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Volatiles composition and extraction kinetics from Schinus terebinthifolius and Schinus molle leaves and fruit

Abstract

Essential oils extracted from Schinus molle L. and Schinus terebinthifolius Raddi, Anacardiaceae, leaves and fruit hydrodistillation, as well as, their chemical composition and extraction kinetic were evaluated. For this proposal, 6 h extraction and aliquots collected at sequencing different times (0.5, 1, 2, 4 and 6 h) were carried out allowing calculating accumulated content (% w/w) and verifying essential oil chemical profile. β-caryophyllene (35.2%), α-pinene (28.1%) and germacrene D (15.5%) represent S. terebinthifolius dried leaves essential oil major components, as well as, α-pinene (44.9%), germacrene D (17.6%) and β-pinene (15.1%) in the fruit. Cubenol (27.1%), caryophyllene oxide (15.3%) and spathulenol (12.4%) represent S. molle dried leaves essential oil major components, and β-pinene (36.3%) α-pinene (20.3%), germacrene D (12.1%) and spathulenol in the fruit. Essential oil extraction kinetics showed a hyperbolic distribution; monoterpene content presented exponential decay in time function and sesquiterpene showed exponential growth. Faster monoterpene extraction than the sesquiterpene extraction was observed, however, both presented increasing exponential distribution.

Keywords
Essential oil; Hydrodistillation; Terpenes; Schinus genus; Anacardicaceae

Introduction

Economic potential for aromatic plants and their essential oils employment is relevant, but just a little explored in Brazil, however, studies searching for natural products employed on human and animal health were intensified (Adorjan and Buchbauer, 2010Adorjan, B., Buchbauer, G., 2010. Biological properties of essential oils: an updated review. Flavour Frag. J. 25, 407-426.; Silva and Fernandes Júnior, 2010Silva, N., Fernandes Júnior, A., 2010. Biological properties of medicinal plants: a review of their antimicrobial activity. J. Venom. Anim. Toxins Incl. Trop. Dis. 16, 402-413.; Lange et al., 2013Lange, B.M., Lange, I., Turner, G.W., Herron, B.K., 2013. Medicinal & Aromatic plants utility of Aromatic plants for the biotechnological production of sustainable chemical and pharmaceutical feedstocks. Med. Aromat. Plants 2, 1-10.).

Another factor stimulating essential oils studies has been the search for natural active substances presenting insecticidal, fungicidal and bactericidal activities, as well as, low environmental impact and human health damage, serving as an alternative to agriculture pesticides use (Santos et al., 2010Santos, A.C.A., Rossato, M., Serafini, L.A., Bueno, M., Crippa, L.B., Sartori, V.C., Dellacassa, E., Moyna, P., 2010. Efeito fungicida dos óleos essenciais de Schinus molle L. e Schinus terebinthifolius Raddi, Anacardiaceae, do Rio Grande do Sul. Rev. Bras. Farmacogn. 20, 154-159.; Regnault-Roger et al., 2012Regnault-Roger, C., Vincent, C., Arnason, J.T., 2012. Essential oils in insect control: low-risk products in a high-stakes world. Annu. Rev. Entomol. 57, 405-424.; El-Wakeil, 2013El-Wakeil, N.E., 2013. Botanical pesticides and their mode of action. Gesunde Pflanz. 65, 125-149.; Ootani et al., 2013Ootani, M.A., Aguiar, R.W., Carlos, A., Ramos, C., Brito, R., Batista, J., Cajazeira, P., 2013. Use of essential oils in agriculture. J. Biotechnol. Biodivers. 4, 162-175.; Regnault-roger, 2013Regnault-roger, C., 2013. Essential oils in insect control. In: Ramawat, K.G., Mérillon, J.-M. (Eds.), Natural Products. Springer, Berlin, Heidelberg, pp. 4087–4107.).

Two Anacardiaceae family tree species (Schinus molle L. and Schinus terebinthifolius Raddi) are important in regarding to the natural resources exploitation possibility from their special metabolism (Kramer, 1957Kramer, F.L., 1957. The pepper tree Schinus molleL. Econ. Bot. 11, 322-326.; Morton, 1978Morton, J.F., 1978. Brazilian pepper - its impact on people, animals and the environmental. Econ. Bot. 32, 353-359.; Mack, 1991Mack, R.N., 1991. The commercial seed trade: an early disperser of weeds in the United States. Econ. Bot. 45, 257-273.; Goldstein and Coleman, 2004Goldstein, D.J., Coleman, R.C., 2004. Schinus molleL. (Anacardiaceae) Chicha production in the Central andes. Econ. Bot. 58, 523-529.). The first one is native from northern South America arid regions, including Peru, Chile and Argentina, as well as, their fruit are not suitable for human feeding in the reason of toxic properties (Blood, 2001Blood, K., 2001. Environmental weeds: a field guide for SE Australia. C.H. Jerram and Associates, Mount Waverley.). The second one has widely been distributed in the Brazilian Atlantic forest from south to northeast Brazil and its fruit are traded as pepper (poivre-rose), greatly appreciated in European cooking (Gomes et al., 2013aGomes, L.J., Silva-Mann, R., Mattos, P.P., Rabbani, A.R.C., 2013a. Pensando a Biodiversidade: Aroeira (Schinus terebinthifoliusRaddi.). UFS, São Cristovão., bGomes, V., Agostini, G., Agostini, F., Atti dos Santos, A.C., Rossato, M., 2013b. Variation in the essential oils composition in Brazilian populations of Schinus molle L. (Anacardiaceae). Biochem. Syst. Ecol. 48, 222-227.).

Some studies have reported S. terebinthifolius and S. molle essential oils content and chemical composition based on equal or less time period than 90 min distillation (Santos et al., 2009Santos, A.C.A., Rossato, M., Agostini, F., Serafini, L.A., Santos, P.L.D., Molon, R., Dellacassa, E., Moyna, P., 2009. Chemical composition of the essential oils from leaves and fruits of Schinus molle L. and Schinus terebinthifolius Raddi from Southern Brazil. J. Essent. Oil Bear. Plants 12, 16-25.; Dellacassa, 2010Dellacassa, E., 2010. Normalización de productos naturales obtenidos de especies de la flora aromática latinoamericana: proyecto CYTED IV.20. EdiPUCRS.). However, it is supposed these time periods are not sufficient for essential oil compounds complete extraction.

S. molle and S. terebinthifolius leaves and fruit essential oils by hydrodistillation at different sequencing time periods (0.5, 1, 2, 4 and 6 h) were extracted, and results nonlinear analyses allowing observing extraction time modulating essential oil content and quality; decreasing monoterpenes content as increasing sesquiterpenes content on samples analyzed examined in time function.

Materials and methods

Materials

The dichloromethane solvent, alkanes series (C8-C20 e C21-C40) and sodium sulfate anhydrous were purchased from Sigma–Aldrich (Brazil). Nitrogen gas (99.98%) of purity was purchased from White Martins SA (Brazil). Supplies were purchased from Axygen (Brazil) and glass vials for essential oils storage were purchased in Didática-SP (Brazil).

Plant material

Schinus molle L. was collected at Volta Redonda (March 2013), and S. terebinthifolius Raddi at Seropédica (March 2014), both in the city of Rio de Janeiro, Brazil. Fruit and leaf samples were separated for drying at room temperature, protected from light, moisture and stored until the time of distillation. A voucher specimen has been deposited in the herbarium of Biology Institute (UFRRJ) with the following ID: RBR 36405 (S. terebinthifolius) and RBR 35791 (S. molle).

Essential oil extraction

S. terebinthifolius and S. molle dried fruits and leaves, 80 g triplicate separate in organs and species, were homogenized for 3 min in a food processor and then subjected to hydrodistillation using the Clevenger apparatus for 6 h. About 15 ml of distilled water plus essential oil samples were collected in different sequence time periods (0.5, 1, 2, 4 and 6 h) and then partitioned with 3 × 5 ml of dichloromethane, then, the less polar phase was dried over anhydrous sodium sulfate, filtered and concentrated with nitrogen gas at room temperature until constant weight (after three weighing equals). Gravimetric measurements were performed base on the dry weight of leaves and fruits and converted to essential oil percentage (w/w).

Chromatographic analysis and identification

To separate, detect and quantify the constituents, 1 µl of essential oils samples (10 µl ml−1), in the defined times, were injected into the gas chromatography (GC). A Hewlett-Packard 5890 Series II (Palo Alto, USA), equipped with flame ionization detection and a split/splitless injector, in a split ratio of 1:20 was used to separate and detect the constituents in the essential oil. The substances were separated with a fused silica capillary column, similar DB5 with 30 m × 0.25 mm (i.d.) × 0.25 µm (film thickness). Helium was used as the carrier gas at a flow rate of 1.0 ml min−1. The column temperature was programmed as follows: 60 °C for 2 min followed by heating at 5 °C min−1 to 110 °C, followed by heating at 3 °C min−1 to 150 °C and finally followed by heating at 15 °C min−1 until 290 °C and holding constant for 15 min. The injector temperature was 220 °C and the detector temperature was 290 °C. To separate and identify the substances, 1.0 µl of essential oils samples (10 µl ml−1), in the defined times, were injected in the gas chromatograph coupled to mass spectrometer (GC-MS) QP-2010 Plus (Shimadzu, Japan). The flow of the helium gas carrier, the capillary column and the temperature conditions for the GC-MS analysis were the same as described for the GC. The temperature of the injector was 220 °C and the temperature of the interface was 250 °C. Mass spectra were obtained with a quadrupole detector operating at 70 eV, with 40–400 m/z mass range and scanning rate equal to 0.5 scan s−1. The identification of volatile compounds in the essential oil has been based on Linear Retention Indices (LRI) and mass spectra of the samples, compared with authentic standards injected under the same conditions, with the NIST database (2008) and the index Kovats, IK (Adams, 2007Adams, R.P., 2007. Identification of essential oil components by gas chromatography/mass spectroscopy, 4th ed. Allured Publishing Corporation, Carol Stream.). The LRI was calculated based on co-injection of alkanes series (Van Den Dool and Kratz, 1963Van Den Dool, H., Kratz, P.D., 1963. A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J. Chromatogr. A 11, 463-471.).

Statistical analysis

The mean, standard error of the mean, test-t and graphics were calculated and produced by GraphPad Prism 6.0 (GraphPad Software, EUA).

Results and discussion

Essential oil content and extraction kinetics

Differences in essential oils contents between the Schinusspecies and organs were observed. S. terebinthifolius leaves essential oil (0.10%) compared to same species fruit (1.74%) and S. molle leaves (1.10%) presented lower content. S. molle fruit essential oil content (2.30%) was higher than that on from the same species leaves and from S. terebinthifoliusfruit.

S. terebinthifolius leaves essential oil low content does not correspond to those ones presented in the literature (Barbosa et al., 2007Barbosa, L.C.A., Demuner, A.J., Clemente, A.D., De Paula, V.F., Ismail, F.M.D., 2007. Seasonal variation in the composition of volatile oils from Schinus terebinthifolius Raddi. Quim. Nova 30, 1959-1965.; Santos et al., 2009Santos, A.C.A., Rossato, M., Agostini, F., Serafini, L.A., Santos, P.L.D., Molon, R., Dellacassa, E., Moyna, P., 2009. Chemical composition of the essential oils from leaves and fruits of Schinus molle L. and Schinus terebinthifolius Raddi from Southern Brazil. J. Essent. Oil Bear. Plants 12, 16-25.). Moreover, S. terebinthifoliusfruit essential oil content (Gomes et al., 2013aGomes, L.J., Silva-Mann, R., Mattos, P.P., Rabbani, A.R.C., 2013a. Pensando a Biodiversidade: Aroeira (Schinus terebinthifoliusRaddi.). UFS, São Cristovão.) and S. molle leaves and fruit essential oils were similar to those ones presented in the literature (Dikshit et al., 1986Dikshit, A., Nanqvi, A.A., Husain, A., 1986. Schinus molle: a new source of natural fungitoxicant. Appl. Environ. Microbiol. 51, 1085-1088.; Zahed et al., 2010Zahed, N., Hosni, K., Ben Brahim, N., Kallel, M., Sebei, H., 2010. Allelopathic effect of Schinus molle essential oils on wheat germination. Acta Physiol. Plant 32, 1221-1227.; Torres et al., 2012Torres, F.C., Lucas, A.M., Ribeiro, V.L.S., Martins, J.R., von Poser, G., Guala, M.S., Elder, H.V., Cassel, E., 2012. Influence of essential oil fractionation by vacuum distillation on acaricidal activity against the cattle tick. Braz. Arch. Biol. Technol. 55, 613-621.; Scopel et al., 2013Scopel, R., Góes Neto, R., Falcão, M.A., Cassel, E., Vargas, R.M.F., 2013. Supercritical CO2 extraction of Schinus molleL. with co-solvents: mathematical modeling and antimicrobial applications. Braz. Arch. Biol. Technol. 56, 513-519.) and higher to those ones presented by Santos et al. (2009)Santos, A.C.A., Rossato, M., Agostini, F., Serafini, L.A., Santos, P.L.D., Molon, R., Dellacassa, E., Moyna, P., 2009. Chemical composition of the essential oils from leaves and fruits of Schinus molle L. and Schinus terebinthifolius Raddi from Southern Brazil. J. Essent. Oil Bear. Plants 12, 16-25..

It was observed that essential oils chemical profile obtained from this survey was not overall similar to those ones presented by other authors (Santos et al., 2009Santos, A.C.A., Rossato, M., Agostini, F., Serafini, L.A., Santos, P.L.D., Molon, R., Dellacassa, E., Moyna, P., 2009. Chemical composition of the essential oils from leaves and fruits of Schinus molle L. and Schinus terebinthifolius Raddi from Southern Brazil. J. Essent. Oil Bear. Plants 12, 16-25.; Dellacassa, 2010Dellacassa, E., 2010. Normalización de productos naturales obtenidos de especies de la flora aromática latinoamericana: proyecto CYTED IV.20. EdiPUCRS.; Gomes et al., 2013bGomes, V., Agostini, G., Agostini, F., Atti dos Santos, A.C., Rossato, M., 2013b. Variation in the essential oils composition in Brazilian populations of Schinus molle L. (Anacardiaceae). Biochem. Syst. Ecol. 48, 222-227.) as ISO (IRAM-18608-1: 2006) cited by Dellacassa (2010)Dellacassa, E., 2010. Normalización de productos naturales obtenidos de especies de la flora aromática latinoamericana: proyecto CYTED IV.20. EdiPUCRS..

Variations in essential oils contents from plant tissues can be related to different factors, some of them intrinsic and controlled by the plant genetic traits (Souza, 2012Souza, D.C.L., (MSc thesis) 2012. Diversidade Genética, produção de frutos e composição química em Schinus terebinthifolius Raddi. Universidade federal de Sergipe, Brazil, pp. 97.; Gomes et al., 2013bGomes, V., Agostini, G., Agostini, F., Atti dos Santos, A.C., Rossato, M., 2013b. Variation in the essential oils composition in Brazilian populations of Schinus molle L. (Anacardiaceae). Biochem. Syst. Ecol. 48, 222-227.), On the other hand, quantitative traits are susceptible to the edaphoclimatic effects, such as seasonality, water availability and soil nutrients (Sangwan et al., 2001Sangwan, N.S., Farooqi, A.H.A., Shabih, F., Sangwan, R.S., 2001. Regulation of essential oil production in plants. Plant Growth Regul. 34, 3-21.; Lima et al., 2003Lima, H.R.P., Kaplan, M.A.C., Cruz, A.V.D.M., 2003. Influência dos fatores abióticos na produção e variabilidade de terpenóides em plantas. Floresta Ambient 10, 71-77.).

Nonlinear hyperbolic distribution was the model which presented the best fit to essential oils extraction kinetics (Fig. 1), allowing estimating maximum essential oils contents greater than 40, 10, 25 and 15 h as uneconomical extraction time period, however, in the experimental proposed time (6 h), the maximum practically achieved corresponded to 75, 98, 81 and 93% total estimated, Fig. 1ad, respectively.

Fig. 1
Schinus terebinthifolius and Schinus molle leaves and fruit essential oils extraction kinetics by hydrodistillation as function of different sequencing time periods (0.5, 1, 2, 4 and 6 h). Best fit obtained with hyperbolic nonlinear regression (α = 0.05, n = 3), r2 = 0.9183 (a); 0.8865 (b); 0.9739 (c) and 0.9690 (d).

Faster fruit essential oil extraction speed than the leaves extraction speed was observed, thus, to obtaining half of estimated maximum content of essential oils were needed 150 and 75 min for leaves extraction and just 11 and 29 min for fruits from S. terebinthifolius and S. molle, respectively.

Chemical profile of essential oil

In Table 1, α-pinene (28.1%), β-caryophyllene (35.2%) and germacrene D (15.5%) were S. terebinthifolius dried leaves major compounds, as well as, α-pinene (44.9%), β-pinene (15.1%) and germacrene D (17.6%) were in the fruits S. terebinthifolius were the; in the dried leaves of S. molle were the sesquiterpenes cubenol (27.1%), caryophyllene oxide (15.3%) and spathulenol (12.4%); in the dried leaves of S. molle were the monoterpenes α-pinene (20.3%), β-pinene (36.3%) and the sesquiterpenes germacrene D (12.1%) and spathulenol (11.4%).

Table 1
Schinus molle and S. terebinthifolius leaves and fruit essential oils composition after 6 h extraction by hydrodistillation.

It can be observed some similarity in the essential oil profile of S. terebinthifolius with regarding the majority compounds from fruits and leaves (α-pinene, β-caryophyllene and germacrene D) and also compared with essential oils from fruits of S. molle(α-pinene, β-pinene, germacrene D and spathulenol), whose difference is due to the presence of spathulenol. On the other hand, the same similarity was observed between the leaves and fruits of S. molle, which showed only the spathulenol in common (Table 1).

In Tables 25 can be noted the chemical variation of essential oils as a function of extraction time. The essential oil obtained from the leaves of S. terebinthifolius (Table 2) was what had the lowest number of different compounds, only six substances. Despite the sesquiterpene content to increase with the time of distillation, it was observed that the sesquiterpene was completely extracted in the first half-hour of distillation.

Table 2
Schinus terebinthifolius dried leaves essential oils composition after 6 h extraction by hydrodistillation at different sequencing time periods (0.5, 1, 2, 4 and 6 h).
Table 3
Schinus terebinthifolius dried fruit essential oils composition after 6 h extraction by hydrodistillation at different sequencing time periods (0.5, 1, 2, 4 and 6 h).
Table 4
Chemical profile of Schinus molle dried leaves essential oils composition after 6 h extraction by hydrodistillation at different sequencing time periods (0.5, 1, 2, 4 and 6 h).
Table 5
Chemical profile of Schinus molle dried fruits essential oils composition after 6 h extraction by hydrodistillation at different sequencing time periods (0.5, 1, 2, 4 and 6 h).

The essential oil obtained from fruits of S. terebinthifoliusexhibited a more complex profile comparing to the leaves, totaling 26 identified substances (Table 3). Some substances, especially sesquiterpenes were not observed during the first distillation time. For example, γ-murolene and δ-cadinene, which to be start extracted from the second hour of distillation.

The chemical analysis of the essential oil of S. molle leaves allowed the identification of 21 different substances (Table 4). Also the analysis of chemical composition as a function of extraction time allowed to evaluate that the monoterpenes were extracted in their totality until the second hour of distillation, while that some sesquiterpenes, for example, α-cadinol and globulol have been extracted after the second hour distillation.

In Table 5 can be observed twenty different substances that have been identified. It was found with the time, decrease of monoterpene content extracted, for example, the content of monoterpenes α-pinene and β-pinene decreased respectively from 24.3 and 46.6 to 2.2% and 3.1%. On the other hand, the sesquiterpene spathulenol increased from 1.9 to 28.2%, in function of time.

In the extractions involving the fruits and leaves of S. terebinthifolius and S. molle were revealed similar behavior in the extraction process of monoterpenes and sesquiterpenes in function of time (Fig. 2), for which was noted decrease of monoterpenes content and increase of sesquiterpenes content in the samples analyzed, which are in agreement with those reported by Marongiu et al. (2004)Marongiu, B., Porcedda, A.P.S., Casu, R., Pierucci, P., 2004. Chemical composition of the oil and supercritical CO2 extract of Schinus molle L.. Flavour Fragr. J 19, 554-558. and Barbosa et al. (2007)Barbosa, L.C.A., Demuner, A.J., Clemente, A.D., De Paula, V.F., Ismail, F.M.D., 2007. Seasonal variation in the composition of volatile oils from Schinus terebinthifolius Raddi. Quim. Nova 30, 1959-1965..

