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Interactions of Opuntia ficus-indica with Dactylopius coccus and D. opuntiae (Hemiptera: Dactylopiidae) through the Study of Their Volatile Compounds

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29 February 2024

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Abstract
Opuntia ficus-indica has always interacted with many phytophagous insects at its center of origin; two of them are Dactylopius coccus and D. opuntiae. D. coccus, or true cochineal, is produced to extract carminic acid, and D. opuntiae or wild cochineal is a key invasive pest of O. ficus-indica in more than 20 countries around the world. Despite the economic and environmental relevance of this cactus and, D. opuntiae and D. coccus, there are few studies that have explored volatile organic compounds (VOCs) derived from the plant-insect interaction. The aim of this work was to determine VOCs of D. coccus and D. opuntiae feeding on cultivars suitable for their development and to identify different VOCs in cladodes infested by each Dactylopius species. Volatiles were identified through their essential oils, which were obtained by hydrodistillation. A total of 66 VOCs from both Dactylopius species were identified, and 125 from the Esmeralda and Rojo Pelón cultivars infested by D. coccus and D. opuntiae, respectively, were determined. Differential VOCs production due to infestation by each Dactylopius species was also found. Some changes in methyl salicylate, terpenes such as linalool or the alcohol p-vinylguaiacol were related to Dactylopius feeding on cladodes of their respective cultivars. Changes in these VOCs and their probable role in plant defense mechanisms should receive more attention because this knowledge could improve D. coccus rearing, or to its inclusion in breeding programs for D. opuntiae control in regions where it is a key pest of O. ficus-indica.
Keywords: 
Subject: Environmental and Earth Sciences  -   Ecology

1. Introduction

Dactylopiidae, or cochineals, is a family of scale insects that includes only the genus Dactylopius and 11 recognized species [1] that are endemic to North and South America [2,3]. An important characteristic of these insects is that they produce carminic acid, probably as a defense mechanism against predation [4,5,6]. All the species of the genus are considered obligate parasites of Cactacea with high food specificity, particularly for the genera Nopalea Salm-Dyck and Opuntia Miller [7].
Because of the high carminic acid concentration (~20-25%) of Dactylopius coccus Costa, the true cochineal, it is the only species of commercial interest for production. It is reared on Opuntia ficus-indica (L.) Miller, the cactus pear. Carminic acid is recognized as a natural dye with cosmetic, food, pharmaceutical, textile and plastic applications [8]. In addition, it is currently used in biomedicine [9] and as a photosynthesizing pigment in solar cells [10]. In contrast, Dactylopius opuntiae Cockerell, or wild cochineal, whose carminic acid content is less than 5%, is not considered useful for obtaining this substance. Rather, it is considered the key pest of O. ficus-indica in commercial plantations in Mexico [11,12], where plant and insect are native [7,13]. Additionally, D. opuntiae is an invasive pest in at least 20 countries in America, Europe, Africa, and Asia [14,15,16] where O. ficus-indica was adopted or naturalized and became one of the most important cultivated cactus species in the world because of its economic, environmental, and ecological benefits [13,14,17,18].
From a scientific perspective, most of D. coccus research has focused on the basic biology of the species and the quest to understand the mechanisms of carminic acid production and its possible physiological or ecological functions [4,19,20]. On the other hand, research on D. opuntiae has focused on control tactics because it is a key pest of O. ficus-indica [14,15,21,22]. The different cultivars of O. ficus-indica used as hosts of both Dactylopius species are likely to have particular physical and chemical characteristics, as well as volatile organic compounds (VOCs) that influence the trophic plant-insect and plant-pest-natural enemy relationship, as has been shown in other models of tritrophic interactions where volatiles cause positive or negative responses in terms of attraction and establishment of insects of the same or different species [23,24].
Volatile organic compounds (VOCs) are synthesized as products of plant metabolism and they are emitted into the environment [25] in response to biotic complexes or abiotic stresses [23,26]. These VOCs and essential oils are released from the leaves, flowers, and fruits into the atmosphere and from the roots into the soil [27,28]. This set of volatiles, essential in the defense mechanisms of plants against herbivores or in interspecific communication [23,24,27] is called volatilome and its analysis, using direct and non-direct approaches based on gas chromatography-mass spectrometry (GC-MS), is generally called volatilomics. A field that is continuously growing with the development of analytical and data processing methods [29]. In this regard, some research has been carried out on VOCs of O. ficus-indica emanating from cladodes, flowers, fruits, and the oils of its seeds [30,31,32,33,34,35]. These studies concluded that VOCs composition is a function of the geographical area, species or cultivar, plant structure, state of development and season, among other factors. However, none of these relatively recent papers included interaction with any of the important Dactylopius species, nor did they relate the production of VOCs to insect infestation. To our knowledge, there is only one study that evaluated VOCs in O. ficus-indica cladodes uninfested and infested by D. coccus [36]. This study reported eight types of compounds in uninfested cladodes and nine in cladodes infested by the insect. Furthermore, no other work is known to have explored VOCs of either Dactylopius species.
Because plant VOCs play an important role in interactions between insects and other organisms, e.g., pathogens or predators and parasitoids [23,24,37], as well as in the plant's response to insect attacks [38], the objectives of this work were 1) to determine the VOCs of D. coccus and D. opuntiae feeding on O. ficus-indica, and 2) to establish the changes in the composition and proportion of VOCs in cladodes of O. ficus-indica uninfested and infested with Dactylopius. This information could contribute to understanding the variation between cultivars of both species of insects and to exploring the potential of the biological functions that these compounds play in interspecies communication.

