Next Article in Journal
Effect of 5-Aminolevulinic Acid (ALA) on the Biochemical and Physiological Parameters of Postharvest Quality of Polygonatum multiflorum L. All. ‘Variegatum’ Cut Foliage
Next Article in Special Issue
Modification of the TOMCAST Model with Aerobiological Data for Management of Potato Early Blight
Previous Article in Journal
Agricultural Uses of Juglone: Opportunities and Challenges
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 10
Issue 10
10.3390/agronomy10101501
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Yeasts Associated with the Olive Fruit Fly Bactrocera oleae (Rossi) (Diptera: Tephritidae) Lead to New Attractants

by
Elda Vitanović
1,2,
Julian M. Lopez
3,
Jeffrey R. Aldrich
1,4,
Maja Jukić Špika
2,5,*,
Kyria Boundy-Mills
3 and
Frank G. Zalom
1
1
Department of Entomology and Nematology, University of California, Davis, CA 95616, USA
2
Institute for Adriatic Crops and Karst Reclamation, Put Duilova 11, 21000 Split, Croatia
3
Department of Food Science and Technology, Phaff Yeast Collection, University of California, Davis, CA 95616, USA
4
Jeffrey R. Aldrich Consulting LLC, P.O. Box 121, Marcell, MN 56657, USA
5
Ctr Excellence Biodivers & Mol Plant Breeding, Svetošimunska Cesta 25, 1000 Zagreb, Croatia
*
Author to whom correspondence should be addressed.
Agronomy 2020, 10(10), 1501; https://doi.org/10.3390/agronomy10101501
Submission received: 1 September 2020 / Revised: 28 September 2020 / Accepted: 30 September 2020 / Published: 2 October 2020
(This article belongs to the Special Issue Integrated Pest Management of Horticultural Crops)
Browse Figures
Versions Notes

Abstract

:
The olive fruit fly (Bactrocera oleae Rossi) is the primary insect pest in all olive-growing regions worldwide. New integrated pest management (IPM) techniques are needed for B. oleae to mitigate reliance on pesticides used for its control which can result in negative environmental impacts. More effective lures for monitoring olive flies would help to know when and where direct chemical applications are required. The aim of this research was to find new, more effective methods for B. oleae detection and monitoring. Twelve insect-associated yeasts were selected and tested as living cultures in McPhail traps for the attraction of olive flies. Certain yeasts were more attractive than others to B. oleae; specifically, Kuraishia capsulata, Lachancea thermotolerans, Peterozyma xylosa, Scheffersomyces ergatensis, and Nakazawae ernobii, than the industry-standard dried torula yeast (Cyberlindnera jadinii; syn. Candida utilis). The attractiveness of dry, inactive (i.e., non-living) formulations of these five yeasts was also tested in the field. Inactive formulations of K. capsulata, P. xylosa, N. ernobii, and L. thermotolerans were significantly more attractive to B. oleae than commercially available torula yeast. Green lacewing, Chrysoperla comanche (Stephens) (Neuroptera: Chrysopidae), adults were incidentally caught in traps baited with the live yeast cultures. This is the first field study that compares olive fly attraction to yeast species other than torula yeast. Commercialization of yeasts that are more attractive than the torula standard would improve monitoring and associated control of the olive fruit fly.

1. Introduction

The olive fruit fly (Bactrocera oleae Rossi) is the most damaging olive pest in the world. Olive losses from this tephritid routinely range up to 15% [1], but in years and at sites with high fly populations, total yield loss can occur [2]. These losses affect table olive production more than olive oil production since damaged fruit cannot be processed as table olives. In olive oil production, B. oleae directly affects the amount and quality of the oil. Historically, olive fly control has been based solely on insecticides [3,4,5]. However, chemical control negatively affects biodiversity in the olive canopy by reducing the number of beneficial organisms that include predatory arthropods, such as spiders, insects from the order Neuroptera, Coleoptera, and Diptera, and parasitoids (Order Hymenoptera) ([3,4,5,6] and references therein). The intensive use of pesticides for B. oleae control has stimulated researchers to seek new methods that will preserve olive orchard biodiversity [6]. Dipteran responses to yeast volatiles have been reported by many researchers ([7,8,9,10,11] and references therein). In addition, interactions between yeast and Drosophila species have been repeatedly investigated and documented ([7,12,13,14,15,16,17] and references therein). Drosophila use yeasts as food for larvae, nutrients for egg production, and in courtship [18]. Becher et al. [19] pointed out that Drosophila melanogaster is primarily attracted to volatiles associated with yeasts found on host fruit rather than to fruit odor itself. The same authors also stated that volatile compounds emitted by the yeasts are usually found in flowers and nectar and that they are common floral signals and insect attractants. Releases of these volatiles attract many different insect species before the emergence of plant flowering and may contribute to the evolution of pollination by insects. Unlike drosophilid flies, interactions between yeasts and tephritid fruit flies have not been well investigated [20]. Piper et al. [20] suggested that a better understanding of interactions between yeasts and tephritids could lead to the development of new formulations of attractants in “attract and kill” lures, as well as improvement in insect mass rearing insect methodology in Sterile Insect Technique (SIT) control programs [21]. Interactions between B. oleae and gut microbiota, such are fungi [22] and bacteria [23,24,25], have been investigated for similar reasons. Bactrocera oleae is reportedly also attracted to host plant volatiles [26,27,28,29], as well as intra- [30,31] and inter-specific semiochemicals [32]. However, the interaction between B. oleae and yeasts other than torula yeast (Cyberlindnera jadinii; syn. Candida utilis) remains little studied.
Over 400 yeasts were isolated from infested olives, adult flies, and potential feeding sites during preliminary studies [33]. Of these yeasts, over 130 insect-associated strains showed promise for attracting B. oleae as well or better than the industry standard torula yeast pellet. The aim of the research reported herein was to find the most attractive yeast strains from among the plethora of promising species for the attraction of the olive fruit fly.
Bait pellets consisting of hydrolyzed torula yeast and boric acid were developed in 1971 for monitoring of the Caribbean fruit fly [34]. This pellet lure is now used for monitoring and/or control of many tephritids ([35] and references therein), including B. oleae [36]. Burrack et al. [36] found that commercial torula yeast pellets were more effective for attracting olive fruit flies in the field than other attractants, such as lures based on ammonia or pheromones. In our previous study [33], we found that volatiles produced by active torula yeast formulation in potato dextrose broth (PDB) differed greatly from those produced by an inactive commercial pellet of the same yeast species suspended in water. However, from a practical standpoint, the commercialization of yeast for the attraction of tephritid fruit flies is much more easily accomplished with the dry, inactive form of yeast than for active, living cultures [33]. Therefore, the five most attractive yeast species, as found here through testing, were also tested as water suspensions of their non-living freeze-dried residue as a step toward advancing a more commercially-acceptable form that could be used for B. oleae detection and monitoring.
Finally, in the course of the current investigation, many adults of one species of the green lacewing, Chrysoperla comanche (Stephens) (Neuroptera: Chrysopidae), were incidentally caught in traps baited with live yeast cultures [37]. Data comparing the attractiveness of yeast to B. oleae versus C. comanche attraction are also presented.

