Abstract
In insects, cuticular lipids prevent water loss and act as semiochemicals. Because of their ecological function, the profile change across the insects’ sex and development offers insight into insect biology and possible tools for pest management. Here, the first work on cecidomyiid cuticular extracts is proposed considering Dasineura oleae (Diptera: Cecidomyiidae) males and females at different adult ages (0–12 h, 12–24 h, 24–36 h) and distinct sexual conditions (virgin and mated). A set of 49 compounds were recorded (12 alkanes, 1 monomethyl alkane, 11 fatty acids, 4 esters, 1 aldehyde, 1 allylbenzene, 1 amine, 1 flavonoid, 1 ketone, 1 phenol, 1 steradiene, 1 sterol, 1 terpene, 1 triterpene and 11 unknown compounds), and 18 of them showed significant differences between groups. Among alkanes, hexacosane (nC26) exhibited a decreasing trend from the youngest to the oldest females, while pentacosane (nC25) and nonacosane (nC29) showed a decreasing trend from 0 to 12 h to 12–24 h virgin females. In addition, nonadecane (nC19) was significantly more abundant in the youngest males compared to older males and females. The alkanes nC25, nC26 and nC29 have been reported to be age-related also in other dipterans, while nC19 has been described as gender-specific chemical cue for platygastrid parasitoids. Further behavioural trials and analyses are required to assign the specific ecological roles to the characterized compounds. Our results may contribute to develop new low-impact control strategies relying on the manipulation of D. oleae’s chemical communication (e.g. disruption of mating or species recognition).
Highlights
• Cuticular hydrocarbons are often involved in dipteran intraspecific communication.
• We explored the cuticular profile of D. oleae at different age, sex, mating condition.
• Five alkanes and one mono-methyl alkane showed differences among groups.
• Linoleic acid is the most abundant compound in virgins, absent in mated insects.
• Eleven compounds disappear in mated insects, but were present in all virgins.
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Introduction
Insect cuticle is covered with a very thin layer of wax consisting of lipids. Among lipids are included hydrocarbons, alcohols, waxes, glycerides, phospholipids, glycolipids, and fatty acids (Drijfhout et al. 2010). Insect cuticular hydrocarbons (CHCs) are essential to withstand environmental stress and desiccation since they cover the entire body surface of insects forming several layers made up of numerous compounds that can be adjusted according to environmental needs (Golebiowski et al. 2011; Chung and Carroll 2015; Otte et al. 2018; Menzel et al. 2019). CHCs are synthetized in secretory cells, called oenocytes, located in the abdominal epidermis (Krupp and Levine 2010) and transferred to insect cuticle (Chung and Carroll 2015). Insect CHCs are classified as long-chain hydrocarbons (20–40 carbons), mainly alkanes, alkenes, alkadienes, methyl-branched alkanes and methyl-branched alkenes (Gibbs 2002; Chung and Carroll 2015; Otte et al. 2018). Their biological functionality is determined by physical properties, such as viscosity and melting point (Menzel et al. 2019). Recently, Menzel et al. (2019) demonstrated that the waterproof characteristic of insect cuticle is due to biphasic CHC layers forming a solid-liquid mixture under ambient conditions. However, even if the main function of CHCs remains desiccation prevention (Mullen et al. 2007), CHCs are also involved in many aspects of chemical communication. Some CHCs play important roles in insect mimicry, labour division (i.e. in social insects) and mating, acting as close-contact pheromones (Ferveur 2005; Howard and Blomquist 2005; Hoffmann et al. 2006; Chung and Carroll 2015; Scolari et al. 2021). Within some insect families, such as Drosophilidae (Jackson and Bartelt 1986), Vespidae (Neves et al. 2012) and Apidae (Vernier et al. 2019), it has been proved that the expression of hydrocarbons undergoes consistent changes in terms of compound composition and concentration during the whole insect development (Butterworth et al. 2020a; Cortot et al. 2022). Particularly, CHCs can be expressed differently in the various developmental stages (Kuo et al. 2012; Butterworth et al. 2019), especially during the pre-reproductive adult phase (Butterworth et al. 2020a), and between the two sexes (Buellesbach et al. 2013; Dapporto et al. 2013; Stinziano et al. 2015). These differences act as indicators of sexual maturity and reproductive viability (Butterworth et al. 2020a). Moreover, in intraspecific relationships, they influence the recognition between species and the attraction of potential mates (Singer 1998; Monnin 2006; Ingleby 2015). Even if the study of CHCs related to insect aging may be an important tool for forensic entomology, few works are nowadays available on this topic (Butterworth et al. 2020a). Furthermore, a better understanding the role of CHCs in insect ecology may lead to the development of new pest control and monitoring (e.g. disruption of mating or species recognition), since for most insect pests the Integrated Pest Management (IPM) and Biological Control strategies rely on manipulating chemical communication (Snellings et al. 2018).
Among dipterans having agricultural importance, the characterization of cuticular compounds has been performed only on few pests, including livestock parasites (e.g. blowflies) (see Braga et al. 2016; Bernhardt et al. 2017; Butterworth et al. 2018, 2020a, b), and fruit flies, such as Drosophila spp. (Cobb and Ferveur 1995; Jennings et al. 2014; Snellings et al. 2018; Cortot et al. 2022), Ceratitis spp. (Vaníčková et al. 2014), Bactrocera spp. (Carlson and Yocom 1986; Galhoum 2017; Park et al. 2020), Anastrepha spp. (Vaníčková et al. 2012) and Zeugodacus cucurbitae (Carlson and Yocom 1986). To the best of our knowledge, reports on the characterization of cecidomyiid (Diptera: Cecidomyiidae) cuticular profiles are not available so far, even if several gall midges are considered serious crop pests worldwide (Hall et al. 2012).
Dasineura oleae (Angelini) (Diptera: Cecidomyiidae) is a gall inducer on Olea europaea L., endemic in the Mediterranean Basin (Doğanlar et al. 2011; Simoglou et al. 2012; Tondini and Petacchi 2019; Caselli et al. 2021a; Picchi et al. 2021; Magagnoli et al. 2022). It has been commonly discussed as a minor pest in the olive orchard but starting from 2012 its relevance has increased in many regions of the Mediterranean where several outbreaks have been reported (Picchi et al. 2017; Tondini and Petacchi 2019). To date, notions about the control strategies of this pest are scanty and not up to date. Thus, to be in keeping with IPM control strategies, research on low environmental impact approaches is urgently needed.
Here, we present a descriptive study on D. oleae aiming to characterize its CHCs profile. Analyses of virgin and mated individuals of both sexes at different ages were conducted to understand differences among treatments and to lay the foundations for potential alternative control tools against D. oleae.
Materials and Methods
Insect Collection
Shoots with galled leaves by D. oleae were collected during March and April 2021 from an infested olive orchard located in Gavorrano (Grosseto, Italy) (42°54’28.30’’ N, 11°00’10.65’’E) considering the timing of the emergence of D. oleae reported by Caselli et al. (2021b) at the same place in 2020. After collection, shoots with a maximum of 2 leaves having 5 galls each were selected and placed in plastic transparent containers (diameter 87 mm, length 115 mm) closed at one extremity with a chiffon fabric (mesh size 0.04 mm) to allow aeration. The shoot stems were immersed in tap water to prevent fast foliar desiccation. Infested olive shoots were replaced every 4 days in order to have fresh specimens.
From the first emergence, the containers were controlled every 12 h (at 9.00 a.m. and 9.00 p.m.) and the emerged individuals were isolated in single vials (one insect per vial). Insects were maintained alive and starved until they reached a required age (0–12 h, 12–24 h, 24–36 h), then they were killed by freezing (-20 °C) and separated by age in groups of 25 individuals (males and females). For each of the 3 age groups, 5 replicates were done and if both males and females were found in the same container at the same collection time, they were not considered. All groups were stored at -20 °C (Fig. 1).
The collection of mated individuals was based on our laboratory observations, as no mating behaviours (e.g. female calling behavior) have been described for D. oleae. We observed that males of this species were capable of mating multiple times, so we placed two virgin males with five virgin females in a Petri dish and observed for copulation to occur. After 6 h, males and females were separated and frozen at -20 °C in groups of 25 individuals (age: 6–18 h). Five replicates per sex were done (Fig. 1).
CHC Extraction and Analysis
For each sample, the midges (25 individuals of the same age group and sex) were placed in a 1.5 ml GC vial (LGG-Labware, Germany), and 500 µL pentane were added in the vial. The vials were then agitated in an ultrasound bath (ultrasonic cleaner 5510, 40 kHz, Branson, USA) for 2 min. The extract was transferred to a clean vial using a 500 µL glass syringe (Hamilton, Merck KGaA, Darmstadt, Germany), while insects remained in the old vial. The new vials were then opened under a gentle stream of nitrogen gas to allow the solvent to evaporate. Upon complete evaporation, 200 µL of a solution of heptane and pentadecane 10− 4, as internal standard, were added to the vial and manually agitated for 1 min to allow solubilization of the dried residues. The samples were analysed by injecting 2 µL into a GC (7890, Agilent Technologies, Santa Clara, USA) splitless mode equipped with a mass selective detector-MS (5975 C, Agilent Technologies). A GC/MS nonpolar HP-5 MS column (Agilent Technology, 30 m x 0.25 mm x 0.25 μm film thickness) was used for separation with a constant helium flow of 1.2 mL/min at an average velocity of 39.62 cm/s. The oven temperature program was started at 35 °C for 2 min and heated to 280 °C at a rate of 7.5 °C/min, held for 5 min. The total run time was 39.66 min. The mass spectrometric detector was operated in scan mode (m/z 20–550 amu). The compounds were initially identified by comparing their mass spectra with those found in two libraries: NIST 20 (National Institute of Standards and Technology 2020) and Wiley 7 (John Wiley, NY, USA); a mixture of n-alkane standards (nC8-nC20, Sigma-Aldrich, St. Louis, Missouri, USA) was used to calculate the linear retention indexes (LRI) of the detected compounds (Van den Dool and Kratz 1963). The compounds were identified based on the comparison of their retention index with the retention indexes reported in the literature (PubChem, Nist, Pherobase). The compounds were finally confirmed by comparing their retention times with those available from synthetic standards (Sigma-Aldrich, St. Louis, Missouri, USA). Compounds that were also detected in a negative control (solvent only) were considered contaminants. The total ion current (TIC) amount of each compound was compared to that of the internal standard pentadecane (nC15) 10− 4 and the values are reported as a percentage proportion.
Data Analysis
The statistical analysis was performed using the software R (R Core Team 2021). Each compound was tested for variations due to age (0-12 h, 12-24 h, 24-36 h) and sex (female, male) in virgin individuals and for variations due to mating condition (virgin 12-24 h, mated 6-18 h) and sex (female, male) in virgin and mated individuals by ANOVA test. Values were square root transformed to achieve normalization. A post-hoc pairwise Tukey-test with Bonferroni correction was applied to discriminate among the groups (“multcomp” package, Hothorn et al. 2008).
A dimension reduction principal component analysis (PCA) was performed using the R package “factoextra” (Kassambara and Mundt 2020). The PCA calculated the combination of the compound area data by extracting eigenvalues and eigenvectors of a correlation matrix and then highlighting principal components. A two-dimensional score plot was created to compare the cuticular profiles of the different groups.
All the data are reported as mean ± standard deviation. The figures were created by using the R packages “ggplot2” and “cowplot” (Wickham 2016; Wilke 2020).
Results
A total of 49 compounds were detected from the analyses of the cuticular extractions of D. oleae virgin and mated individuals (Table 1).
Authors’ observations allow to affirm that each male mated more than once with different virgin females, while females appeared to be monogamous.
Identification was not possible for 11 compounds as reported in the last part of Table 1. To better understand differences among chemical classes, compounds showing statistically differences were grouped as reported in Fig. 2.
Compounds of Virgins
Among the collected compounds, 13 were characteristic of only virgin males and females, and only one was present in females of 1st age (i.e. unknown 5) and 2 were present in individuals of 1st and 2nd age (i.e. stearic acid and unknown 6). Ethyl linoleate was one of the compounds absent in mated individuals, and its amount remained constant within virgin males, while it significantly increased in 12–24 h females (F2,24=7.45, p = 0.0038). Myristoleic acid showed a decreasing amount with age in both sexes (F2,24=36.40, p < 0.001) and an overall lower amount in males (F1,24=10.95, p = 0.031). The amount of α-tocopherol, absent in mated individuals, did not follow any trends, but in males was almost double to that in females (F1,24=42.76, p < 0.001). Dihydroactinidiolide was lower in virgin males than in virgin females (F1,24=99.9, p < 0.001).
Compounds of the Mated
Four compounds found only in mated individuals; two of them where characteristic of both sexes (i.e. undecane, unknown 4), and two were found only in mated males (i.e. unknown 3, hexadecane). Other compounds were instead absent from the virgins of a sex and appeared only after mating. Tetradecanal was present only in virgin females and decreased with age (F2,24=91.24, p < 0.001), but in mated individuals of both sexes it was at least two-fold higher (F1,12=100.91, p < 0.001), even if mated males had less than mated females (F1,12=7.17, p = 0.021). Like tetradecanal, octacosane was not present in virgin males, appearing then in mated ones in a lower amount than in mated females (F1,12=7.78, p = 0.016). The amine N-(2-phenylethyl) acetamide was detected in all the males but in the females only after mating. The amount in mated females and virgin males averages about half than in the mated males but no significant difference was found between the groups (F2,12= 1.89, p = 0.26).
Compounds that Decrease in Mated
The amount of ethyl hexadecanoate was significantly lower in mated females and males (F1,16=135.9, p < 0.001) whilst linoleoylglycerol increased in females after mating but decreased in males (F1,12=71.06, p < 0.001). The amount of 3,5-stigmastadiene was significantly lower in mated individuals of both sexes (F1,15=81.84, p < 0.001) compared to the virgins. Caprylic acid decreased in mated males in respect to mated females (F1,12=8.74, p = 0.012) and virgin males (F1,10=6.58, p = 0.024), but not in mated females (F1,12=1.03, p = 0.16). β-Ionone was lower in virgin males (F1,24=98.2, p < 0.001) and decreased significantly after the mating (F1,11=121.8, p < 0.001). The amount of nonadecane (F1,16=0.09, p = 0.76), methyl linoleate (F1,16=0.33, p = 0.57) did not show any differences between mated females and males. Nonadecane was more abundant in virgin males (F1,23=4.81, p = 0.038), but decreased after mating (F1,16=7.13, p = 0.016). Also methyl linoleate decreased in mated insects (F1,16=93.20, p < 0.001).
Compounds that Decrease with Age
Capric acid differed between sex of virgins (F1,24=4.45, p = 0.045) and decreased with age (F1,24=53.88, p < 0.001) and mating condition (F1,15=17.53, p < 0.001). Similarly, lauric acid differed between sex of virgins (F1,24=6.04, p = 0.021) and decreased with age (F1,24=91.14, p < 0.001) and mating condition (F1,16=59.35, p < 0.001). Palmitic acid decreased with age (F2,24=8.24, p = 0.002) and after mating (F1,16=5.47, p = 0.032). Palmitoleic acid amount decreased with age (F2,24=11.33, p = 0.0003) and in mated (F1,15=35.40, p < 0.001). Myristic acid (F2,24=94.17, p < 0.001) showed the same trend, decreasing with age in both virgin sexes, and was lower in males (F1,24=21.87, p < 0.001). Furthermore, the amount of myristic acid did not differ between the sex of mated midges (F1,16=1.06, p = 0.33).
Compounds that Differ Between Sex
Dihydroactinidiolide was lower in virgin males than in virgin females (F1,24=99.9, p < 0.001). Heptacosane was lower in virgin males (F1,24=7.07, p = 0.013). Unknown 9 was higher in males than in females both virgin (F1,24=98.81, p < 0.001) and mated (F1,14=29.32, p < 0.001) but decreased after mating (F1,14=157.4, p < 0.001). A decreasing trend was recorded for hexacosane in virgin females (F2,24=3.25, p = 0.024) and its amount was overall lower in males, both virgin (F1,24=16.13, p = 0.0005) and mated (F1,16=8.32, p = 0.0108). 9-Methylnonacosane was not recorded in virgin males but appeared in the mated ones. The amount of pentacosane was lower in males than in females, both in virgin (F1,24=22.13, p < 0.001) and mated (F1,16=7.88, p = 0.012). The same was reported for nonacosane in virgin (F1,24=7.82, p = 0.01) and mated males (F1,16=5.61, p = 0.03).
Having used pentadecane as an internal standard did not allow to assess whether this compound is part of the insect cuticular hydrocarbons. However, statistical analysis did not reveal differences between pentadecane absolute values (F7,32= 1, p = 0.49), which were instead extremely similar, with no variation between groups.
PCA allowed to determine the clustering of the cuticular compounds based on sex and age (Fig. 3). The individuals are clearly clustered together, showing a general transition along PC1 (43.5%) according to age. While the virgins are divided by sex on PC2 (16.9%), the transition to the mated individuals showed a remarkable deviation along the principal components.
Discussion
Dipteran cuticular hydrocarbons have received wide attention, but no information is currently available on any cecidomyiid species. Here, the first report on cuticular extracts characterizing a gall midge, D. oleae, is proposed.
Insect cuticular hydrocarbons are mainly present in two forms, as saturated (alkanes) and unsaturated compounds (alkenes) (Sharma et al. 2020). In this work, five linear alkanes and one monomethyl alkane showed differences between groups, while no alkenes were recorded. Among alkanes, pentacosane, octacosane and nonacosane were present. These compounds are three main components of the Aedes aegypti L. (Diptera: Culicidae) cuticular profile and are used in medical entomology to estimate female mosquito age (Desena et al. 1999; Gerade et al. 2004). Similarly, in the D. oleae cuticular profile, the female amount of pentacosane and nonacosane changes with age. Pentacosane is also known as a fertility signal in the subsocial bee Ceratina calcarata Robertson (Hymenoptera: Apidae), acting as a precursor of queen sexual pheromone (Pizzi and Rehan 2021). It is particularly abundant in sexually mature flies belonging to Chrysomya varipes (Macquart) (Diptera: Calliphoridae) species (Butterworth et al. 2020a), and it is a cuticular component of the Drosophila melanogaster Meigen (Diptera: Drosophilidae) profile (Rajpurohit et al. 2016). Contrary to pentacosane and nonacosane, the amount of octacosane remained unvaried among the ages of virgin females but changed after mating. Octacosane seems to be a common insect hydrocarbon, since it is also present in the cuticular profile of Blattella germanica (L.) (Blattodea: Blattellidae) (Augustnowicz et al. 1986), Melipona quadrifasciata (le Peletier) (Hymenoptera: Apidae) (Borges et al. 2012) and workers of Oecophylla smaragdina (Fabricus) (Hymenoptera: Formicidae) (Azhagu Raj et al. 2017). Hexacosane showed a decreasing trend from the youngest to oldest virgin females of D. oleae, as already demonstrated for the mosquito Ae. aegypti (Polerstock et al. 2002). It is also present in the female cuticular profile of other dipterans, such as Lucilia cuprina (Wiedemann) and Hemilucilia segmentaria (Fabricus) (Diptera: Calliphoridae) (Rocha Barbosa et al. 2017). In our study, the amount of nonadecane was almost double in 0–12 h virgin males compared to 0–12 h virgin females. Differences of this compound among sexes have been already documented in the stink bug Nezara viridula (L.) (Hemiptera: Pentatomidae), where its egg parasitoid, Trissolcus basalis (Wollaston) (Hymenoptera: Platygastridae), uses nonadecane as a gender-specific chemical cue of N. viridula, showing a significant preference for females which extract did not contain this compound (Colazza et al. 2007). Since several species of D. oleae parasitoids are platygastrids (Stavraki 1970; Moallem 1975; Doğanlar 2011; Baidaq et al. 2015; Batta 2019; Tondini and Petacchi 2019), the implication of nonacosane in D. oleae-parasitoid interactions requires further investigation. The only methyl branched alkane recorded in our study was 9-methylnonacosane. It is known to be part of the epicuticular profile of the redbanded stink bug Piezodorus guildinii (Westwood) (Heteroptera: Pentatomidae), an important pest of soybean crops in South America (Sessa et al. 2021).
Environmental factors (e.g. air, water vapor, ultraviolet radiation) can alter and breakdown insects’ cuticular hydrocarbons disrupting chemical communication (Hatano et al. 2020). Therefore, some species have adapted to this phenomenon by emitting volatile organic compounds (VOCs) that might be recorded in cuticular extracts (Hatano et al. 2020). For example, the volatile long-range pheromones often included aldehydes originated through the oxidation (e.g. photooxidation, autoxidation) of non-volatile cuticular waxes (Bartelt et al. 2002). Moreover, whole body extraction may also allow to dissolve non-cuticular compounds as for instance those present in the secretion of exocrine glands (Provost et al. 2008). In our study, tetradecanal was typical of D. oleae virgin females and mated individuals of both sexes. It is known as the most abundant aldehyde from males of the sawfly Cephus cintus Norton (Hymenoptera: Cephide) (Bartelt et al. 2002), and as one of the representative components of the Acheta domesticus (L.) (Orthoptera: Gryllidae) profile (Warthen and Uebel 1980). Furthermore, tetradecanal was found to have different roles depending on sex, as in the case of Rossomyrmex minuchae Tinaut (Hymenoptera: Formicidae), in which tetradecanal has been recorded as the major component of queen Dufour’s glands having a repellent effect on ants belonging to another species that is usurped by Rossomyrmex queens for new host nests (Ruano et al. 2005). In Bombus spp. Latreille (Hymenoptera: Apidae) tetradecanal is instead used by males as a territorial-marking pheromone (Urbanová et al. 2004). Being tetradecanal found in mated males (but in lower amount than in mated females), we question whether it could be passed from the females to the males during the mating, and what possible ecological role it might have. The same was observed also for octacosane, thus suspecting a similar route of transmission while mating.
Among fatty acids found in the cuticular extracts of D. oleae, myristic acid, myristoleic acid and palmitoleic acid significantly decreased in virgin individuals from the youngest to oldest. Concerning the mating condition, it is interesting to note that linoleic acid is present just in virgin individuals and completely absent in mated ones, and its amount in all the virgin ages is 2–3 times more abundant compared the internal standard. However, to the best of our knowledge a potential role of these acids in insect chemical communication is still uninvestigated. Fatty acids methyl and ethyl esters are common in the honeybee (Apis mellifera L.), and are fundamental for the chemical communication of larvae, workers and queen (Slessor et al. 2005). Furthermore, in the solitary bee Osmia rufa (Hymenoptera: Megachilidae) they constitute the main components of the sexual pheromone (Krieger et al. 2006). In our work, ethyl linoleate and methyl linoleate were recorded having different amounts between groups, but no literature was found on their ecological role as pheromones in insects. Furthermore, we recorded hexadecenoic acid ethyl ester and linoleoylglycerol, showing differences in mated individuals. Ethyl hexadecanoate is known as a volatile compound of Protaetia brevitarsis Lewis (Coleoptera: Scarabeidae) larvae (Yeo et al. 2013), while in adult insects it is a gender specific compound of Bicyclus martius sanaos (Hewitson) (Lepidoptera: Nymphalidae) males (Wang et al. 2014). Ethyl hexadecanoate has been previously identified in Heliconius butterflies as a component of a complex mixture of esters, acids, and hydrocarbons acting as anti-aphrodisiac transferred to males from females during mating (Wang et al. 2014). In our study however, this compound did not show any gender specificity and the lowest amount was found in mated females, inducing to consider another function compared to Heliconius butterflies. Linoleoylglycerol has been found as a component of fatty larval tissue of D. melanogaster (Tortoriello et al. 2013). However, no other information on its role as insect compound is currently available.
In this study, α-tocopherol was absent in mated individuals and showed its major abundance in young males and females. Generally, it is not considered as a compound for chemical communication, but is commonly found in insects’ food sources, as for D. melanogaster (Parker and McCormick 2005). Even if the feeding habits of D. oleae adults are currently unknown, we speculate that α-tocopherol may be extracted from the cuticula of the gall midge as a larvae food contaminant. Indeed, α-tocopherol is normally found in olive leaves and its amount depends on O. europaea variety (Tarchoune et al. 2019). α-Tocopherol has been found also in the nutritional analysis results of Hermetia illucens L. larvae, Chilecomadia moorei Silva larvae and Musca domestica L. adults, used as feed species for captive insectivorous (Finke 2012). Another probable food contaminant we found in the D. oleae profile was 3,5-stigmastadiene, a basic compound in oils and fats (Piironen et al. 2000). 3,5-Stigmastadiene is commonly used as marker to ascertain the authenticity of vegetable oils (Gallina Toschi et al. 1996; Giuffrè 2021), such as olive (Crews et al. 2014), argan (Mohammed et al. 2021), avocado (Flores et al. 2019) and grape seed (Matthäus 2008), since high amounts of this compound have been associated with exposure to high temperatures and refining, normal practices in food frauds (Piironen et al. 2000; Flores et al. 2019). In the D. oleae cuticular profile, mated individuals of both sexes showed a significantly lower amount of 3,5-stigmastadiene, suggesting an energy consumption due to copula or a partial loss following the time after emergence. A similar consideration can be made for γ-sitosterol, as it is a common compound of plant leaves, including those of O. europaea (Gül and Şeker 2006; Canbarro et al. 2019).
In our study, the amine N-(2-phenylethyl)acetamide was found in males and mated females. It has been described as a secondary component of the trail pheromonal blend released by the rectal bladders of Camponotus spp. (Hymenoptera: Formicidae) (Kohl et al. 2001, 2003). Furthermore, N-(2-phenylethyl)acetamide has been detected in the anal secretions of Nicrophorus vespilloides Herbst (Coleoptera: Silphidae) as a probable regulator of carrion microbial colonization (Degenkolb et al. 2011). To the best of our knowledge, this compound has been frequently isolated as a biologically inactive by-product of antibiotic fermentation (Degenkolb et al. 2011), but it has never been associated to insect sex or mating condition. Its presence in only the mated females may represent a sign of the successful mating, being therefore passed from the male to the female as a marking pheromone. This hypothesis could explain why N-(2-phenylethyl)acetamide was not present in the virgin females, and fits with the observed mating behaviour, where each male mates with several virgin partners. Mated females were observed to be ignored by males (authors’ personal observation). Such compounds have been reported as a mate-guarding strategy to prevent other males’ courtship in various insect species (Laturney and Billeter 2016). In Drosophila melanogaster, (Z)-vaccenyl acetate and (Z)-7-tricosene, have been associated with chemical mate-guarding. These are produced respectively in the ejaculatory bulb and in oenocytes cells in the subepidermal abdomen and cause reduced male courtship and mating delays when applied on the females or released in the environment (Zawistowski and Richmond 1986; Ejima et al. 2007). Whether such an effect can be elicited in D. oleae requires further investigations and behavioural trials.
