Aphid Cerosipha forbesi control using Piper macedoi Yunck essential oil in strawberry crop

Abstract Strawberry is a food rich in bioactive compounds with great antioxidant potential. However, due to the high incidence of pests that affect crop cultivation, phytosanitary management still lacks control methods for agroecological cultivation. Thus, the present research aimed to evaluate the chemical composition and the potential of the essential oil of the leaves of Piper macedoi in the control of Cerosipha forbesi in laboratory and semi-field conditions. The concentration of essential oil in the leaves of P. macedoi that showed the highest mortality was 2.0 ml/L of oil, with a mortality above 91% under laboratory conditions. A mortality rate of 80% for all concentrations tested was observed after 24 h in all conditions tested. Thus, using essential oil from the leaf of P. macedoi can be a highly viable strategy in managing the aphid C. forbesi since it showed high mortality rates with small doses of oil. Graphical Abstract


Introduction
Society's concern is growing about the consumption of healthy foods, such as vegetables and fruits, as well as conservationist and sustainable management practices throughout the production process in the field (nowicka et al. 2019).Strawberry is a food rich in bioactive compounds with excellent antioxidant potential (Zhang et al. 2008).However, due to the high incidence of pests that affect crop cultivation, phytosanitary management still has a scarcity of control methods for use in organic and agroecological cultivation.in addition, there is an intense use of chemical insecticides during production (Bernardi et al. 2013;Shahbazi 2018;Shahbazi et al. 2021).
aphids (Cerosipha forbesi) are considered highly harmful insects to the strawberry crop (Fragaria x ananassa duch), which reduce photosynthesis and fruit quality due to sap suction and dissemination of viruses in plants (Cédola and Greco 2010).aiming at lowering agricultural losses caused by insect pests, as well as the use of synthetic chemicals in the planting of strawberries.the secondary plant metabolites stand out as an alternative because they have important biological activities (Simões et al. 2007), highlighting, for example, the insecticidal activity already demonstrated by different essential oils of plants (dzenda et al. 2008;Belmain et al. 2012;Yakhlef et al. 2020).
in this scenario, plants of the genus Piper stand out, which have varied biological activities with one of the most versatile secondary metabolisms (de Lira pimentel et al. 2022).Piper macedoi Yunck belongs to this genus and is a plant with potential chemical compounds with insecticidal activity in the essential oil of its leaves.However, there still needs to be studied on its actions against insects.thus, it is crucial to develop knowledge about the secondary metabolites of plants, aiming at the selection of new potential insecticides for managing insect pests that cause less impact on the strawberry production chain.the present research aimed to evaluate the potential of the essential oil of P. macedoi leaves in controlling C. forbesi in laboratory and semi-field conditions.
the importance of knowing the chemical composition of essential oil is directly linked to the potential applications of its chemical compounds.For example, P. macedoi Yunck is a plant with potential bioactive compounds in the essential oil of its leaves, such as those presented as results of this research.However, few studies on its chemical composition reveal the importance of studying this plant.in this context, only one phytochemical investigation on the essential oil of the leaves of P. macedoi was found (oliveira et al. 2016), in which the chemical composition of the oil from the leaves of this species collected in patis city, north of minas Gerais in 2010 and identified as main compounds, both for wild plants and for cultivated plants, trans-Bocimene, and asaricin.these two compounds were not found in the present chemical analysis, and this is due to some parameters that, when varied, cause changes in the chemical composition of essential oil.these are related to the geographic location of the plant (mgbeahuruike et al. 2017), collection time, plant-environment interactions, abiotic and biotic factors (Simões et al. 2007;morais 2009;Kerebba et al. 2019).the variation of these factors can change the synthesis of secondary metabolites and consequently influence the final chemical composition of essential oil (morais 2009).
the chemical compounds found in the essential oil of P. macedoi leaves have several biological activities already described in the literature.the compound piperitone, the majority in this research, has insecticidal activity (Ketoh et al. 2006;drioueche et al. 2022).the linalool compound also has larvicidal activity (pereira et al. 2021).it is also noteworthy that the bicyclogermacrene has antimicrobial activity (Costantin et al. 2001;deuschle et al. 2007) and the α-pinene compound (Sumitomo et al. 2015).