2. Materials and Methods

2.1. Experiment in 2015

2.1.1. Preparation of 12 Insect-Associated Yeasts

Twelve yeast strains from a preliminary screening of over 130 insect-associated yeast strains that showed promise for attracting B. oleae [33] were selected for field testing (Table 1).
All yeast cultures were prepared in duplicate. All yeast strains were revived from cryopreserved stocks onto potato dextrose agar (PDA) and incubated at room temperature for five days. Yeast seed cultures were prepared by inoculating 10 mL of potato dextrose broth (PDB; DifcoTM, Sparks, NJ, USA) with about 1 µL of cells from each fresh plate, and incubating at room temperature in a roller drum [38]. After three days, 5 mL of each yeast culture was added to flasks containing 200 mL PDB and incubated four days with shaking at 200 rpm and 30 °C. After four days, flask yeast cultures were diluted with PDB so that all had equivalent OD 600 [39], and then 200 mL of each live yeast culture was transferred into a sterile 250 mL bottle. Bottles with active yeast formulations were chilled then transported to the olive orchard.

2.1.2. Field Testing

All active yeast formulations were placed in duplicate in plastic McPhail traps (Great Lakes IPM, Inc., Vestaburg, MI, USA) in an organic olive orchard at UC Davis (coordinates: 38.535861, −121.795023), beginning on 29 October 2015. Traps were placed randomly in every third row with a distance of four trees between traps in the row at 1.5–2 m high in the shade of the olive canopy for 10 days. Positive control traps containing torula yeast pellet solution (5 g of torula in 200 mL deionized water) (ISCA Technologies Inc., Riverside, CA, USA), and negative control traps containing 200 mL of deionized water, or 200 mL of PBD solution were also included in duplicate. Because PDB supports microbial growth in this non-aseptic environment, it was necessary for the PDB-baited traps to be replaced every two days. Two traps for each treatment (yeast) were placed in the olive orchard, and the total number of olive fruit flies in each of them was counted daily by removing all insects with a strainer, and then returning the yeast cultures to the respective trap.

2.2. Experiment in 2016

2.2.1. Preparation of the Five Most Attractive Insect-Associated Yeasts

The five most attractive yeast strains from the fall 2015 test were selected for spring 2016 field testing. These were K. capsulata, P. xylosa, N. ernobii, L. thermotolerans, and S. ergatensis. These yeasts were revived and grown in the same manner as described above, as was the commercially available formulation of torula yeast (Cyberlindnera jadinii; syn. Candida utilis).

2.2.2. Preparation of Dry Yeast

Freeze-dried preparations of the five yeast strains that attracted the highest number of olive fruit flies in the fall 2015 trial were prepared for the spring 2016 field trial (Figure 1).
Liquid yeast extract/malt extract (YM) broth media (10 g/L dextrose, 3 g/L yeast extract (Marcor Development Corporation, KODA Distribution Group, Carlstadt, NJ, USA), 3 g/L malt extract (Home Brew Stuff, Inc., Idaho, USA), 5 g/L Bacto peptone (Thermo Fisher Scientific, Waltham, MA, USA), and 10 g/L glucose (Bulkfoods-Natural Food Inc., Toledo, OH, USA) was used to cultivate yeasts for attraction studies. For most yeast strains, yeast extract/malt extract media (YM) broth was prepared at five times (5×) the standard concentration of all ingredients to boost yeast biomass productivity, except for the yeasts S. ergatensis and N. enobii for which three times (3×) the normal concentration of YM was used instead because it resulted in higher cell biomass. Each yeast strain was revived on PDA plates and incubated for three days at room temperature. A loopful of cells was added to 10 mL either 3× YM (S. ergatensis) or 5× YM (remaining yeasts) broth in triplicate in a 50-mL conical bio-reaction tube (Cat.# 229475, BR tubes, Celltreat, Shirley, MA, USA) and incubated 24 h at 200 rpm 30 °C. This seed culture was then inoculated into 790 mL of the same media in 2.8 L Fernbach flasks and incubated 96 h at 200 rpm at 30 °C, except S. ergatensis, which was grown at 25 °C. Cells were washed three times by centrifuging at 4000 rpm for 10 min at room temperature, then resuspending cells in 150 mL deionized water. The cell pellets were frozen 24 h at −80 °C, then freeze-dried for 48 h below −47 °C, vacuum >0.12 Pa in a Labconco Freeze Zone 4.5 freeze dryer. Freeze-dried cell mass was transferred to a pre-weighed plastic bag, weighed, then stored at −80 °C.
For field bioassays, 5 g of each yeast strain was suspended in 200 mL of deionized water in 250 mL bottles.

2.2.3. Field Testing

McPhail traps baited with the various active and inactive yeast-strain formulations were deployed as described for 2015 in 2 sets (10 days each), beginning on May 11, 2016. In addition to commercial torula yeast pellets as a positive control and deionized water as a negative control, as described previously, 5× and 3× YM media were also included as negative controls. The 5× and 3× YM media in traps were replaced every two days. The total number of olive fruit flies per trap was counted daily by removing all insects with a strainer, and then returning the yeast cultures of each respective trap.
In the course of the spring 2016 investigation, we noticed that traps baited with all yeast formulations captured many green lacewings (Neuroptera: Chrysopidae) as well, and these were counted too.

2.3. Statistical Analysis

Data were subjected to non-parametric χ2 goodness of fit test to compare the attractiveness of active and inactive formulations of yeasts to olive fruit fly and to green lacewings. For the frequencies (e.g., less than 10 on average), V-square statistics as a Chi-square corrected for sample size [40,41] were used. The correction of the significance value was performed by the Bonferroni test [42,43] for controlling the effect of multiple testing. Analyses were performed by Statistica software version 12.0 (StatSoft, Inc., Tulsa, OK, USA, 2013).

