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. 2023 Sep 2;13(10):328. doi: 10.1007/s13205-023-03757-y

Water stress and exogenous carnitine on growth and essential oil profile of Eryngium foetidum L.

Sabrina Kelly dos Santos 1, Daniel da Silva Gomes 1, Ana Flávia Pellegrini de Oliveira 2, Agnne Mayara Oliveira Silva 3, Vitória Stefany de Moura 3, Moises Henrique Almeida Gusmão 4, Elyabe Monteiro de Matos 4, Lyderson Facio Viccini 4, Richard Michael Grazul 2, Juliane Maciel Henschel 1, Diego Silva Batista 1,3,✉
PMCID: PMC10475002  PMID: 37667775

Abstract

Water stress influences plant growth and metabolism. Carnitine, an amino acid involved in lipid metabolism, has been related to responses of plants to abiotic stresses, also modulating their metabolites. Culantro (Eryngium foetidum L.) is a perennial herb, rich in essential oils, native to Latin America, commonly used due to its culinary and medicinal properties. Here, we investigated the effect of exogenous carnitine on morphophysiology and the essential oil profile of culantro plants under water stress. For this, plants were grown under three water conditions: well-watered, drought stress, and re-watered; and sprayed with exogenous carnitine (100 µM) or water (control). Culantro growth was impaired by drought and enhanced by re-watering. Carnitine, in turn, did not reverse drought effects on growth, and impaired the growth of re-watered plants, also improving photosynthetic pigment content. Water conditions and carnitine application changed the essential oil profile of the plants. Drought and re-watering improved the production of eryngial, which was even increased with exogenous carnitine in re-watered plants. In addition, hydroquinone was only produced with the combination of re-watering and carnitine application. The application of exogenous carnitine can be a strategy to induce the production of essential oil compounds with cosmetic and pharmaceutical importance in culantro.

Supplementary Information

The online version contains supplementary material available at 10.1007/s13205-023-03757-y.

Keywords: Culantro, Drought stress, Medicinal plants, Re-watering, Secondary metabolites profile, Sesquiterpenes

Introduction

Water stress is a main environmental factor affecting the morphophysiology and production of plants (Liang et al. 2019; Soares et al. 2022). Thus, plants have strategies to prevent water loss in order to maintain optimal water balance, such as stomatal closure, osmoregulation, reactive oxygen species (ROS) scavenging, and production of secondary metabolites (Gupta et al. 2020), the latter are organic molecules produced by plants, classified into alkaloids, phenolics, and terpenoids (Takshak and Agrawal 2019). These compounds act as chemical regulators and messengers in plants, playing a fundamental role in fertilization, defense against pathogens and herbivores, and tolerance to abiotic stresses (Böttger et al. 2018). Due to their aromatic and therapeutic properties, they are used for dyes, medicines, artificial flavoring products, nutraceuticals, perfumes, among others (Wink 2015; Kulak et al. 2019).

Culantro (Eryngium foetidum L.) belongs to the Apiaceae family and is a perennial herb native to Central America, with autogamous characteristics and propagation mainly through seeds (Singh et al. 2014; Rodrigues et al. 2022). This species is commonly used in folk medicine to treat burns, earaches, fever, hypertension, constipation, asthma, stomach pain, worms, diarrhea, rheumatism, cramps, and to stimulate appetite (Shavandi et al. 2012; Singh et al. 2013; Rodrigues et al. 2022). Culantro is widely used as a flavoring condiment in foods, having great relevance for the Amazonian food culture (Rodrigues et al. 2022), also having impact on human health, inhibiting the growth of pathogenic bacteria, such as Helicobacter pylori, showing anti-leishmanial activity against Leishmania tarentolae and L. donovani, and being effective against trypanosomes, nematodes, and fungi (Paul et al. 2010; Jaramillo et al. 2011; Rojas-Silva et al. 2014; Mabeku et al 2016). Furthermore, culantro is rich in essential oils stored on its secretory ducts (Bhavana et al. 2013; Rodrigues et al. 2020, 2022), with a characteristic flavor and aroma due an aliphatic aldehyde called eryngial ((E)-2-dodecenal), which is present mostly on the leaves (Quynh and Kubota 2012; Rodrigues et al. 2020).