2. Results

Through essential oils it was possible to recover and identify about 80 % and 90 % of the volatile organic compounds (VOCs) of D. coccus and D. opuntiae, respectively. The Dactylopius species had 20 VOCs in common. In addition, 12 and 34 VOCs were specifically produced by D. coccus and D. opuntiae, respectively (Figure 1). Thus, the volatilome of each species was 32 or 54 compounds, and the proportion of each compound varied greatly between species (Table 1). The VOCs belonged to eight chemical groups, of which three had the highest relative abundance. Carboxylic acids and their derivatives was the most important group, accounting for 59.28 % and 78.29 % of the VOCs abundance for D. coccus and D. opuntiae, respectively. The second group was alcohols only for D. coccus (12.15 %), and the third group was aldehydes with 5.8 % and 7.68 % of the relative abundance for D. coccus and D. opuntiae, respectively. The alkanes recovered were less than 2.5 % for both species. The remaining four groups of recovered compounds (ether, terpenes, ketones, alkenes) were less than 0.55 % of relative abundance per group (Table 1).
As mentioned above, the number and abundance of volatiles in each group of compounds also varied greatly in each Dactylopius species. For example, in the carboxylic acids and their derivatives, tetradecanoic acid was the most abundant in both species but decanoic acid, lactic acid and dodecanoic acid presented greater relative abundance in D. coccus. On the other hand, for D. opuntiae, 2-ethylhexanoic acid and cis-5-dodecenoic acid were detected only in this species in greater relative abundance. Hexadecanoic acid, (Z,Z)-9,12-octadecadienoic acid, (Z)-9-octadecenoic acid and octadecanoic acid occurred in both species, but their abundance differed considerably between species; again, they were more abundant for D. opuntiae (Table 1)
The Esmeralda and Rojo Pelón cultivars had VOCs production profiles that differed before and after Dactylopius infestation. In both cultivars, 28 VOCs were commonly produced and identified. In addition, 35 specific compounds were identified in Esmeralda and 19 in Rojo Pelón (Figure 2). After infestation by each Dactylopius species in the respective O. ficus-indica cultivar, a contrasting difference occurred between uninfested and infested cladodes of each cultivar (Table 2). The changes were not only in the number of VOCs, but in their abundance and variation. Sometimes they decreased, sometimes they increased, sometimes some VOCs were no longer detected, and of course there were also some de novo compounds (Table 2). After infestation by D. coccus, the Esmeralda cultivar increased the number of volatiles from 63 (uninfested) to 87, of which 48 were produced de novo and belonged to nine chemical groups. In the case of Rojo Pelón D. opuntiae, uninfested cladodes produced 47 VOCs and after infestation they decreased to 38, 13 of which were identified as de novo, belonging to seven chemical groups (Table 2, Figure S1 and Figure S2).
Although there was an enormous variation between the number and proportion of VOCs before and after infestation, it was observed that four chemical groups maintained the highest abundance in both infested cultivars. These groups were a) carboxilic acid and derivatives, b) terpenes, c) alcohols, and d) aldehydes and derivatives. Another group, the heterocycles, was only abundant for the uninfested Rojo Pelón cultivar (8.91 %), but after D. opuntiae infestation it decreased to less than 1.4 %. The rest of the recovered chemical groups (ethers, ketones, aromatic derivatives and alkanes) were less than 1.16 % of the relative abundance per group in either cultivar infested by the respective Dactylopius species. Two of these groups (ethers and aromatic derivatives) were not detected in the infested Rojo Pelón cultivar (Table 2).
As indicated above, because of Dactylopius infestation in each cultivar, there were many changes in the relative abundance of compounds and production of some de novo compounds. The de novo compounds were mostly of low relative abundance (equal to or less than 1.0 %), except for some terpenes and alcohols. For example, in the uninfested Rojo Pelón cultivar the relative abundance of terpenes was around 0.8 %, but this relative abundance of terpenes changed to 15.5 % after D. opuntiae infestation. On the other hand, the relative abundance of terpenes in the Esmeralda cultivar decreased from 18 to 13.9 % due to D. coccus infestation (Table 2). The amount and type of terpenes were different between infested O. ficus-indica cultivars, but monoterpenes or their derivatives predominated in both cases (Figure 3).
The terpenes Linalool oxide, trans-Linalool oxide and the alcohol 3,7,11,15-Tetramethyl-2-hexadecenol reached a relative abundance of 5.06 %, 5.7 % and 1.8 % in the Esmeralda cultivar infested by D. coccus. On the other hand, the terpenes Linalool, Geraniol and the alcohol 3,7,11,15-Tetramethyl-2-hexadecenol registered 5.6 %, 1.84 % and 3.5 % of the relative abundance in the Rojo Pelón cultivar infested by D. opuntiae, respectively. Also, p-Vinylguaiacol increased 2.3 % in relative abundance after D. opuntiae infestations (Table 2).