3. Results

3.1. Experiment in 2015

Attraction of B. oleae to 12 Insect-Associated Yeasts

During November 2015, 657 olive fruit flies (370 males and 287 females) were captured in McPhail traps baited with active cultures of 12 insect-associated yeast strains (Table 1). A significant difference in fly attraction was noted (χ2 = 317.64; p0.05 = 23.68) (Figure 2). Traps baited with L. thermotolerans captured the most olive fruit flies, followed by N. ernobii and P. xylosa. Among the 12 active yeast formulations, six of them (L. thermotolerans, N. ernobii, P. xylosa, S. ergatensis, K. kapsulata, and C. jadinii) captured significantly greater numbers of olive fruit flies than did the PDB, water, or torula pellet control traps. McPhail traps baited with V. cf. foliicola, W. subpelliculosus, O. pini, J. aff. sakaguchii, and S. terrea did not differ in B. oleae captures compared to torula yeast pellets, but they did capture significantly more flies than did the PDB or water control traps. Only the F. oeirensis baited traps captured significantly fewer B. oleae than those baited with torula pellets (Figure 2).
Results in Figure 2 show that there were significant differences in the attraction of the sexes (χ2 = 10.48, df = 1, p = 0.0012) with males exhibiting 23 percent greater attraction to B. oleae than females overall. However, not all tested yeast strains showed differences in the attraction of the sexes. Individually only S. terrea, J. aff. sakaguchii, and N. ernobii were more attractive to males than females. Traps that contained F. oeirensis caught the same number of both sexes.

3.2. Experiments in 2016

3.2.1. Attraction of B. oleae to the Five Most Active and Inactive Yeasts

During May 2016, 394 olive fruit flies were collected in McPhail traps containing active or inactive formulations representing the five most attractive yeast strains from the 2015 field trial. Traps containing active yeast formulations accounted for 112 of the flies caught, and they were significantly less attractive to B. oleae then traps containing inactive yeast formulations (χ2 = 73.35; p0.05 = 3.84). The attractiveness of the single yeast strain and their relationship to the control samples is shown in Figure 3.
The attraction of B. oleae to the active and inactive formulations of K. capsulata, P. xylosa, and N. ernobii is presented in Figure 3A–C, and a significant difference in adult captures among these yeast strains was found (χ2 = 184.95; χ2 = 267.76; χ2 = 408.28; p0.05 = 12.59). Mean (±SD) B. oleae captures in McPhail traps containing inactive formulations of K. capsulata (14.75 ± 4.78), P. xylosa (20.00 ± 12.02), and N. ernobii (22.5 ± 16.82) were significantly greater when compared to traps that contained active formulations of the same yeast strains and to all control traps (torula yeast, water, PDB, media 3× and media 5×). There were no differences in attractiveness to B. oleae between active formulations of K. capsulata, P. xylosa, and the industry-standard (inactive torula yeast pellet), but active yeast formulations mentioned were more attractive to B. oleae than the other control attractants. The N. ernobii active formulation was significantly less attractive to B. oleae than was torula yeast, and no difference in attractiveness was noted compared to other control attractants.
The differences in attractiveness between active and inactive formulations of L. thermotolerans and S. ergatensis to olive fruit fly were also tested (Figure 3D–E). There was no significant difference in mean (±SD) B. oleae attraction between McPhail traps containing active (6.75 ± 4.57) and inactive (6.75 ± 3.09) formulations of L. thermotolerans or between traps containing active (8.50 ± 2.38) and inactive (6.50 ± 3.11) formulations of S. ergatensis. The number of flies captured in McPhail traps containing either active or inactive formulations of L. thermotolerans and S. ergatensis was significantly greater than control traps that contained water, PDB, 3× YM broth, or 5× YM broth. However, B. oleae captured in traps containing either the active or inactive L. thermotolerans formulations or the active S. ergatensis were significantly greater compared to captures in traps torula yeast pellets, while the number captured in traps containing the inactive S. ergatensis formulation was not different. When considering the total number of flies captured in McPhail traps, significant differences in attraction were observed between the sexes for both active (χ2 = 6.03, df = 1, p = 0.0140; 69 males: 43 females) and inactive yeast strain formulations (χ2 = 22.69, df = 1, p ≤ 0.0001; 181 males: 101 females).

3.2.2. Attraction of a green lacewing to the five most active and inactive yeasts

In a previous study, we noted that one species of green lacewing, C. comanche, was highly attracted to active formulations of different yeast strains that included two of the five yeasts, L. thermotolerans and C. terreus, that were deployed in the present study [37].
McPhail traps containing active formulations of insect-associated yeast strains placed in an olive orchard in spring 2016 showed significant differences (χ2 = 258, p0.05 = 14.07) in attraction to C. comanche (Figure 4).All tested yeast strain active formulations were significantly more attractive than were the control traps (torula yeast, PDB, and water). Mean (±SD) captures were significantly greater in traps baited with L. thermotolerans (30.75 ± 23.12) than in those baited with K. capsulata (21.00 ± 10.61), C. silvicola (19.75 ± 16.27) or S. ergatensis (18.00 ± 7.11).
Results of the attractiveness of inactive formulations to C. comanche placed in the same olive orchard in spring 2016 were similar to those for the active formulations (Figure 5), and as for active formulation, there were significant differences between formulations (χ2 = 262, p0.05 = 15.51).
Traps baited with the inactive formulation of L. thermotolerans captured significantly more C. comanche than did the other inactive yeast formulations (29.50 ± 16.27). L. thermotolerans and K. capsulata (14.75 ± 12.24) baited traps caught significantly more C. comanche than did the control traps containing 5× YM broth, 3× YM broth, torula yeast, or water. There was no difference in captures between McPhail traps that contained inactive formulations of S. ergatensis (10.50 ± 9.40), P. xylosa (7.75 ± 3.68), or N. ernobii (7.50 ± 5.19) (Figure 5). Traps baited with the latter three yeast strains captured significantly more C. comanche than did traps containing torula yeast pellets and water as a control.
Chi-square analysis revealed that significantly more C. comanche were attracted to traps baited with active yeast formations than inactive formulations (χ2 = 24.90, df = 1, p ≤ 0.0001). Of the 689 total C. comanche captured in traps baited with the yeast strains evaluated, 410 were recorded in traps baited with active formulations and 279 with inactive formulations (Figure 4 and Figure 5).