Mitigation strategies can be used to attenuate water stress in plants (Sai et al. 2016). The application of bioregulators, such as amino acids like proline (Ami et al. 2020; Santos et al 2022a), arginine (Nargesi et al. 2022), and carnitine (Charrier et al. 2012; Turk et al. 2019a, b; Santos et al. 2022b), has been studied. Carnitine is a quaternary ammonium compound involved in metabolic functions like energy metabolism and stress tolerance (Charrier et al. 2012). This amino acid participates in the degradation of triglycerides to fatty acids and their transportation into mitochondria, stimulating respiration, being essential for energy storage, cell structure, and signal transduction (Bourdin et al. 2007; Frank et al. 2015; Oney-Birol 2019; Turk et al. 2019a, b). In addition, exogenous carnitine has been pointed as a bioregulator, modulating plant growth under non-stressful conditions (Charrier et al. 2012; Santos et al. 2022c) and mitigating moderate water stress in plant species, such as arugula (Santos et al. 2022b) and radish (Henschel et al. 2023). This way, the objective of this study was to evaluate the action of carnitine on growth, morphophysiology and the essential oil profile of culantro plants under water stress.

Materials and methods

Experimental location and plant material

The experiment was conducted between January and May 2022, in a greenhouse covered with transparent film, located in the experimental area of the Seedling Production Laboratory of the Center for Human, Social and Agrarian Sciences/Federal University of Paraiba (CCHSA/UFPB), in Bananeiras, Paraiba, Brazil (6° 45ʹ S, 35° 38ʹ W, elevation of 526 m). Culantro seeds (E. foetidum) were, donated by growers from local rural communities in the municipality of Areia, Paraíba, Brazil (6° 57ʹ S, 35° 41ʹ W, elevation of 623 m).

Irrigation and bioregulators treatments

The culantro seeds were sown in trays containing 200 cells. At 35 days after sowing (DAS), when plants presented four fully expanded leaves, they were transplanted to polyethylene bags (22 × 28 cm) containing commercial substrate (Mecplant®, Telêmaco Borba, Brazil). The bags were irrigated until 100% bag capacity (BC) for fifteen days. 50 DAS, the plants were subjected to the treatments: well-watered (80% BC), drought (40% BC), and re-watered (12 days without irrigation with subsequent irrigation with 80% BC, with the application of water (control) or 100 µM carnitine (l-carnitine, Growth Supplements, Tijucas, Brazil) (Santos et al. 2022c), using hand sprayers every 6 days (50, 56, 62, 68, 74, 80, 86, 92, and 98 DAS). The duration of water restriction of 12 days was established based on previous survival tests. Carnitine solution was dissolved in distilled water with addition of the surfactant polysorbate 80 (Tween-80®, 0.03%) (v/v) to increase adhesion to the leaves.

Morphophysiological analysis

At 100 DAS, photosynthetic pigments content, gas exchange parameters, and chlorophyll a fluorescence were measured, and 102 DAS growth parameters were measured. The leaf area, number of leaves, specific leaf area, and root length were determined through image analysis using the software ImageJ (Abramoff et al. 2004). Five plants were collected and separated into shoots and roots using a scalpel and weighed for the determination of the fresh mass. After morphologic measurements, shoots and roots of culantro plants were oven-dried at 65 °C until a constant weight to determine their dry weight. The shoot/root ratio was determined as the dry weight of shoots divided by the dry weight of roots. The total biomass was determined as the sum of dry weight of shoots and roots.

Gas exchange measurements were performed using an open-flow gas exchange system infrared gas analyzer (IRGA, LCpro-SD Portable Photosynthesis System, ADC BioScientific, Hoddesdon, UK). The analyses were made on fully expanded leaves of five plants per treatment between 8 and 11 h a.m. The conditions in the leaf chamber consisted of an ambient temperature and reference CO2 and artificial photosynthetically active radiation of 1000 μmol m−2 s−1 with 10% blue light. The net carbon assimilation rate (A, µmol CO2 m−2 s−1), stomatal conductance (gS, mol H2O m−2 s−1), internal CO2 concentration (Ci, mmol CO2 mol−1 air) and leaf transpiration rate (E, mmol H2O m−2 s−1), and water use efficiency (A/E), carboxylation efficiency (A/Ci) were determined. Light response curves of photosynthesis were studied by varying photosynthetic photon flux density (PPFD) from 0 to 1800 mol m−2 s−1. Light response curve measurements were made on fully expanded leaves of three plants per treatment between 8 and 11 h a.m. From light response curves, were calculated the following parameters: dark respiration (Rdark) (µmol m−2 s−1), apparent quantum yield (mol/mol), light compensation point (LCP) (µmol m−2 s−1), maximum gross assimilation rate (Amax) (µmol m−2 s−1), and light saturation point (LSP) (µmol m−2 s−1).