3. Discussion

Previous assays of Dactylopius VOCs extraction such as Headspace (HS-SPME) and extraction by Autosampler Headspace coupled to CG-MS (HS-CG-MS) did not provide the results expected for GC-MS analysis. Thus, to identify the volatiles from Dactylopius and its cultivar hosts, we preferred to do so using their essential oils. Essential oils were obtained by the hydrodistillation method (Table S1), which is frequently used to obtain essential oils from plants that contain low vapor pressure compounds, or low volatile compounds. This technique is also used for concentrating compounds with lower concentrations in the essential oil and allows working with a larger sample mass than microextraction techniques, which can potentially improve characterization of insect VOCs [39].
In the volatilome of D. coccus and D. opuntiae, 32 and 54 VOCs were identified for each species, respectively. To our knowledge, neither of these volatilomes had been reported previously, and this may be the first contribution of this work. By their composition, these VOCs corresponded to eight different chemical groups, but there were three groups of greater abundance. These were a) carboxylic acids and their derivatives, 59.28% and 78.29% abundance for D. coccus and D. opuntiae, respectively, b) alcohols, which were abundant only for D. coccus (12%), and c) aldehydes, 5.8% and 7.68% abundance for D. coccus and D. opuntiae, respectively (Figure S3 and Figure S4). This composition could be one of the reasons that results were not obtained with the HS-SPME and HS-CG-MS techniques. The VOCs of Dactylopius species are mostly fatty acids, some of which may be part of the fat content of the insects, or of the complexity of their waxy coat [40,41]. In fact, each VOC in those groups may have more than one role in structure, function, metabolism, and probably in intra or interspecific communication. For example, D. coccus produces a sex pheromone [42], and D. opuntiae is suspected to do so as well [43]. Regarding tetradecanoic acid, which is one of the most abundant VOCs for both species of Dactylopius, and hexadecanoid acid, relevant to D. opuntiae, they have many functions in insect metabolism. One of these is to participate in metabolic pathways of sex pheromones of some Lepidoptera such as Spodoptera lottoralis Boisduval and Plodia interpunctella Hubner [44,45], but none of these compounds appear to have relevance in the pheromones of Coccoidea [46], which is the superfamily to which the Dactylopiidae belong. The methodology for identifying insect pheromones begins with live females at a particular moment of maturity and sexual behavior, and so much work remains to be done to decipher the main functions of the VOCs that turned out to be more abundant, and that could lead to novel acids with shorter chains and perhaps more specific for each Dactylopius species.
The volatilome of Esmeralda and Rojo Pelón cultivars were different before and after Dactylopius infestation. The variation in compound production in cladodes of both cultivars prior to infestation (by Dactylopius) may be specific to each cultivar, as variations of other bioactive and volatile compounds have been reported in different cultivars of O. ficus-indica [30,34,47]. However, variation in the number and abundance of VOCs within each cultivar after infestation can be attributed to D. coccus or D. opuntiae feeding on its corresponding cultivar host, as has been demonstrated in other plants where the change in production of VOCs, particularly terpenes and sesquiterpenes, was directly associated with phytophagous insect feeding [23,24,48,49].
In the volatilome of Esmeralda and Rojo Pelón, before or after Dactylopius infestation, four chemical groups were identified as the most abundant: a) carboxylic acid and derivatives, b) terpenes, c) alcohols, and d) aldehydes and derivatives (Figure S5 and Figure S6). The structural composition of the host, particularly the quantity of waxes, could be related to the abundance of some of these VOCs in both cultivars [47,50]. This suggestion is related to the anatomical and physiological adaptations of cacti to develop in arid environments, such as a thick and impermeable epidermis covered by a layer of waxy cuticle, a hypodermis with chollenchyma, plenty of cells with mucilage distributed in the parenchyma, and crassulaceae acid metabolism (CAM) among other characteristics [50]. Of the first and most abundant chemical groups (a), it is probable that we should mention the methyl salicylate, which increased in abundance after infestation by D. coccus (about 5 %) in the Esmeralda cultivar. The same compound was identified de novo in the Rojo Pelón cultivar infested by D. opuntiae, although low in abundance (0.3 %). Methyl salicylate is a phenolic compound that has been reported to be an Herbivore-Induced Plant Volatile (=HIPV) [49,51,52]. Some of these HIPVs can induce direct defense against the phytophagous insect and indirect defense by attracting their natural enemies. It is also useful in communication among plants damaged by phytophagy and others that are not yet damaged. For example, methyl salicylate emitted by plants with phytophagous mite damage was attractive to Phytoseiulus persimilis Athias-Henriot (Phytoseiidae) [51,52]. In the same way, it was observed that emission of this compound, after damage by psyllids in pear trees, was attractive to the predatory bug Anthocoris nemoralis F. (Hemiptera: Anthocoridae) [53].
In general, a slight decrease in terpene abundance (18 to 14%) was observed after D. coccus infestation, but a considerable increase (0.8 to 15%) occurred after D. opuntiae infestation. In the Esmeralda cultivar, β-Linalool abundance decreased from 5.0 to 0.3 %, but Linalool oxide and trans-Linalool oxide increased to 5.0 and 5.7 %. On the other hand, in the cultivar Rojo Pelón infested by D. opuntiae, five de novo terpenes were identified, of which the most abundant was Linalool (5.6%). Terpenes are one of the most studied groups of HIPVs, and it has been shown that some of them have a relevant role in the direct defense system against phytophages, and some volatile terpenes constitute indirect defenses of plants as they attract natural enemies such as predators and parasitoids [23,24,27,48,49].
Linalool is a monoterpene that occurs naturally in flowers and aromatic plants, but it is also produced in response to feeding by phytophagous insects and it is part of the indirect defenses of plants [54]. For example, an increase in linalool production in tobacco plants caused by feeding Lepidoptera larvae increased the rate of egg predation and decreased the oviposition of another Lepidoptera [55]. Linalool also increased due to phytophages feeding on corn, bean, cotton, and potato plants [23], or by a zoophytophagous mirid feeding on pepper plants, and favored the action of natural enemies of their pests [49]. This can suggest that significant changes in the abundance of methyl salicylate from the above group and terpenes, particularly linalool, are probably related to each Dactylopius species feeding on its corresponding cultivar host.
The alcohol of greatest abundance and change was p-vinylguaiacol. This compound is common in plants and is part of many essential oils. In addition, it can be found in the gut of some insects probably by the process of lignin degradation [56]. Regarding secondary plant defenses due to damage by phytophagous insects, p-vinylguaiacol stimulated the ovipositional behavior of the natural enemy Coleomegilla maculata [57], and it was also a deterrent to the oviposition of the cerambycid Monochamus alternatus [56]. Therefore, it is suggested that some changes in p-vinylguaiacol abundance may be a consequence of Dactylopius feeding.
In this work, 66 VOCs of both Dactylopius species were identified, and 125 of the Esmeralda and Rojo Pelón cladodes infested by D. coccus and D. opuntiae, respectively. A proportion of VOCs were commonly produced in both insect species or cultivars, but others were specific to each species or cultivar (Figure 4). This is a first approach to the diversity of VOCs produced by O. ficus-indica, and the changes that occur due to D. coccus and D. opuntiae feeding on cultivars suitable for the development of each Dactylopius species. More time and work will now be needed to understand the functions performed by the most relevant compounds in these interactions.
If knowledge of the interaction is improved, for example, if it is confirmed that some terpenoids favor the direct or indirect defenses of O. ficus-indica against D. coccus or D. opuntiae, this information could be considered in breeding programs. These programs could be aimed to improve rearing of D. coccus, or to induce resistance to D. opuntiae. In this regard, breeding programs for O. ficus-indica resistant to D. opuntiae have already been developed in Brazil and Morocco, and these have focused on physical and biochemical defense mechanisms [15,21,58]. For example, selecting cultivars with high concentrations of calcium oxalates can physically and biochemically limit phytophagous insects [59,60]. However, there are no known breeding programs for O. ficus-indica that consider the abundance of terpenes in cultivars, and the response this can trigger in the plant's direct or indirect defenses. This mechanism would be classified as biochemical defense, and measuring terpenes in different cultivars could improve the direction and understanding of the response. This observation highlights the need to better understand the interaction between O. ficus-indica and Dactylopius, because it can increase the possibilities of making proposals for sustainable management in the production of D. coccus, or in the control of D. opuntiae.