4. Discussion

This is the first in-depth study of yeast strains other than the commercially-available Cyberlindnera jadinii; syn. Candida utilis) (torula yeast) dry pellet vis-à-vis olive fruit fly attraction. Commercialization of yeast strains that are more attractive than the industry standard torula yeast pellet would improve its monitoring and potentially its control, too.
In an earlier field study [33], we evaluated 12 yeast strains as active yeasts formulations for B. oleae attraction and found that certain yeast strains were more attractive than others. Five of them were significantly more attractive to B. oleae than the torula yeast pellets (Figure 2). We also felt that evaluating inactive formulations of these yeasts (which is similar in concept to that of torula yeast pellet) might afford more uniform release of volatiles over time than the active formulations that had been previously evaluated and would provide better shelf life making them more attractive and usable as commercial baits.
The effectiveness of inactive and active formulations of five yeasts, K. capsulata, L. thermotolerans, P. xylosa, S. ergatensis, and N. ernobii, were compared to one another and commercial torula yeast pellets in a California olive orchard. Inactive formulations of K. capsulata, P. xylosa, N. ernobii, and L. thermotolerans yeasts were significantly more attractive to olive fruit flies when compared to commercial torula yeast pellets, while the inactive formulation of S. ergatensis was not. Of these, the inactive formulation of N. ernobii was the most attractive to B. oleae among the yeasts and formulations evaluated, resulting in 2.6-fold more flies being captured in plastic McPhail traps relative to torula yeast pellets. Bactrocera oleae were also attracted to active formulations of N. ernobii, P. xylosa, K. capsulata, and L. thermotolerans, although trap captures were lower in all cases relative to inactive formulations of the same yeasts. As anticipated, B. oleae trap captures proved somewhat inconsistent between years when using the active formulations of these yeasts. For example, the N. ernobii active formulation was second most attractive among the yeast strains tested in fall 2015, yet no B. oleae were captured in the spring 2016 study. Bactrocera oleae were also more attracted to active formulations of P. xylosa and K. capsulate in 2015 relative to 2016, while active formulations of L. thermotolerans were relatively attractive in both years. The reasons for this inconsistency in attraction for the active formulations of these yeasts are not known, but the cooler conditions present at the time of the fall 2015 field study relative to the spring 2016 trial could have been a factor influencing yeast fermentation during these studies or could affect fly populations. Consistency of active formulations seasonally and under different ambient field conditions could perhaps be improved with additional research.
The study results suggest that inactive formulations of N. ernobii, P. xylosa, K. capsulate, or L. thermotolerans could be used as attractants for B. oleae detection, monitoring, and/or control, and that attraction to these yeasts could prove more effective than to torula yeast. These four yeast strains are more attractive to olive fruit fly than torula yeast, and this could be due to their host associations in nature. The original sources from which these yeast strains were collected (insects) differs from that of torula yeast (C. jadinii; syn. C. utilis), which is associated with plants. The L. thermotolerans strain used in this study was first isolated from a male olive fruit fly trapped in a plastic McPhail trap [33]. The P. xylosa used in this study was first isolated from a Drosophilidae species, Drosophila miranda, while the K. capsulata and N. ernobii were first isolated from beetles (Table 1) [33]. Our results are also consistent with the numerous studies of interactions between other Diptera species and yeasts (e.g., [8,9,10,11,14,15,16] and references therein).
In a previous study [33], solid phase microextraction/gas chromatography/mass spectrometry (SPME/GC/MS) analysis of active formulations of three of these yeast strains identified five volatile compounds that were attractive to B. oleae in a laboratory Y-tube olfactometer assay. Bactrocera oleae were also highly attracted to these yeasts in our field studies. The same study [33] showed that volatile compounds produced by active torula yeast (C. jadinii; syn. C. utilis) in PDB greatly differed from those produced by inactive commercial torula yeast pellets suspended in water and that inactive torula yeast pellets were much more attractive to B. oleae than active C. jadinii; syn. C. utilis [33]. Identification of the volatile profiles of inactive formulations of K. capsulata, P. xylos, L. thermotolerans, and N. ernobii could lead to the discovery of specific volatile compounds that may be responsible for olive fruit fly attraction that can be used as improved attractants in integrated pest management (IPM) programs.
We observed that plastic McPhail traps baited with inactive and active formulations of K. capsulata, P. xylosa, N. ernobii, L. thermotolerants, or S. ergatensis also captured many different dipterans as well as other insects. This is unsurprising as it is well known that many insects from several orders, including beetles, flies, ants, and bees, interact with yeasts [44,45,46,47,48] In both years of our study, plastic McPhail traps containing L. thermotolerans captured the greatest number and diversity of insects compared to the other yeast strains. Nakazawa ernobii attracted the greatest number of wasps, especially the active yeast formulation (data not shown). Previous researches on eusocial insects extensively describe their associations with yeasts and other microbes [49,50,51].
The discovery that inactive yeasts were more attractive than the corresponding active formulations sheds doubt on the assumption of mutualism between olive fruit fly and yeasts, the nature of which is reconsidered. In contrast, the concomitant data presented showing that many adults of one species of green lacewing, C. comanche, were incidentally caught in traps baited with live yeast cultures, substantiates the existence of a truly mutualistic relationship between this group of aphid predators and yeast. According to Hagen, et al. [52], yeasts are involved in the nutritional ecology of green lacewings, but the relationship between them is still not well-understood [53]. Because of that, our discovery stimulated us to collect them to investigate which of tested yeasts will be more attractive to lacewings than to B. oleae or vice versa. Generally, McPhail traps that contained active yeast formulations caught a greater number of C. comanche compared to the traps containing their inactive formulations, especially K. capsulata, L. thermotolerans, and S. ergatensis. These yeast strains were significantly more attractive to C. comanche than to B. oleae. Volatile compounds emitted by active yeast cultures were likely more attractive to C. comanche than inactive formulations. By contrast, olive fruit flies were more attracted to inactive yeast formulations. Only the inactive formulation of L. thermotolerans was significantly more attractive to C. comanche than to B. oleae. This is important because our results indicate that inactive formulations of K. capsulata, P. xylosa, L. thermotolerans, and N. ernobii have the potential to be used as new attractants for detection, monitoring, and/or control of olive fruit fly. Therefore, the use of L. thermotolerans as a pest management tool could lead to the disruption of C. comanche, which are common natural enemies in agroecosystems but are used in augmentation biological control programs [54].

