesting the identification of the four-component blend could have been expedited. Interestingly, the co-attractiveness of some of the 12 individual compounds, including a key attractant, methionol, appears to change when they were tested under different background odor environments, suggesting that background odor can influence detection of potential attractants. Our findings provide a potentially useful approach to efficiently identify behaviorally bioactive fermentation chemicals. Key words: fermentation volatile, bioassay, background odor, attractant, spotted wing drosophila Fermentation volatiles produced by yeasts and acetic acid bacteria developed based on fermentation bait volatiles and are currently can attract a wide variety of insects and have been extensively used being widely used. Despite the large potential benefits, however, the to manipulate insect pest behavior for integrated pest management, tedious and time-consuming nature of behavioral tests (Turlings including various species of beetles (Nout and Bartelt 1998), flies et al. 2004), the lack of clarity in choosing different behavioral test- (Lee et al. 2012; Landolt et al 2015; Cha et al. 2016b, 2018), moths ing protocols (e.g., subtraction vs. addition approaches; Linn et al. (Yamazaki 1998, Sussenbach and Fiedler 1999, Laaksonen et  al. 1984), and the unexpected discrepancies in behavioral responses 2006, Pettersson and Franzén 2008) and vespid wasps (Dvorak and from laboratory and field experiments ( Knudsen et  al. 2008) have Landolt 2006, Noll and Gomes 2009, De Souza et al. 2011, Landolt often slowed the process of identifying key attractant components et al. 2014a,b). and the development of a synthetic lure. Therefore, a straightfor- The implementation of management program often favors using ward behavioral testing method that can be conducted in a relatively synthetic chemical attractants over bait materials, as a well-char- simple laboratory setting and at the same time generate field-worthy acterized chemical lure composed of essential attractant compo- results would facilitate the development of effective attractant lures. nents may be easier to deploy, longer lasting, and more selective Recently a chemical lure composed of acetic acid, ethanol, ace- than fermentation baits (e.g., Cha et al. 2015). For example, chem- toin and methionol was isolated, identified, optimized and com - ical lures for Vespula spp. (Landolt 1998) and Drosophila suzukii mercialized from a fermentation bait for D.  suzukii (Cha et  al. (Matsumura) (Diptera: Drosophilidae) (Cha et al. 2014) have been 2012, 2014, 2017, 2018), which is more efficient and selective Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. 946 Downloaded from https://academic.oup.com/ee/article/47/4/946/4970129 by DeepDyve user on 13 July 2022 Environmental Entomology, 2018, Vol. 47, No. 4 947 than the original material of a wine plus vinegar mixture (Cha Here, we report on a simple laboratory multiple-choice assay et al. 2013, 2015). However, the lure development was slow, tak- approach that uses a mixture of acetic acid and ethanol as a basal ing more than 2 yr of continuous laboratory two-choice assays attractant and tests co-attractiveness of all of the individual EAD- and field-trapping experiments in multiple locations, even after active compounds separately but concurrently. The new assay was 12 candidate attractant chemicals were determined using gas conducted by revisiting the 12 EAD-active wine and vinegar chem- chromatography-electroantennographic detection (GC-EAD). One icals involved in the development of the four-component chem- of the major reasons behind the delay was discrepancies in behav- ical lure for D.  suzukii. In the multiple-choice assay, all of the 12 ioral testing results between laboratory choice assays (Cha et  al. EAD-active compounds were available to SWD to respond to in 2012) and field trapping experiments ( Cha et al. 2014; summarized the headspace inside the cage, but released from separate individ- in Table  1). The co-attractiveness (Meagher and Landolt 2008, ual traps with acetic acid and ethanol as a basal attractant. This Landolt et al. 2014a,b) of some of the 12 EAD-active compounds laboratory assay allowed us to quickly predict which compounds to a mixture of acetic acid and ethanol were different in laboratory would be co-attractive with acetic acid plus ethanol for SWD in and field, resulting in different blend compositions that resulted the field, which was essential to achieve the same level of attraction in different attractiveness in the field. The discrepancy could have from D. suzukii to the original benchmarking mixture of wine and been due to the differences in background odor available in two- vinegar. choice laboratory assays versus field trapping experiments ( Cha et al. 2014). As the 12 EAD-active compounds were ubiquitous fer- mentation volatiles, field sites may have had a mixture of these 12 Materials and Methods compounds and even other volatile compounds in the background, Insects released from various materials including fermenting SWD host For multiple-choice bioassays, a colony of SWD was maintained at fruits, while in laboratory only the chemicals tested in a specific the New York State Agricultural Experiment Station, Geneva, New two-choice assay were present as the background. York. Flies were reared at 21.5 ± 0.9°C, 23.7 ± 0.1 % RH, 16:8 (L:D) The two major fermentation volatiles, acetic acid and ethanol, h on standard cornmeal diet (1 liter distilled water, 40  g sucrose, have been shown to be involved in insect attraction to fermentation 25 g cornmeal [Quaker Oats Co., Chicago, IL], 9 g agar [No. 7060, sources as individual compounds or as a mixture. In some cases, Bioserve, Flemington, NJ], 14  g torula yeast [No. 1720, Bioserve], a mixture of acetic acid and ethanol was sufficiently attractive to 3 ml glacial acetic acid [Amresco, Solon, OH], 0.6 g methyl paraben explain such attraction, while in other cases additional fermenta- [No 7685, Bioserve], and 6.7 ml ethanol). tion volatiles in addition to acetic acid and ethanol were necessary. For example, a mixture of acetic acid and ethanol was as attractive Chemicals as the original material of yeast-sugar fermenting solution for an avian parasitic fly, Philornis downsii (Cha et al. 2016) or as a wine For this study, we used the 12 EAD-active chemicals (Table  1) plus vinegar bait for false stable flies ( Landolt et al. 2015). In con- that were previously identified from a Merlot wine and a rice trast, in other insects such as D. suzukii, although ethanol and acetic vinegar mixture (Cha et  al. 2012). Ethyl butyrate (99%, CAS acid were essential for the attraction, additional fermentation vola- No. 105-54-4), 3-hydroxybutan-2-one (acetoin) (≥96%, CAS tiles were necessary to achieve the similar level of attraction to the No. 513-86-0), 3-methylbutyl acetate (isoamyl acetate) (98%, original fermentation material (Landolt et al. 2012b). In particular, CAS No. 123-92-2), 2-methylbutyl acetate (99%, CAS No. 624- acetic acid + ethanol was more attractive than either chemical alone 41-9), 3-methylsulfanylpropan-1-ol (methionol) (≥98%, CAS (Landolt et al. 2012a) but less attractive than a mixture of wine and No. 505-10-2), ethyl (2E,4E)-hexa-2,4-dienoate (ethyl sorbate) vinegar that contained the same amount of acetic acid and ethanol, (≥97%, CAS No. 2396-84-1), and 2-phenylethanol (≥99%, CAS suggesting that SWD are responding to some other wine and vinegar No. 60-12-8) were purchased from Sigma-Aldrich (St. Louis, chemicals (Landolt et al. 2012b). MO). Ethyl 2-hydroxypropionate (ethyl lactate) (>97%, CAS No. Table 1. Comparison of co-attractiveness of D. suzukii candidate attractants with acetic acid (AA) and ethanol (EtOH) in 1) a laboratory two- choice experiment (AA + EtOH vs. AA + EtOH + one of the candidate attractant; Cha et al. 2012), 2) a field ‘add-on’ test (AA + EtOH vs. AA + EtOH + one of the candidate attractants; Cha et al. 2014), and 3) multiple-choice assay conducted in this study Candidate co-attractant (SWD antennally active yeast chemicals) Laboratory two-choice test Field add-on test Multi-choice test 3-hydroxy butan-2-one (acetoin)* Positive Positive Positive 3-methylsulfanylpropan-1-ol (methionol)* Neutral Positive Positive Ethyl 2-hydroxypropionate (Ethyl lactate) Negative Positive Neutral 2-methylbutyl acetate Negative Neutral Negative Ethyl (2E,4E)-hexa-2,4-dienoate (Ethyl sorbate) Negative Neutral Neutral 3-methylbutyl 2-hydroxypropionate (Isoamyl lactate) Neutral Negative Neutral Ethyl 3-hydroxybutyrate (Grape butyrate) Neutral Neutral Neutral 2-phenylethanol Neutral Neutral Neutral Diethyl butanedioate (Diethyl succinate) Neutral Neutral Neutral Ethyl butyrate Negative Negative Negative 1-hexanol Negative Negative Negative 3-methylbutyl acetate (Isoamyl acetate) Negative Negative Negative Positive indicates that the compound added attractiveness to AA + EtOH (P < 0.05), negative decreased the attractiveness (P < 0.05), and neutral had no effect (P > 0.05) based on Tukey-Kramer tests (Cha et al. 2012, 2014 and Fig 1). *(bold) indicates two key chemicals in the four-component essential blend (acetic