Fig. 2
Monoterpenes and sesquiterpenes content and accumulated content from Schinus terebinthifolius and Schinus molle leaves and fruit essential oils by hydrodistillation as function of different sequencing time periods (0.5, 1, 2, 4 and 6 h). Best fit obtained with exponential nonlinear regression (α = 0.05; n = 4), r2 = 0.9843; 0.9670; 0.9867 (a); 0.9947; 0.9885; 0.9923 (b); 0.9749; 0.9968; 0.9883 (c) e 0.9949; 0.9924; 0.9968 (d), respectively to and , .

On the other hand, the accumulated contents of all terpenoids have been increasing in the function of time elapsed extraction. Based on this result can be inferred about extraction speed of terpenes, since it took around 1 and 4 h for 80% extraction of monoterpenes and sesquiterpenes, respectively.

This fact is related to ability of diffusion of volatile molecules from the site of synthesis and storage, crossing the plant tissue, until reaching the atmosphere after to be carried by steam. Thus, how much greater is the impediment, smaller is diffusion and greater will be time required for extraction these volatiles (Reverchon et al., 1995Reverchon, E., Porta, G., Della Senatore, F., 1995. Supercritical CO2 extraction and fractionation of lavender essential oil and waxes. J. Agric. Food Chem. 43, 1654-1658.).

In this way, volatile with lower molecular weight and lower polarity tend to have a better diffusibility, while the volatiles with higher molecular weight and having polarity tend to have a lower diffusivity.

Therefore, the extraction time suitable to extract a real chemical profile of essential oil, as quality and content of volatiles, depends of an extraction time that is not too small. On the other hand, long extraction times besides the necessary, can increase the costs of the operation, without thereby significantly increase the content of essential oil extracted.

Acknowledgments

Authors gratefully acknowledge FAPERJ (E-26/110.746/2012) and CAPES for financial support. We also thank Dr. Pedro G. Filho (IB, UFRRJ/Brazil) to collaborate in this study.

References

  • Adams, R.P., 2007. Identification of essential oil components by gas chromatography/mass spectroscopy, 4th ed. Allured Publishing Corporation, Carol Stream.
  • Adorjan, B., Buchbauer, G., 2010. Biological properties of essential oils: an updated review. Flavour Frag. J. 25, 407-426.
  • Barbosa, L.C.A., Demuner, A.J., Clemente, A.D., De Paula, V.F., Ismail, F.M.D., 2007. Seasonal variation in the composition of volatile oils from Schinus terebinthifolius Raddi. Quim. Nova 30, 1959-1965.
  • Blood, K., 2001. Environmental weeds: a field guide for SE Australia. C.H. Jerram and Associates, Mount Waverley.
  • Dellacassa, E., 2010. Normalización de productos naturales obtenidos de especies de la flora aromática latinoamericana: proyecto CYTED IV.20. EdiPUCRS.
  • Dikshit, A., Nanqvi, A.A., Husain, A., 1986. Schinus molle: a new source of natural fungitoxicant. Appl. Environ. Microbiol. 51, 1085-1088.
  • El-Wakeil, N.E., 2013. Botanical pesticides and their mode of action. Gesunde Pflanz. 65, 125-149.
  • Goldstein, D.J., Coleman, R.C., 2004. Schinus molleL. (Anacardiaceae) Chicha production in the Central andes. Econ. Bot. 58, 523-529.
  • Gomes, L.J., Silva-Mann, R., Mattos, P.P., Rabbani, A.R.C., 2013a. Pensando a Biodiversidade: Aroeira (Schinus terebinthifoliusRaddi.). UFS, São Cristovão.
  • Gomes, V., Agostini, G., Agostini, F., Atti dos Santos, A.C., Rossato, M., 2013b. Variation in the essential oils composition in Brazilian populations of Schinus molle L. (Anacardiaceae). Biochem. Syst. Ecol. 48, 222-227.
  • Kramer, F.L., 1957. The pepper tree Schinus molleL. Econ. Bot. 11, 322-326.
  • Lange, B.M., Lange, I., Turner, G.W., Herron, B.K., 2013. Medicinal & Aromatic plants utility of Aromatic plants for the biotechnological production of sustainable chemical and pharmaceutical feedstocks. Med. Aromat. Plants 2, 1-10.
  • Lima, H.R.P., Kaplan, M.A.C., Cruz, A.V.D.M., 2003. Influência dos fatores abióticos na produção e variabilidade de terpenóides em plantas. Floresta Ambient 10, 71-77.
  • Mack, R.N., 1991. The commercial seed trade: an early disperser of weeds in the United States. Econ. Bot. 45, 257-273.
  • Marongiu, B., Porcedda, A.P.S., Casu, R., Pierucci, P., 2004. Chemical composition of the oil and supercritical CO2 extract of Schinus molle L.. Flavour Fragr. J 19, 554-558.
  • Morton, J.F., 1978. Brazilian pepper - its impact on people, animals and the environmental. Econ. Bot. 32, 353-359.
  • Ootani, M.A., Aguiar, R.W., Carlos, A., Ramos, C., Brito, R., Batista, J., Cajazeira, P., 2013. Use of essential oils in agriculture. J. Biotechnol. Biodivers. 4, 162-175.
  • Regnault-roger, C., 2013. Essential oils in insect control. In: Ramawat, K.G., Mérillon, J.-M. (Eds.), Natural Products. Springer, Berlin, Heidelberg, pp. 4087–4107.
  • Regnault-Roger, C., Vincent, C., Arnason, J.T., 2012. Essential oils in insect control: low-risk products in a high-stakes world. Annu. Rev. Entomol. 57, 405-424.
  • Reverchon, E., Porta, G., Della Senatore, F., 1995. Supercritical CO2 extraction and fractionation of lavender essential oil and waxes. J. Agric. Food Chem. 43, 1654-1658.
  • Sangwan, N.S., Farooqi, A.H.A., Shabih, F., Sangwan, R.S., 2001. Regulation of essential oil production in plants. Plant Growth Regul. 34, 3-21.
  • Santos, A.C.A., Rossato, M., Agostini, F., Serafini, L.A., Santos, P.L.D., Molon, R., Dellacassa, E., Moyna, P., 2009. Chemical composition of the essential oils from leaves and fruits of Schinus molle L. and Schinus terebinthifolius Raddi from Southern Brazil. J. Essent. Oil Bear. Plants 12, 16-25.
  • Santos, A.C.A., Rossato, M., Serafini, L.A., Bueno, M., Crippa, L.B., Sartori, V.C., Dellacassa, E., Moyna, P., 2010. Efeito fungicida dos óleos essenciais de Schinus molle L. e Schinus terebinthifolius Raddi, Anacardiaceae, do Rio Grande do Sul. Rev. Bras. Farmacogn. 20, 154-159.
  • Scopel, R., Góes Neto, R., Falcão, M.A., Cassel, E., Vargas, R.M.F., 2013. Supercritical CO2 extraction of Schinus molleL. with co-solvents: mathematical modeling and antimicrobial applications. Braz. Arch. Biol. Technol. 56, 513-519.
  • Silva, N., Fernandes Júnior, A., 2010. Biological properties of medicinal plants: a review of their antimicrobial activity. J. Venom. Anim. Toxins Incl. Trop. Dis. 16, 402-413.
  • Souza, D.C.L., (MSc thesis) 2012. Diversidade Genética, produção de frutos e composição química em Schinus terebinthifolius Raddi. Universidade federal de Sergipe, Brazil, pp. 97.
  • Torres, F.C., Lucas, A.M., Ribeiro, V.L.S., Martins, J.R., von Poser, G., Guala, M.S., Elder, H.V., Cassel, E., 2012. Influence of essential oil fractionation by vacuum distillation on acaricidal activity against the cattle tick. Braz. Arch. Biol. Technol. 55, 613-621.
  • Van Den Dool, H., Kratz, P.D., 1963. A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J. Chromatogr. A 11, 463-471.
  • Zahed, N., Hosni, K., Ben Brahim, N., Kallel, M., Sebei, H., 2010. Allelopathic effect of Schinus molle essential oils on wheat germination. Acta Physiol. Plant 32, 1221-1227.

Publication Dates

  • Publication in this collection
    Jul-Aug 2015

History

  • Received
    28 May 2015
  • Accepted
    08 July 2015
Sociedade Brasileira de Farmacognosia Universidade Federal do Paraná, Laboratório de Farmacognosia, Rua Pref. Lothario Meissner, 632 - Jd. Botânico, 80210-170, Curitiba, PR, Brasil, Tel/FAX (41) 3360-4062 - Curitiba - PR - Brazil
E-mail: revista@sbfgnosia.org.br