5. Conclusions

The behavioral response of olive fruit fly to 12 insect-associated yeast strains was confirmed. Our data indicated that B. oleae were more attractive to some yeast strains than others. Further, plastic McPhail traps containing certain inactive yeast formulations also captured significantly more adult flies than those baited with the commercial standard, torula yeast. Of all yeast strains evaluated, inactive formulations of K. capsulata, P. xylosa, N. ernobii, and L. thermotolerans were significantly more attractive to B. oleae compared with torula yeast pellets. These four yeast strains represent promising candidates as attractants for B. oleae detection, monitoring, and/or control. Results from the present study confirmed those of a prior study that suggested differential attraction of the green lacewing, C. comanche, to different yeast strains also highlight opportunities for future research toward understanding and perhaps utilizing the behavioral response of beneficial insects to yeasts.
This is the first study to investigate the interaction between insect-associated yeast strains and B. oleae in an olive orchard. Results set the foundation for using insect-associated yeasts as attractants for detection, monitoring and/or control of olive fruit fly, and have implications for the management of other tephritids as well.

Author Contributions

Conceived and designed the experiments, E.V., J.R.A., K.B.-M., and F.G.Z.; performed the laboratory and field experiments and analyzed the data, E.V., J.M.L., J.R.A., K.B.-M., and F.G.Z.; statistical analyses, M.J.Š.; writing—original draft preparation, E.V., J.M.L., M.J.Š.; writing—review and editing, J.R.A., K.B.-M., and F.G.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Fulbright Scholar Program Award 68150029 to E.V. in 2015/2016, and the Department of Entomology and Nematology University of California, Davis, CA, USA. In addition, this research was supported by the project KK.01.1.1.04.0002 New methods in olive pests controlling using plant volatiles, Split, Croatia, funded by European Union.

