Figueiredo et al. Chemistry Central Journal (2018) 12:52 https://doi.org/10.1186/s13065-018-0428-z

RESEARCH ARTICLE Open Access Chemical variability in the essential oil of leaves of Araçá ( guineense Sw.), with occurrence in the Amazon Pablo Luis B. Figueiredo1*, Renan C. Silva2, Joyce Kelly R. da Silva3, Chieno Suemitsu4, Rosa Helena V. Mourão5 and José Guilherme S. Maia1

Abstract Background: , known as Araçá, is a Brazilian botanical resource with commercial application perspectives, based on the functional elements of its fruits and due to the use of its leaves as an anti-infammatory and antibacterial agent. The essential oils of leaves of twelve specimens of Araçá were analyzed by GC and GC-MS to identify their volatile constituents and associate them with the biological activities reputed to the . Results: In a total of 157 identifed compounds, limonene, α-pinene, β-caryophyllene, epi-β-bisabolol, caryophyllene oxide, β-bisabolene, α-copaene, myrcene, muurola-4,10(14)-dien-1-β-ol, β-bisabolol, and ar-curcumene were the pri- mary components in descending order up to 5%. Hierarchical Cluster Analysis (HCA) and Principal Component Analy- sis (PCA) displayed three diferent groups with the following chemical types: limonene/α-pinene, β-bisabolene/epi-β- bisabolol, and β-caryophyllene/caryophyllene oxide. With the previous description of another chemical type rich in spathulenol, it is now understood that at least four diferent chemotypes for P. guineense should occur. Conclusions: In addition to the use of the Araçá fruits, which are rich in minerals and functional elements, it should be borne in mind that the knowledge of the chemical composition of the essential oils of leaves of their diferent chemical types may contribute to the selection of varieties with more signifcant biological activity. Keywords: Psidium guineense, , essential oil composition, chemical variability

Background Psidium guineense Swartz [syn. Guajava guineensis Myrtaceae comprises 132 genera and 5671 species of (Sw.) Kuntze, Myrtus guineensis (Sw.) Kuntze, Psidium and , which are distributed mainly in tropical araca Raddi, P. guyanense Pers., P. laurifolium O. Berg, and subtropical regions of the world, particularly South P. rotundifolium Standl., P. sprucei O. Berg, among oth- America, Australia and Tropical Asia [1]. It is one of the ers [5] (www.tropicos.org/Name/22102032) is a native most prominent families in , represented by 23 gen- or small up to about 6 m high occurring in all era and 1034 species, with occurrence in all regions of the Brazilian biomes, commonly known as Araçá. It has a country [2, 3]. Psidium is a with at least 60 to 100 berry-type fruit with yellow, red or purple peel and whit- species, occurring from and to Argen- ish pulp, rich in minerals and functional elements, such tina and Uruguay. Terefore, it is naturally an American as vitamin C and phenolic compounds [6–9]. Te leaves genus, although P. guajava, P. guineense and P. cattleya- and pulp of Araçá have been used as an anti-infamma- num are subtropical and tropical species in many other tory remedy