4. Materials and Methods

4.1. Chemicals

The reagents used in this study were N, O-bis(trimethylsilyl) trifluoroacetamide (BSTFA), trimethylsilyl chloride (TMCS), boron trifluoride methanol solution (Sigma-Aldrich, St Louis, MO, USA) ethylic ether (JT Baker, Deventer, Holland).

4.2. Insects and Uninfested and Infested O. ficus-indica Cultivars

Dactylopius coccus and Opuntia ficus-indica Esmeralda cultivar (infested and uninfested) were originally obtained from a local provider in Jerez, Zacatecas, Mexico. Dactylopius opuntiae and O. ficus-indica Rojo Pelón cultivar (infested and uninfested) were collected from an experimental field of Colegio de Postgraduados, Campus San Luis Potosí (Salinas, SLP). These cactus pear cultivars were selected with the knowledge that each one is favorable for the development of the respective Dactylopius species [58]. The taxonomic identity of Dactylopuis species was corroborated by S. J. Méndez-Gallegos using De Lotto (1974) [40] and Ferris (1955) keys [61]. To increase material for the samples and analyses, D. coccus and D. opuntiae colonies were reared on the respective cultivars mentioned under greenhouse conditions (15 ± 2 °C, 22 ± 2 °C and 50 % RH).

4.3. Essential oil of Dactylopius Species and Hosts

One hundred grams of adult female D. coccus and D. opuntiae and 1000 g of infested and uninfested O. ficus-indica cladodes were hydrodistilled at the temperature of boiling water. The volatile organic compounds (VOCs) were extracted from the condensed water by liquid-liquid extraction with ethyl ether. The solvent was distillated, and the residual water was removed from organic phase with anhydrous sodium sulfate. The sample was then concentrated (to 1 mL) at 40 °C under vacuum, and the solvent was eliminated at atmospheric pressure at 0 °C.

4.4. Derivatization for Alcohol Detection

Essential oils were diluted to 2 % in 500 µL heptane and introduced into a 10 mL microwave reaction tube with gasket. Then, 100 µL of BSTFA/TMCS solution (9:1 v/v) was added to the same tube as a silanizing agent. The mixture was reacted at 90 °C under microwave irradiation (250W microwave power) for 10 min using the Discover System 908,005 (CEM Corporation, NC, USA) with autogenous pressure.

4.5. Derivatization for Aldehydes and Carboxylic Acid Detection

Essential oils were diluted to 2 % in 500 µL heptane and introduced into a 10 mL microwave reaction tube with gasket. Then, 500 µL of boron trifluoride 14 % in methanol solution was added to the same tube. The mixture was reacted at 90 °C under microwave irradiation (250 W microwave power) for 10 min using the Discover System 908005 with autogenous pressure.

4.6. Essential Oil GS-MS Analysis

Samples without derivatization were diluted to 2 % in heptane, using 1 µL of each sample for the analysis, and each sample was analyzed in triplicate. GC-MS analysis was performed using a 7802A Network GC System coupled to a 5977E Network mass selective detector (MSD).
The separation was performed using an HP-5 capillary column (0.25 mm i.d. 30 mm, 0.25 mm film thickness) (J&W, Folsom, CA, USA). The injector was operated in splitless mode at 300 °C, with a flow of 1.0 mL/min, and the oven temperature was programmed to 40 °C for 3 min, and then heated at 3 °C/min to 300 °C with a holding time of 5 min at the final temperature. The MSD was operated at 70 eV; the ion source was set at 150 °C and the transfer line at 300 °C. VOCs were identified by interpreting their mass spectra fragmentation in the mass range of 15 to 800 atomic mass units. The software MassHunter (Agilent B.07.01.1805) was used for data recording. The compounds were identified by comparing the obtained mass spectra with those of reference compounds from the National Institute of Standards and Technology (NIST11) and Wiley 09. The identities of the compounds were confirmed by the Kovats retention index calculated for each peak with reference to the n-alkane standards (C7–C38) running under the same conditions.