acid, ethanol, acetoin and methionol). Downloaded from https://academic.oup.com/ee/article/47/4/946/4970129 by DeepDyve user on 13 July 2022 948 Environmental Entomology, 2018, Vol. 47, No. 4 97-64-3), 3-methylbutyl 2-hydroxypropionate (isoamyl lactate) Results (>98%, CAS No. 19329-89-6), and diethyl butanedioate (diethyl The results from the laboratory multiple-choice test showed that succinate) (>99%, CAS No. 123-25-1) were purchased from TCI two compounds, acetoin and methionol, were co-attractive with a America (Morris, Portland, OR). Ethyl 3-hydroxybutyrate (grape mixture of acetic acid and ethanol (basal attractant), significantly butyrate) (99%, CAS No. 5405-41-4) was purchased from Arcos increasing the number of D.  suzukii trapped by 4.5- and 2.6-fold, Organics (New Jersey). Ethanol (200 proof, CAS No. 64-47-5), respectively, compared to the control traps baited with the mixture acetic acid (99.8%, CAS No. 64-19-7), and 1-hexanol (>95%, of acetic acid and ethanol (F  = 37.81, P < 0.0001; Fig. 1). 12,48 CAS No. 111-27-3) were purchased from Pharmco (Brookfield, In each experiment listed in Table  1, an EAD-active compound CT), Fisher Scientific (Pittsburgh, PA, USA), and J.  T. Baker was indicated ‘positive’ (i.e., co-attractive) when adding the com- (Philipsburg, NJ), respectively. pound to the mixture of 1.6% acetic acid and 7.2% ethanol resulted in a significant increase in D.  suzukii trap catches (P  <  0.05; Cha Multiple-Choice Assay et al. 2012, 2014 and Fig. 1) compared to the acetic acid and etha- The multiple choice assay (N  =  5) was conducted with an arena nol mixture, ‘neutral’ when adding the compound did not influence design using a dome cage (60  cm W × 60  cm L × 60  cm H; trap catches (P > 0.05; Cha et al. 2012, 2014 and Fig. 1), and ‘nega- BugDorm-2120 Insect tent; shop.bugdorm.com). Within each arena, tive’ (i.e., antagonistic) when the compound significantly decreased 13 traps were positioned in a circle (20 cm diameter) at equal dis- D. suzukii trap catches (P < 0.05; Cha et al. 2012, 2014 and Fig. 1). tance with each trap 9.7 cm apart along the circumference. We used Co-attractiveness of seven EAD-active compounds (acetoin, grape an aluminum foil-covered 100-ml glass beaker with a cut centrifuge butyrate, 2-phenylethanol, diethyl succinate, ethyl butyrate, 1-hex- vial (0.7 cm diameter) inserted in the foil for SWD entry, as a trap anol, and isoamyl acetate) did not change over three different tests (Cha et al. 2012). All 13 traps had 20 ml 1.6% acetic acid + 7.2% (Table  1). However, co-attractiveness of the other five compounds ethanol with soap as a basal attractant and drowning solution. One changed among different tests. For example, the co-attractiveness of of the traps served as a control and the remaining 12 traps had one methionol and ethyl sorbate was changed from positive and neutral, of the 12 EAD-active compounds added to the control blend, loaded respectively, when they were tested in field experiments or in mul - as described in Cha et al. (2012) and released from 1.5-ml vial with tiple-choice assays, to neutral and negative, respectively, when they 3-mm hole with a piece of cotton. A  cotton ball (3  cm diameter) were tested in a two-choice assay, suggesting a potential role of back- soaked with distilled water was placed in the center of arena to pro- ground odor on the behavioral implication of a chemical compound. vide water to SWD. Adult flies (160–235, roughly 1:1 male: female ratio, 7–10-d-old) Discussion were released in each arena. Choice assays started at 1:00 p.m. each day (21.5 ± 0.9°C, 23.7 ± 0.1% RH, 16:8 [L:D] h). The number of Acetoin and methionol, along with acetic acid and ethanol, are key flies inside treatment and control traps was counted after 20 h. attractant components for D.  suzukii. Previously these chemicals were discovered after 2 yr of extensive laboratory and field trapping Statistical Analysis experiments. However, based on the results from this study, the same A randomized complete block design was used. Trap catches were outcome could have been achieved with 1 wk of laboratory experi- analyzed with block as a random factor and different odor sources ments. The main problem was that the laboratory two-choice assay as a fixed factor using Proc Mixed ( SAS Institute 2009). Fly catch used in Cha et al. (2012) failed to recognize methionol as an attract- data were square-root transformed to improve normality and ive blend component for D. suzukii. This resulted in the formulation homoscedasticity (Zar 1984). The means were compared using the of a sub-optimally