for wound healing and oral antibacterial parts of the world [4]. agent [10, 11], as well as it presented antibacterial activ- ity against pathogenic microorganisms [11–13]. Some *Correspondence: [email protected] essential oils of Araçá were previously described: Foliar 1 Programa de pós‑graduação em Química, Universidade Federal do Pará, oil from a specimen growing in Arizona, USA, with pre- 66075‑900 Belém, PA, Brazil dominance of β-bisabolene, α-pinene and limonene [14]; Full list of author information is available at the end of the article

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foliar oil from a specimen collected in Roraima, Bra- Te oils were analyzed on a GCMS-QP2010 Ultra sys- zil, with β-bisabolol, epi-α-bisabolol and limonene as tem (Shimadzu Corporation, Tokyo, Japan), equipped the main constituents [15]; and another foliar oil from a with an AOC-20i auto-injector and the GCMS-Solution specimen sampled in do Sul Brazil, where software containing the NIST (Nist, 2011) and FFNSC spathulenol was the primary volatile compound [16]. 2 (Mondello, 2011) libraries [17, 18]. A Rxi-5ms (30 m x Te present work aimed at investigating the variability 0.25 mm; 0.25 μm flm thickness) silica capillary column of the chemical composition of the essential oils of dif- (Restek Corporation, Bellefonte, PA, USA) was used. ferent specimens of Psidium guineense, occurring in the Te conditions of analysis were: injector temperature of Amazon region, to contribute to the knowledge of its 250 °C; Oven temperature programming of 60-240 °C chemical types. (3 °C/min); Helium as carrier gas, adjusted to a linear velocity of 36.5 cm/s (1.0 mL/min); split mode injection Experimental for 1 μL of sample (oil 5 μL : hexane 500 μL); split ratio Plant material 1:20; ionization by electronic impact at 70 eV; ionization Te leaf samples of twelve Psidium guineense specimens source and transfer line temperatures of 200 and 250 °C, were collected in Pará state, Brazil. Collection site and respectively. Te mass spectra were obtained by auto- voucher number of each specimen are listed in Table 1. matic scanning every 0.3 s, with mass fragments in the Te plant vouchers after the identifcation were depos- range of 35-400 m/z. Te retention index was calculated ited in the Herbaria of Embrapa Amazônia Oriental, in for all volatile components using a homologous series Belém (IAN) and Santarém (HSTM), Pará state, Brazil. of C8-C20 n-alkanes (Sigma-Aldrich, USA), according Te leaves were dried for two days in the natural environ- to the linear equation of Van den Dool and Kratz (1963) ment and, then, subjected to essential oil distillation. [19]. Te quantitative data regarding the volatile con- stituents were obtained by peak-area normalization using Isolation and analysis of the composition of oils a GC 6890 Plus Series, coupled to FID Detector, oper- Te leaves were ground and submitted to hydrodistilla- ated under similar conditions of the GC-MS system. Te tion using a Clevenger-type apparatus (3 h). Te oils were components of oils were identifed by comparing their dried over anhydrous sodium sulfate, and their yields retention indices and mass spectra (molecular mass and were calculated by the plant dry weight. Te moisture fragmentation pattern) with data stored in the GCMS- content of the samples was calculated using an Infrared Solution system libraries, including the Adams library Moisture Balance for water loss measurement. Te pro- (2007) [20]. cedure was performed in duplicate. Statistical analysis Te multivariate analysis was performed using as vari- Table 1 Identifcation data and collection site of the speci- ables the constituents with content above than 5%. For mens of Psidium guineense the multivariate analysis, the data matrix was standard- ized by subtracting the mean and then dividing it by the Samples Collection site Herbarium Nº Local coordinates standard deviation. For hierarchical cluster analysis, the PG-01 Curuçá, PA, Brazil IAN-195396 0°72’65” S/47°84’07” W complete linkage method and the Euclidean distance PG-02 Curuçá, PA, Brazil IAN-195397 0°43’40” S/47°50’58” W were used. Minitab software (free 390 version, Minitab PG-03 Curuçá, PA, Brazil IAN-195398 0°72’67” S/47°85’13” W Inc., State College, PA, USA), was used for these analyzes. PG-04 Curuçá, PA, Brazil IAN-195399 0°72’57” S/47°84’84” W PG-05 Curuçá, PA, Brazil IAN-195400 0°72’57” S/47°84’07” W Results and discussion Yield and composition of the oils PG-06 Santarém, PA, Brazil HSTM-3611 2°27’48.7” S/54°44’04” W PG-07 Monte Alegre, PA, HSTM-6763 1°57’24.9” Psidium guineense is a botanical resource that presents Brazil S/54°07’07.8” W commercial application perspectives, based on its fruits PG-08 Monte Alegre, PA, HSTM-6763 1°57’24.9” and functional elements, as well as due to the use of its Brazil S/54°07’07.8” W leaves as anti-infammatory and antibacterial agent [6– PG-09 Santarém, PA, Brazil HSTM-6775 2°25’14.6” 14]. For this study were selected twelve Araçá specimens, S/54°44’25.8” W with occurrence in various localities of Pará state (PA), PG-10 Santarém, PA, Brazil HSTM-3603 2°25’08.4” S/54°44’28.3” W Brazil (see Table 1), and which showed diferent compo- PG-11 Santarém, PA, Brazil HSTM-6769 2°29’16.8” sition for the leaf oils. Te yields of the oils from these S/54°42’07.9” W twelve Araçá samples ranged from 0.1 to 0.9%, where the PG-12 Ponta de Pedras, PA, HSTM-6759 2°31’08.3” higher yields were from specimens sampled in the North- Brazil S/54°52’25.8” W east of Pará, Brazil (0.4-0.9%), and the lower yields were Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 3 of 11

from collected in the West of Pará, Brazil (0.1- another specimen collected in Roraima, Brazil, pre- 0.3%). Te identifcation of the constituents of the oils by sented β-bisabolol as the main component, followed by GC and GC-MS was 92.5% on average, with a total of 157 limonene and epi-α-bisabolol [15]. On the other hand, compounds, where limonene (0.3-47.4%), α-pinene (0.1- a specimen sampled in Mato Grosso do Sul, Brazil, pre- 35.6%), β-caryophyllene (0.1-24.0%), epi-β-bisabolol (6.5- sented an essential oil with a very high value of spathule- 18.1%), caryophyllene oxide (0.3-14.1%), β-bisabolene nol [16]. Terefore, it is possible that there is a signifcant (0.1-8.9%), α-copaene (0.3-8.1%), myrcene (0.1-7.3%), variation in the essential oils of diferent types of Araçá. muurola-4,10(14)-dien-1-β-ol (1.6-5.8%), β-bisabolol (2.9-5.6%), and ar-curcumene (0.1-5.0%) were the pri- Variability in oils composition mary components, in descending order up to 5% (see Fig- Te multivariate analysis of PCA (Principal Component ure 1 and Table 2). In general, the constituents identifed Analysis) (Fig. 2) and HCA (Hierarchical Cluster Analy- in oils belong to the terpenoids class, with the following sis) (Fig. 3) were applied to the primary constituents predominance: monoterpene hydrocarbons (0.9-76.9%), present in oils (content ≥ 5.0%), for the evaluation of oxygenated sesquiterpenes (5.2-63.5%), sesquiterpene chemical variability among the P. guineense specimens. hydrocarbons (5.6-46.7%), and oxygenated monoterpe- Te HCA analysis performed with complete binding nes (1.9-8.8%). and Euclidean distance showed the formation of three Comparing these results with the composition of other diferent groups. Tese were confrmed by the PCA anal- essential oils described for the same plant, a specimen ysis, which accounted for 79.5% of the data variance. Te of P. guineense sampled in Arizona, USA, has also been three groups were classifed as: found to contain β-bisabolene, α-pinene, and limonene Group I Characterized by the presence of the monoter- as its primary constituents [14]. In addition, the oil from penes α-pinene (13.4-35.6%) and limonene (3,7-37,2%),

Fig. 1 Main constituents identifed in the oils of P. guineense: (1) α-pinene, (2) myrcene, (3) limonene, (4) β-caryophyllene, (5) caryophyllene oxide, (6) α-copaene, (7) ar-curcumene, (8) β-bisabolene, (9) muurola-4,10(14)-dien-1-β-ol, (10) epi-β-bisabolol, (11) β-bisabolol Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 4 of 11 5.4 7.3 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.3 0.1 0.8 0.1 0.6 0.1 0.6 PG-12 0.1 0.1 0.1 0.1 0.1 1.7 0.1 0.1 0.3 0.5 0.1 0.1 PG-11 1.2 0.2 1.3 0.3 0.7 0.3 47.4 PG-10 0.2 0.1 0.1 0.1 0.1 0.1 0.7 0.2 0.1 0.1 1.0 0.3 0.6 0.4 0.1 0.1 23.4 PG-09 9.6 0.4 1.6 0.2 0.4 0.1 0.1 0.1 0.2 0.8 0.4 0.1 0.3 0.2 0.2 PG-08 0.1 0.1 0.8 0.1 2.0 4.3 0.1 0.1 0.1 0.2 0.1 0.2 0.2 PG-07 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.3 0.1 0.6 3.9 1.6 0.5 0.1 0.9 0.3 0.4 0.2 0.3 0.3 1.7 0.7 26.4 PG-06 14.0 0.1 0.1 0.1 0.2 0.1 0.3 0.2 0.1 0.7 0.1 0.5 0.1 0.9 1.7 1.3 1.4 0.1 0.3 0.1 0.4 0.1 0.2 0.2 1.0 0.4 34.0 PG-05 37.2 0.1 1.0 0.1 0.1 0.1 0.1 1.5 0.8 1.3 1.4 0.7 0.1 0.6 0.1 0.1 0.1 0.1 0.1 0.4 0.3 13.4 26.5 PG-04 0.9 0.1 0.1 0.2 0.1 0.1 0.1 0.2 0.1 0.9 0.4 0.2 1.1 1.4 1.2 1.0 0.1 0.7 0.2 0.1 0.4 0.1 0.2 0.2 1.3 0.4 17.7 30.4 PG-03 0.5 0.1 0.1 0.5 1.8 1.4 0.5 0.1 0.4 0.1 0.1 0.1 0.1 0.1 0.1 0.6 0.2 26.1 30.7 PG-02 0.1 0.3 2.1 0.2 0.3 3.7 0.3 0.1 0.1 0.6 0.1 0.1 0.1 0.1 0.1 0.4 0.1 0.2 0.1 1.0 0.7 35.6 PG-01 Constituents (%) Constituents (2 E )-Hexenal (3 Z )-Hexenol α-Pinene α-Fenchene Benzaldehyde β-Pinene 6-methyl-5-Hepten-2-one Myrcene p -Mentha-1(7),8-diene α-Terpinene p -Cymene Limonene 1,8-Cineole ( Z )-β-Ocimene ( E )-β-Ocimene γ-Terpinene Terpinolene Linalool endo -Fenchol 4,8-dimethyl-( E )-Nona-1,3,7-triene - p -Mentha-2,8-dien-1-oltrans α-Campholenal Limona ketone cis - p -Mentha-2,8-dien-1-ol - p -Menth-2-en-1oltrans -Pinocarveol trans hydrate Camphene Hydrocinnamaldehyde Borneol Terpinen-4-ol - p -Mentha-1(7),8-dien-2-oltrans -Isocarveoltrans α-Terpineol -Carveoltrans acetate endo -Fenchyl a a a a b a a a a a a b b a b a a a a b a a a a a a a a a a a a a a a (L) 1135 RI 1020 1218 1189 1044 1054 1114 988 1136 1133 1122 1131 850 952 1186 932 1113 1122 1165 1014 1095 981 1165 1174 1145 1187 1086 1032 1215 948 974 1024 1032 1003 846 P. guineense oil samples of P. essential of twelve composition and volatile Yield (C) 1139 1023 1187 RI 2 Table 1046 1057 1114 990 1138 1134 1120 1130 850 957 1191 1221 933 1116 1125 1166 1016 1100 985 1161 1177 1148 1186 1088 1035 1218 946 977 1028 1031 1005 848 Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 5 of 11 0.2 0.4 0.1 0.1 0.1 2.8 0.1 0.3 24.0 PG-12 0.1 0.1 0.1 0.1 0.2 0.5 0.2 0.1 0.5 0.3 0.7 0.2 0.3 0.2 1.1 1.1 0.8 PG-11 0.5 0.2 0.4 0.5 0.2 0.6 0.2 2.3 2.0 0.9 0.4 0.5 PG-10 0.1 0.1 0.3 1.1 0.6 1.0 1.0 0.1 0.2 0.3 0.5 1.3 0.4 0.1 0.1 0.9 1.0 0.2 0.1 2.5 1.9 PG-09 0.6 0.8 0.6 0.3 0.2 0.3 0.1 1.1 0.3 0.3 0.3 0.1 0.3 0.1 0.2 4.7 0.2 PG-08 0.5 0.1 0.8 0.9 0.1 0.2 0.3 0.2 0.1 0.3 1.0 1.2 1.3 0.4 0.3 0.2 1.4 4.2 0.1 0.2 0.4 PG-07 5.2 0.2 0.2 0.1 0.4 0.1 0.1 0.1 3.7 1.5 1.6 0.8 0.1 0.9 0.1 PG-06 0.2 0.1 0.4 0.1 0.2 0.8 3.0 0.9 0.8 0.6 0.1 0.1 0.1 PG-05 7.2 0.1 0.6 0.2 0.1 0.1 0.1 0.5 0.2 1.7 0.2 0.5 0.3 PG-04 8.1 0.1 0.6 0.1 0.4 0.1 0.1 0.1 0.1 0.7 0.3 0.1 1.0 0.1 0.3 0.3 PG-03 6.2 0.1 0.2 2.8 0.6 0.3 0.1 0.1 1.1 0.1 0.1 0.7 0.2 PG-02 8.1 6.1 1.5 1.5 0.1 0.2 0.1 0.1 0.1 0.1 0.2 0.9 0.2 PG-01 Constituents (%) Constituents cis -p-Mentha-1(7),8-dien-2-ol Carvone cis -Chrysanthenyl acetate acetate Bornyl Pinocarvyl acetate trans- geranate Methyl Myrtenyl acetate δ-Elemene -Carvyltrans acetate Neryl acetate Cyclosativene α-Copaene acetate Geranyl iso -Italicene Sesquithujene α-Cedrene Acora-3,7(14)-diene β-Caryophyllene β-Cedrene β-Copaene γ-Elemene -α-Bergamotene trans acetate Perillyl Aromadendrene but-2-anoate ethyl Phenyl ( Z )-β-Farnesene Guaia-6,9-diene epi -β-Santalene Amorpha-4,11-diene acetone Geranyl α-Humulene ( E )-β-Farnesene β-Santalene allo -Aromadendrene α-Acoradiene β-Acoradiene a a a a a a a a a a a a a a a a a a a a a a b a a a a a a a a a a a a a (L) 1432 1440 RI 1410 1449 1442 1453 1434 1287 1445 1430 1435 1460 1335 1374 1452 1239 1261 1457 1417 1339 1405 1407 1469 1369 1359 1439 1454 1298 1322 1464 1324 1379 1439 1419 1227 1401 continued (C) 1436 1444 1412 1452 1444 1452 2 Table RI 1435 1286 1447 1431 1436 1461 1336 1378 1455 1243 1267 1460 1423 1338 1406 1416 1467 1367 1364 1441 1458 1300 1324 1464 1326 1383 1440 1426 1226 1401 Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 6 of 11 0.1 1.0 2.6 0.8 0.4 0.4 0.1 0.1 3.2 0.1 0.1 0.2 0.7 0.2 3.2 0.2 PG-12 1.8 0.2 0.7 1.0 1.4 0.5 0.4 0.7 0.4 2.5 4.0 0.1 0.6 1.6 2.2 0.1 PG-11 5.2 0.8 1.0 2.0 0.4 0.3 2.9 