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Article

Synthetic Carvacrol Derivatives for the Management of Solenopsis Ants: Toxicity, Sublethal Effects, and Horizontal Transfer

by
Jaciele O. Dantas
1,
Sócrates C. H. Cavalcanti
2,
Ana Paula A. Araújo
3,
Arie F. Blank
4,
Jefferson E. Silva
1,
Marcelo C. Picanço
5,
Eraldo Lima
5,
Valfran S. Andrade
1,
Thaysnara B. Brito
2 and
Leandro Bacci
4,*
1
Postgraduate Program in Agriculture and Biodiversity, Universidade Federal de Sergipe, São Cristóvão 49100-000, SE, Brazil
2
Department of Pharmacy, Universidade Federal de Sergipe, São Cristóvão 49100-000, SE, Brazil
3
Department of Ecology, Universidade Federal de Sergipe, São Cristóvão 49100-000, SE, Brazil
4
Department of Agronomic Engineering, Universidade Federal de Sergipe, São Cristóvão 49100-000, SE, Brazil
5
Department of Entomology, Universidade Federal de Viçosa, Viçosa 36571-000, MG, Brazil
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(10), 1988; https://doi.org/10.3390/agriculture13101988
Submission received: 19 July 2023 / Revised: 4 October 2023 / Accepted: 9 October 2023 / Published: 13 October 2023
(This article belongs to the Special Issue Sustainable Crop Production and Pest Control)
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Abstract

:
Ants belonging to the genus Solenopsis are highly significant invasive pests worldwide. The control of these insects has historically relied on the use of synthetic insecticides, which, unfortunately, has led to a range of ecological repercussions. In light of these challenges and the limited availability of registered products for managing these pests, our study set out to synthesize and assess the insecticidal properties of carvacrol derivatives. The lethal and sublethal effects caused by these derivatives were compared to the essential oil of Lippia gracilis (50.7% carvacrol) and to the base molecule—carvacrol. Carvacryl benzoate was the most toxic derivative to Solenopsis sp., with an LD50 of 3.20 μg/ mg. This compound was about 2 and 7.6 times more toxic than carvacrol at the doses needed to kill 50 and 90% of populations, respectively. The workers of Solenopsis sp. showed a rapid reduction in survival when exposed to carvacrol (LT50 = 8.43 h) and carvacryl benzoate (LT50 = 8.87 h). Insects treated with sublethal doses of the compounds did not show significant effects on self-cleaning, allogrooming and aggregation, with the exception of those treated with L. gracilis essential oil. The oil increased self-cleaning and reduced allogrooming and aggregation. Ants treated with carvacrol and carvacryl benzoate travelled greater distances and had higher movement speeds when compared to the control. These compounds exhibited decreased meanders and angular velocities. When live workers were exposed to dead individuals at the LD90 of the compounds, carvacryl benzoate was the derivative that most reduced survival due to horizontal transfer. These findings underscore the considerable potential of carvacrol derivatives, specifically carvacryl benzoate, as an alternative approach to managing ants of the Solenopsis genus.

