Introduction
The need for greater agricultural productivity and vector eradication demand initially led to the use of synthetic pesticides, which are only sometimes used below the limit concentrations allowed by related legislation (Nicopoulou-Stamati, Maipas, Kotampasi, Stamatis, & Hens, 2016). Many of these pesticides are organophosphates, which cause residual effects to the environment and adverse effects on human and animal health, such as methylparathion, phorate, and dimethoate (Edwards & Tchounou, 2005; Montana et al., 2021; Scoy, Pennell, & Zhang, 2016). Furthermore, other synthetic pesticides such as carbamates, triazines, pyrethroids, and neonicotinoids can also impact health and the environment (Nicopoulou-Stamati et al., 2016). As well as the organophosphates, carbamates are also acetylcholinesterase inhibitors and are related to neurotoxic events, besides also acting as disrupters of the endocrine/reproductive system (Jamal, Haque, Singh, & Rastogi, 2016; Mnif et al., 2011). This effect is also observed with pyrethroids, whereas triazines can induce breast cancer and endocrine-disrupting effects (Kettles, Browning, Prince, & Horstman, 1997; Mnif et al., 2011). In turn, neonicotinoids are considered safer for animals. However, a recent study demonstrated that this pesticide class increases the expression of the enzyme aromatase, which is related to breast cancer and also plays a vital role during developmental stages (Caron-Beaudoin, Denison, & Sanderson, 2016).
Thus, the search for new alternatives in the control of pests of agricultural and health importance has been encouraged so that new methodologies or products can be more sustainable to the environment and less harmful to human and animal health (Nicopoulou-Stamati et al., 2016). The use of organic products as pest controllers, such as essential oils (EOs), has been heavily explored as biological controllers of plant predators and disease transmitters. These products have advantages such as greater selectivity of target organisms and rapid biodegradability, which causes less intense residual effects compared to synthetics, in addition to being less susceptible to the emergence of resistance by pests (Smith & Perfetti, 2020). Particularly, EOs have constituents from the class of monoterpenes, sesquiterpenes, phenylpropanoids, among others, which have insecticidal or biological control activity and are involved in plant defense against predators, having toxic, repellent or hormonal action on target organisms (Ding-Feng, 2010).
Brazil has an important source of plant resources due to its high biodiversity spread over a territory of more than 8 million km2, which includes six different biomes. Among these biomes is the Atlantic Forest, which has part of its vegetation as a sandbank along the Brazilian coast and has an important preservation unit in Carapebus city, named Restinga de Jurubatiba National Park (Araújo, 1992).
Table 1
Essential oils from Carapebus sandbank plants and affected pests
The species from this locality are still little studied in terms of chemical and pharmacological activity. Those studied have shown interesting activities, considering that the sandbank species are important from the pharmacological point of view, as they produce many secondary metabolites, including EOs (Santos, Fevereiro, Reis, & Barcelos, 2009; Silva, Melo, & Matilde-Silva, 2022).
Among the countries with the highest agricultural production in the world, Brazil produces tons of food of plant origin and a large number of consumers, with a population of over 210 million inhabitants and is one of the main crop producers in the world, providing food for 800 million people around the world (Contini & Aragão, 2020). However, the wide use of pesticides is still a constant reality in Brazilian agribusiness, which often leads to the supply of food that exceeds the safety limits for consumers' health (Disner et al., 2021). On the other hand, Brazil is affected by several tropical diseases, with important transmission vectors such as Aedes aegypti, the transmitter of at least five diseases, including dengue Zika, Chikungunya, Mayaro fever, and yellow fever, so their biological control is important in urban or quickly propagated areas (Clancy et al., 2021). Thus, this review aims to compile and discuss the recent studies carried out with EOs from Carapebus sandbanks species with activity against the main pests that affect the Brazilian territory.
Methodology
The research was carried out using the combination of the name of Carapebus sandbanks species described in the study ofSantos et al. (2009) and the recently described species "Pilocarpus spicatus" and "Zanthoxylum caribaeum" together with the words "essential oil", "insecticidal" and/or "larvicidal" and "activity". Google Scholar and Scopus were used as the research databases. Table 1 summarizes the studies described below.
Pests and vectors affected by essential oils from Carapebus sandbanks
Aedes aegypti
The insecticidal activity against the mosquito A. aegypti was evaluated by several EOs of species from Carapebus sandbanks, among them from the Annonaceae family Annona acutiflora and Xylopia ochrantha. The nanoemulsionated EO from A. acutiflora leaves showed LC50 and LC90 values after 48 h, respectively, of 21.3 and 37.1 ppm against the 3rd instar larvae of A. aegypti. α-santalene (15.5 %), bicyclogermacrene (12.5 %), and α-zingiberene (8.7 %) were the major compounds of the oil (Folly et al., 2021). The EO from X. ochrantha leaves presented a low activity with LC50 and LC90 equal to 217,685 ppm and 459,716 ppm within 48 hours, respectively. The main substances of the oil were bicyclogermacrene (25.2 %) and germacrene D (20.9 %) (Viana et al., 2022). For the EO extracted from the resin of Protium heptaphyllum, the larvicidal action showed a potent LC50 equal to 2.91 and 0.17 ppm in 24 and 48 h, respectively. p-cymene (27.70 %) and α-pinene (22.31 %) were the main constituents of the EO (Faustino et al., 2020). In turn, the nanoemulsioned EO from Ocotea indecora leaves presented LC50 values against A. aegypti larvae equal to 61.4 ppm after 48 h. Interestingly, sesquirosefuran was the major compound, presenting 81.4 % of EO composition (Machado et al., 2023). Furthermore, EOs from E. punicifolia leaves collected from two different regions of Brazil (Goiás and Minas Gerais) presented different levels of action on A. aegypti L3 larvae (LC50 = 85.53 μg/mL and 91.52 μg/mL, respectively), besides their main chemical compounds (Bicyclogermacrene (26.73 %), Germacrene D (21.34 %) and β-longipenene (9.42 %) in Goiás and Spathulenol (26.84 %), (Z)-caryophyllene (8.92 %), α-cadinol (6.28 %), γ-cadinene (6.27 %), and caryophyllene oxide (6.02 %) in Minas Gerais) (Silva et al., 2021).
Culex quinquefasciatus
The EO from Eugenia uniflora leaves was active against C. quinquefasciatus, one of the filariasis's main vectors, so it transmits parasites as Wuchereria bancrofti and Brugia malayi, which in turn are the etiological agents of the disease. The EOs had LC50 values between 31.52 and 60.08 mg/L, considered effective against larvae. Curzerene (24.13 %), E-β-ocimene (11.64 %), germacrene B (9.60 %) and germacrone (8.09 %) were the principal constituents of the oil (Oliveira et al., 2022).
Diaphania hyalinata
The leaves EO from E. uniflora was also active against D. hyalinata, an important plant predator, presenting robust oviposition deterrence (2.98 %) and strong repellence against larvae (15.84 % caterpillars). In this assay, Selina-1,3,7(11)-trien8-one (25.42 %), Selina-1,3,7(11)-trien8-one epoxide (15.49 %), and germacrone (11.05 %) were the main compounds of the oil (Lobo, Camara, Melo, & Moraes, 2019).
Dysdercus peruvianus
The nanoemulsion containing the EO from O. indecora was active on D. peruvianus adult, a Hemiptera cotton pest, presenting a LD50 equal to 162.18 μg/insect, with a sesquirosefuran oil concentration of 92 % (Nascimento et al., 2020). The leaves EO from the species Myrciaria floribunda was also effective against this pest with LC50 values (µg/insect) equal to 309.64 after one day of treatment, and 94.42 after 22 days of treatment. 1,8-cineole (38.4 %) was the main compound of the oil (Tietbohl et al., 2014). Moreover, the oil from Zanthoxylum caribaeum leaves is rich in sylvestrene (11.3 %), muurola-4 (14), 5-trans-diene (8.4 %), isodaucene (8.3 %) and α-pinene (7.6 %) showed a LC50 equal to 215 µg/insect, besides it interrupted insect metamorphosis and molting, often in a dose-dependent manner. In addition, nymphs with deformed legs, wings and antennae were observed (Pacheco et al., 2020).