Acknowledgments

Funding from the Fulbright Program of the U.S. Department of State is gratefully acknowledged. Personal thanks are extended to N. Nicola and L.A. Garay for technical assistance, D. Flynn (Executive Director of the UC Davis Olive Center) for providing the olive orchard where our field studies were conducted, and S.L. Winterton of the California State Collection of Arthropods, California Department of Food and Agriculture, Sacramento, for green lacewings identification.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Montiel Bueno, A.; Jones, O. Alternative methods for controlling the olive fly, Bactrocera oleae, involving semiochemicals. IOBC wprs Bull. 2002, 25, 1–11. [Google Scholar]
  2. Collier, T.R.; Van Steenwyk, R.A. Prospects for integrated control of olive fruit fly are promising in California. Calif. Agric. 2003, 57, 28–31. [Google Scholar] [CrossRef]
  3. Cirio, U. Agrochemicals and environmental impact in olive farming. Olivae 1997, 65, 32–39. [Google Scholar]
  4. Civantos, M. Control de plagas y enfermedades del olivar; Consejo Oleicola International: Madrid, Spain, 1999; pp. 1–207. [Google Scholar]
  5. Heim, G. Effect of insecticidal sprays on predators and indifferent arthropods found in olives trees on the north of Lebanon. In Integrated Pest Control in Olive Groves; Cavalloro, R., Crovetti, A., Eds.; CEC/FAO/ IOBC/IJMP: Pisa, Italy, 1985; pp. 456–465. [Google Scholar]
  6. Vitanovic, E.; Ivezić, M.; Kačić, S.; Katalinić, M.; Durbesić, P.; Barčić, J.I. Arthropod communities within the olive canopy as bioindicators of different management systems. Span. J. Agric. Res. 2018, 16, e0301. [Google Scholar] [CrossRef] [Green Version]
  7. Andreadis, S.S.; Witzgall, P.; Becher, P.G. Survey of arthropod assemblages responding to live yeasts in an organic apple orchard. Front. Ecol. Evol. 2015, 3, 1–7. [Google Scholar] [CrossRef] [Green Version]
  8. Biasazin, T.D.; Karlsson, M.F.; Hillbur, Y.; Seyoum, E.; Dekker, T. Identification of Host Blends that Attract the African Invasive Fruit Fly, Bactrocera invadens. J. Chem. Ecol. 2014, 40, 966–976. [Google Scholar] [CrossRef] [PubMed]
  9. Brevault, T.; Quilici, S. Flower and fruit volatiles assist host-plant location in the Tomato fruit flyNeoceratitis cyanescens. Physiol. Èntomol. 2010, 35, 9–18. [Google Scholar] [CrossRef]
  10. Dalby-Ball, G.; Meats, A. Influence of the odour of fruit, yeast and cue-lure on the flight activity of the Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust. J. Èntomol. 2000, 39, 195–200. [Google Scholar] [CrossRef]
  11. Kleiber, J.R.; Unelius, R.; Lee, J.C.; Suckling, D.M.; Qian, M.C.; Bruck, D.J. Attractiveness of Fermentation and Related Products to Spotted Wing Drosophila (Diptera: Drosophilidae). Environ. Èntomol. 2014, 43, 439–447. [Google Scholar] [CrossRef]
  12. Batista, M.R.; Uno, F.; Chaves, R.D.; Tidon, R.; Rosa, C.A.; Klaczko, L.B. Differential attraction of drosophilids to banana baits inoculated with Saccharomyces cerevisiae and Hanseniaspora uvarum within a Neotropical forest remnant. PeerJ 2017, 5, 1–15. [Google Scholar] [CrossRef] [Green Version]
  13. Dweck, H.K.M.; Ebrahim, S.A.; Farhan, A.; Hansson, B.S.; Stensmyr, M.C. Olfactory Proxy Detection of Dietary Antioxidants in Drosophila. Curr. Boil. 2015, 25, 455–466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Mori, B.A.; Whitener, A.B.; Leinweber, Y.; Revadi, S.; Beers, E.H.; Witzgall, P.; Becher, P.G. Enhanced yeast feeding following mating facilitates control of the invasive fruit pestDrosophila suzukii. J. Appl. Ecol. 2016, 54, 170–177. [Google Scholar] [CrossRef]
  15. Murgier, J.; Everaerts, C.; Farine, J.F.; Ferveur, J.F. Live yeasts in juvenile diet induces species-specific effects on Drosophila adult behavior and fitness. Sci. Rep. 2019, 9, 1–12. [Google Scholar] [CrossRef] [Green Version]
  16. K Koerte, S.; Keesey, I.W.; Easson, M.L.A.E.; Gershenzon, J.; Hansson, B.S.; Knaden, M. Variable dependency on associated yeast communities influences host range in Drosophila species. Oikos 2020, 00, 1–19. [Google Scholar] [CrossRef] [Green Version]
  17. Scheidler, N.H.; Liu, C.; Hamby, K.A.; Zalom, F.G.; Syed, Z. Volatile codes: Correlation of olfactory signals and reception in Drosophila-yeast chemical communication. Sci. Rep. 2015, 5, 14059. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Hamby, K.A.; Becher, P.G. Current knowledge of interactions between Drosophila suzukii and microbes, and their potential utility for pest management. J. Pest Sci. 2016, 89, 621–630. [Google Scholar] [CrossRef]
  19. Becher, P.G.; Hagman, A.; Verschut, V.; Chakraborty, A.; Rozpędowska, E.; Lebreton, S.; Bengtsson, M.; Flick, G.; Witzgall, P.; Piškur, J. Chemical signaling and insect attraction is a conserved trait in yeasts. Ecol. Evol. 2018, 8, 2962–2974. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Piper, A.M.; Farnier, K.; Linder, T.; Speight, R.; Cunningham, J.P. Two Gut-Associated Yeasts in a Tephritid Fruit Fly have Contrasting Effects on Adult Attraction and Larval Survival. J. Chem. Ecol. 2017, 43, 891–901. [Google Scholar] [CrossRef]
  21. Deutscher, A.T.; Reynolds, O.L.; A Chapman, T. Yeast: An Overlooked Component of Bactrocera tryoni (Diptera: Tephritidae) Larval Gut Microbiota. J. Econ. Èntomol. 2016, 110, 298–300. [Google Scholar] [CrossRef]
  22. Malacrinò, A.; Schena, L.; Campolo, O.; Laudani, F.; Mosca, S.; Giunti, G.; Strano, C.P.; Palmeri, V. A Metabarcoding survey on the fungal microbiota associated to the olive fruit fly. Microb. Ecol. 2017, 73, 677–684. [Google Scholar] [CrossRef]
  23. Augustinos, A.A.; Tsiamis, G.; Caceres, C.; Abd-Alla, A.M.M.; Bourtzis, K. Taxonomy, diet, and developmental stage contribute to the structuring of gut-associated bacterial communities in thephritid pest species. Front. Microb. 2019, 10, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Blow, F.; Gioti, A.; Goodhead, I.B.; Kalyva, M.; Kampouraki, A.; Vontas, J.; Darby, A.C. Functional Genomics of a Symbiotic Community: Shared Traits in the Olive Fruit Fly Gut Microbiota. Genome Boil. Evol. 2019, 12, 3778–3791. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Koskinioti, P.; Ras, E.; Augustinos, A.A.; Tsiamis, G.; Beukeboom, L.W.; Caceres, C.; Bourtzis, K. The effects of geographic origin and antibiotic treatment on the gut symbiotic communities of Bactrocera oleae populations. Èntomol. Exp. et Appl. 2019, 167, 197–208. [Google Scholar] [CrossRef] [Green Version]
  26. Scalzo, R.L.; Scarpati, M.L.; Verzegnassi, B.; Vita, G. Olea europaea chemicals repellent toDacus oleae females. J. Chem. Ecol. 1994, 20, 1813–1823. [Google Scholar] [CrossRef]
  27. Malheiro, R.; Ortiz, A.; Casal, S.; Baptista, P.; Pereira, J.A. Electrophysiological response of Bactrocera oleae (Rossi) (Diptera: Tephritidae) adults to olive leaves essential oils from different cultivars and olive tree volatiles. Ind. Crop. Prod. 2015, 77, 81–88. [Google Scholar] [CrossRef]