0.7 0.6 0.9 1.9 PG-10 6.4 1.1 1.1 2.3 0.6 1.1 0.4 0.4 3.6 0.2 0.1 0.1 1.0 2.5 0.2 2.7 0.1 0.2 PG-09 0.3 0.1 0.5 0.4 0.6 0.1 4.0 0.3 0.6 4.6 0.5 0.7 0.8 2.4 1.3 3.7 0.4 0.5 PG-08 8.9 5.0 0.4 0.4 2.0 0.9 2.7 0.2 0.1 0.8 0.3 0.1 0.8 0.4 0.3 4.3 1.0 3.0 0.3 2.9 PG-07 0.1 0.3 0.1 0.1 0.2 2.7 0.3 0.1 0.1 3.2 0.2 0.2 0.7 PG-06 0.1 0.3 0.1 0.5 0.1 0.1 0.3 PG-05 0.4 0.1 0.4 0.1 0.8 3.7 0.3 3.8 0.5 0.4 2.6 0.1 0.2 PG-04 0.4 0.9 0.2 1.0 0.5 0.3 1.7 0.1 0.4 PG-03 0.3 0.1 0.9 0.8 0.3 0.3 1.9 0.1 0.1 PG-02 1.0 0.7 0.4 0.1 0.1 0.3 1.0 0.1 0.3 0.3 0.7 PG-01 Constituents (%) Constituents 4,5-di- epi -Aristolochene 10- epi -β-Acoradiene γ-Gurjunene β-Chamigrene γ-Muurolene γ-Curcumene ar-Curcumene γ-Himachalene β-Selinene α-Zingiberene α-Selinene α-Muurolene ( Z )-α-Bisabolene ( E , )-α-Farnesene δ-Amorphene β-Bisabolene β-Curcumene γ-Cadinene ( Z )-γ-Bisabolene 7- epi -α-Selinene δ-Cadinene β-Sesquiphellandrene (E)-γ-Bisabolene -Cadina-1,4-dienetrans Italicene ether 10- epi - cis -Dracunculifoliol ( E )-α-Bisabolene Selina-3,7(11)-diene α-Calacorene Germacrene B E -Nerolidol Caryolan-8-ol alcohol Caryophyllenyl ar -Tumerol Spathulenol Globulol a a a a a a a a a a a a a a a b a a a a a a a a a a b a a a a a a b a a (L) 1524 1478 1511 1544 1561 1570 1474 RI 1476 1508 1529 1533 1475 1479 1520 1540 1545 1578 1590 1498 1540 1577 1488 1500 1505 1481 1513 1559 1536 1514 1481 1514 1521 1571 1493 1506 1471 continued (C) 1522 1479 1509 1544 1565 1572 1474 1477 1510 1532 RI 2 Table 1534 1477 1482 1519 1539 1543 1579 1584 1497 1543 1580 1488 1502 1509 1486 1516 1559 1534 1512 1479 1516 1525 1570 1495 1502 1471 Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 7 of 11 4.4 0.5 0.5 0.7 1.3 1.7 1.0 1.5 2.6 3.1 0.3 14.1 PG-12 5.6 2.3 0.8 0.8 2.1 4.3 1.1 1.1 2.5 1.2 2.4 1.6 0.2 1.4 18.1 PG-11 8.2 0.1 0.7 0.5 1.2 0.3 0.4 3.9 1.2 0.4 1.0 0.8 PG-10 9.5 0.5 0.1 1.7 0.7 1.8 0.3 0.5 0.7 3.6 1.3 0.2 0.5 0.3 1.1 0.3 0.4 PG-09 6.5 0.6 0.2 0.4 0.7 1.0 3.4 1.1 0.5 1.6 1.8 4.8 1.9 0.8 0.6 0.1 0.8 0.3 1.6 PG-08 8.1 0.1 0.4 0.9 1.3 1.5 1.5 0.4 1.0 0.6 3.8 2.9 1.0 0.2 1.2 1.0 0.2 0.2 1.1 PG-07 0.1 0.1 3.7 0.7 2.7 2.1 0.3 0.8 2.6 0.1 1.3 PG-06 0.4 0.2 0.6 0.3 0.2 0.4 0.1 1.6 0.1 0.6 PG-05 0.1 4.2 0.2 0.1 1.1 0.2 2.3 0.1 1.7 PG-04 0.3 0.5 1.2 0.3 3.6 0.2 0.1 1.7 1.8 PG-03 2.4 0.7 0.9 0.1 0.3 1.8 0.9 2.0 PG-02 5.8 2.5 0.2 0.4 1.3 3.1 1.9 1.1 1.8 1.4 PG-01 Constituents (%) Constituents Gleenol Caryophyllene oxide β-Copaen-4-α-ol Viridiforol Cubeban-11-ol Guaiol Cedrol ( Z )-8-hydroxy-Linalool Humulene Epoxide Copaborneol 1,10-di- epi -Cubenol 10- epi -γ-Eudesmol epi -Cubenol α-Acorenol Muurola-4,10(14)-dien-1-β-ol β-Acorenol Gossonorol Caryophylla-4(12),8(13)-dien-5β-ol Caryophylla -4(12),8(13)-dien-5α-ol epi -α-Cadinol epi -α-Murrolol Hinesol α-Muurolol β-Eudesmol α-Cadinol Pogostol Selin-11-en-4α-ol Intermedeol α-Bisabolol Oxide B epi-β-Bisabolol β-Bisabolol epi -β-Caryophyllene 14-hydroxy-9- Cadalene A Helifolenol Khusinol epi -α-Bisabolol a a a a a a a a b b a a a a a a a a b a a a a a a a a b a a a a a a a a (L) 1668 1600 1656 1652 1675 1622 1674 RI 1670 1658 1613 1642 1640 1600 1638 1619 1636 1582 