4.7. Statistical Analysis

The relative percentage of each metabolite was calculated considering the peak area obtained by GC-MS of each metabolite in relation to the total area of peaks analyzed. Data represent the mean of the relative percentage of three repeats ± SD. Metabolites grouped by type for each essential oil were compared with the Mann Whitney U test considering the peak area of each metabolite and a p ≤0.05. The data in the graphics were expressed as median and range of each group. GraphPad Prism 5 was used to perform the analysis. Venn diagrams were constructed using an online tool (http://jvenn.toulouse.inra.fr/app/example.html accessed on 23 Nov 2023) [62].

5. Conclusions

This work presents an approach to better understand the interaction between O. ficus-indica, D. coccus and D. opuntiae through identifying volatile compounds in their essential oils. The abundance and proportion of VOCs of D. coccus and D. opuntiae were determined in the Esmeralda and Rojo Pelón cultivars, viable for the development of each insect species, respectively. Differential VOC production due to infestation by each Dactylopius species in each cultivar was also identified. Changes in methyl salicylate, terpenes and p-vinylguaiacol and their likely role in plant defense mechanisms should receive more attention because they could contribute to the development of proposals to improve D. coccus rearing, or for the control of D. opuntiae in those regions in the world where it is a key pest of O. ficus-indica.

Supplementary Materials

The following supporting information can be downloaded at the website of this paper posted on Preprints.org. Table S1 show the yields of essential oils of Dactylopius species and Opuntias varieties. Figures S1 y S2 show O. ficus-indica with Dactylopius species relationships by Venn diagrams, Figures S3-S6 show compounds group of Dactylopius species and O. ficus-indica cultivars.

Author Contributions

Conceptualization, M.M.G.-C. and J.S.M.-G.; methodology, E.R.-L., M.M.G.-C., J.S.M.-G.; formal analysis, E.G.P., E.R.-L., M.M.G.-C. and J.S.M.-G.; investigation, E.G.P., E.R.-L., M.M.G.-C., J.S.M.-G., J. A. M.-R., J. C. P.-H., A. B.-V., A. F.-V.; writing—original draft preparation, E.G.P, J.S.M.-G.; writing—review and editing, E.R.-L., M.M.G.-C., J. A. M.-R., J. C. P.-H., A. B.-V., A. F.-V; supervision, M.M.G-C., J.S.M-G.; funding acquisition, M.M.G-C. All authors have read and agreed to the published version of the manuscript.

Funding

The present study was financially supported by the CONAHCYT from México (Ciencia de Frontera, funding number: 320298)

Data Availability Statement

The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.