Conclusions
The study of the D. oleae cuticular profile showed a clear set of 49 compounds. Among them cuticular hydrocarbons such as alkanes and one monomethyl alkane were recorded. Furthermore, other compounds (e.g. fatty acids) were registered. Eighteen compounds were found to exhibit variations in relation to either mating condition or age after emergence. We suggest that these differences, having effect on courtship and mating, may be considered for developing potential alternative control methods, as already suggested for other dipteran pests (e.g. Drosophila suzukii). Anyway, to gain a deeper understanding of their potential role in chemical communication of D. oleae, additional studies utilizing behavioural trials are necessary.
Data Availability
Not applicable.
Code Availability
Not applicable.
References
Augustnowicz M, Maliński E, Warnke Z, Szafranek J, Nawrot J (1986) Cuticular hydrocarbons of the german cockroach, Blattella germanica L. Comp Biochem Physiol B 86B(3):519–523. https://doi.org/10.1016/0305-0491(87)90441-X
Azhagu Raj R, Sathish R, Prakasam A, Krishnamoorthy D, Balachandar M, Tomson M (2017) Extraction and analysis of cuticular hydrocarbons in the weaver ant Oecophylla smaragdina (Fabricus) (Hymenoptera: Formicidae). Int J Fauna Biological Stud 4(1):102–107
Baidaq ZM, Ramadhane AM, Abu Tara R (2015) Biological synchronization of the endo-parasitoid Platygaster demades Walker (Hymenoptera: Platygastridae) with its host the olive leaf midge Dasineura oleae F. Loew (Diptera: Cecidomyiidae). Int J Agric Environ Sci 2(3):1–8. https://doi.org/10.14445/23942568/IJAES-V2I3P101
Bartelt RJ, Cossé A, Petroski RJ, Weaver DK (2002) Cuticular hydrocarbons and novel alkenediol diacetates from wheat stem sawfly (Cephus cintus): natural oxidation to pheromone components. J Chem Ecol 28(2):385–405. https://doi.org/10.1023/A:1017994410538
Batta YA (2019) New findings on infestation and phenology of Dasineura oleae Angelini (Diptera, Cecidomyiidae): an emerging pest on olive trees in the Palestinian Territories. J Plant Dis Prot 126(1):55–66. https://doi.org/10.1007/s41348-018-0196-y
Bernhardt V, Pogoda W, Verhoff MA, Toennes SW, Amendt (2017) Estimating the age of the adult stages of the blow flies Lucilia sericata and Calliphora vicina (Diptera: Calliphoridae) by means of cuticular hydrocarbon n-pentacosane. Sci Justice 57(5):361–365. https://doi.org/10.1016/j.scijus.2017.04.007
Borges AA, Ferreira- Caliman MJ, Nascimiento FS, Campos LAO, Tavares MG (2012) Characterization of cuticular hydrocarbons of diploid and haploid males, workers and queens of the stingless bee Melipona quadrifasciata Insectes Soc 59:479–486. https://doi.org/10.1007/s00040-012-0242-x
Braga MV, Pinto ZT, de Carvalho Quieroz MM, Blomquist GJ (2016) Effect of age on cuticular hydrocarbon profiles in adult Chrysomya putoria (Diptera: Calliphoridae). Forensic Sci Int 259:e37–e47. https://doi.org/10.1016/j.forsciint.2015.11.006
Buellesbach J, Gadau J, Beukeboom LW, Echinger F, Raychoudhury R, Werren JH, Schmitt T (2013) Cuticular hydrocarbon divergence in the jewel wasp Nasonia: evolutionary shifts in chemical communication channels? J Evol Biol 26(11):2467–2478. https://doi.org/10.1111/jeb.12242
Butterworth NJ, Byrne PG, Keller PA, Wallman JF (2018) Body odor and sex: do cuticular hydrocarbons facilitate sexual attraction in the small hairy maggot blowfly? J Chem Ecol 44:248–256. https://doi.org/10.1007/s10886-018-0943-3
Butterworth NJ, Byrne PG, Wallman JF (2019) The blow fly waltz: field and laboratory observations of novel and complex dipteran courtship behavior. J Insect Behav 32(2):109–119. https://doi.org/10.1007/s10905-019-09720-1
Butterworth NJ, Drijfhout FP, Byrne PG, Keller PA, Wallman JF (2020) Major transitions in cuticular hydrocarbon expression coincide with sexual maturity in a blowfly (Diptera: Calliphoridae). J Chem Ecol 46(7):610–618. https://doi.org/10.1007/s10886-020-01194-2
Butterworth NJ, Wallman JF, Drijfhout FP, Johnson NP, Keller PA, Byrne PG (2020) The evolution of sexual dimorphic cuticular hydrocarbons in blowflies (Diptera: Calliphoridae). J Evol Biol 33(10):1468–1486. https://doi.org/10.1111/jeb.13685
Canbarro NI, Mazutti MA and do, Carmo Ferreira M (2019) Drying of olive (Olea europaea L.) leaves on a conveyor belt for supercritical extraction of bioactive compounds: Mathematical modeling of drying/extraction operations and analysis of extracts. Ind Crops Prod 136:140–151. https://doi.org/10.1016/j.indcrop.2019.05.004
Carlson DA, Yocom SR (1986) Cuticular hydrocarbons from six species of tephritid fruit flies. Arch Insect Biochem Physiol 3:397–412. https://doi.org/10.1002/arch.940030407
Caselli A, Francini A, Minnocci A, Petacchi R (2021) Dasineura oleae: morphological and physiological characterization following the midge attack on olive leaves. J Plant Dis Prot 128(1):173–182. https://doi.org/10.1007/s41348-020-00380-4
Caselli A, Favaro R, Petacchi R, Angeli S (2021b) Infestation of the gall midge Dasineura oleae provides first evidence of induced plant volatiles in olive leaves. Bull Entomol Res 1–13. https://doi.org/10.1017/S0007485321001000
Chung H, Carroll SB (2015) Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. BioEssays 37(7):822–830
Cobb M, Ferveur JF (1995) Evolution and genetic control of mate recognition and stimulation in Drosophila Behav Processes 35:35–54. https://doi.org/10.1016/0376-6357(95)00052-6
Colazza S, Aquila G, De Pasquale C, Peri E, Millar JG (2007) The egg parasitoid trissolcus basalis uses n-nonadecane, a cuticular hydrocarbon from its stink bug host Nezara virdula, to discriminate between females and males. J Chem Ecol 33:1405–1420. https://doi.org/10.1007/s10886-007-9300-7
Cortot J, Farine JP, Ferveur JF, Everaerts C (2022) Aging-related variation of cuticular hydrocarbons in wild type and variant Drosophila melanogaster J Chem Ecol 48:152–164. https://doi.org/10.1007/s10886-021-01344-0
Crews C, Pye C, Macarthur R (2014) An improved rapid stigmastadiene test to detect addition of refined oil to extra virgin oil. Food Res Int 60:117–122. https://doi.org/10.1016/j.foodres.2013.11.023
Degenkolb T, Düring RA, Vilcinskas A (2011) Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions. J Chem Ecol 37:724–735. https://doi.org/10.1007/s10886-011-9978-4
Dapporto L, Baracchi D, Benassai D, Capretti P, Roversi PF, Turillazzi S (2013) Major changes in the sex differences in cuticular chemical profiles of the western conifer seed bug (Leptoglossus occidentalis) after laboratory rearing. J Insect Physiol 59(7):738–744. https://doi.org/10.1016/j.jinsphys.2013.03.012
Desena ML, Edman JD, Clark JM, Symington SB, Scott TW (1999) Aedes aegypti (Diptera: Culicidae) age determination by cuticular hydrocarbon analysis of female legs. J Med Entomol 36(6):824–830. https://doi.org/10.1093/jmedent/36.6.824
Doğanlar M (2011) Parasitoids complex of the olive leaf gall midge, Dasineura oleae (Angelini, 1831) and Lasioptera oleicola Skuhravá (Diptera: Cecidomyiidae) in Hatay Turkey, with descriptions of new genus and species from Tetrastichinae (Hymenoptera: Eulophidae). Türkiye Entomologji Derneği 35(2):245–264
Doğanlar M, Sertkaya E, Skuhravá M (2011) Pest status of olive leaf gall midge Dasineura oleae (Angelini, 1831), description of Lasioptera oleicola Skuhravá sp. new (Diptera: Cecidomyiidae) and effectiveness of parasitoids on their populations in Hatay Turkey. Türkiye Entomoloji Dergisi 35:265–284
Drijfhout F, Kather R, Martin SJ (2010) The role of cuticular hydrocarbons in insects. In: Zhang W, Liu H (eds) Behavioral and chemical ecology, Chap. 3. Nova Science Publisher, p 2
Ejima A, Smith BPC, Lucas C, van der Goes W, Miller CJ, Carlson JR, Levine JD, Griffith LC (2007) Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 17(7):599–605. https://doi.org/10.1016/j.cub.2007.01.053
Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35(3):279–295. https://doi.org/10.1007/s10519-005-3220-5
Finke MD (2012) Complete nutrient content of four species of feeder insects. Zoo Biol 32(1):27–36. https://doi.org/10.1002/zoo.21012
Flores M, Saravia C, Vergara CE, Avila F, Valdés H, Ortiz-Viedma J (2019) Avocado oil: characteristics, properties, and applications. Molecules 24(11):2172. https://doi.org/10.3390/molecules24112172
Galhoum A (2017) Taxonomic studies on two tephritid species (Order: Diptera), Bactrocera oleae and B. zonata, using the cuticular hydrocarbons profile. Al-Azhar Bull Sci 28:45–54. https://doi.org/10.21608/ABSB.2017.8166
Gallina Toschi T, Bendini A, Lercker G (1996) Evaluation of 3,5-stigmastadiene content of edible oils: comparison between the traditional capillary gas chromatographic methods and the on-line high performance liquid chromatography-capillary gas chromatographic analysis. Chromatographia 43(3/4):195–199. https://doi.org/10.1007/BF02292950
Gerade BB, Lee SH, Scott TW, Edman JD, Harrington LC, Kitthawee S, Jones JW, Clark KM (2004) Field validation of Aedes aegypti (Diptera: Culicidae) age estimation by analysis of cuticular hydrocarbons. J Med Entomol 41(2):231–238. https://doi.org/10.1603/0022-2585-41.2.231
Gibbs AG (2002) Lipid melting and cuticular permeability: new insights into an old problem. J Insect Physiol 48(4):391–400. https://doi.org/10.1016/S0022-1910(02)00059-8
Giuffrè AM (2021) n-Alkanes and n-alkenes in virgin olive oil from Calabria (South Italy): the effects of cultivar and harvest date. Foods 10(2):290. https://doi.org/10.3390/foods10020290
Golebiowski M, Boguś MI, Paszkiewicz M, Stepnowski P (2011) Cuticular lipids of insects as potential biofungicides: methods of lipid composition analysis. Anal Bioanal Chem 399:3177–3191. https://doi.org/10.1007/s00216-010-4439-4
Gül MK, Şeker M (2006) Comparative analysis of phytosterol components from rapeseed (Brassica napus L.) and olive (Olea europaea L.) varieties. Eur J Lipid Sci Technol 108(9):759–765. https://doi.org/10.1002/ejlt.200600085
Hall DR, Amarawardana L, Cross JV, Francke W, Boddum T, Hillbur Y (2012) The chemical ecology of cecidomyiid midges (Diptera: Cecidomyiidae). J Chem Ecol 38:2–22. https://doi.org/10.1007/s10886-011-0053-y
Hatano E, Wada-Katsumata A, Schal C (2020) Environmental decomposition of olefinic cuticular hydrocarbons of Periplaneta americana generates volatile pheromone that guides social behaviour. Proc R Soc B 287(1921):20192466. https://doi.org/10.1098/rspb.2019.2466
Hoffmann KH, Dettner K, Tomaschko KH (2006) Chemical signals in insects and other arthropods: from molecular structure to physiological functions. Physiol Biochem Zool 79(2):344–356. https://doi.org/10.1086/499991
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363. https://doi.org/10.1002/bimj.200810425
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. https://doi.org/10.1146/annurev.ento.50.071803.130359
Ingleby FC (2015) Insect cuticular hydrocarbons as dynamic traits in sexual communication. Insects 6(3):732–742. https://doi.org/10.3390/insects6030732
Jackson LL, Bartelt RJ (1986) Cuticular hydrocarbons of Drosophila virilis: comparison by age and sex. Insect Biochem 16(2):433–439. https://doi.org/10.1016/0020-1790(86)90056-9
Jennings JH, Etges WJ, Schmitt T, Hoikkala A (2014) Cuticular hydrocarbons of Drosophila montana: Geographic variation, sexual dimorphism and potential roles as pheromones. J Insect Physiol 61:16–24. https://doi.org/10.1016/j.jinsphys.2013.12.004
Kassambara A, Mundt F (2020) Factoextra: Extract and visualize the results of multivariate data analyses. R package version 1.0.7. https://CRAN.R-project.org/package=factoextra. Accessed Oct 2022
Kohl E, Hölldobler B, Bestmann H (2001) Trail and recruitment pheromones in Camponotus socius (Hymenoptera: Formicidae). Chemoecology 11:67–73. https://doi.org/10.1007/PL00001834