1. Introduction

Ants belonging to the Solenopsis Westwood genus (Hymenoptera: Formicidae)—known as fire ants or red fire ants [1,2]—originate from South America, but have spread to various parts of the world, being found in countries such as the United States [3], South Korea [4], Japan, China and New Zealand [5]. The Solenopsis genus has a high species diversity [6], with about half of them found in the Neotropical region [7]. These ants are considered invasive, mainly in disturbed habitats [8,9]. Several features make Solenopsis sp. good invaders, such as a high dispersal capacity [10] and a high aggressiveness [1,11], in addition to being good competitors [12] and having large colonies.
The invasion of Solenopsis sp. in new areas makes management difficult, causing major impacts to public health and agriculture [5,13,14]. In general, it is estimated that the economic costs caused by ants of the genus Solenopsis in invaded areas can reach about USD 3.49 billion [15]. In agricultural areas, ants cause direct damage to several crops [2,3], in addition to indirect damage, via reducing the natural biological control of populations of sucking insect pests. This occurs through mutualistic interactions with sucking insects, where ants perform pest defense against predators in exchange for honeydew (a sugary substance) [2,16,17]. They are very aggressive; thus, they can also attack several species, causing ecological disturbances [3]. In relation to public health, they can contribute to the dissemination of disease pathogens such as Enterococcus spp., Staphylococcus spp. and Streptococcus spp. in hospital environments [18], and their stings can cause irritation and, in more severe cases, anaphylaxis and breathing difficulties [19,20]. In addition, they can cause damage to equipment and buildings [15].
These impacts of Solenopsis sp. invasion require control measures, with direct application to anthills and adjacent areas [21]. Attempts at control are mainly made with organosynthetic insecticides [22] from the pyrethroid group [23], neonicotinoids and growth regulators [24]. The products used can be slow-acting (e.g., toxic baits) or fast-acting (e.g., contact insecticides); the use of repellents and fumigants is also common [18]. However, the persistent and inappropriate use of these products can lead to ecological disturbances, either directly or through residual action [22,25].
In this context, plant essential oils and their primary constituents have demonstrated efficacy as insecticides and act more sustainably [26]. The monoterpene carvacrol, for example, has bioactivity on the tick Rhipicephalus (Boophilus) microplus [27] and insect pests such as the termite Cryptotermes brevis [28] and the Diaphania hyalinata larvae [29]. Furthermore, the synthetic modification of natural compounds has frequently resulted in structures exhibiting enhanced bioactivity and expanded therapeutic potential [30,31]. Carvacrol is a significant phenolic compound containing a reactive hydroxyl group. Diverse chemical reactions can be utilized to introduce new functional groups or modify existing ones in the carvacrol molecule, resulting in the production of carvacryl derivatives. Carvacryl derivatives have been applied across a broad spectrum of biological tests, revealing their diverse capabilities, which encompass anticancer, antihelminthic, antimicrobial and larvicidal properties [32]. Thus, natural compounds and their derivatives can induce various effects on insects by acting as repellents, attractants and oviposition deters [25,30], in addition to causing behavioral changes that can alter insect communication [28,33]. Such effects may be desirable for controlling eusocial insects, for which interindividual communication is of paramount importance for colony cohesion [34,35,36,37].
Prophylactic strategies are recognized for promoting the first line of defense of eusocial insects against pathogens, increasing colony health and viability [38]. Among such strategies, necrophoresis (removal of bodies) and allogrooming (interindividual cleaning) can reduce infection within colonies. Such behaviors are adaptative, since colonies often have high densities of genetically related individuals, constantly involved in collaborative activities [39]. However, studies report that contacts between colonial individuals can contribute to the transfer of insecticides, increasing the spread of contaminants within the nest. This horizontal transfer of insecticides may thus constitute an important control mode [40,41].
Considering the global significance of ants from the Solenopsis genus, the search for alternative control strategies is highly important. Solenopsis saevissima (Smith) and S. invicta Buren originate from South America [42] and are the most abundant and widely distributed fire ants in Brazil [43]. Although it is relatively easy to distinguish this genus from others, identifying the species level can be considerably challenging due to a limited number of distinguishing characteristics [44]. Therefore, in this study, we utilize essential oil from L. gracilis and its primary component, carvacrol, as well as its derivatives, as our main source of bioactive compounds. Carvacrol was used to synthesize nine new derivative molecules. Consequently, in an effort to explore new control alternatives, this research evaluates the lethal and sublethal effects (behavioral changes) as well as the horizontal transfer of these compounds in Solenopsis sp. worker ants.

2. Materials and Methods

2.1. Insects

In this research, we collected worker ants from a single species of the genus Solenopsis (unidentified), employing attractive food baits (animal protein) distributed near nests located in a home environment in the municipality of Aracaju, SE, Brazil (10°53′ S, 37°06′ W). The ants were collected with a soft bristle brush, placed in 200 mL plastic pots, covered with organza fabric and sent to the Integrated Pest Management Laboratory located at the UFS, São Cristóvão, SE, Brazil (10°54′ S, 37°04′ W).
The insects were then placed in plastic containers (11 cm × 7.5 cm), covered with plastic film (G-útil Guarufilme, Guarulhos, SP, Brazil) and maintained under controlled conditions (27 ± 2 °C, 70 ± 5% RH and 12 h photoperiod) for 24 h for acclimatization until the experiments were carried out. During this period, only distilled water was provided to the workers.

2.2. Synthesis of Carvacrol Derivatives

The derivatives were synthesized at the Pharmaceutical Chemistry Laboratory of the UFS University through nucleophilic nuclear substitution and esterification reactions. Nine compounds were synthesized from the base molecule carvacrol: carvacryl acetate, carvacryl benzoate, carvacryl butyrate, carvacryl hexanoate, carvacryl isobutyrate, carvacryl isovalerate, carvacryl pivaloate, carvacryl trichloroacetate and carvacryl ethyl ether (Figure 1).
The ether compound was synthesized according to the method described by Collen [45]. To obtain the esters, we used methodologies adapted from Dolly and Barba, Ben Arfa et al. and Morais et al. [46,47,48] using THF (tetrahydrofuran) as a solvent [30].
The progress of the reactions was monitored using thin-layer chromatography (TLC), which was examined under ultraviolet light at 256 nm and compared to the initial substance (carvacrol). The derivatives were purified by employing silica gel 60 as the stationary phase and pure hexane as the mobile phase. Melting points were determined using a Logen Scientific melting point apparatus without any corrections. All the chemicals utilized in the reactions, as well as the monoterpene carvacrol, were sourced from Sigma-Aldrich Chemical Co. (St. Louis, MO, USA).

2.3. Bioassays

The synthetic derivatives were compared with the precursor molecule carvacrol and with the essential oil of Lippia gracilis Schauer (Lamiales: Verbenaceae), which is notably abundant in carvacrol (50.7%) [29]. The essential oil of L. gracilis was obtained from plants that are maintained at the UFS Active Germplasm Bank—located at the experimental farm—UFS Rural Campus, São Cristóvão, SE, Brazil (10°55′ S, 37°11′ W). The extraction, identification and quantification of compounds were carried out following the procedures outlined in Santos et al. [49].
Bioassays were conducted with precise climate conditions (27 ± 2 °C, 70 ± 5% relative humidity, and a 12 h photoperiod) in the laboratory. The compounds were diluted in acetone solvent (Panreac, UV-IR-HPLC-GPC PAI-ACS, 99.9% purity) and applied topically (0.5 µL) to the prothorax of the worker ants using a Hamilton® microsyringe (Reno, NV, USA). In the negative control group, only acetone was used.
In order to facilitate the application of the compounds, the individuals were immobilized at −19 °C (Eletrolux®, Curitiba, PR, Brazil) for 90 s. Preliminary tests have indicated that this method has no discernible impact on the survival and behavior of the ants. To determine the doses to be applied, fifty workers were weighed (Shimadzu, AUW220D, Jandira, SP, Brazil) to obtain the average mass of the insects.
In the acute toxicity bioassays, we employed the following treatments: the essential oil of L. gracilis, the base molecule carvacrol and nine synthetic derivatives. Meanwhile, in the behavioral bioassays, we used the essential oil of L. gracilis, carvacrol and its most potent synthetic derivative.

2.3.1. Acute Toxicity

The bioassays to determine the dose–response curves and lethal doses were carried out using a completely randomized design, comprising eight replications for each treatment. The experimental units consisted of groups of six to seven worker ants belonging to Solenopsis sp., all of uniform size, totaling 4144 individuals. This approach was employed to determine both the dose–response curves and lethal doses. Initially, tests were carried out with three doses (1, 5 and 10 µg of substance/mg of insect) in order to obtain mortalities between 5 and 95%. At least 5 intermediate doses were used to establish the dose–response curves. The doses used were as follows: 1.5, 3, 6, 10, 12 and 15 µg/mg (L. gracilis essential oil); 1, 3, 8, 12, 22 and 30 µg/mg (carvacrol); 2.5, 5, 8, 10, 15, 20 and 25 µg/mg (carvacryl acetate); 1, 1.5, 2, 4, 6, 8, 10 and 15 µg/mg (carvacryl benzoate); 2, 4, 10, 12, 15, 20 and 35 µg/mg (carvacryl butyrate); 1, 2, 3, 6, 8, 12, 24 and 40 µg/mg (carvacryl ethyl ether); 2.5, 5, 10, 15, 20 and 25 µg/mg (carvacryl hexanoate); 2.5, 5, 8, 15, 20 and 25 µg/mg (carvacryl isobutyrate); 2.5, 5, 9, 10, 15, 20 and 25 µg/mg (carvacryl isovalerate); 2, 4, 10, 12, 15, 20 and 35 µg/mg (carvacryl pivaloate); and 1.25, 4, 8, 20, 25 and 40 µg/mg (carvacryl trichloroacetate).
The ants were placed in a Petri dish (Global Trade Technology, Monte Alto, SP, Brazil) (6 × 1.5 cm) lined with filter paper (Unfil) moistened with 0.4 mL of distilled water and covered with plastic film (G-util Guarufilme, Guarulhos, SP, Brazil). Mortality assessment was performed 48 h after setting up the bioassays. The mortality evaluation was based on the mobility of ants after being stimulated with a soft bristle brush. Insects that did not move after the stimulus were considered dead.
In the bioassays conducted to generate survival curves and determine the lethal time of the compounds on Solenopsis sp. worker ants, we employed the LD90 values obtained from acute toxicity bioassays. The procedures were similar to those used in toxicity bioassays, with the exception of doses, number of repetitions and evaluation time. Fifteen repetitions were performed with seven worker ants per dish and three treatments plus the control, totaling 420 individuals. The first mortality assessments were performed every 10 min for 2 h, then every 30 min for 6 h, followed by 1 h assessments during the first 12 h and every 2 h for the first 24 h. Subsequently, evaluations were carried out at intervals of 4 h in the following 12 h and every 12 h for 100 h.

2.3.2. Individual and Collective Behavior

For this experiment, we observed the individual behavior of treated Solenopsis sp. (individual behavior) (n = 1) and the interaction of a group of ants not exposed to the compounds (6 ants) with a treated one (collective behavior) (n = 7).
The experimental designs followed a completely randomized approach, involving 60 repetitions for each treatment, along with an additional 60 repetitions for the control group. In these experiments, Solenopsis sp. worker ants were exposed to two conditions: acetone (serving as the negative control) and the LD30 concentrations of the compounds, as determined in the acute toxicity bioassays. Before being exposed to the treatments, the ants were placed in a Petri dish (6 × 1.5 cm) lined with filter paper moistened with 0.4 mL of distilled water for 5 min for acclimatization.
In the experiment to evaluate individual behavior, after acclimatization and immobilization, the individuals were treated and placed in Petri dishes individually, totaling 240 individuals. After 1 min of exposure, self-cleaning behavior was observed. As for the collective behavior experiment, after acclimatization and immobilization, an ant was randomly removed from the group of seven ants and marked with non-toxic yellow paint (Acrilex Tintas Especiais S.A., São Bernardo do Campo, SP, Brazil). After 3 min of marking with the ink, the ant received the treatment, and after 1 min, it was subsequently placed back into the Petri dish with the other untreated ants. One min after the relocation on the board, the observation of antenation, allogrooming and aggregation behaviors began. Preliminarly tests indicated that the paint did not affect the survival and behavior of the ants.
In both bioassays, observations were performed for one continuous minute, with a one-minute interval between them, during a period of 10 min, totaling 5 min of observation for each insect. Overall, behaviors were recorded for 2400 min (2 bioassays × 4 treatments × 60 repetitions × 5 min of observation).

2.3.3. Walking Behavior

Individual walking behavior was evaluated with workers of Solenopsis sp. subjected to the LD30 of each treatment and acetone (negative control). The experiments were conducted following a completely randomized design, comprising 60 repetitions for each treatment, totaling 240 individuals. The bioassays were performed in Petri dish arenas (6 × 1.5 cm) lined with moistened filter paper and covered with plastic film.
After 1 min of placing the individuals in the arena, recording began for a period of 600 s using a video camera (Panasonic SD5 Superdynamic—model WV-CP504, São Paulo, SP, Brazil) equipped with a Spacecom lens (1/3″ 3–8 mm) attached to a computer. The distance traveled (mm), velocity (mm/s), meander (°/mm) and angular velocity (°/s) were captured in Ethovision XT software (version 8.5; Noldus Integration System, Sterling, VA, USA) and data were analyzed using Studio 9 software (Pinnacle Systems, Moutain View, CA, USA).

2.3.4. Horizontal Transfer of Compounds

The objective of this experiment was to assess the potential transfer of the compounds utilized in this study from dead ants to live ants that were not subjected to the treatments. Two proportions were used in the experiments, [1:20] = 1 dead ant to 20 live ants and [1:5] = 4 dead ants to 20 live ants. The design was completely randomized with ten repetitions, totaling 800 live individuals and 200 cadavers. The bioassays were performed in Petri dish arenas (6 × 1.5 cm) lined with filter paper moistened with 0.4 mL of distilled water and covered with film plastic.
Dead ants were obtained after 24 h of exposure of the workers to the LD90 of the compounds. For the control, cadavers were obtained after application of acetone and freezing in a freezer at −19 °C for 30 min. The number of live and dead ants was evaluated after 1, 2, 4, 6, 10, 14, 26, 38, 50, 62, 74, 86, 98, 110 and 122 h after setting up the experiments.

2.4. Statistical Analysis

Mortality data underwent Probit analysis to establish the dose–response curves for each treatment, utilizing the PROC PROBIT procedure in SAS (SAS Institute, Cary, NC, USA, 2008, version 9.1). These curves were then employed to calculate the lethal doses required to induce 30%, 50% and 90% mortality (LD30, LD50 and LD90), along with their corresponding 95% confidence intervals (LC95). The determination of the most toxic synthetic derivative was performed using the criterion of non-overlapping confidence intervals with the origin of the interval in the LD50.
For analysis of survival, horizontal transfer and their respective lethal times, Kaplan–Meier estimators were used through the Log-Rank test (SigmaPlot, version 14). From this analysis, survival curves and lethal times (LT50) were obtained for each treatment. The Holm–Sidak multiple comparison method was used at a significance level of 0.05 to compare the curves (SigmaPlot, version 14). LT50 values were compared by the criterion of non-overlapping confidence intervals with the origin of the interval.
Data on individual and collective behavior, as well as walking behavior (n = 60), of the ants exposed to the compounds were initially subjected to normality testing using the Shapiro–Wilk test (p > 0.05) and variance homogeneity assessment through the Brown–Forsythe test (p > 0.05). Given that these variables did not meet the assumptions of normality and homogeneity, the data were subsequently analyzed using a non-parametric Kruskal–Wallis analysis of variance (p < 0.05), followed by Dunn’s multiple comparison method to assess the impact of the treatments relative to the control group. All behavioral data analyses were performed using SigmaPlot.