attractive blend that was not statistically different Tukey-Kramer test (SAS Institute 2009). but numerically inferior to the target mixture of wine and vinegar in Fig. 1. Mean (±SEM) numbers of Drosophila suzukii flies captured in traps baited with a control (a mixture of 1.6% acetic acid and 7.2% ethanol; AA + EtOH) and 12 different ‘add-on’ blends (AA + EtOH + one of the EAD-active compounds listed in Table  1). AT: Acetoin, EL: Ethyl lactate, IAA: Isoamyl acetate, MBA: 2-methylbutyl acetate, GB: Grape butyrate, PE: 2-phenylethanol, EB: Ethyl butyrate, HX: 1-hexanol; MT: Methionol, IAL: Isoamyl lactate, ES: Ethyl sorbate, DS: Diethyl succinate. Different letters on bars indicate significant differences by Tukey-Kramer tests at P < 0.05. Statistical tests were based on square-root- transformed data. Means from untransformed data are shown. Downloaded from https://academic.oup.com/ee/article/47/4/946/4970129 by DeepDyve user on 13 July 2022 Environmental Entomology, 2018, Vol. 47, No. 4 949 the field ( Cha et al. 2012). Methionol was identified as an attractant cases, including pheromone and host plant attraction, insects typi- component and added to the blend later based on a field repetition cally do not respond to single compounds). However, we expect it of a similar experiment (Cha et al. 2014). Although the exact olfac- will be relatively successful for insects that respond to fermenta- tory mechanisms underlying our finding are still not clear, it appears tion baits as well as other baits like decomposing plant or animal evident that the background odor available to D. suzukii can mod- material where the same principal would apply. For example, this ulate the attractiveness of some potential attractant compounds, approach may be useful to identify attractants for insects respond- an important aspect to consider during the process of identifying ing to protein baits with basal attractants such as chemicals con- behavior modifying chemicals. The key to the success of our multi- taining ammonia (e.g., ammonium acetate, ammonium carbonate, ple-choice approach is to first determine a basal attractant that other ammonium bicarbonate, etc; Epsky et  al. 2004, Yee et  al. 2005). potential attractants are co-attractive to. For a fermentation bait, This type of interference from background odors may be more acetic acid, ethanol or the mixture are likely candidates for the basal common when ubiquitous volatiles from plants, microbes, or food attractant (Landolt et al. 2015, Cha et al. 2016). are involved in the attraction, compared to pheromone attraction, Comparing the co-attractiveness of multiple compounds simul- which may be chemically more distinctive and less influenced by a taneously but released individually from multiple point sources is background odor. a novel approach to directly identify key components of behavior modifying chemicals. In this study, acetoin and methionol were co-attractive to acetic acid plus ethanol mixture and this comprised Acknowledgments the same four-component blend that was developed previously from We thank Gabrielle Brind’Amour and Shinyoung Park for maintaining the extensive trapping experiments (Cha et al. 2012, 2014) and further insect colony and technical assistance and two anonymous reviewers for improved by optimizing proportionality of the blend components insightful comments. This research was supported in part by funding from the (Cha et al. 2017). While there have been several studies employing Washington Tree Fruit Research Commission, Cornell University’s New York State Agricultural Experiment Station federal formula funds, project 2015- multiple-choice assays to facilitate screening of attractants, these 16-180, New York State Agriculture and Markets (C0011GG) and National studies generally compared attractiveness of different mixtures or Institute of Food and Agriculture (2016-0228-08). extracts and involved elaborate special multi-arm glass olfactometer, such as four- (Vet et al. 1983), six- (Turlings et al. 2004), and eight- arm olfactometers (Liu and Şengonca 1994, Abraham et al. 2015). References Cited Our design may be more flexible, as it does not require a specialized Abraham, J., A. Zhang, S. Angeli, S. Abubeker, C. Michel, Y. Feng, and olfactometer and thus is not as limited in terms of the number of C.  Rodriguez-Saona. 2015. Behavioral and antennal responses of co-attractants that can be tested together. 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Environmental EntomologyOxford University Press

Published: Aug 11, 2018

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