Kohl E, Hölldobler B, Bestmann HJ (2003) Trail pheromones and Dufour gland contents in three Camponotus species (C. castaneus, C. balzani, C. sericeiventris: Formicidae, Hymenoptera). Chemoecology 13:113–122. https://doi.org/10.1007/s00049-003-0237-1
Krieger GM, Van Ducheteau A, Ibarra F, Francke W, Ayasse M (2006) Identification of queen sex pheromone components of the bumblebee Bombus terrestris J Chem Ecol 32:453. https://doi.org/10.1007/s10886-005-9013-8
Krupp JJ, Levine JD (2010) Dissection of oenocytes from adult Drosophila melanogaster J Vis Exp 41:2242. https://doi.org/10.3791/2242
Kuo TH, Yew JY, Fedina TY, Dreisewerd K, Dierick HA, Pletcher SD (2012) Aging modulates cuticular hydrocarbons and sexual attractiveness in Drosophila melanogaster J Exp Biol 215(5):814–821. https://doi.org/10.1242/jeb.064980
Laturney M, Billeter JC (2016) Drosophila melanogaster females restore their attractiveness after mating by removing male anti-aphrodisiac pheromones. Nat Commu 7(1):1–11. https://doi.org/10.1038/ncomms12322
Magagnoli S, Tondini E, Ratti C, Burgio G, Petacchi R (2022) A new PCR based molecular method for early and precise quantification of parasitization in the emerging olive pest Dasineura oleae Pest Manag Sci 78(5):1842–1849. https://doi.org/10.1002/ps.6802
Matthäus B (2008) Virgin grape seed oil: is it really nutritional highlight? Eur J Lipid Sci Technol 110:645–650. https://doi.org/10.1002/ejlt.200700276
Menzel F, Morsbach S, Martens JH, Räder P, Hadjaje S, Poizat M, Abou B (2019) Communication versus waterproofing: the physics of insect cuticular hydrocarbons. J Exp Biol 222(23):jeb210807. https://doi.org/10.1242/jeb210807
Moallem MK (1975) Cycle biologique de l’endoparasite Platygaster sp. et son impact sur la proliferation de Dasineura oleae Réunion Sur La Protection Phytosanitaire de l’olivier. Instituto Nacional de Investigaciones Agrarias (INIA), Sfax, Tunisia, pp 277–283
Mohammed F, Guillaume D, Warland J, Abdulwali N (2021) Analytical methods to detect adulteration of argan oil: a critical review. Microchem J 168:106501. https://doi.org/10.1016/j.microc.2021.106501
Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530
Mullen SP, Mendelson TC, Schal C, Shaw KL (2007) Rapid evolution of cuticular hydrocarbons in a species radiation of acoustically diverse hawaiian crickets (Gryllidae: Trigonidiinae: Laupala). Evol 61(1):223–231. https://doi.org/10.1111/j.1558-5646.2007.00019.x
Neves EF, Andrade LHC, Súarez YR, Lima SM, Antonialli-Junior WF (2012) Age-related changes in the surface pheromones of the wasp Mischocyttarus consimilis (Hymenoptera: Vespidae). Genet Mol Res 11(3):1891–1898. https://doi.org/10.4238/2012.July.19.8
Otte T, Hilker M, Geiselhardt S (2018) Phenotypic plasticity of cuticular hydrocarbon profiles in insects. J Chem Ecol 44(3):235–247. https://doi.org/10.1007/s10886-018-0934-4
Park SJ, Pandey G, Castro-Vargas C, Oakeshott JG, Taylor PW, Mendez V (2020) Cuticular chemistry of the Queensland fruit fly Bactrocera tyoni (Froggatt). Molecules 25:4185. https://doi.org/10.3390/molecules25184185
Parker RS, McCormick CC (2005) Selective accumulation of a α-tocopherol in Drosophila is associated with cytochrome P450 tocopherol-ω-hydroxylase activity but not α-tocopherol transfer protein. Biochem Biophys Res Commun 338(3):1537–1541. https://doi.org/10.1016/j.bbrc.2005.10.124
Picchi MS, Marchi S, Petacchi R (2017) Cecidomia delle foglie dell’olivo: nuovo rischio o vecchio problema? L’Informatore Agrario 16:49–52
Picchi MS, Tondini E, Albertarelli N, Monteforti G, Petacchi R (2021) Following the pest outbreak: preliminary findings on the landscape effect on Dasineura oleae and its parasitoids in central Italy. Phytoparasitica. https://doi.org/10.21203/rs.3.rs-174210/v1
Piironen V, Lindsay DG, Miettinen TA, Toivo J, Lampi AM (2000) Plant sterols: biosynthesis, biological function and their importance to human nutrition. J Sci Food Agric 80(7):939–966. https://doi.org/10.1002/(SICI)1097-0010(20000515)80:7%3C939::AID-JSFA644%3E3.0.CO;2-C
Pizzi NJ, Rehan SM (2021) Characterization of cuticular hydrocarbons in a subsocial bee, Ceratina calcarata Insectes Soc 68:351–358. https://doi.org/10.1007/s00040-021
Polerstock AR, Eigenbrode SD, Klowden MJ (2002) Mating alters the cuticular hydrocarbons of female Anopheles gambiae sensu stricto and Aedes aegypti (diptera: Culicidae). J Med Entomol 39(3):545–552. https://doi.org/10.1603/0022-2585-39.3.545
Provost E, Blight O, Tirard A, Renucci M (2008) Hydrocarbons and insects’ social physiology. In: RP Maes (ed) Insect physiology: new research. Nova Science Publisher, pp 19–72
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed Dec 2021
Rajpurohit S, Hanus R, Vrkoslav V, Behrman EL, Bergland AO, Petrov D, Cvačka J, Schmidt PS (2016) Adaptive dynamics of cuticular hydrocarbons in Drosophila J Evol Biol 30(1):66–80. https://doi.org/10.1111/jeb.12988
Rocha Barbosa R, Braga MV, Blomquist GJ, de Carvalho Quieroz MM (2017) Cuticular hydrocarbons profile as a chemotaxonomic tool for three blowfly species (Diptera: Calliphoridae) of forensic interest. J Nat Hist 51(25–26):1491–1498. https://doi.org/10.1080/00222933.2017.1337944
Ruano F, Hefetz A, Lenoir A, Francke W, Tinaut A (2005) Dufour’s gland secretion as a repellent used during usurpation by the slave-maker ant Rossomyrmex minuchae J Insect Physiol 51(10):1158–1164. https://doi.org/10.1016/j.jinsphys.2005.06.005
Scolari F, Valerio F, Benelli G, Papadopoulos NT, Vaníčková L (2021) Thephritid fruit fly semiochemicals: current knowledge and future perspectives. Insects 12(5):408. https://doi.org/10.3390/insects12050408