3. Results

3.1. Acute Toxicity

All synthetic carvacrol derivatives exhibited bioactivity against Solenopsis sp. The lethal doses required to eliminate 50% of the ant populations ranged from 3.2 to 10.8 µg/mg (Table 1). Carvacryl benzoate was the most toxic derivative for ants (3.2 µg/mg; CI95%: 2.86–3.57). Its LD50 was smaller than those observed for the essential oil of L. gracilis (6.11 µg/mg; CI95%: 5.16–7.20) and its major compound carvacrol (6.79 µg/mg; CI95%: 5.19–8.71). The other synthetic derivatives showed similar or lower toxicities than the base molecule carvacrol (Table 1).
The greatest slope of the dose–response curves was observed for carvacryl benzoate (3.2 ± 0.24). This compound was 3.2 and 7.6 times more toxic than essential oil from L. gracilis and carvacrol at the dose considered standard control in Brazil (LD90) [50,51], respectively (Table 1).
Survival of Solenopsis sp. exposed to the LD90 of the essential oil of L. gracilis, its major compound carvacrol and the most toxic synthetic derivative (carvacryl benzoate) significantly reduced over time (χ2 = 359.4; d.f. = 3; p < 0.001) (Figure 2). The survival of Solenopsis sp. worker ants exhibited a rapid decline upon exposure to carvacrol (LT50 = 8.43 h; CI95% = 5.37–11.50) and carvacryl benzoate (LT50 = 8.87 h; CI95% = 7.04–10.7) (Figure 2). In fewer than 60 h, all individuals died, and there was no statistically significant difference between the survival curves of ants exposed to these two compounds (Statistic = 1.17, p = 0.279). On the other hand, the essential oil of L. gracilis caused slower mortality in Solenopsis sp. This oil took 39.6 h (CI95% = 32.7–46.5) to kill 50% of tested individuals (Figure 2). Despite reducing survival more slowly, the oil caused 100% mortality within 84 h of exposure (Figure 2).

3.2. Individual and Collective Behavior

Data on individual self-cleaning behavior (H = 27.49; d.f. = 3; p < 0.001) and collective allogrooming (H = 14.96; d.f. = 3; p = 0.002) and aggregation (H = 14.79; d.f. = 3; p = 0.002) from Solenopsis sp. varied between treatments. The antennation behavior did not vary between treatments (H = 3.33; d.f. = 3; p = 0.343) (Figure 3).
The ants showed a higher number of self-cleaning and lower numbers of allogrooming and aggregation when exposed to the LD30 of the essential oil of L. gracilis (Figure 3). Ants treated with carvacrol and carvacryl benzoate exhibited no significant alteration in this behavior compared to the control group (Figure 3).

3.3. Walking Behavior

The distance covered (H = 30.15; d.f. = 3; p < 0.001) and the speed (H = 23.55; d.f. = 3; p < 0.001) of Solenopsis sp. varied between treatments (Figure 4). Workers treated with carvacrol and carvacryl benzoate covered a higher distance (Figure 4A) at increased speed (Figure 4B).
Individuals treated with the LD30 of these compounds showed a notable increase in the distance walked, with a 27.28% and 38.47% rise compared to the control (817.7 mm), respectively (Figure 4A). The displacement behavior of the ants treated with the essential oil of L. gracilis did not differ from the control (Figure 4).
The meander behavior (H = 47.28; d.f. = 3; p < 0.001) and angular velocity (H = 22.74; d.f. = 3; p < 0.001) of Solenopsis sp. varied between treatments (Figure 5). The normal walking activity (control) of Solenopsis sp. involved greater changes in direction of movement by distance traveled (meander = 89.6 ± 7.7°/mm) and by time (angular velocity = 26.4 ± 2.1°/s) (Figure 5). Workers treated with carvacrol and carvacryl benzoate had a reduced meander (62.2 ± 7.1 and 36.1 ± 4.6°/mm) and angular velocity (20.0 ± 2.1 and 14.7 ± 1.4°/s) versus the control, respectively (Figure 5). Workers treated with these two compounds exhibited a more circular movement pattern along the edge of the arena and with little change in direction (2D and 3D graphics) (Figure 5). The essential oil of L. gracilis did not affect these parameters (Figure 5).

3.4. Horizontal Transfer of Compounds

In general, mixing dead ants submitted to the LD90 of the compounds with live ants reduced the survival of workers of Solenopsis sp. over time (χ2 = 200.8; d.f. = 7; p < 0.001) (Figure 6). No statistically significant difference was observed between the survival curves of essential oil from L. gracilis (p = 0.833) and carvacrol (p = 0.951) in the two proportions (1:20 and 1:5) (Figure 6).
The greatest horizontal transfer occurred when the ants were treated with carvacryl benzoate and the corpses were placed together with live ants in a 1:5 ratio. At the end of the experiment, this compound caused death in 54% of the ants, requiring 78.5 h (CI95% = 71.9–85.1) for the compound to kill 50% of the individuals (Figure 6).