  28. Scarpati, M.L.; Scalzo, R.L.; Vita, G. Olea europaea Volatiles attractive and repellent to the olive fruit fly (Dacus oleae, Gmelin). J. Chem. Ecol. 1993, 19, 881–891. [Google Scholar] [CrossRef]
  29. Scarpati, M.L.; Scalzo, R.L.; Vita, G.; Gambacorta, A. Chemotropic behavior of female olive fly (Bactrocera oleae, GMEL.) on Olea eruopaea L. J. Chem. Ecol. 1996, 22, 1027–1036. [Google Scholar] [CrossRef]
  30. Canale, A.; Benelli, G.; Salvatore, G. Behavioral and electrophysiological responses to overlooked female pheromone components in the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae ). Chemoecology 2015, 25, 147–157. [Google Scholar] [CrossRef]
  31. Carpita, A.; Canale, A.; Raffaelli, A.; Saba, A.; Benelli, G.; Raspi, A. (Z)-9-tricosene identified in rectal gland extracts of Bactrocera oleae males: First evidence of a male-produced female attractant in olive fruit fly. Naturwissenschaften 2011, 99, 77–81. [Google Scholar] [CrossRef]
  32. Liscia, A.; Angioni, P.; Sacchetti, P.; Poddighe, S.; Granchietti, A.; Setzu, M.; Belcari, A. Characterization of olfactory sensilla of the olive fly: Behavioral and electrophysiological responses to volatile organic compounds from the host plant and bacterial filtrate. J. Insect Physiol. 2013, 59, 705–716. [Google Scholar] [CrossRef]
  33. Vitanović, E.; Aldrich, J.R.; Boundy-Mills, K.; Čagalj, M.; E Ebeler, S.; Burrack, H.; Zalom, F.G. Olive Fruit Fly, Bactrocera oleae (Diptera: Tephritidae), Attraction to Volatile Compounds Produced by Host and Insect-Associated Yeast Strains. J. Econ. Èntomol. 2019, 113, 752–759. [Google Scholar] [CrossRef]
  34. Lopez-D, F.; Steiner, L.F.; Holbrook, F.R. A New Yeast Hydrolysate-Borax Bait for Trapping the Caribbean Fruit Fly. J. Econ. Èntomol. 1971, 64, 1541–1543. [Google Scholar] [CrossRef]
  35. Bortoli, L.C.; Machota, R.; Garcia, F.R.M.; Botton, M. Evaluation of Food Lures for Fruit Flies (Diptera: Tephritidae) Captured in a Citrus Orchard of the Serra Gaúcha. Fla. Èntomol. 2016, 99, 381–384. [Google Scholar] [CrossRef] [Green Version]
  36. Burrack, H.; Connell, J.H.; Zalom, F.G. Comparison of olive fruit fly (Bactrocera oleae (Gmelin)) (Diptera: Tephritidae) captures in several commercial traps in California. Int. J. Pest Manag. 2008, 54, 227–234. [Google Scholar] [CrossRef]
  37. Vitanović, E.; Aldrich, J.R.; Winterton, S.L.; Boundy-Mills, K.; Lopez, J.M.; Zalom, F.G. Attraction of the Green Lacewing Chrysoperla comanche (Neuroptera: Chrysopidae) to Yeast. J. Chem. Ecol. 2019, 45, 388–391. [Google Scholar] [CrossRef]
  38. Sitepu, I.R.; Selby, T.; Lin, T.; Zhu, S.; Boundy-Mills, K.L. Carbon source utilization and inhibitor tolerance of 45 oleaginous yeast species. J. Ind. Microbiol. Biotechnol. 2014, 41, 1061–1070. [Google Scholar] [CrossRef] [Green Version]
  39. Sitepu, I.R.; Sestric, R.; Ignatia, L.; Levin, D.; German, J.B.; Gillies, L.A.; Almada, L.A.; Boundy-Mills, K.L. Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresour. Technol. 2013, 144, 360–369. [Google Scholar] [CrossRef] [Green Version]
  40. Kendall, M.; Stuart, A. The advanced theory of statistics: Inference and relationship, 4th ed.; Charles Griffin: London, UK, 1979; Volume 2, pp. 1–723. [Google Scholar]
  41. Rhoades, H.M.; Overall, J.E. A sample size correction for Pearson chi-square in 2 × 2 contingency tables. Psychol. Bull. 1982, 91, 418–423. [Google Scholar] [CrossRef]
  42. Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 1979, 6, 65–70. [Google Scholar]
  43. Rice, W.R. Analyzing tables of statistical tests. Am. Sociol. Rev. 1989, 78, 1–3. [Google Scholar] [CrossRef]
  44. Mangan, R.L.; Thomas, D.B. Comparison of torula yeast and various grape juice products as attractants for Mexican fruit fly (Diptera: Tephritidae). J. Econ. Èntomol. 2014, 107, 591–600. [Google Scholar] [CrossRef] [PubMed]
  45. Becher, P.G.; Flick, G.; Rozpędowska, E.; Schmidt, A.; Hagman, A.; Lebreton, S.; Larsson, M.C.; Hansson, B.S.; Piškur, J.; Witzgall, P.; et al. Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct. Ecol. 2012, 26, 822–828. [Google Scholar] [CrossRef]
  46. Ganter, P. Yeast and invertebrate associations. In The Yeast Handbook: Biodiversity and Ecophysiology of Yeasts; Peter, G., Rosa, C., Eds.; Springer: Berlin, Germany, 2006; pp. 303–369. [Google Scholar]
  47. Hamby, K.A.; Hernández, A.; Boundy-Mills, K.L.; Zalom, F.G. Associations of Yeasts with Spotted-Wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in Cherries and Raspberries. Appl. Environ. Microbiol. 2012, 78, 4869–4873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Janson, E.M.; Stireman, J.O.; Singer, M.S.; Abbot, P. Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 2008, 62, 997–1012. [Google Scholar] [CrossRef] [Green Version]
  49. Phaff, H.J.; Starmer, W.T. Yeasts associated with plants, insects, and soil. In The Yeasts, 2nd ed.; Rose, A.H., Harrison, J.S., Eds.; Academic Press: Cambridge, MA, USA, 1987; pp. 123–180. [Google Scholar]
  50. Brysch-Herzberg, M. Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiol. Ecol. 2004, 50, 87–100. [Google Scholar] [CrossRef]
  51. Davis, T.S.; Boundy-Mills, K.; Landolt, P.J. Volatile Emissions from an Epiphytic Fungus are Semiochemicals for Eusocial Wasps. Microb. Ecol. 2012, 64, 1056–1063. [Google Scholar] [CrossRef]
  52. Hagen, K.S.; Tassan, R.L.; Sawall, E.F., Jr. Some ecophysiological relationships between certain Chrysopa, honeydews and yeasts. Boll. Lab. Entomol. Agrar. Portici. 1970, 28, 113–134. [Google Scholar]
  53. Gibson, C.M.; Hunter, M.S. Reconsideration of the role of yeasts associated with Chrysoperla green lacewings. Boil. Control. 2005, 32, 57–64. [Google Scholar] [CrossRef]
  54. Daanel, K.M.; Yokota, G.Y. Release Strategies Affect Survival and Distribution of Green Lacewings (Neuroptera: Chrysopidae) in Augmentation Programs. Environ. Èntomol. 1997, 26, 455–464. [Google Scholar] [CrossRef]
Agronomy 10 01501 g001 550
Figure 1. Photomicrographs of active cultures of five insect-associated yeast strains selected for the spring 2016 field testing, grown in 3× or 5× yeast extract/malt extract (YM) broth as described. Photos were taken with a Carl Zeiss Axio Imager.A1, Jena, Germany with a 100X oil immersion objective, phase contrast.
Figure 1. Photomicrographs of active cultures of five insect-associated yeast strains selected for the spring 2016 field testing, grown in 3× or 5× yeast extract/malt extract (YM) broth as described. Photos were taken with a Carl Zeiss Axio Imager.A1, Jena, Germany with a 100X oil immersion objective, phase contrast.
Agronomy 10 01501 g001
Agronomy 10 01501 g002 550