Acknowledgments

We thank to CONACYT for a graduate fellowship for Esperanza García-Pascual (CVU: 1146133). We also thanks to Vicente Rodríguez González (IPICYT) for the access to GC-MS equipment and Brayan Arias-Alvarez, Juan J. Rodríguez-Silva, and María G. Ortega Salazar for the technical assistance.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Comparison of the Dactylopius volatilomes using Venn diagrams based in the number of VOCs obtained through essential oils for each Dactylopius species.
Figure 1. Comparison of the Dactylopius volatilomes using Venn diagrams based in the number of VOCs obtained through essential oils for each Dactylopius species.
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Figure 2. Comparison of volatilomes of the Opuntia ficus-indica uninfested cladodes of each cultivar using Venn diagram, based on the number VOCs obtained through essential oils.
Figure 2. Comparison of volatilomes of the Opuntia ficus-indica uninfested cladodes of each cultivar using Venn diagram, based on the number VOCs obtained through essential oils.
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Figure 3. Amount and type of terpenes released by Opuntia ficus-indica (OFI) after Dactylopius infestation. (a) OFI Esmeralda-D. coccus; (b) OFI Rojo Pelón-D. opuntiae. The red columns represent uninfested cladodes, and blue columns represent cladodes infested by each Dactylopius species. Data are presented as means of the peak area of each terpene (grouped by type and number of compounds).
Figure 3. Amount and type of terpenes released by Opuntia ficus-indica (OFI) after Dactylopius infestation. (a) OFI Esmeralda-D. coccus; (b) OFI Rojo Pelón-D. opuntiae. The red columns represent uninfested cladodes, and blue columns represent cladodes infested by each Dactylopius species. Data are presented as means of the peak area of each terpene (grouped by type and number of compounds).
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Figure 4. Number of VOCs, obtained through its essential oils, identified as common or de novo compounds between uninfested and infested O. ficus-indica (OFI) cultivars by each Dactylopius species. Also, identified de novo VOCs from Dactylopius species.
Figure 4. Number of VOCs, obtained through its essential oils, identified as common or de novo compounds between uninfested and infested O. ficus-indica (OFI) cultivars by each Dactylopius species. Also, identified de novo VOCs from Dactylopius species.
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Table 1. Volatile organic compounds (VOCs) obtained through essential oils of each Dactylopius species.
Table 1. Volatile organic compounds (VOCs) obtained through essential oils of each Dactylopius species.
No. Compounds D. coccus D. opuntiae
RA (%) KI Exp RA (%) KI Exp KI ref
Carboxylic acids and derivatives 59.28% 78.29%
1 Hexanoic acid 1.09±0.08 903
2 2-methylhexanoic acid 0.54±0.01 950
3 Heptanoic acid 0.20±0.05 1021 0.64±0.16 1021 1005
4 2,4-dimethylhexanoic acid 0.37±0.02 1015
5 2-Ethylhexanoic acid 10.90±0.21 1036 1031
6 Lactic acid 5.58±0.58 1061 0.86±0.03 1062 1057
7 Glycolic acid 0.11±0.03 1075 1072
8 2,6-dimethylheptanoic acid 0.61±0.21 1087
9 Octanoic acid 1.90±0.74 1108 2.20±0.24 1108 1108
10 2,3,4-Trimethylpentanoic acid 0.44±0.02 1127
11 Ethyl benzoate 0.12±0.01 1153 1141
12 Ethyl octanoate 0.05±1.77 1188 1175
13 Nonanoic acid 2.32±0.64 1214 3.57±0.37 1214 1205
14 2,4-dimethylnonanoic acid 0.31±0.01 1234
15 Benzoic acid 2.04±0.00 1235 1.04±0.01 1235 1232
16 Ethyl nonanoate 0.26±0.03 1290 1282
17 2-Decenoic acid 0.42±0.02 1310 1290
18 Decanoic acid 8.76±2.53 1316 2.38±0.12 1316 1309
19 Butanedioic acid 0.11±0.03 1318 1314
20 (Z)-4-tert-butylcyclohexyl acetate 0.80±0.02 1358 0.12±0.03 1356 1346
21 Ethyl decanoate 0.18±0.02 1388 1382
22 Undecanoic acid 0.63±0.02 1414 1410
23 cis-5-Dodecenoic acid 3.18±0.04 1504
24 Dodecanoic acid 4.93±0.90 1512 1509
25 Nonanedioic acid 0.40±0.03 1535 1511
26 Ethyl dodecanoate 1.06±0.07 1580 1566
27 Tridecanoic acid 0.49±0.04 1606 1606
28 p-Hydroxybenzoic acid 0.24±0.00 1615 0.05±0.01 1616 1621
29 Hexyl salicylate 1.05±0.01 1660 0.57±0.02 1658 1684
30 (Z)-9-Tetradecenoic acid 0.42±0.05 1702 0.22±0.09 1707 1691
31 Tetradecanoic acid 21.25±2.90 1717 30.15±1.35 1718 1713
32 Ethyl tetradecanoate 0.40±0.01 1793 1782
33 (Z)-9-Hexadecenoic acid 0.56±0.12 1909 1885
34 Hexadecanoic acid 2.30±1.83 1934 5.89±0.42 1934 1909
35 Ethyl hexadecanoate 0.23±0.01 1974 1968
36 Heptadecanoic acid 1.03±0.06 2039 2009
37 (Z,Z) 9,12-Octadecadienoic acid 0.83±0.73 2105 3.76±0.67 2105 2087
38 (Z) -9-Octadecenoic acid 0.82±1.11 2112 2.44±0.33 2112 2088
39 Octadecanoic acid 1.69±2.32 2139 2.58±0.22 2140 2133
40 Ethyl octadecanoate 0.33±0.03 2208 2181
41 Dehydroabietic acid 1.58±0.00 2375 0.12±0.02 2376 2385
Aldehydes 5.80 7.68
42 Hexanal 1.79±0.36 964
43 Heptanal 1.24±0.11 1066 1069
44 Octanal 0.23±0.07 1165 1162
45 Nonanal 0.34±0.11 1235 2.57±0.17 1268 1267
46 Decanal 0.28±0.02 1367 1366
47 Dodecanal 0.28±0.10 1663
48 α-Hexylcinnamaldehyde 5.46±0.08 0.11±0.12 1719 1728
49 Heptadecanal 1.18±0.33 2088
Ether 0.09
50 Benzyl methyl ether 0.09±0.01 966
Terpene 0.54 0.08
51 p-Cymene 0.08±0.04 1018 1025
52 α-Ionone 0.36±0.15 1415 1413
53 β-Ionone 0.18±0.02 1472 1486
Ketones 0.54
54 Benzophenone 0.09±0.02 1600 1611
55 2-Nonadecanone 0.45±0.08 2116 2087
Alcohols 12.15 0.62
56 Phenol 0.31±0.09 1045 1043
57 2-Ethylhexanol 0.22±0.04 1095
58 1-Dodecanol 4.31±0.00 1559 0.09±0.01 1559 1575
59 1-Tridecanol 0.42±0.00 1659 1656
60 1-Tetradecanol 3.43±0.00 1765 1770
61 1-Hexadecanol 3.47±0.00 1977 1965
62 1-Octadecanol 0.52±0.00 2175 2159
Alkene 0.42
63 1-Tridecene 0.42±0.00 1284 1287
Alkane 1.80 2.41
64 Hexadecane 1.80±0.00 1581 1.11±0.29 1581 1600
65 Octadecane 0.25±0.00 1797 1800
66 Heneicosane 1.05±0.21 2309
Total 79.57 90.13
RA Relative Abundance, KI Exp Kovats Index Experimental, KI Ref Kovats Index reference.
Table 2. Volatilomes of Opuntia ficus-indica (OFI) cultivars before and after infestation by Dactylopius species.
Table 2. Volatilomes of Opuntia ficus-indica (OFI) cultivars before and after infestation by Dactylopius species.
No. Compounds OFI
Esmeralda		 OFI Esmeralda
infested by D. coccus 		KIExp OFI
Rojo Pelón		 OFI Rojo Pelón infested by D. opuntiae KIExp KIRef
RA (%) RA (%) RA (%) RA (%)
Carboxilic acid and derivatives 48.79 44.28 31.78 20.05
1 Hexanoic acid 0.83±0.63 0.82±0.00 942 904
67 3-Methyl-2-pentenoic acid 0.35±0.32 959 926
68 2-Hexenoic acid 0.66±0.01 0.36±0.00 972 939
69 4-Oxopentanoic acid 0.22±0.14 991 956
70 Heptanoic acid 0.59±0.50 0.39±0.05 1022 0.39±0.11 0.25±0.15 1030 1005
5 2-Ethylhexanoic acid 0.11±0.07 1044 1031
71 4-Methylvaleric acid 0.15±0.10 1033 1039
72 2-Methyl-4-pentenoic acid 0.11±0.16 1062
73 Lactic acid 3.22±1.91 1.63±0.16 1065 1057
15 Benzoic acid 1.49±1.77 0.29±0.03 1080 2.06±0.13 0.50±0.09 1080 1084
74 Methyl benzoate 0.41±0.14 1081 0.91±0.34 1084
9 Octanoic acid 1.23±1.52 1112 1.21±0.07 1.34±0.07 1112 1109
11 Ethyl Benzoate 0.05±0.01 1156 0.08±0.04 0.24±0.11 1152 1141
75 Benzeneacetic acid 0.17±0.05 1160 1150
76 Salicylic acid 0.18±0.25 1171 1176
77 Methyl salicylate 1.21±0.37 6.96±0.14 1181 0.32±0.07 1172 1176
78 2-Nonenoic acid 0.86±0.00 1179 0.33±0.08 1184
13 Nonanoic acid 1.09±0.24 0.76±0.07 1216 1.45±0.12 1.72±0.14 1212 1206
79 Ethyl salycilate 1.03±0.01 1244 1241
18 Decanoic acid 0.77±0.75 0.63±0.00 1318 0.79±0.08 1311 1309
19 Butanedioic acid 0.49±0.19 1320 1314
80 Gliceric acid 0.73±0.02 1346 1342
81 2-Methoxybenzoic acid 0.10±0.01 1331 1362
82 Methyl 2-methoxy benzoate 0.45±0.10 1319 1295
83 Glutaric acid 0.16±0.03 1410 1400
22 Undecanoic acid 0.16±0.02 0.14±0.07 1417 0.08±0.02 0.12±0.08 1408 1410
24 Dodecanoic acid 5.70±6.08 2.77±0.06 1516 7.19±0.50 2.35±0.16 1505 1509
84 2,5-Dimethoxy benzenemethanol acetate 0.13±0.04 1523
26 Ethyl Dodecanoate 0.26±1.27 0.17±0.09 1582 0.33±0.01 1571 1581
28 p-Hydroxybenzoic acid 0.94±0.45 1620 1621
29 Hexylsalicylate 0.25±3.04 0.46±0.07 1662 1652
85 Methyl tetradecanoate 0.84±0.16 1719 1714
27 Tridecanoic acid 0.06±0.04 1611 1606
86 12-Methyltridecanoic acid 0.07±0.00 1678 1680
31 Tetradecanoic acid 2.98±3.09 1.36±0.06 1720 1.56±0.10 0.19±0.07 1714 1714
87 Methyl benzoate 1.46±0.03 1752
88 Benzyl Benzoate 2.65±0.51 1741 0.15±0.04 1754 1765
32 Ethyl tetradecanoate 0.10±0.13 1784 1782
89 Nonanedioic acid 0.28±0.01 1808 1788
90 Pentadecanoic acid 0.42±0.47 0.43±0.02 1826 1807
91 Isopropyl tetradecanoate 0.05±0.34 1820 1827
92 Benzyl salicylate 0.31±0.12 1855 1860
34 Hexadecanoic acid 7.19±2.16 4.88±0.16 1935 9.35±0.74 8.25±0.45 1916 1909
93 15-Methylhexadecanoic acid 0.17±0.03 2040 1974
37 (Z,Z)-9,12-Octadecadienoic acid 1.90± 0.44 1.03±0.12 2106 0.88±0.14 2.20±1.43 2087 2087
38 (Z)-9-Octadecenoic acid 2.35±1.66 1.94±0.10 2113 2.47±0.98 2090 2100
39 Octadecanoic acid 2.53±0.59 1.76±0.01 2141 2.76±0.15 0.59±0.15 2119 2133
94 Methyl octadecanoate 0.33±0.04 1809
40 Ethyl octadecanoate 0.11±0.00 2199 2202
41 Dehydroabietic acid 9.32±2.24 9.99±0.04 2376 0.46±0.05 0.39±0.02 2344 2373
Aldehides and derivatives 2.15 6.25 4.3 4.82
42 Hexanal 0.44±0.44 0.47±0.00 984 964
43 Heptanal 0.18±0.02 1069 1068
95 Benzaldehyde 0.15±0.07 1094 0.32±0.03 0.55±0.33 1094 1080
96 Diethyl acetal hexanal 0.25±0.14 0.46±0.10 1086 1082
97 5,5-Dimethyl-3-oxo-1-cyclohexene-1-carboxaldehyde 0.15±0.03 1104
44 Octanal 0.17±0.01 1160 0.40±0.05 0.09±0.05 1165 1167
98 Phenylacetaldehyde 0.62±0.61 0.56±0.06 1198 0.82±0.06 0.81±0.17 1201 1208
45 Nonanal 0.53±0.21 1.03±0.01 1271 1.73±0.12 1.32±0.09 1265 1267
46 Decanal 0.14±0.00 1370 0.14±0.08 1366 1366
99 Nonanaldimethylacetal 0.21±0.10 0.37±0.05 1374 1379
100 3-(4-(tert-butyl)phenyl-2-methylpropanal 0.30±0.04 1497 1500
101 4-Hydroxy-3-methoxybenzaldehyde 0.10±0.04 0.62±0.02 1524 0.89±0.04 2.05±0.01 1511 1544
102 3-Ethoxy-4-hydroxybenzaldehyde 0.11±0.02 1554 1560
48 α-Hexylcinnamaldehyde 1.22±0.74 1725 1726
103 Octadecanal 0.32±0.13 2187
Heterocycles 0.67 8.91 1.38
104 2-Isopropyl-3-metoxypirazina 0.25±3.25 1070 1080
105 2-Methoxy-3-isopropylpyrazine 0.30± 7.22 1.05±0.33 1083 1089
106 Ethyl 2-(5-methyl-5-vinyltetrahydrofuran-2-yl)propan-2-yl carbonate 8.18±0.10 1064 1090
107 3-Isobutyl-2-methoxypyrazine 0.43±0.03 1164 1170
108 3-Ethyl-4-methyl-1H-pyrrole-2,5-dione 0.35±0.03 1209 1192
109 3-Hydroxy-2-methylpyran-4-one 0.07±0.00 1266 1293
110 2,3-Dihydro-2,2,4,6-tetramethylbenzofuran 0.33±0.01 1410
Ethers 0.31 0.16
50 Benzylmethylether 0.31±0.20 966 966
111 1,2-Dimethoxybenzene 0.16±0.02 1111 1106
Ketones 1.95 1.16 1.17 0.61
112 5-Hexen-2-one 0.29±0.01 1007
113 2,2,6-Trimethylcyclohexanone 0.14±0.09 1031
114 Acetophenone 0.57±0.08 1047 0.45±0.05 1055 1049
115 Isophorone 0.24±0.06 0.01±0.22 1106 0.17±0.03 1038 1094
116 Phenylacetone 0.48±0.05 0.44±0.00 1114 0.24±0.02 0.16±0.07 1110 1116
117 4-Oxoisophorone 0.13±0.02 1131 0.07±0.04 1125 1105
118 2-(1-Hydroxybut-2-enylidene)cyclohexanone 0.14±0.03 1145
119 1-(1-cyclohexen-1-yl)(-1-1-Butenone) 0.70±0.34 1214
54 Benzophenone 0.11±0.07 0.14±0.01 1607 0.41±0.05 1584 1607
Terpenes 17.89 13.92 0.8 15.52
120 Limonene 0.85±0.23 1023 1020
121 Linalool oxide 8.48±0.58 5.06±0.42 1063 1064
122 trans-Linalool oxide 5.70±0.03 1064 1068
123 1,5,5-Trimethyl-3-methylene cyclohexene 0.55±0.63 1071
124 β-Linalool 5.00±0.58 0.26±0.35 1088 1082
125 α-Terpineol 2.00±0.36 1178 1172
126 Linalool 0.19±0.22 1232 5.61±0.10 1227 1227
127 Geraniol 0.44±0.27 0.33±0.04 1250 1.84±0.06 1357 1238
128 Nerol 0.33±0.06 1232 0.79±0.04 1328 1260
129 β-Damascenone 0.18±0.17 1362 0.55±0.30 1360 1361
52 α-Ionona 0.09±0.26 1404 1413
130 α-Isomethylionone 0.88±0.15 1453 1478
53 β-Ionone 0.40±0.06 1460 0.18±0.04 1458 1486
131 Dihydroactinidiolide 0.38±0.13 0.30±0.02 1537 1532
132 Neophytadiene 0.39±0.08 1832 1842
133 28-Nor-17β(H)-hopane 0.45±0.01 2942
134 β-Sitosterol 0.35±0.03 6.55±0.04 3244 3284
Alcohols 12.72 9.91 29.37 30.78
135 1,2-Dihydroxy-4-methylpentane 0.27±0.02 990
136 Hexanol 0.06±0.01 9994 992
137 (Z)-2-Hexen-1-ol 0.36±0.19 1010 7.65±0.18 4.21±0.08 1025 1001
56 Phenol 0.22±0.09 0.16±1.30 1045 1043
138 Heptanol 0.11±0.23 1067 1092
57 2-Ethylhexanol 0.58±0.23 0.22±0.24 1099 2.13±0.09 1.49±0.05 1103
139 Benzylalcohol 0.27±0.11 0.56±0.22 1143 0.90±0.02 2.08±0.06 1132 1156
140 1-Octanol 0.29±0.14 1158 1.27±0.04 1.51±0.18 1177 1177
141 Guaiacol 0.35±0.03 1209 1192
142 Nonanol 0.07±0.01
143 Glycerol 0.33±0.52 1290 1.46±0.09 1288 1292
144 p-Vinylguaiacol 10.62±7.24 1.76±0.34 1305 14.67±0.93 17.03±5.14 1294 1282
145 1-Methyl-1(4-methyl-3-cyclohexenyl)ethanol 0.63±0.00 1318 1309
146 Isododecanol 0.09±0.01 1479
58 1-Dodecanol 0.47±0.09 0.60±0.01 1563 0.76±0.04 1553 1575
60 1-Tetradecanol 0.66±0.00 1756 1768
61 1-Hexadecanol 0.23±0.07 0.98±0.08 1978 0.53±0.03 1960 1965
62 1-Octadecanol 0.92±0.04 2177 2159
147 3,7,11,15-Tetramethyl-2-hexadecenol 1.82±0.15 2198 3.52±0.17 2173 2179
148 Octacosanol 0.94±0.04 3125 3154
Aromatic derivatives 0.77
149 1,2-Dihydro-1,1,6-trimethyl naphthalene 0.18±0.07 1338 1332
150 10,18,Bisnorabieta-8,11,13.triene 0.59±0.03 2041
Alkanes 0.69 0.55 0.78
64 Hexadecane 0.69±0.19 0.07±0.01 1585 1600
151 Heptadecane 0.12±0.05 1692 1700
152 Nonadecane 0.36±0.06 1906 1900
153 Eicosane 0.19±2.08 1992 2000
66 Heneicosane 0.23±0.42 2092 2100
154 Docosane 0.36±0.07 2188 2200
Total 85.27 76.9 77.11 73.16
RA Relative Abundance, KI Exp Kovats Index Experimental, KI Ref Kovats Index reference.
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