Oncopeltus fasciatus
The leaves EO from Myrciaria floribunda demonstrated insecticidal activity against O. fasciatus, a milkweed bug. The LD50 values (µg/insect) were equal to 112.44 after one day of treatment and 72.18 after 22 days of treatment (Tietbohl et al., 2014).
Rhipicephalus microplus
R. microplus, a tickle that affects cattle productivity, is one of the most evaluated pests for insecticidal activity of sandbank plants. In this context, the EO from Cordia curassavica exhibited a larvicidal effect (59.0 % at 25.0 mg/mL) and insecticidal action against engorged females (96.9 % at 25.0 mg/mL). α-pinene (49. 0 %) and β-caryophyllene (12.4 %) were the major compounds of the oil (Carvalho-Castro et al., 2019). Ocotea notata was another plant with activity against this pest. The oil from leaves reduced the survival by 90% after incubation for 15 days, and there was 100% reduction in posture inhibition and reproductive capacity. Trans-muurola-4(14),5-diene (15.61 %) and bicyclogermacrene (12.69 %) were the main substances in this study (Moussavou et al., 2019). As observed with D. peruvianus, the oil from the species O. indecora also presented insecticidal activity against R. microplus. The adult immersion test detected efficacy higher than 90% from the concentration 25 mg/mL upward. In larval-packed tests performed after 48 h, only the 100 mg/mL concentration resulted in mortalities above 70%. On the other hand, the EO caused an average of 95.8% repellency from 0.78 to 100 mg/mL. The LC50 for the larval packed tests (24 and 48 h) were 59.68 and 25.59 mg/mL, respectively, whereas LC50 and LC90 for the immersion test showed 4.96 and 17.37 mg/mL, and in the repellence test, they presented 0.04 and 1.24 mg/mL, respectively (Figueiredo et al., 2018). Furthermore, the EO from Pilocarpus spicatus leaves showed 98.10 % repellency against the larvae, when used a concentration equal to 50 mg/mL, after 10 hours. Limonene (46.8 %) was the principal compound of this oil (Nogueira et al., 2020). The EO from Z. caribaeum leaves also demonstrated effect against R. microplus, so that 5% concentration caused 65% mortality on the 1st day after treatment, 85% on the 2nd day, and 100% on the 5thday (Nogueira et al., 2014).
Rhodnius prolixus
The EO from M. floribunda leaves demonstrated insecticidal activity against the 5th instar of R. prolixus, an important Triatomine species that transmits Trypanosoma cruzi, the etiological agent of Chagas Disease, presenting an LD50 equal to 742.29 µg/insect, with 24h after the treatment. Interestingly, the oil showed more activity when compared with its major compound, 1,8-cineol (10.4 %), which suggests the synergism effect, taking into count other relevant compounds such as β-selinene (8.4 %), (E)-nerolidol (5.5 %) and β-curcumene (5.2 %). Moreover, disruption of metamorphosis on averaged nymphs and juvenoid-like insects was also observed (Tietbohl et al., 2020). High levels of toxicity and paralysis, together with discrete molting inhibition, were caused by topical application of either 0.5 µL or 1.0 µL per insect of the EO from P. spicatus on nymphae. The mortality rate was 90.5 and 91.1% in 24 hours. Partial fagoinhibition, high molting inhibition, prolonged intermolting period, and a high number of paralyzed insects were observed with oral treatment (5-10 µL oil per ingested blood meal) (Mello et al., 2007). Furthermore, topical treatment with the crude EO of Z. caribaeum induced high levels of paralysis (from 18.88 to 33.33 %) and mortality (from 80 to 98.9 %) of nymphae, depending on the dose applied (0.5 to 5.0 μL/insect). Feeding treatment with the crude EO also induced high levels of mortality (from 48.8 to 100 %), but low levels of paralysis (from 2.22 to 7.77 %), depending on the dose applied (0.5 - 5.0 μL/mL of blood). Sylvestrene (11.3 %), muurola-4,5-trans-diene (8.4 %), isodaucene (8.3 %), and α-pinene (7.6 %) were the major constituents of the oil (Nogueira et al., 2014).