1683 1613 1679 1618 1632 1674 1590 1627 1630 1638 1644 1671 1651 1649 1636 1592 1595 1586 1640 continued (C) 1659 1601 1660 1654 1677 1625 1678 1671 2 Table RI 1659 1615 1639 1646 1599 1641 1609 1637 1586 1685 1611 1680 1617 1631 1674 1589 1630 1632 1639 1649 1675 1655 1653 1635 1594 1596 1585 1645 Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 8 of 11 0.1 0.2 0.8 0.1 1.4 0.8 0.2 14.6 40.1 33.6 90.5 PG-12 0.1 0.1 0.1 3.4 4.9 2.8 3.8 0.9 3.2 0.6 0.2 20.7 63.5 88.9 PG-11 2.2 0.3 0.4 0.6 2.8 0.8 0.2 51.1 21.3 23.0 99.0 PG-10 0.1 2.6 0.2 0.9 1.0 1.4 3.9 0.5 0.1 26.4 34.3 30.2 95.3 PG-09 4.0 0.1 0.2 0.2 0.7 4.5 0.9 0.1 11.0 28.0 36.5 80.9 PG-08 2.8 0.1 0.1 0.1 0.1 7.8 1.9 0.4 0.2 46.7 31.2 88.0 PG-07 0.1 1.1 8.8 0.8 0.3 PG-06 48.1 18.6 15.9 92.2 0.2 0.2 0.4 6.5 5.6 5.2 1.9 0.4 PG-05 76.9 96.1 0.7 0.2 0.2 4.6 2.7 3.6 4.7 2.4 0.9 45.5 21.1 22.5 96.2 PG-04 0.2 0.1 3.7 1.5 2.1 0.2 7.5 2.1 0.6 54.0 14.0 17.8 95.4 PG-03 0.1 0.1 1.3 2.2 1.9 0.3 3.9 1.8 0.6 61.6 14.6 15.1 97.0 PG-02 0.2 0.4 0.3 0.1 6.6 0.3 0.6 42.9 19.5 21.8 91.1 PG-01 Constituents (%) Constituents α-Bisabolol Acorenone Juniper camphor Eudesm-7(11)-en-4-ol (2 E ,6 Z )-Farnesal (2 Z ,6 E )-Farnesol (2 E ,6 )-Farnesol (2 E ,6 )-Farnesal Xanthorrhizol Isobaeckeol β-Bisabolenal acetate Farnesyl acetate (2 E ,6 )-Farnesyl benzoate Geranyl a a b a a a a a a a a b a a (L) retention time of literature retention 1713 1696 1700 RI 1958 1724 1753 1768 1845 1832 1692 1740 1722 1751 1685 (L) RI continued retention time calculated; ­ time calculated; retention (C) Mondello [ 18 ] Adams [ 20 ] Adams (C)

1714 1696 1698 1962 RI 2 Table 5% Italic: above main constituents RI a b 1722 1757 1767 Monoterpenes hydrocarbons 1843 1841 1692 1741 1721 1751 1687 Oxygenated monoterpenes Oxygenated Sesquiterpene hydrocarbons Oxygenated sesquiterpenes Oxygenated Others Total (%) Total Yield of oil (%) Yield Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 9 of 11

Fig. 2 Dendrogram representing the similarity relation in the oils composition of P. guineense

Fig. 3 Biplot (PCA) resulting from the analysis of the oils of P. guineense composed by the specimens PG-01 to PG-06, collected in Group II Characterized by the presence of the ses- Curuçá (PG -01 to PG-05) and Santarém (PG-06), Pará quiterpenes β-bisabolene (4.0-8.9%) and epi-β-bisabolol state, Brazil, with 49.2% similarity between the samples. (6.5-18.1%), consisting by PG-07 to PG-10 specimens Figueiredo et al. Chemistry Central Journal (2018) 12:52 Page 10 of 11

collected in Monte Alegre (PG-07 and PG-08) and San- Abbreviations HCA: Hierarchical Cluster Analysis; PCA: Principal Component Analysis; GC: tarém (PG-09 and PG-10), Pará State, Brazil, with 50.3% Gas chromatography; GC-MS: Gas chromatography-Mass spectrometry; IAN: similarity between samples. Herbarium of Embrapa Amazônia Oriental; HSTM: Herbarium of Santarém. Group III Characterized by the presence of a signifcant Authors’ contributions content of β-caryophyllene (24.0%) and caryophyllene PLBF participated in the collection and preparation the plants to the herbaria, oxide (14.1%), constituted by the PG-12 specimen, col- run the laboratory work, analyzed the data and contributed to the drafted lected in the city of Ponta de Pedras, Pará state, Brazil, paper. RCS helped with lab work. JKRS guided the lab work and data analysis. CS identifed the plants and managed their introduction in herbaria. RHVM which presented zero% similarity with the other groups. helped with lab work and data analysis. JGSM proposed the work plan, Tus, based on the study of these essential oils, the guided the laboratory work and drafted the manuscript. All authors read and multivariate analysis (PCA and HCA) has suggested approved the fnal manuscript. the existence of three chemical types among the twelve Author details specimens of P. guineense collected in diferent locations 1 Programa de pós‑graduação em Química, Universidade Federal do Pará, 2 of the Brazilian Amazon. It would then be the chemical 66075‑900 Belém, PA, Brazil. Faculdade de Química, Universidade Federal do Pará, Belém, PA, Brazil. 3 Programa de Pós‑Graduação em Biotecnologia, types α-pinene/limonene (Group I), β-bisabolene/epi- Universidade Federal do Pará, Belém, PA, Brazil. 4 Laboratório de Botânica, β-bisabolol (Group II) and β-caryophyllene/caryo- Universidade Federal do Oeste do Pará, Santarém, PA, Brazil. 5 Laboratório de phyllene oxide (Group III). Taking into account that Bioprospecção e Biologia Experimental, Universidade Federal do Oeste do Pará, Santarém, PA, Brazil. two essential oils with a predominance of α-pinene/ limonene and β-bisabolene/epi-β-bisabolol, respectively, Acknowledgements were previously described [14, 15], it is understood The authors would like to thank CAPES, a Brazilian Government’s research funding agency, for its fnancial support. that adding these two chemical types to that one rich in β-caryophyllene + caryophyllene oxide, which was Competing interests a product of this study, besides the other chemical type The authors declare that they have no competing interests. with a high value of spathulenol, before reported by Nas- Ethics approval and consent to participate cimento and colleagues (2018) [16], will be now, at least, Not applicable. four chemical types known for the P. guineense essential oils. Publisher’s Note Several studies have demonstrated the anti- Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional afliations. infammatory activities of limonene, α-pinene and β-caryophyllene, the primary constituents found in the Received: 26 February 2018 Accepted: 30 April 2018 oils of P. guineense presented in this paper. Limonene showed signifcant anti-infammatory efects both in vivo and in vitro, suggesting a benefcial role as a diet supple- ment in reducing infammation [21]; limonene decreased References the infltration of peritoneal exudate leukocytes and 1. Govaerts R, Sobral M, Ashton P, Barrie F, Holst B, Landrum L, Lucas E, reduced the number of polymorphonuclear leukocytes, Matsumoto K, Mazine F, Proença C, Soares-Silva L, Wilson P, Niclughdha E: World checklist of selected plant families – Myrtaceae. 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