Effects of essential oil from P. macedoi leaves on C. forbesi
Figures S1 and S2 express the mean mortality in percentage (%) obtained by nn measured as a function of concentrations (mL/L).the dotted line is the mean of the prediction, and the blue shade is the regression's uncertainty (standard deviation), both obtained by the pG method.Regression of data obtained in semi-field after four h and 24h resulted in correlation coefficients (R 2 ) equal to 0.95 and 1.0, respectively.in the laboratory results, regressions for data obtained after 24 h and after 48 h showed R 2 values equal to 0.96 and 0.73, respectively.Figure S1 presents the regression plots using the pG method, as described in the statistical details. after 24 h, the statistics showed that LC 90 = 1.48 mL/L, as seen in Figure S1a.on the other hand, after 48 h, the mortality rate was consistently above 90% for all concentrations evaluated.
in estimating the lethal concentration (LC 50 and LC 90 ) of the essential oil tested, the data were adapted to the probit model, providing pearson's Chi-square values, p-value, degree of freedom, and confidence intervals at 95% probability.For tests with P. macedoi leaf essential oil, LC 50 (Ci 95 ) of 0.0632 mL/L (8.1734 × 10 −6 ; 1.8289 × 10 −1 ) and LC 90 (Ci 95 ) of 3.5751 mL/L were presented.(1.3889; 8.3275 × 10 +3 ). the visualization of the LC 50 and LC 90 results of essential oils is presented in table S2.Regression plots using the pG method for measurements after four h and 24h are shown in Figures S1a and S2a, respectively.Regression and statistics details can be obtained in the 'statistical details' section.We observed that after four h, the statistics showed that LC 50 = 1.03 mL/L, as seen in Figure S2a.However, it was not possible after 4 h to observe LC 90 .For observations after 48 h, we obtained LC 50 = 0.1 mL/L and LC 90 = 1.15 mL/L.the insecticidal activity in P. macedo essential oils is due to all its constituents, mainly the major components.When passing through the respiratory tract, quickly interfering with physiological functions, or acting as acetylcholinesterase inhibitors, they generate synaptic collapse and lead to the insect's death (Shaaya and Rafaeli 2007;Hashem et al. 2018;pereira Filho et al. 2021).piperitone was responsible for 27.6% of the relative composition of the oil.Studies confirm the insecticidal activity of this constituent, stating that piperitone affects the functions of the central nervous system, promoting rapid paralysis in the insect, also presenting low toxicity to mammals and rapid degradation in the environment (Ketoh et al. 2006;drioueche et al. 2022).the other major compounds, such as sylvane, bicyclogermacrene, germacrene-d, and nerolidol, were not found in studies relating to their insecticidal action and respective mechanisms of action.
the site of action of essential oils is the octopaminergic, acting on octopamine, an excitatory neurotransmitter associated with the median dorsal neuron.its toxicity is due to the action on this site, which stimulates or inhibits octopamine (dos Santos et al. 2021).When the functioning of octopamine is disrupted, a disruption in the functioning of the insect's nervous system occurs.However, this neurotransmitter is present only in invertebrates, which makes essential oils safe for mammals, thus making the use of insecticides based on essential oils less toxic for humans, in addition to suggesting selectivity to non-target invertebrates, natural enemies (ayvaz et al. 2010;Ríos et al. 2017;pavela and Sedlák 2018).

Conclusion
Small concentrations of essential oil from the leaves of P. macedoi show high percentages of mortality of C. forbesi aphids, indicating a surprising insecticidal potential of this oil.the concentration of essential oil from the leaves of P. macedoi that showed the highest mortality was 2.0 ml/L of oil, with a mortality above 91% under laboratory conditions (in vitro).For all concentrations tested, a mortality rate of 80% was observed after 24 h, and the neurotoxic action of the oil on the insect had a rapid effect.the lethal concentration estimated to cause mortality in 50% of individuals was 0.0632 mL/L and for mortality in 90% of individuals, it was around 3.5751 mL/L under semi-field conditions.thus, using essential oil from the leaf of P. macedoi can be a highly viable strategy in managing C. forbesi aphids since it presented high mortality rates with small doses of oil, evidencing its viability.

Disclosure statement
no potential conflict of interest was reported by the authors.

Funding
the author(s) reported there is no funding associated with the work featured in this article.