4. Discussion

Essential oils derived from plants and their individual compounds are considered biorational and environmentally safe products [52]. Here, we show that the essential oil of L. gracilis, its major constituent carvacrol and the synthetic derivative compound carvacryl benzoate showed relevant lethal and sublethal effects on the control of ants of the genus Solenopsis.
Compounds from essential oils of plants act on several sites of action, including octopamine receptors, sodium channels, acetylcholine receptors, glutamate-mediated chloride channels and GABA receptors [52], having potential for use in integrated pest management programs [53]. Carvacrol has already proven to be toxic to several pests such as Cimex lectularius Linnaeus (Hemiptera: Cimicidae) [54], Musca domestica (Diptera: Muscidae) [55], Sitophilus zeamais (Coleoptera: Curculionidae) Motschulsky [56], Helicoverpa armigera (Lepidoptera: Noctuidae) Hübner [57] and Diaphania hyalinata (Lepidoptera: Crambidae) [29]. Although there is no consensus regarding its molecular mechanism and its main target of action, it is believed that carvacrol inhibits the activity of the enzyme acetylcholinesterase [58]. It is known, however, that carvacrol also acts as a positive allosteric modulator in the GABA receptor, enhancing the uptake of Cl- anions in the presence of GABA. Thus, this xenobiotic can act on different sites of action [52] and have multiple targets [59].
Carvacrol is a phenolic monoterpenoid compound, obtained from the essential oil of several plant species [30,60]. Studies on synthetic derivatives make it possible to assess which structural properties of a molecule are involved in its activity, thus allowing the discovery of new synthetic routes and the large-scale production of bioactive molecules [61]. Among the synthetic carvacrol derivatives used in this study, carvacryl benzoate was the most toxic, showing a lower LD50 than that of the parent compound (carvacrol). The intensity of the toxic effect may be related to chain length, functional groups or substituent position (e.g., meta or ortho) [62].
Although all compounds were toxic to Solenopsis sp. workers, mortality occurred more quickly with carvacrol and its derivative carvacryl benzoate (LT50 ~9 h), while the mortality of ants treated with essential oil from L. gracilis was slower (LT50 ~40 h). This difference may be related not only to the toxicity of the compound itself, but also to the interaction with sublethal effects that can alter the behavior of ants. Through interindividual behaviors such as allogrooming and aggregation, contaminated ants can transfer toxic compounds to other members of the colony. Here, we found that ants treated with essential oil from L. gracilis had increased self-cleaning behavior and reduced allogrooming, possibly avoiding contact with other nest mates. Additionally, essential oil also caused less aggregation, which may be related to a possible repellent effect of essential oil on ants, resulting in repulsion between individuals. Although these behaviors reduce contact between ants, these results indicate the possibility of using essential oil from L. gracilis as a repellent for Solenopsis sp. Repellent action is a desirable effect to prevent the presence of ants in unwanted places [61]. In turn, carvacrol and its derivative carvacryl benzoate did not have changed self-cleaning and allogrooming behaviors in relation to the control, which may result in rapid horizontal contamination within the colony. This horizontal transfer is of great relevance for the management of ants [40,41], especially when the location of the anthill is difficult to access [62].
This horizontal transfer, associated with the high toxicity of carvacryl benzoate, had a negative effect on the insects, increasing the speed of death of recipient ants. This effect was even more intensified when there was a higher cadaver/healthy worker ratio. Thus, since carvacryl benzoate was more toxic and could result in a greater number of corpses inside the nest, this compound could result in a high horizontal transfer rate between workers of Solenopsis sp. In colonies of Solenopsis sp., the oldest workers are the most exposed to the action of insecticides, as they are close to the nest and the foraging areas [61]. The impact of contaminants on these ants can result in a lower ability of the colony to obtain food, with lower rates of recruitment and energy exchange among nestmates.
Sublethal effects can also interfere with foraging by altering the walking ability and orientation of Solenopsis sp. workers. Our results show that the normal activity of Solenopsis sp. involves slower walking and changes in movement direction (average angle the subject turned during the video) by distance covered (meander—°/s) and by time (angular velocity—°/s). This behavior is possibly related to the pattern of exploration of the environment in these ants.
Animals that exhibit greater changes in the direction of movement increase their chances of finding nearby resources, while fewer meanders and a low angular velocity may be related to the search for more distant resources [63]. The exposure of ants to carvacrol and carvacryl benzoate caused an increase in the distance covered and walking speed, as well as a reduction in the number of meanders and angular speed, likely making this behavior more directional. Some authors point out that the increase in walking speed could indicate an attempt to escape by ants in order to avoid the contaminant [37,64]. Future studies could evaluate how such compounds interfere with the way ants explore the environment and with their ability to acquire energy.
In conclusion, the results obtained in this work suggest an avoidance behavior of nest mates treated with the essential oil of L. gracilis and demonstrate the activity of carvacrol and especially its derivative carvacryl benzoate on mortality, behavioral changes and the spread of compounds among nest mates. Thus, our work demonstrates the potential of these compounds for the development of new products for the management of Solenopsis ants.