Figure 2. Total number of Bactrocera oleae captured in traps that contained active culture formulations of 12 yeast strains and controls field-tested in fall 2015. Bars associated with different lowercase letters are significantly different at p ≤ 0.05 by the Chi-square test. Asterisks represent significant differences in the attraction of the sexes within the same yeast strain, while different uppercase letters indicate differences in the attraction of the sexes in all tested traps (p ≤ 0.05 by Chi-square test).
Figure 2. Total number of Bactrocera oleae captured in traps that contained active culture formulations of 12 yeast strains and controls field-tested in fall 2015. Bars associated with different lowercase letters are significantly different at p ≤ 0.05 by the Chi-square test. Asterisks represent significant differences in the attraction of the sexes within the same yeast strain, while different uppercase letters indicate differences in the attraction of the sexes in all tested traps (p ≤ 0.05 by Chi-square test).
Agronomy 10 01501 g002
Agronomy 10 01501 g003 550
Figure 3. Bactrocera oleae collected in McPhail traps containing active and inactive formulations of (A) Kuraishia capsulata, (B) Peterozyma xylosa, (C) Nakazawaea ernobii, (D) Lachancea thermotolerans, and (E) Scheffersomyces ergatensis as attractants placed in olive orchard. Results presented are mean values of four measurements (duplicate traps in two independent repetitions). Bars labeled by different letters are significantly different at p ≤ 0.05 by the Chi-square test. Error bars indicate SE. Control traps were torula yeast, water, PDB, media 3×, and media 5× (see also Table 1).
Figure 3. Bactrocera oleae collected in McPhail traps containing active and inactive formulations of (A) Kuraishia capsulata, (B) Peterozyma xylosa, (C) Nakazawaea ernobii, (D) Lachancea thermotolerans, and (E) Scheffersomyces ergatensis as attractants placed in olive orchard. Results presented are mean values of four measurements (duplicate traps in two independent repetitions). Bars labeled by different letters are significantly different at p ≤ 0.05 by the Chi-square test. Error bars indicate SE. Control traps were torula yeast, water, PDB, media 3×, and media 5× (see also Table 1).
Agronomy 10 01501 g003
Agronomy 10 01501 g004 550
Figure 4. Chrysoperla comanche collected in McPhail traps containing active formulations of Peterozyma xylosa, Scheffersomyces ergatensis, Nakazawaea ernobii, Kuraishia capsulata, and Lachancea thermotolerans as attractants placed in an olive orchard in spring 2016. Results are mean values of four measurements (duplicate traps in two independent repetitions). Bars labeled by different letters are significantly different at p ≤ 0.05 by the Chi-square test. Error bars indicate SE.
Figure 4. Chrysoperla comanche collected in McPhail traps containing active formulations of Peterozyma xylosa, Scheffersomyces ergatensis, Nakazawaea ernobii, Kuraishia capsulata, and Lachancea thermotolerans as attractants placed in an olive orchard in spring 2016. Results are mean values of four measurements (duplicate traps in two independent repetitions). Bars labeled by different letters are significantly different at p ≤ 0.05 by the Chi-square test. Error bars indicate SE.
Agronomy 10 01501 g004
Agronomy 10 01501 g005 550
Figure 5. Chrysoperla comanche collected in McPhail traps containing inactive formulations of Nakazawae ernobii, Peterozyma xylosa, Scheffersomyces ergatensis, Kuraishia capsulate, and Lanhancea thermotolerans as attractants placed in an olive orchard in spring 2016. Results are mean values of four measurements (duplicate traps in two independent repetitions). Bars labeled by different letters are significantly different at p ≤ 0.05 by the Chi-square test. Error bars indicate SE. Asterisks represent a significant difference in mean number of C. comanche captured in traps with inactive compared with active formulations (see Figure 4) of the same yeast strains.
Figure 5. Chrysoperla comanche collected in McPhail traps containing inactive formulations of Nakazawae ernobii, Peterozyma xylosa, Scheffersomyces ergatensis, Kuraishia capsulate, and Lanhancea thermotolerans as attractants placed in an olive orchard in spring 2016. Results are mean values of four measurements (duplicate traps in two independent repetitions). Bars labeled by different letters are significantly different at p ≤ 0.05 by the Chi-square test. Error bars indicate SE. Asterisks represent a significant difference in mean number of C. comanche captured in traps with inactive compared with active formulations (see Figure 4) of the same yeast strains.
Agronomy 10 01501 g005
Table
Table 1. Yeast strains from the Phaff Yeast Culture Collection (UCDFST).
Table 1. Yeast strains from the Phaff Yeast Culture Collection (UCDFST).
Yeast Strain and UCDFST ID NumberGeographic SourceHabitat Source
Kuraishia capsulata UCDFST 68-897.1British Columbia, CanadaBeetle frass in Pinus contorta
Peterozyma xylosa UCDFST 52-162California, USADrosophila miranda
Ogataea pini UCDFST 52-128California, USAFrass of bark beetle Ips oregoni in Pinus contorta
Solicoccozyma terrea UCDFST 05-757California, USABactrocera oleae (olive fruit fly) adult male
Nakazawaea ernobii UCDFST 51-28UnknownCaeca of larva of Ernobius mollis beetle
Lachancea thermotolerans UCDFST 04-833California, USABactrocera oleae (olive fruit fly) adult male
Vishniacozyma cf. foliicola UCDFST 05-508California, USABactrocera oleae (olive fruit fly) adult female
Scheffersomyces ergatensis UCDFST 80-53SpainErgastes faber beetle
Filobasidium oeirensis UCDFST 05-501California, USABactrocera oleae (olive fruit fly) adult male
Wickerhamomyces subpelliculosus UCDFST 76-85USAFermenting cucumbers
Jianyunia aff. sakaguchii UCDFST 73-1015California, USABark beetle frass in Abies magnifica
Cyberlindnera jadinii (syn. Candida utilis, Torula yeast) UCDFST 75-33USATorula yeast cultivation tank

Share and Cite

MDPI and ACS Style

Vitanović, E.; Lopez, J.M.; Aldrich, J.R.; Jukić Špika, M.; Boundy-Mills, K.; Zalom, F.G. Yeasts Associated with the Olive Fruit Fly Bactrocera oleae (Rossi) (Diptera: Tephritidae) Lead to New Attractants. Agronomy 2020, 10, 1501. https://doi.org/10.3390/agronomy10101501

AMA Style

Vitanović E, Lopez JM, Aldrich JR, Jukić Špika M, Boundy-Mills K, Zalom FG. Yeasts Associated with the Olive Fruit Fly Bactrocera oleae (Rossi) (Diptera: Tephritidae) Lead to New Attractants. Agronomy. 2020; 10(10):1501. https://doi.org/10.3390/agronomy10101501

Chicago/Turabian Style

Vitanović, Elda, Julian M. Lopez, Jeffrey R. Aldrich, Maja Jukić Špika, Kyria Boundy-Mills, and Frank G. Zalom. 2020. "Yeasts Associated with the Olive Fruit Fly Bactrocera oleae (Rossi) (Diptera: Tephritidae) Lead to New Attractants" Agronomy 10, no. 10: 1501. https://doi.org/10.3390/agronomy10101501

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop