Química Nova

Chemical analysis of essential oils on Piper species from

Colombian Amazon

Journal: Química Nova

Manuscript ID Draft

Manuscript Type: Original Article

Fo

Date Submitted by the

n/a
Author:
rR

Complete List of Authors: Vargas Gallego, Juan Camilo; Universidad de Nariño, Departamento de
química
Arturo Perdomo, David; Universidad de Narino
Maldonado Rodriguez, Jhon; Universidad de la Amazonia
ev

Centeno Betanzos, Lucia; Universidad Nacional Autonoma de Mexico

Correa, Marco; Universidad de la Amazonia

Keyword: Piper, chemotype, essential oil, hydrodistillation, GC/MS

iew

Please, specify if the

submission is for a Regular Regular Issue
Issue or Special Issue:
On
ly

https://mc04.manuscriptcentral.com/qn-scielo
Page 1 of 13 Química Nova

1
2
3 GRAPHICAL ABSTRACT
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
Fo

22
23
24
rR

25
26
27
28
ev

29
30
31
iew

32
33 Chemical profile of essential oil of five Piper species from southeastern of Colombia was carried
34
35 out by hydrodistillation and GC/MS analysis and new chemotypes was obtained
36
On

37
38
39
40
ly

41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
1

https://mc04.manuscriptcentral.com/qn-scielo
 Química Nova Page 2 of 13

1
2
3 Chemical analysis of essential oils on Piper species from Colombian Amazon
4
5
6
7 Juan Camilo Vargas Gallegoa,*,, David Arturo Perdomoa, Jhon Ironzi Maldonado
8
Rodriguezb, Lucía Yoselina Centeno Betanzosc and Marco Aurelio Correa Múnerad
9
10
11
aDepartamento de química, Universidad de Nariño, Pasto, Nariño; bDepartamento de química,
12
13
14 Universidad de la Amazonía, Florencia, Caquetá; cInstituto de Ecología, Universidad Nacional
15 Autónoma de México, Ciudad de México; México. d Departamento de biología, Universidad de la
16
17 Amazonía, Florencia, Caquetá.
18
19
20
21
( ) Manuscript with supplementary material
Fo

22 (x) Manuscript without additional material

23
24
rR

25
26 *e-mail: camilovargas@udenar.edu.co
27
28
ev

29
30
31
iew

32
33
34
35
36
On

37
38
39
40
ly

41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
2

https://mc04.manuscriptcentral.com/qn-scielo
Page 3 of 13 Química Nova

1
2
3 Piper included many species and a broad range of applications, for this reason, the essential oils of
4
5 five species from Caquetá Colombia were analysed by GC-MS and their phytochemical profile
6
7 were established as follows: monoterpene/sesquiterpene chemotype (α-pinene, β-
8
pinene/spathulenol, β-eudesmol) in P. soledadense, sesquiterpene chemotype in three species;
9
10 germacrene D and β-bisabolene in P. tuberculatum, (E)-caryophyllene and germacrene D in P.
11
12 peltatum, (E)-nerolidol, bicyclogermacrene, and β-elemene in P.crasinervium and phenylpropanoid
13
14 type (dillapiole) in P. aduncum. The yield in oils varied between 0.04% - 1.01% w/w, new
15 chemotypes in Piper species and the first chemical reports of Piper soledadense were described.
16
17
18
19 Keywords: Piper; chemotype; essential oil; hydrodistillation; GC/MS.
20
21
Fo

22
23
24
rR

25
26
27
28
ev

29
30
31
iew

32
33
34
35
36
On

37
38
39
40
ly

41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
3

https://mc04.manuscriptcentral.com/qn-scielo
 Química Nova Page 4 of 13

1
2
3 INTRODUCTION
4
5
6
Caquetá has great biodiversity due to its geographical position; it is in the southeast of Colombia, in
7 the North of this region has places since 3000 m with Andean and sub-Andean forest vegetation and
8
9 the middle and south region the predominant Amazon planes cross with high number of hydric
10
11 sources as the Caquetá, Apaporis, Orteguaza and Yarí rivers.1 One of the plant families with great
12 diversity in this area is Piperaceae, with five genera, amongst them Piper, which contains more than
13
14 1800 species in America and more than 400 species in Colombia2 of the latter more than 50 have
15
16 been described for Caquetá3-7 this stimulates research of Colombian biodiversity because very few
17
18
phytochemical studies have been carried out about this genus in the southeastern region of the
19 country, especially of essential oils.
20
21 Due to difficulties in accessing hospital centres because of the large distances or poor roads, the use
Fo

22
23 of medicinal plants has become a crucial resource for the communities.8 Several reports indicate that
24
some indigenous communities or common people make traditional use of plants of the Piperaceae
rR

25
26 family.9-11 Such is the case of the Coreguaje community in the municipality of Milan-Caquetá, in
27
28 which three species of the Piper genus (P. peltatum, P. bredemeyeri, and P. sp) and two species of
ev

29
30 the Peperomia genus (P. macrostachya and P. rotundifolia), are used with medicinal properties12.
31 Another study presents 13 plants of the Piper genus used by the indigenous communities of Caquetá
iew

32
33 such as the Embera-Katio, Coreguaje, and Uitoto. Of these plants, it is worth mentioning that Piper
34
35 peltatum and Piper tricuspe are used for snake bites.13
36
Some reports of biological properties and chemical profile of Piper essential oils from the Amazon
On

37
38 region have been established,14-16 however in Colombia, in this geographic area, very few works have
39
40 been published despite its medicinal uses.
ly

41
42 Thus, the aim of this research was determinate the chemical profile of the essential oil of five
43
Piperaceae species as a contribution to the systematic study of the volatile compounds of the genus
44
45 Piper from Caquetá in the Colombian Amazon, a region very low studied since chemical point of
46
47 view despite its high biodiversity.
48
49
50 EXPERIMENTAL PART
51
52
53
54
Reagents
55 Sodium sulphate and dichloromethane were purchased from Panreac (Barcelona, Spain), standards
56
57 of n-alkanes mixture (C7- C30) were purchased from Sigma-Aldrich (St. Louis USA).
58
59
60
4

https://mc04.manuscriptcentral.com/qn-scielo
Page 5 of 13 Química Nova

1
2
3 Plant material
4
5 The species P. aduncum L. (1° 36’ 21” N - 75 36’ 28” W), P. tuberculatum Jacq. (1° 36’ 29” N – 75°
6
7 36’ 21” W) and P. peltatum L. (1° 36’ 22” N – 75° 36’ 28” W) were collected in the department of
8
Caquetá between April and June 2017, inside the central campus, while P. crassinervium Kunth (1°
9
10 37’ N – 75° 36’ W) and Piper soledadense Trel. (1° 29’ 59.8” N - 75° 39’ 22.6” W) in September of
11
12 the same year at the Macagual campus, both in the University of the Amazonia. A voucher of each
13
14 species was left in the Herbarium of the University of the Amazonia and identified with codes 1939,
15 14682, 1041, 15275, and 6175, respectively.
16
17
18
19 Extraction
20
21
The plant material was dried at room temperature (100 g of leaves), ground manually and
Fo

22 extracted by Clevenger hydrodistillation apparatus for three hours with 1.2 L of deionised
23
24 water in a 2L flask. The essential oil was dried with anhydrous sodium sulphate and kept
rR

25
26 refrigerated on an amber glass vial until analysis. The procedure was realised for once due to
27
availability of plant material. The yields were calculated in dry basis (%w/w).
28
ev

29
30
31 GC/MS essential oils analysis
iew

32
33 Gas chromatography analysis was done on Shimadzu GC-MS QP 2010S chromatograph and mass
34
35
spectrometer. It was used a SHRXi-5MS column (30m x 0.25 mm x 0.25μm), helium UAP as the
36 carrier gas, injection volume was 1μL and injector temperature was 250°C on split mode 1:50, the
On

37
38 oven temperature was programmed as follows: 40°C x 5 min, then increased to 250°C in rates of
39
40 5°C/min, then 250°C x15 min, interface temperature was 280°C. Mass spectra were recorded to 70
ly

41
e-V, in full scan mode 40 – 400 uma and EI ionisation mode. The experimental spectra were
42
43 compared with NIST and Wiley Library. The retention index was calculated as follows:17,18
44
45 RI = 100*Pz + 100*[(RT(x) - RT(Pz))/ (RT(Pz+1) - RT(Pz))] see table 1.
46
47
48 RESULTS AND DISCUSSION
49
50
51 Chemical profiles were found with variability in the content of sesquiterpene compounds, but these
52
53 being predominant in four species P. crassinervium, P. peltatum, P. tuberculatum, and P.
54
55
soledadense, 84.6%, 76.0%, 66.6% and 55.7% respectively, although in the last the majority
56 compounds were monoterpenoids, while the profile of P. aduncum presented a phenylpropanoid
57
58 (dillapiole) with more than 60% of the essential oil. The yields (w/w) were very variable finding
59
60
5

https://mc04.manuscriptcentral.com/qn-scielo
 Química Nova Page 6 of 13

1
2
3 values in P. peltatum with 0.04% and P. crassinervium with 0.06%, 0.29% in P. tuberculatum, 0.40%
4
5 in P. soledadense, and 1.01% in P aduncum (see Table 1).
6
7
8
9 Table 1. Chemical profile of Piper species of dry leaves from Caquetá
10
11
12
Compounds RI* RI1** RI2** P.a P.c P.p P.s P.t
13
14 2-E-hexenal 857 846 853.0 - 0.1 - - -
15 α-pinene 937 932 936.2 0.6 4.0 3.0 19.3 4.7
16 Camphene 952 946 950.3 - 0.3 1.5 1.0 -
17 Sabinene 978 969 973.0 - - - - 0.5
18 β-pinene 980 974 977.7 2.1 1.0 1.2 13.2 4.2
19
20
β-myrcene 997 974 977.7 - 0.2 0.4 0.8 0.4
21 α-phellandrene 1010 1002 1004.0 0.4 - - - 0.7
Fo

22 δ-3-carene 1020 1008 1011.3 - - 0.9 - -

23 Limonene 1037 1024 1029,5 - 0.1 5.4 1.6 1.3
24 β-(Z)-ocimene 1046 1032 1037.8 3.1 - - - 0.8
rR

25
β-(E)-ocimene 1057 1044 1047.7 6.4 - - - 8.5
26
27 Terpinolene 1096 1086 1086.9 0.2 - - - -
28 Linalool 1116 1095 1099.0 0.4 0.4 - - -
ev

29 3-Z-Hexenyl tiglate 1334 1319 - - 0.1 - - -

30 δ-elemene 1353 1335 1337.0 0.2 1.7 - 1.1 -
31 α-cubebene 1364 1345 1351.4 - 0.2 0.4 - -
iew

32
33
α-ylangene 1392 1373 1369.9 0.3 - - - -
34 α-copaene 1394 1374 1376.2 - 0.6 1.3 - 1.9
35 β-bourbonene 1404 1387 1384.2 - - - - 1.0
36 β-elemene 1411 1389 1390.4 - 15.7 - 1.2 2.7
On

37 α-gurjunene 1430 1409 1408.6 - - - -

38
(E)-cariophyllene 1443 1417 1420.1 5.0 10.7 29.8 6.0 2.6
39
40 Alloaromadendrene 1464 1458 1459.9 - 0.9 - - -
Geranyl acetone 1467 1453 1451.8 - - 0.7 - -
ly

41
42 (E)-β-farnesene 1471 1454 1455.9 - - - - 0.7
43 Linalool isovalerate 1477 1466 - 0.8 - - - -
44 α-humulene 1481 1452 1453.1 - 2.7 3.2 2.4 1.4
45
46
Germacrene D 1508 1484 1480.6 4.2 9.4 21.4 4.3 18.3
47 β-selinene 1512 1489 1486.1 0.9 - - - -
48 α-selinene 1516 1498 1493.4 - - - - 0.7
49 Bicyclogermacrene 1524 1500 1494.1 - 18.3 7.6 3.3 5.4
50 β-bisabolene 1531 1505 1508.4 - - - - 17.2
51
Germacrene A 1536 1508 1502.1 - 0.6 - - -
52
53 δ-cadinene 1547 1522 1523.2 - 1.6 0.9 1.3 5.8
54 Hedycaryol 1582 1543 - - - - - 2.4
55 (E)-nerolidol 1589 1561 1560.9 - 20.7 4.7 - 4.1
56 Germacrene D-4-ol 1612 1574 1574.2 - - - - 1.3
57 Spathulenol 1618 1577 1576.4 - 1.4 - 11.8 1.1
58
59 Caryophyllene oxide 1620 1582 1580.6 - - 6.2 - -
60 Viridiflorol 1633 1598 1590.8 4.4 - - - -
6

https://mc04.manuscriptcentral.com/qn-scielo
Page 7 of 13 Química Nova

1
2
3 Ledol 1638 1602 1608 - - - 2.2 -
4
Dillapiole 1660 1620 1621.7 64.4 - - - -
5
6 Alloaromadendrene 1661 1639 1636 - - - 8.7 -
7 epoxide
8 α-cadinol 1679 1652 1651.9 0.4 - 0.5 - 1.1
9 β-eudesmol 1698 1652 1651.9 - - - 11.2 7.8
10 Bulnesol 1704 1670 1665.7 - - - 2.2 0.4
11
12
Monoterpenoids - - - 13.2 6.0 12.4 35.9 21.1
13 Sesquiterpenoids - - - 16.2 84.5 76.0 55.7 71.8
14 Phenylpropanoids - - - 64.4 - - - -
15 Others - - - - 0.2 0.7 - -
16 Total identified - - - 93.8 90.7 89.1 91.6 92.9
17
18
% w/w oil yield - - - 1.01 0.06 0.04 0.40 0.29
19 *RI: Retention Index SHRXi-5MS column.
20 **RI1 ADAMS 17 and RI2 NIST 18.
21 P.a: Piper aduncum, P.c: Piper crassinervium, P.p: Piper peltatum, P.s: Piper soledadense, P.t: Piper
Fo

tuberculatum.
22
23
24
rR

25 Piper soledadense essential oil was constituted by a mixture of sesquiterpenoids (55.7%) and
26
27 monoterpenoids (35.9%), α-pinene (19.3%) and β-pinene (13.2%) were the majority compounds in
28
ev

the oil. Oxygenated sesquiterpenoids as spathulenol (11.8%), β-eudesmol (11.2%) and

29
30 alloaromadendrene epoxide (8.7%) were the representative volatile compounds in sesquiterpenoids
31
iew

32 mixture with 31.7% (see Figure 1). Previous reports on some Piper species showed profiles with α-
33
34 pinene and β-pinene as principal monoterpenoids and higher content of sesquiterpenoids. P hispidum
35 from Venezuela19 with α-pinene (15.3%), β-pinene (14.8%) as major compounds and relation of
36
On

37 monoterpenoids/sesquiterpenoids 41.4/58.6, Piper crassinervium from Brazil20 had a volatile profile

38
39 with α-pinene (11.5%), β-pinene (11.6%) as major constituents, however non-oxygenated
40
sesquiterpenoids predominated in both species. Piper anonofolium from Brazilian Amazon had a
ly

41
42 chemical profile enriched in monoterpenoids, α-pinene (40.9-53.1%), β-pinene (17.2 -22.9%)
43
44 however low sesquiterpenoid content was shown.21
45
46 To our knowledge, this is the first report of the chemical profile of Piper soledadense, obtained from
47 Amazonia, which allows us to know the biodiversity of south-eastern Colombia.
48
49
50
51 In P. peltatum essential oil was possible to identify 89% of the components of which 76% corresponds
52
53
to sesquiterpenes (see Table 1), however, two of them account for a little more than 50% (E)-
54 caryophyllene (29.8%), germacrene D (21.4%) (see Figure 1). These two compounds with
55
56 bicyclogermacrene (7.6%), caryophyllene oxide (6.2%), and limonene (5.4%) are a new chemotype
57
58 in this species.
59
60
7

https://mc04.manuscriptcentral.com/qn-scielo
 Química Nova Page 8 of 13

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
Fo

22
23
24
rR

25
26
27
28
ev

29
30
31
iew

32
33
34
35
36
On

37
38
39
Figure 1. Chromatograms of essential oils of Piper from Caquetá
40
ly

41
42 Two previous studies of P. peltatum have described chemical profiles also enriched in sesquiterpenes.
43
44 On one hand, Photomorphe peltata collected in Cuba22 showed a mixture with caryophyllene oxide
45
46 (22.9%), spathulenol (9.0%), trans-calamannene (5.4%) and α-copaene (5.2%). In that case, the
47
leaves were dried as in our work but with a longer extraction time (5h) and a yield of 0.1%, while in
48
49 P. peltata collected in Brazil23 a profile with β-caryophyllene (68.0%), germacrene D (6.2%), α-
50
51 humulene (5.9%), and (E)-nerolidol (4.9%) with the same yield (0.1%) was obtained, however in this
52
53 study, the extraction was performed of fresh leaves. In the work conducted in Brazil, most
54 components were found as those found in our study, maybe because both plants were collected in the
55
56 Amazon region with similar environmental conditions in the two countries.
57
58
59 Alternatively, the essential oil of P. tuberculatum presented a chemotype, germacrene D (18.3%), β-
60
8

https://mc04.manuscriptcentral.com/qn-scielo
Page 9 of 13 Química Nova

1
2
3 bisabolene (17.2%), β-(E)-ocimene (8.5%) and β-eudesmol (7.8%) (see Figure 1), showing mainly
4
5 sesquiterpenes (see Table 1) in contrast to other reported studies. At least four studies in Brazil of
6
7 leaves of this species show chemotype (E)-caryophyllene, with values between 26% and 45% of the
8
essential oil;24-27 however, only one was performed using dried leaves obtaining a yield of 0.8%,
9
10 higher than that obtained in our study, containing a mixture of the sesquiterpenes (E)-caryophyllene
11
12 (40.2%), β-farnesene (8.3%) and the monoterpenes α and β-pinene (10.4% and 12.5%), and (E)-
13
14 ocimene (8.5%), which differs from the data reported in our work.
15
16 Another study on P. tuberculatum in Brazil28 reports a profile with germacrene D as the major
17
18 component, with chemotype germacrene D/isocaryophyllene/germacrene B; however, given the
19
20 geographical differences, the characteristics of the material collected (fresh leaves) and the shorter
21
Fo

22
extraction time, it does not allow us to make a comparison with our species studied, concerning to oil
23 yield and chemical profile.
24
rR

25
26 In Colombia, there are few studies on the content of essential oil in dry leaves for this species and
27
28 works with the chemical profile germacrene D/β-bisabolene have not yet been reported, which allows
ev

29
us to speak of a new chemotype for the species P. tuberculatum in the Colombian Amazon region.
30
31
iew

32 Piper aduncum is a species with a wide distribution in the world, it can present a varied volatile
33
34 profile with more than seven chemotypes.29,30 In the Amazon, the dillapiole chemotype is one widely
35
36 reported. In Ecuador, for example, values between 45% and 48 % of this metabolite are
On

37 characteristic31,32 while in Brazil the values are wider between 31% and 97%,33,34 being Belen species
38
39 with closest values to those found for the species in this study (see Figure 1), and yields like those of
40
the Brazilian species, above 1%. Few differences between the monoterpenoid/sesquiterpenoid
ly

41
42
43
content can be shown, similar content in those from Colombia (13.2/16.5%) with viridiflorol and
44 (17.7/13.7%) plus piperitone and bicyclogermacrene from Brazil. In other countries of the Amazon
45
46 region, some studies show different chemotypes such as the asarone in Peru35 and 1,8- cineol in
47
48 Bolivia36 (see Table 2).
49
50
51
52
53
54
55
56
57
58
59
60
9

https://mc04.manuscriptcentral.com/qn-scielo
 Química Nova Page 10 of 13

1
2
3 Table 2. P. aduncum profiles from different Amazonia countries
4
5
6
P.aduncum Caquetá - Belen - Ecuador Brazil (different Loreto - Bolivia
7 compounds Colombia Brazil (Dry (Dry amazon regions Perú (Dry
8 (%) (Dry aerial parts) aerial - dry aerial (Dry leaves)
9 leaves) 35 parts) 32 parts) 34 leaves) 36 37
10
Dillapiole 62.2 64.4 45.9 31.5 - 97.3 - -
11
12 β-(E)-ocimene 6.4 3.0 10.4 0.3 - 2.5 2.3 6.4
13 (E)-cariophyllene 5.0 2.5 2.6 0.3 - 3.5 2.8 0.8
14 Viridiflorol 4.4 - - - - -
15
Germacrene D 4.2 2.7 - 0.1 - 2.8 7.5 0.9
16
17 Piperitone - 3.3 8.5 1.6 - 15.1 - -
18 β-(Z)-ocimene 3.1 1.5 2.2 0.1 - 1.3 - 2.4
19 Asarone - - - - 39.3 -
20
Bicyclogermacrene - 2.0 1.5 0.3 - 0.8 5.9 3.8
21
Fo

22 Methyl eugenol - - - - 12.9

23 1,8-cineol - - 1.3 - - 42.5
24 α-pinene 0.6 1.2 1.4 0.3 - 4.6 - 8.9
rR

25
β-pinene 2.1 1.5 1.3 0.2 - 2.1 1.3 7.0
26
27 Essential oil yield 1.0 1.2 0.8 1.2 - 3.3 1.1 0.7
28 (%)
ev

29
30
31
iew

32
Piper crassinervium presented a profile with 85.5 % of sesquiterpenes, amongst which there were
33 oxygenated and non-oxygenated compounds in a 1:2 ratio. Amongst the oxygenated sesquiterpenes,
34
35 (E)-nerolidol (20.7%) was found, this metabolite being the major component of the essential oil of P.
36
crassinervium. Among the non-oxygenated sesquiterpenes, several compounds were found,
On

37
38
bicyclogermacrene (18.3 %), β-elemene (15.7 %), (E)-caryophyllene (10.7 %), germacrene D (9.4
39
40 %), which together correspond to 54.1 % of the essential oil, which means that these five
ly

41
42 sesquiterpenes mentioned here between oxygenated and non-oxygenated are equivalent to more than
43
44 70 % of the essential oil of P. crassinervium (see Figure 1).
45 Several studies on P. crassinervium volatile compounds have been reported, but few have been
46
47 performed on a dry basis. One of them conducted in Brazil 28 also presented a profile with
48
49 sesquiterpenes, however, the majority of compounds showed a 1:1 ratio between oxygenated/non-
50
51
oxygenated sesquiterpenes, such as β-eudesmol (10.1%), spathulenol (9.8%), (E)-nerolidol (8.2%)
52 equivalent to 28.1% of the essential oil and germacrene D (14.0%), β-caryophyllene (8.1%),
53
54 bicyclogermacrene (9.2%) equivalent to 31.3% of the essential oil, being this different from that
55
56 found in this study. Another study of the same species on a dry basis also carried out in Brazil 20
57
presented a chemotype different from the previous one and the one reported here, being the majority
58
59 compounds of monoterpene type such as α-pinene (11.5%), and β-pinene (11.6%).
60
10

https://mc04.manuscriptcentral.com/qn-scielo
Page 11 of 13 Química Nova

1
2
3
4
5 CONCLUSIONS
6
7 The chemical profile of the essential oils of five species of the Piper genus from south-eastern
8
Colombia in the Amazon region is described for the first time, which allowed the determination of
9
10 two new chemotypes in P. peltatum and P. tuberculatum, a phenylpropanoid chemotype in P.
11
12 aduncum agreed with previous studies from Amazonia, and non-oxygenated sesquiterpenes profile
13
14 in P. crassinervium, and the first report of Piper soledadense volatile profile. This work is important
15 as a contribution to the systematic chemical study of Piper genus in the Colombian Amazon,
16
17 particularly in Caquetá a rich area in its species.
18
19
20
21
Fo

22 ACKNOWLEDGEMENTS
23
24 We give our most sincere thanks to the University of Nariño and the University of the Amazonia for
rR

25
26 all support provided for the realisation of this work, and W. Trujillo for providing the photos of P.
27
soledadense and P crassinervium in graphical abstract.
28
ev

29
30
31 REFERENCES
iew

32
33
34 1. Barrera, J.; Constantino, E.; Espinosa, J.; Hernández, O.; Naranjo, L.; Niño, I.; Polanco, R.;
35 Restrepo, J.; Revelo, J.; Salazar, C.; et al; Escenario de conservación en el piedemonte
36
On

37 Andino – Amazónico de Colombia. Chapter 4: Parques Nacionales – Instituto Alexander

38
39 Von Humboldt, 2007. [Accessed 2021 May 30].
40
http://repository.humboldt.org.co/handle/20.500.11761/33651. Spanish.
ly

41
42 2. Ulloa, C.; Acevedo, P.; Beck, S.; Belgrano, M.; Bernal, R.; Berry, P.; Brako, L.; Celis, M.;
43
44 Davidse, G.; Forzza, R.; et al. Sci. 2017, 358, 1614. [DOI: 10.1126/science.aao0398]
45
46 3. Trujillo, W. Rev. Colomb. Amazon. 2013, 6, 111. Spanish.
47 4. Trujillo, W.; Hoyos, F; Momentos de Cienc. 2013, 10(2), 88. Spanish.
48
49 5. Trujillo, W., Jaramillo, A. Phytotaxa 2019, 408(1), 59. [DOI:
50
51 https://doi.org/10.11646/phytotaxa.408.1.4]
52
53
6. Trujillo, W.; Jaramillo, A; Brittonia 2021, 73, 67.
54 7. Trujillo, W; Rapid color guide #370. Version 1, 2014. [Accessed 2021 Jul 24].
55
56 https://fieldguides.fieldmuseum.org/sites/default/files/rapid-color-guides-pdfs/370.pdf.
57
58 8. Orozco, M.; Caballero, K.; Stashenko, E.; Olivero, J; J. Essent. Oil Bear. Plants 2019.
59
22(1), 18. [https://doi.org/10.1080/0972060X.2019.1585966]
60
11

https://mc04.manuscriptcentral.com/qn-scielo
 Química Nova Page 12 of 13

1
2
3 9. Marques, A.; Peixoto, A.; de Paula, R.; Nascimento, M.; Soares, L.; Velozo, L.; Guimarães,
4
5 E.; Kaplan, M; J. Essent. Oil Bear. Plants 2015. 18(1), 74.
6
7 [https://doi.org/10.1080/0972060X.2014.974075]
8
10. Thin, D.; Chinh, H.; Luong, N.; Hoi, T.; Dai, D.; Ogunwande, I.; J. Essent. Oil Bear. Plants
9
10 2018, 21(1), 181. [https://doi.org/10.1080/0972060X.2018.1424040]
11
12 11. Wu, X.; Chen, M.; Wang, Y.; Yu, S.; Xia, Y.; Dong, C.; Hou, Z.; Cao, Y; J. Essent oil Bear.
13
14 Plants 2021, 24(1), 86. [https://doi.org/10.1080/0972060X.2021.1886997]
15 12. Trujillo, W.; Correa, M; Caldasia 2010, 32(1), 1. Spanish.
16
17 13. Trujillo, W.; Gonzalez, V; Mundo Amazon. 2011, 2, 283. Spanish.
18
19 14. Souza, A., Lisboa, R., Marçal, M., Bichara, M. J. Essent oil Bear. Plants. 2010, 13(3), 347.
20
21
[https://doi.org/10.1080/0972060X.2010.10643833]
Fo

22 15. Conçalves, R., dos Santos, V., Guidi, L., Miller, A., Maia, G., Cavalante, A., Takeara, R. J.
23
24 Essent Oil Bear. Plants 2019, 22(3), 811. [https://doi.org/10.1080/0972060X.2019.1631720]
rR

25
26 16. Majolo, C., Castro, P., Praia, A., Maia, F., Ervatti, P., Ribeiro, H., Campos, E. J. Essent oil
27
Bear. Plants 2019, 22(3), 746. [https://doi.org/10.1080/0972060X.2019.1645047]
28
ev

29 17. Adams R. P; Identification of essential oil components by gas chromatography/ mass

30
31 spectrometry, 4th ed., Allured Publishing Corporation: Carol stream, 2007.
iew

32
33 18. Babushok, V; Linstrom, P; Zenkevich, I; NIST. J Phys Chem Ref data 2011, 40(4), 1.
34 19. Morales, A.; Rojas, J.; Moujir, L.; Araujo, L.; Rondón, M; J Appl. Pharm. Sci. 2013, 3(6),
35
36 16- [DOI: 10.7324/JAPS.2013.3603]
On

37
38 20. Perigo, C.; Torres, R.; Bernacci, L.; Guimaraes, E.; Haber, L.; Facanali, R.; Vieira, M.;
39
40
Quecini, V.; Ortiz, M; Ind. Crops Prod. 2016, 94, 518.
ly

41 [https://doi.org/10.1016/j.indcrop.2016.09.028]
42
43 21. Andrade, E.; Ribeiro, A.; Guimarães, E.; Maia J; J. Essent Oil Bear. Plants 2005, 8(3), 289.
44
45 [https://doi.org/10.1080/0972060X.2005.10662140]
46 22. Pino, J.; Marbot, R.; Bello, A.; Urquiola, A; J. Essent. oil Res. 2004, 16, 124.
47
48 [https://doi.org/10.1080/10412905.2004.9698670]
49
50 23. Moraes, M.; Machado, S.; Ortiz, M; Journal Essent oil Res. 2004, 16, 15.
51
52
[https://doi.org/10.1080/10412905.2004.9698670]
53 24. Cysne, J.; Canuto, K.; Pessoa, O.; Nunes, E.; Silveira, E; J. Braz. Chem. Soc. 2005, 16,
54
55 1378. [https://doi.org/10.1590/S0103-50532005000800012]
56
57 25. Facundo, V.; de Morais, S; J. Essent. Oil Res. 2005, 17, 304.
58
[https://doi.org/10.1080/10412905.2005.9698910]
59
60
12

https://mc04.manuscriptcentral.com/qn-scielo
Page 13 of 13 Química Nova

1
2
3 26. Debonsi, H.; Morandim, A.; Marques, M.; Young, M.; Kato, M; Quím. Nova 2006, 29(3),
4
5 467. [https://doi.org/10.1590/S0100-40422006000300012]
6
7 27. Lavor, P.; Santiago, G.; da Silva, R.; de Sousa, L.; Bezerra, G.; Romero, N.; Arriaga, A.;
8
Lemos, T.; Alves, P.; Gomes, P; Nat. Prod. Commun. 2012, 7(10), 1391.
9
10 28. Morandim, A.; Pin, A.; Santo, A.; de Oliveira, H.; Soares, M.; Alecio, A.; Kato, M.; de
11
12 Oliveira, J.; Furlan, M; J. Med. Plants Res. 2010, 4(17), 1810.
13
14 29. da silva, J.; Trindade, R.; Alves, N.; Figueiredo, P.; Maia, J.; Setzer, W; Int. J. Mol. Sci.
15 2017, 18, 2571. [https://doi.org/10.3390/ijms18122571]
16
17 30. Salehi, B.; Zakaria, Z.; Gyawali, R.; Ibrahim, S.; Rajkovic, J.; Shinwari, Z.; Khan, T.;
18
19 Sharifi-Rad, J.; Ozleyen, A.; Turkdonmez, E.; et al; Mol. 2019, 24, 1364.
20
21
[https://doi.org/10.3390/molecules24071364]
Fo

22 31. Guerrini, A.; Sacchetti G.; Rosi, D.; Paganetto, G.; Muzzoli, M.; Andreotti, E.; Tognolini,
23
24 M.; Maldonado, M.; Bruni, R.; Environ. Toxicol. Pharmacol. 2009, 27, 39.
rR

25
26 [https://doi.org/10.1016/j.etap.2008.08.002]
27
32. Radice, M.; Pietrantoni, A.; Guerrini, A.; Tachini, M.; Sacchetti, G.; Chiurato, M.; Venturi,
28
ev

29 G.; Fortuna, C; Plant Biosyst - Int J Deal Asp. Plant Biol. 2018, 153(3), 1.
30
31 [https://doi.org/10.1080/11263504.2018.1478902]
iew

32
33 33. Maia, J.; Zohhbi, M.; Andrade, E.; Santos, A.; da Silva, M.; Luz, A.; Bastos, C; Flavour
34 Fragr. J. 1998, 13, 269. [https://doi.org/10.1002/(SICI)1099-
35
36 1026(1998070)13:4%3C269::AID-FFJ744%3E3.0.CO;2-A]
On

37
38 34. Souto, E.; Harada, A.; Andrade, E.; Maia, J; Neotrop Entomol. 2012, 41(6), 510.
39
40
35. Ingaroca, S.; Castro, A.; Ramos, N;. Rev. Soc. Quím. Perú. 2019, 82(2), 268.
ly

41 36. Lopez J.; Collin G.; Garneau, F.; Jean, F.; Gagnon, H; J. Essent. Oil Bear. Plants. 2008,
42
43 11(1), 53. [https://doi.org/10.1080/0972060X.2008.10643597]
44
45
46
47
48
49
50
51
52 (keep this figure at the very end of the last page)
53
54
55
56
57
58
59
60
13

https://mc04.manuscriptcentral.com/qn-scielo