Sessa L, Calderón-Fernández GM, Abreo E, Altrier N, Mijailovsky SJ, Girotti JR, Pedrini N (2021) Epicuticular hydrocarbons of the redbanded stink bug Piezodorus guildinii (Heteroptera: Pentatomidae): sexual dimorphism and alteration in insect collected in insecticide-treated soybean crops. Pest Manag Sci 77(11):4892–4902. https://doi.org/10.1002/ps.6528
Sharma A, Drijfhout FP, Tomberlin JK, Bala M (2020) Cuticular hydrocarbons as a tool for determining the age of Chrysomya rufifacies (diptera: Calliphoridae) larvae. J Forensic Sci. https://doi.org/10.1111/1556-4029.14572
Simoglou KB, Karataraki A, Roditakis NE, Roditakis E (2012) Euzophera bigella (Zeller) (Lepidoptera: Pyralidae) and Dasineura oleae (F. Low) (Diptera: Cecidomyiidae): emerging olive crop pests in the Mediterranean? J Pest Sci 85:169–177. https://doi.org/10.1007/s10340-012-0418-1
Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38(2):394–405. https://doi.org/10.1093/icb/38.2.394
Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L). J Chem Ecol 31:2731–2745. https://doi.org/10.1007/s10886-005-7623-9
Snellings Y, Herrera B, Wildemann B, Beelen M, Zwarts L, Wenseleers T (2018) The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii Sci Rep 8:4996. https://doi.org/10.1038/s41598-018-23189-6
Stavraki H (1970) Contribution a l’inventaire du complexe parasitaire de quelques insectes nuisibles a l’olivier en Greece. Entomophaga 15:225–231. https://doi.org/10.1007/BF02371000
Stinziano JR, Sové RJ, Rundle HD, Sinclair BJ (2015) Rapid desiccation hardening changes the cuticular hydrocarbon profile of Drosophila melanogaster Comp Biochem Physiol A 180:38–42. https://doi.org/10.1016/j.cbpa.2014.11.004
Tarchoune I, Sgherri C, Eddouzi J, Zinnai A, Quartacci MF, Zarrouk M (2019) Olive leaf addition increases olive oil nutraceutical proprieties. Molecules 24(3):545. https://doi.org/10.3390/molecules24030545
Tondini E, Petacchi R (2019) First observations on the parasitoid complex and on the biology of Dasineura oleae during an outbreak in Tuscany, Italy. Bull Insectol 72(1):93–102
Tortoriello G, Rhodes BP, Takacs SM, Stuart JM, Basnet A, Raboune S, Widlanski TS, Doherty P, Harkany T, Bradshaw HB (2013) Target lipidomics in Drosophila melanogaster novel 2-monoacylglycerols and N-acyl amides. PLoS ONE 8(7):e67865. https://doi.org/10.1371/journal.pone.0067865
Urbanová K, Halík J, Hovorka O, Kindl J, Valterová (2004) Marking pheromones of the cuckoo bumblebee males (Hymenoptera, Apoidea, Bombus Latreille): compositions of labial gland secretions of six species found in the Czech Republic. Biochem Syst Ecol 32(11):1025–1045. https://doi.org/10.1016/j.bse.2004.02.010
Van Den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr A 11:463–471. https://doi.org/10.1016/s0021-9673(01)80947
Vaníčková L, Svatoš, Kroiss J, Kaltenpoth M, Rufino Do Nascimento R, Hoskovec M, Břízová R, Kalinová B (2012) Cuticular hydrocarbon of the South America fruit fly Anastrepha fraterculus: variability with sex and age. J Chem Ecol 38:1133–1142. https://doi.org/10.1007/s10886-012-0177-8
Vaníčková L, Virgilio M, Tomčala A, Břízová R, Ekesi S, Hoskovec M, Kalinová B, Do Nascimento RR, De Meyer M (2014) Resolution of three cryptic agricultural pests (Ceratitis fasciventris, C. anonae, C. rosa, Diptera: Tephritidae) using cuticular hydrocarbon profiling. Bull Entomol Res 104(5):631–638. https://doi.org/10.1017/S0007485314000406
Vernier CL, Krupp JJ, Marcus K, Hefetz A, Levine JD, Ben-Shahar Y (2019) The cuticular hydrocarbon profiles of honey bee workers develop via a socially-modulated innate process. Elife 8:e41855
Wang HL, Brattström O, Brakefield PM, Francke W, Löfstedt C (2014) Identification and biosynthesis of novel male specific esters in the wings of the tropical butterfliy, Byciclus martius sanaos J Chem Ecol 40:549–559. https://doi.org/10.1007/s10886-014-0452-y
Warthen JD, Uebel EC (1980) Comparison of the unsaturated cuticular hydrocarbons of male and female house crickets, Acheta domesticus (L.) (Orthoptera: Gryllidae). Insect Biochem 10(4):435–439. https://doi.org/10.1016/0020-1790(80)90015-3
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wilke CO (2020) cowplot: Streamlined Plot Theme and Plot Annotations for ‘ggplot2’. R package version 1.1.0. https://CRAN.R-project.org/package=cowplot. Accessed Dec 2021
Yeo H, Youn K, Kim M, Yun EY, Hwang JS, Jeong WS, Jun M (2013) Fatty acid composition and volatile constituent of Protaetia brevitarsis larvae. Prev Nutr Food Sci 18(2):150–156
Zawistowski S, Richmond RC (1986) Inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cis-vaccenyl acetate. J Insect Physiol 32(3):189–192
Acknowledgements
The authors are grateful to Marco Ferrali and Gaia Monteforti for their laboratory assistance with Dasineura oleae rearing, and to Stefano Brizzolara for his technical assistance. The authors would like to thank Luisa Amadori and Francesco Giuseppe Campo for permission to perform monitoring and sampling in their olive farms.
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Open access funding provided by Scuola Superiore Sant'Anna within the CRUI-CARE Agreement. This work has been realized with the funding provided by the scholarship granted by the Agrobiosciences Ph.D. program at Scuola Superiore Sant’Anna of Pisa to Alice Caselli.
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Conceptualization and methodology: AC, RF, RP and SA; literature search: AC, RF, MV; writing - original draft preparation: AC, RF, MV; writing - review and editing: AC, RF, RP, MV and SA. All authors have read and agreed to the published version of the manuscript.
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Caselli, A., Favaro, R., Petacchi, R. et al. The Cuticular Hydrocarbons of Dasineura Oleae Show Differences Between Sex, Adult Age and Mating Status. J Chem Ecol 49, 369–383 (2023). https://doi.org/10.1007/s10886-023-01428-z
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DOI: https://doi.org/10.1007/s10886-023-01428-z