Author Contributions

Conceptualization, A.P.A.A., J.O.D. and L.B.; methodology, J.E.S., M.C.P. and L.B.; validation, L.B.; formal analysis, J.E.S. and L.B.; investigation, J.O.D., J.E.S., V.S.A. and T.B.B.; resources, S.C.H.C., A.F.B., M.C.P. and E.L.; data curation, J.O.D., V.S.A. and T.B.B.; writing—original draft preparation, J.O.D. and J.E.S.; writing—review and editing A.P.A.A. and L.B.; visualization, S.C.H.C., A.P.A.A., A.F.B. and M.C.P.; supervision, L.B.; project administration, L.B.; funding acquisition, S.C.H.C., A.F.B., M.C.P., E.L. and L.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brasil (CNPq), the Fundação de Apoio à Pesquisa e a Inovação Tecnológica do Estado de Sergipe (FAPITEC/SE)—Brasil, the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, the Financiadora de Estudos e Projetos—Brasil (FINEP), and INCT Semioquímicos na Agricultura, Processo 465511/2014-7.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data sharing is not applicable to this article.

Acknowledgments

The authors acknowledge Universidade Federal de Sergipe and funding sources for the financial support to publish this paper.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Synthetic derivatives of carvacrol [30].
Figure 1. Synthetic derivatives of carvacrol [30].
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Figure 2. Survival curves and lethal time (LT50) of Solenopsis sp. exposed to Lippia gracilis essential oil (green), carvacrol (yellow) (main oil compound) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol). Survival curves followed by the same letter do not differ significantly by the Holm–Sidak method (p > 0.05). Squares indicate the mean (±confidence interval to 95%) of the LT50 (lethal time required to kill 50% of the population).
Figure 2. Survival curves and lethal time (LT50) of Solenopsis sp. exposed to Lippia gracilis essential oil (green), carvacrol (yellow) (main oil compound) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol). Survival curves followed by the same letter do not differ significantly by the Holm–Sidak method (p > 0.05). Squares indicate the mean (±confidence interval to 95%) of the LT50 (lethal time required to kill 50% of the population).
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Figure 3. Individual cleaning (A) and collective cleaning and aggregation behavior (B) of Solenopsis sp. exposed to the LD30 of the essential oil of Lippia gracilis (green), carvacrol (yellow) (major compound in the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol). Means (±standard error) of the histograms followed by an asterisk differ from the control by Dunn’s test (p < 0.05).
Figure 3. Individual cleaning (A) and collective cleaning and aggregation behavior (B) of Solenopsis sp. exposed to the LD30 of the essential oil of Lippia gracilis (green), carvacrol (yellow) (major compound in the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol). Means (±standard error) of the histograms followed by an asterisk differ from the control by Dunn’s test (p < 0.05).
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Figure 4. Distance covered (mm) (A) and walking speed (mm/s) (B) of individual workers of the genus Solenopsis sp. exposed to the LD30 of Lippia gracilis essential oil (green), carvacrol (yellow) (major compound in the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol) for 600 s in 6 × 6 cm arenas. Histograms with means (± standard error) followed by an asterisk differ from the control by Dunn’s test (p < 0.05). The circles and the shaded area in the Radar plot represent the mean and standard error, respectively.
Figure 4. Distance covered (mm) (A) and walking speed (mm/s) (B) of individual workers of the genus Solenopsis sp. exposed to the LD30 of Lippia gracilis essential oil (green), carvacrol (yellow) (major compound in the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol) for 600 s in 6 × 6 cm arenas. Histograms with means (± standard error) followed by an asterisk differ from the control by Dunn’s test (p < 0.05). The circles and the shaded area in the Radar plot represent the mean and standard error, respectively.
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Figure 5. Meander behavior (o/mm), angular velocity (o/s) and 2D and 3D walking paths of workers of the genus Solenopsis sp. exposed to the LD30 of Lippia gracilis essential oil (green), carvacrol (yellow) (major compound in the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol) for 600 s in 6 × 6 cm arenas. Histograms with means (±standard error) followed by an asterisk differ from the control in a Dunn’s test (p < 0.05).
Figure 5. Meander behavior (o/mm), angular velocity (o/s) and 2D and 3D walking paths of workers of the genus Solenopsis sp. exposed to the LD30 of Lippia gracilis essential oil (green), carvacrol (yellow) (major compound in the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol) for 600 s in 6 × 6 cm arenas. Histograms with means (±standard error) followed by an asterisk differ from the control in a Dunn’s test (p < 0.05).
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Figure 6. Survival curves and lethal time (LT50) of Solenopsis sp. exposed to corpses of ants subjected to LD90 of Lippia gracilis essential oil (green), carvacrol (yellow) (major compound of the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol) in two proportions (cadaver: live workers). [1:20] = 1 corpse: 20 live workers and [1: 5] = 1 corpse: 5 live workers. Survival curves followed by the same letter do not differ significantly by the Holm–Sidak method (p > 0.05). Squares indicate the mean (confidence interval ± 95%) of the LT50 (lethal time required to kill 50% of the individuals).
Figure 6. Survival curves and lethal time (LT50) of Solenopsis sp. exposed to corpses of ants subjected to LD90 of Lippia gracilis essential oil (green), carvacrol (yellow) (major compound of the oil) and carvacryl benzoate (red) (most toxic synthetic derivative of carvacrol) in two proportions (cadaver: live workers). [1:20] = 1 corpse: 20 live workers and [1: 5] = 1 corpse: 5 live workers. Survival curves followed by the same letter do not differ significantly by the Holm–Sidak method (p > 0.05). Squares indicate the mean (confidence interval ± 95%) of the LT50 (lethal time required to kill 50% of the individuals).
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Table 1. Acute toxicity after 48 h of topical exposure to the essential oil of Lippia gracilis, its major compound carvacrol and nine synthetic derivatives of carvacrol on workers of the ant Solenopsis sp.
Table 1. Acute toxicity after 48 h of topical exposure to the essential oil of Lippia gracilis, its major compound carvacrol and nine synthetic derivatives of carvacrol on workers of the ant Solenopsis sp.
Compoundsn 1LD30
(CI 95%) 2		LD50
(CI 95%) 2		LD90
(CI 95%) 2		Slope
±SE 3		χ2p 4
μg/mg
Essential oil of Lippia gracilis3363.42
(2.66–4.14)		6.11
(5.16–7.20)		25.2
(19.0–38.3)		2.08
±0.23		7.410.12
Carvacrol3362.76
(1.81–3.75)		6.79
(5.19–8.71)		60.9
(39.2–118)		1.35
±0.16		0.760.94
Carvacryl acetate3924.09
(3.17–4.94)		6.92
(5.86–7.97)		24.9
(20.2–33.5)		2.30
±0.24		6.390.27
Carvacryl benzoate4482.21
(1.92–2.49)		3.20
(2.86–3.57)		7.97
(6.90–9.53)		3.24
±0.24		4.810.57
Carvacryl butyrate3923.73
(2.67–4.75)		7.50
(6.09–8.99)		41.2
(30.5–64.0)		1.73
±0.19		8.620.13
Carvacryl ethyl ether4483.81
(3.12–4.51)		6.87
(5.88–8.04)		29.1
(22.7–40.3)		2.05
±0.17		7.960.24
Carvacryl hexanoate3366.25
(5.02–7.39)		10.5
(8.99–12.2)		37.1
(28.9–53.3)		2.33
±0.25		6.460.17
Carvacryl isobutyrate3363.46
(2.45–4.40)		6.54
(5.28–7.84)		30.9
(23.3–47.4)		1.90
±0.22		3.540.47
Carvacryl isovalerate3926.16
(3.79–8.18)		10.8
(8.10–14.5)		42.3
(26.8–112)		2.16
±0.33		9.920.08
Carvacryl pivaloate3923.05
(2.41–3.70)		5.85
(4.88–7.03)		28.7
(21.4–43.0)		1.85
±0.17		6.800.24
Carvacryl trichloroacetate3364.05
(3.00–5.12)		7.92
(6.39–9.66)		40.7
(30.4–60.7)		1.80
±0.18		5.990.20
1 number of insects tested. 2 lethal doses required to kill 30, 50 and 90% of populations and their respective confidence intervals to 95%. 3 Slope ± standard error. 4 p-value (not significant).
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MDPI and ACS Style

Dantas, J.O.; Cavalcanti, S.C.H.; Araújo, A.P.A.; Blank, A.F.; Silva, J.E.; Picanço, M.C.; Lima, E.; Andrade, V.S.; Brito, T.B.; Bacci, L. Synthetic Carvacrol Derivatives for the Management of Solenopsis Ants: Toxicity, Sublethal Effects, and Horizontal Transfer. Agriculture 2023, 13, 1988. https://doi.org/10.3390/agriculture13101988

AMA Style

Dantas JO, Cavalcanti SCH, Araújo APA, Blank AF, Silva JE, Picanço MC, Lima E, Andrade VS, Brito TB, Bacci L. Synthetic Carvacrol Derivatives for the Management of Solenopsis Ants: Toxicity, Sublethal Effects, and Horizontal Transfer. Agriculture. 2023; 13(10):1988. https://doi.org/10.3390/agriculture13101988

Chicago/Turabian Style

Dantas, Jaciele O., Sócrates C. H. Cavalcanti, Ana Paula A. Araújo, Arie F. Blank, Jefferson E. Silva, Marcelo C. Picanço, Eraldo Lima, Valfran S. Andrade, Thaysnara B. Brito, and Leandro Bacci. 2023. "Synthetic Carvacrol Derivatives for the Management of Solenopsis Ants: Toxicity, Sublethal Effects, and Horizontal Transfer" Agriculture 13, no. 10: 1988. https://doi.org/10.3390/agriculture13101988

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