Levels of photosynthetic pigments were determined according to Santos et al. (2008), with modifications, following the equation of Wellburn (1994). For this, four disks (1 cm2) from fully expanded leaves of four plants per treatment were incubated for 48 h in dark conditions with 7 mL dimethyl sulfoxide (Santos et al. 2008). Then, the extract was read at 480, 649, and 665 nm using a spectrophotometer (GTA-96 UV–Vis, Global Trade Technology, São Paulo, Brazil). The levels of chlorophyll a, chlorophyll b, chlorophyll a/b ratio, total chlorophylls, and total carotenoids were determined.

The relative water content (RWC) was determined according to Barrs and Weatherley (1962), with modifications. Ten leaf disks (1 cm2) were collected from fully expanded leaves of five plants per treatment and immediately weighed (fresh mass, FM). The disks were incubated for 6 h in distilled water, weighed for turgid mass (TM), and oven-dried at 65 °C for 24 h for dry mass (DM) determination. RWC was calculated as [(FM-DM)/(TM-DM)] × 100, and expressed as a percentage (%).

Microextraction of essential oils

Approximately 500 mg of leaves were collected and stored at − 18 °C in test tubes with a screw cap, following Castro et al. (2020), with modifications. After freezing, 1 mL methanol was added to each sample. To accelerate the extraction process, samples were immersed in an ultrasonic bath (Ultra Cleaner 800, UNIQUE) at 40 kHz and room temperature for 10 min. Subsequently, the supernatant was filtered through a sterile cotton wick. Resulting samples of 1 μL clear solution containing the extracted oils were analyzed by gas chromatography.

Qualitative analysis of essential oils

Qualitative analysis of essential oils was carried out on a gas chromatographer coupled to a mass spectrometer (GCMS-QP2010 Plus; Shimadzu, Kyoto, Japan) and an Rtx-5MS® column (Restek, Bellefonte, PA, USA) of 30 m × 0.25 mm, with three technical replicates. The initial oven temperature was 50 °C, where it was maintained for 3 min, followed by an increase of 6 °C min−1 to 240 °C. The injector was operated in split mode (1:10) at 240 °C, and the interface and mass detector were operated at 250 °C.

Helium was used as the carrier gas, with a flow of 1.69 mL min−1. The constituents were identified by comparing the obtained mass spectra with those of the NIST 9.0 database (correlation > 95%) and confirmed by the corresponding retention index (Kováts Index) compared to published data.

Experimental design and statistical analysis

The experiment was in a completely randomized design, in a 2 × 3 factorial scheme (carnitine application × water condition) with two simultaneously repetitions, ten replicates for each combination of water level and carnitine treatment, and the experimental unit composed by one bag with one plant each. For all the analyses, sampling was done through a draw to ensure randomization. The model used for the analysis of variance was: Yijk = μ + Wi + Cj + (WC) ij + Eijk; where: Yijk = are the observations of the dependent variables, μ = the overall mean effect, Wi = effect of the level ith of water factor, Cj = effect of the level ith of carnitine factor, (WC) ij = effect of the interaction ijth water level × carnitine, and Eijk = random error component. The data were tested for normality and homogeneity using the Shapiro–Wilk and Bartlett tests, respectively, subjected to analysis of variance, and the means compared by Tukey’s test (P ≤ 0.05) using the Genes software (Cruz 2016).

Volatiles profile data were submitted to multivariate analysis. The distance between the treatments was determined using canonical discriminant analysis in a three-dimensional scatter plot. The treatments were separated into different groups using the Tocher optimization method and generalized squared interpoint distance of Mahalanobis (D2). The grouping quality was evaluated using the co-optical correlation coefficient (r). The relative contribution of each variable to discriminate treatments was quantified using Singh (1981) criterion.

Results

Drought and exogenous carnitine modulate morphophysiology of culantro plants

Water levels and carnitine application affected most morphophysiological parameters (Online Resource 1, Supplementary Table 1), with drought stress affecting overall plant growth (Fig. 1a). Re-watered plants doubled leaf dry and fresh mass, root dry and fresh mass, and total biomass compared to well-watered plants (Fig. 1b–f). Carnitine application increased the shoot/root ratio of re-watered compared to well-watered and drought plants. Similarly, in control plants, the highest shoot/root ratio occurred upon re-watering (Fig. 1g).