Discussion
Recent studies with EOs from plants present in the Carapebus sandbank are promising in terms of insecticidal and larvicidal activity, taking into account that EOs are more biodegradable products and, therefore, have less impact on the environment, in addition to being, in general, less toxic to human and animal health (Samada & Tambunam, 2020). Another advantage is the lower rate of emergence of resistance by pests due to the greater chemical diversity presented by natural products (Ding-Feng, 2010). Some EOs have even been studied in nanoemulsion form, which facilitates the dispersion of these substances in the aquatic environment, in addition to promoting greater bioavailability of the active ingredients (Jaiswal, Dudhe, & Sharma, 2015). The EOs studied for the insecticide/larvicide evaluations showed mainly hydrocarbon sesquiterpenes and, in second place, monoterpenes among the groups of major substances. Monoterpenes, for example, p-cimene and α-pinene, can disrupt the cellular membrane function due its low polarity characteristic, which disaggregates the lipid structure that makes up the inner layer of the membrane (Salakhutdinov, Volcho, & Yarovaya, 2017). The effect on insects also includes the fact that they have greater ease of penetration into the respiratory system of target organisms (Langsi et al., 2020). In addition, it is already described in the literature that the monoterpenoid 1,8-cineole, major compound of Myrciaria floribunda EO, inhibit the acetylcholinesterase activity from insects (Abdelgaleil, Mohamed, Badawy, & El-Arami, 2009). Limonene, the main substance of Pilocarpus spicatus oil, also demonstrated an inhibition effect on ovoposition and egg hatching of insects, besides causing repellency and toxicity (Karr & Coats, 1988). In turn, some EOs rich in sesquiterpenoids showed greater activity, as with Annona acutiflora and Eugenia punicifolia against Aedes aegypti, and Eugenia uniflora against Culex quinquefasciatus. The first two presented the bicyclogermacrene as the majority, which has already demonstrated intense insecticidal activity against the genus Anopheles, Aedes, and Culex (Govindarajan & Benelli, 2016). On the other side, interesting structures such as curzerene (present in Eugenia uniflora against C. quinquefasciatus), a furanogermacrenoid, and sesquirosefuran, a furanosesquiterpene present in Lauraceae species, also appeared as majorities in oils with higher activity. Curzerene has already proven to be effective against mosquitoes of the Anopheles, Aedes, and Culex genus (Govindarajan et al., 2018), while sesquirosefuran is described as a semiochemical (Petroski, Tellez, & Behle, 2005). Furthermore, it also presents termiticidal properties (Ozaki, 1999). In this way, these EOs, in addition to presenting an interesting potential to be used as organic insecticides, also contribute to the valorization of native species, which includes taking measures to preserve these species and maintain local biodiversity. Among the most promising EOs, P. heptaphyllum can be mentioned, with high potency against A. aegypti, while O. indecora proved to be quite efficient against R. microplus, presenting a lower LC50 value than against A. aegypti, which demonstrates selectivity of the oil. However, studies that aim to elucidate the mechanisms involved in insecticide and larvicide tests should be carried out for a better understanding of how EOs act and whether there is influence of synergism between the components. In addition, field trials must be carried out with the most promising oils, so that the real applicability is measured.
Conclusion
This review demonstrates the importance of EOs from native species located in the sandbanks of the municipality of Carapebus as an alternative in the fight against agricultural pests and disease transmitters that affect the Brazilian territory, thus being a possible biosustainable resource, in addition to contributing to the preservation of local species. Taking into account the efficiency of the EOs described in this review, the oils from P. heptaphyllum and O. indecora proved to be promising resources against A. aegypti and R. microplus, respectively. However, further studies on field efficiency and pharmacological mechanism should be conducted to obtain more relevant information on the use of these resources and a better understanding of their actions against the mentioned pests.