Fig. 1.

Fig. 1

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Growth of 102-day-old Eryngium foetidum L. plants sprayed with water or carnitine, and grown under different water conditions. Representative plants of each condition (a); Leaf fresh mass (b); Leaf dry mass (c); Root fresh mass (d); Root dry mass (e); Total biomass (f); and Shoot/root ratio (g). Columns represent the mean of five replicates, and bars represent the standard error. Means followed by the same letter do not differ by Tukey’s test (P ≤ 0.05). Capital letters compare water conditions within carnitine levels, and lowercase letters compare between carnitine and control within each water condition

Drought increased root length and decreased the leaf area and number of leaves compared to the well-watered and re-watered plants (Fig. 2a–c). Re-watered treatment doubled the number of leaves and leaf area compared to well-watered treatment; however, these increases were reversed by carnitine application. There was no difference among treatments for specific leaf area (Fig. 2d).

Fig. 2.

Fig. 2

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Growth parameters of 102-day-old Eryngium foetidum L. plants sprayed with water or carnitine, and grown under different water conditions. Root length (a); number of leaves (b); leaf area (c); and specific leaf area (d). Columns represent the mean of five replicates, and bars represent the standard error. Means followed by the same letter do not differ by Tukey’s test (P ≤ 0.05). Capital letters compare water conditions within carnitine levels, and lowercase letters compare between carnitine and control within each water condition

The application of carnitine increased the content of chlorophyll a, total chlorophylls, and total carotenoid in the well-watered plants, and chlorophyll a and total carotenoids in re-watered plants. In contrast, carnitine reduced chlorophyll a in drought stressed plants compared to the control (Fig. 3a–d).

Fig. 3.

Fig. 3

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Contents of photosynthetic pigments of 100-day-old Eryngium foetidum L. plants sprayed with water or carnitine, and grown under different water conditions. Chlorophyll a (a); Chlorophyll b (b); Total chlorophylls (c); and total carotenoids (d). Columns represent the mean of four replicates, and bars represent the standard error. Means followed by the same letter do not differ by Tukey’s test (P ≤ 0.05). Capital letters compare water conditions within carnitine levels, and lowercase letters compare between carnitine and control within each water condition

There was no difference among the treatments for carbon assimilation rate, stomatal conductance, internal CO2 concentration, and carboxylation efficiency (Fig. 4a–d). Carnitine application increased respiration in the dark in re-watered treatment, but not in well-watered and drought (Fig. 4e). Similarly, carnitine increased the LCP in re-watered and drought, but not in well-watered plants (Fig. 4f).

Fig. 4.

Fig. 4

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Gas exchange parameters of 100-day-old Eryngium foetidum L. plants sprayed with water or carnitine, and grown under different water conditions. A, net carbon assimilation rate (a); gs, stomatal conductance (b); E, evapotranspiration rate (c); A/E, water use efficiency (d); Ci, internal CO2 concentration (e); A/Ci, carboxylation efficiency (f); Rdark, dark respiration (g); and LCP, light compensation point (h). Columns represent the mean of four replicates, and bars represent the standard error. Means followed by the same letter do not differ by Tukey’s test (P ≤ 0.05). Capital letters compare water conditions within carnitine levels, and lowercase letters compare between carnitine and control within each water condition

The essential oil profile of culantro is modified by drought and applying carnitine

The water levels and the addition of carnitine significantly altered two of the main compounds detected: hydroquinone and eryngial (Online Resource 1, Supplementary Table 1). The first three canonical variables explained 94.1% of the variability among the treatments based on the essential oils profile, allowing for a three-dimensional scatter plot representation (Fig. 5a). The treatments were separated into four groups: group 1 (green circle), well-watered plants; group 2 (red circle), well-watered and drought control plants; group 3 (blue circle), drought plants with carnitine application; and group 4 (yellow circle) re-watered plants with carnitine application.

Fig. 5.

Fig. 5

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Essential oil profile of 102-day-old Eryngium foetidum L. plants sprayed with water or carnitine, and grown under different water conditions. 3D scatter-plot of the first three canonical variables (% total variance explained by each canonical component is indicated in parentheses; treatments indicated by the same color were assembled into the same group by the Tocher optimization method and the generalized squared interpoint distance of Mahalanobis; WW-Ctrl: well-watered + water application, WW-CA: well-watered + carnitine application, DR-Ctrl: drought + water application, DR-CA: drought + carnitine application, RW-Ctrl: re-watered + water application, RW-CA: re-watered + carnitine application) (a); Relative contributions of the original variables, calculated using the Singh method, to the canonical variables (b); production of eryngial (c); and production of hydroquinone (d). Means followed by the same letter do not differ by Tukey’s test (P ≤ 0.05). Capital letters compare among water conditions, and lowercase letters compare between carnitine and control within each water condition

The relative contributions of the original variables showed that eryngial and hydroquinone were the most prominent compounds, contributing 38.13% and 24.81, respectively, to the total variance (Fig. 5b). Drought and re-watering augmented eryngial content, compared to well-watered plants. In the re-watered, the application of carnitine even increased this compound (Fig. 5c). Hydroquinone, in turn, was only detected in re-watered plants treated with carnitine (Fig. 5d).

Discussion

Water is important for plant growth and food production; thus, it is essential to comprehend plant responses under drought conditions to increase crop production (Henschel et al. 2022). Here, the aerial part growth of culantro plants was impaired by drought and increased by re-watering, while root growth was increased by drought (Fig. 1). Drought-induced reductions in cell division and turgor are responsible for the decrease in leaf area (Tardieu et al. 2014); however, even under water stress, plants can maximize water uptake from the soil by increasing the root growth, which is one of the main survival strategies of plants under drought conditions. During periods of water scarcity, the root system undergoes morphological changes to enhance its ability to absorb water and nutrients, such us deeper roots due increased root growth rate and greater lateral root growth, and these modifications can be attributed to coordinated cell division, elongation, and differentiation events in the root apex (Lynch et al. 2018; Dinneny 2019; Gupta et al. 2020). Here, there probably were changes in cell division and differentiation, as evidenced by the increase in root length.

Re-watering increased the number of leaves and leaf area, which increased the photosynthetic capacity of plants, increasing the fresh and dry mass (Figs. 1, 2, 4). This increase in plant growth after a period of water stress followed by re-watering is an important plant survival strategy, since enhances its adaptation to drought (Sun et al. 2016; Gupta et al. 2020). Here, carnitine not increased root mass (Fig. 1), unlike reported by Lelandais-Brière et al. (2007) and Santos et al. (2022c), in which carnitine application increased root density and growth in Arabidopsis and culantro, respectively. Re-watering altered the shoot/root ratio of the plants compared to drought, leading to more biomass allocated to shoots than roots (Fig. 1). Rapid leaf growth after re-watering is essential to maximize light capture and, consequently, biomass accumulation (Xu and Zhou 2006; Toscano et al. 2014).

The fact that drought reduce leaf growth, resulting in a higher cell density per area (Ren et al. 2019), can explain the increase in pigment levels under this condition. Carnitine application increased the photosynthetic pigments content in well-watered and re-watered (Fig. 3), showing that this compound can act in the signaling of the synthesis pathways of these pigments within the chloroplast. Increased dark respiration in re-watered + carnitine (Fig. 4g) may have occurred due the transport of acyl-CoA to mitochondria during gluconeogenesis, which is mediated by carnitine. This process increases plant respiration, which can contribute to the recovery of growth and regeneration (Steiber et al. 2004). This higher respiration caused by carnitine application also increased LCP, indicating lower light use efficiency (Song et al. 2015).

Secondary metabolites are responsible for plant adaptation and survival, especially under unfavorable conditions (Takshak and Agrawal 2019). Plants modulate their secondary metabolism in response to stress factors, which can improve the quality of medicinal and aromatic plants (Szabó et al. 2017; Costa et al. 2020). Culantro is recognized by its aroma, given by the essential oils (Singh et al. 2014). Water stress induces changes in the profile of essential oils in culantro, and the application of carnitine in these plants under drought induced further qualitative changes in the composition of volatiles (Fig. 5a, b). The compounds that contributed the most to the difference among these profiles were eryngial and hydroquinone (Fig. 5b–d). Amino acids have been reported to alter the profile of secondary metabolites in plants, as demonstrated by Talaat et al. (2014), where the application of tyrosine and phenylalanine resulted in qualitative differences in the essential oils in Ammi visnaga. Amino acids participate in the synthesis of other compounds, such as proteins, vitamins, enzymes, and terpenoids. The canonical discriminant analysis showed that watering treatment and carnitine application interact to determine the essential oil profiles of the culantro plants (Fig. 5a). Martins et al. (2003) and Chandrika et al. (2015) found different profiles of essential oils in culantro depending on the geographic location where it was collected, showing that ambient conditions influence the composition of these compounds. Rodrigues et al. (2020) also reported that mineral fertilizer composition can change the essential oil composition in the leaves and roots of culantro.

Here, drought and re-watering increased the production of eryngial, which is the major component of culantro essential oil (Darriet et al. 2014; Thomas et al. 2017; Rodrigues et al. 2020). Eryngial is an aliphatic and aromatic aldehyde with antibacterial activity and responsible for the flavor and aroma of culantro and other plants (Abiko et al. 2020; Karakaya et al. 2020). In addition, it has anthelmintic, antibacterial, and anti-inflammatory activity, being characterized as a yellowish oil with a pungent odor (Paul et al. 2011; Forbes et al. 2014). Considering that aldehydes, such as eryngial, are derived from α- or β-oxidation of fatty acids (Bridgemohan et al. 2021), and that carnitine is involved in fatty acids catabolism (Bourdin et al. 2007), it may explain the increase in eryngial upon carnitine application found here.

Besides, in re-watered plants, carnitine induced the production of hydroquinone, which is an aromatic phenolic compound derivative from benzene (Cabrera-Alonso et al. 2019; Sun et al. 2021). Hydroquinone is used in the production of antioxidants, agrochemicals, and photographic paper (Jeyanthi et al. 2021). In the cosmetic industry, it is also used as a skin lightener and to treat hyperpigmentation, such as melasma, freckles, senile lentigines, and chloasma (Elferjani et al. 2017). Furthermore, it also shows antibacterial activity against Staphylococcus aureus and Pseudomonas aeruginosa (Ma et al. 2019; Jeyanthi et al. 2021). Hydroquinone has been found in some plant species, such as Majorana hortensis, Arctostaphylos uva-ursi, Vaccinium vitis idaea, Pyrus communis, and Ecdysanthera rosea (Zhu et al. 2010; Rychlinska and Nowak 2012). However, here we report the presence of hydroquinone in culantro for the first time. It is noteworthy that this compound only appeared with the specific combination of re-watering with carnitine application. The carnitine metabolism in plants and its relation with secondary metabolites are still unclear, but here the application of this amino acid increased the production of eryngial and promoted the production of hydroquinone, indicating that this compound may be related to secondary metabolites pathways.

Conclusion

Culantro plants increase biomass when subjected to a period of drought followed by rehydration. Foliar application of carnitine leads to changes in the synthesis of photosynthetic pigments and essential oil profile, including the induction of hydroquinone production when this application is combined with re-watering. The application of exogenous carnitine can be a strategy to induce the production of essential oil compounds of cosmetic and pharmaceutical importance in culantro. However, more research is needed to understand the action of carnitine in the production of secondary metabolites in plants.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 49 KB) (49.2KB, docx)

Acknowledgements

We thank A. M. Santos and S. M. Santos for kindly donating seeds for the experiments. We also acknowledge the National Council for Scientific and Technological Development (CNPq—Brazil), Research Support Foundation of the State of Paraíba/Federal University of Paraíba (FAPESQ/UFPB), Minas Gerais State Research Foundation (FAPEMIG), and Coordination for the Improvement of Higher Education Personnel (CAPES) for the scholarships granted to students.

Author contributions

SKS, JMH, and DSB designed the study; SKS, DSG, AFPO, AMOS, VSM, MHAG, EMM, and RMG performed the experiments and the analyses; SKS, EMM, JMH, and DSB analyzed the data; SKS, EMM, LFV, RMG, JMH, and DSB wrote the article with input from all other authors. All authors read and approved the manuscript.

Funding

This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brasília, DF, Brazil: Grants no. PQ 304214/2022-1 to DSB and 301858/2023-3 to JMH], Fundação de Apoio à Pesquisa do Estado da Paraíba/Universidade Federal da Paraíba (FAPESQ/UFPB), Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior (CAPES), and the Public Call n. 03 Produtividade em Pesquisa PROPESQ/PRPG/UFPB [Grant Proposal code PVO13257-2020 to DSB].

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Declarations

Conflict of interest

The authors have no competing interests to declare that are relevant to the content of this article.

Research involving human participants and/or animals

Not applicable.

Informed consent

Not applicable.

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Supplementary Materials

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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