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. 2019 Oct 27;24(21):3871. doi: 10.3390/molecules24213871

Chemical Compositions and Mosquito Larvicidal Activities of Essential Oils from Piper Species Growing Wild in Central Vietnam

Le Thi Huong 1, Nguyen Huy Hung 2,*, Do Ngoc Dai 3, Thieu Anh Tai 4, Vu Thi Hien 5, Prabodh Satyal 6, William N Setzer 6,7,*
Editor: Josphat Matasyoh
PMCID: PMC6864731  PMID: 31717867

Abstract

Mosquitoes are the deadliest animals on earth and are the vectors of several neglected tropical diseases. Recently, essential oils have emerged as potential renewable, cost-effective, and environmentally benign alternatives to synthetic pesticides for control of mosquitoes. In this work, thirteen species of Piper were collected from different areas of central Vietnam. The essential oils were obtained by hydrodistillation and analyzed by gas chromatography–mass spectrometry. The essential oils were screened for mosquito larvicidal activity against Aedes aegypti. Four of the Piper essential oils showed outstanding larvicidal activity against Ae. aegypti, namely P. caninum, P. longum, P. montium, and P. mutabile, with LC50 and LC90 values less than 10 µg/mL. Multivariate analysis has correlated concentrations of β-caryophyllene, β-bisabolene, α-pinene, and β-pinene with mosquito larvicidal activity.

Keywords: piperaceae, mosquito-borne diseases, natural pest control

1. Introduction

The genus Piper is the largest in the Piperaceae and is made up of around 1050 species, many of which are important in traditional medicine and as culinary spices [1]. For example, P. nigrum (black pepper) fruit is the most consumed spice in the world, P. longum (long pepper) fruiting spikes are used similarly, P. methysticum (kava) root is used to produce an intoxicating herbal medicine, P. betle (betel) leaves are used to wrap areca (Areca catechu) nuts or tobacco (Nicotiana spp.) for chewing, and P. cubeba (cubeb) fruits are used to produce an essential oil [2]. The genus has shown high ethnobotanical utility worldwide and is of interest to a variety of fields and industries, including pharmaceutical botany, traditional medicine, aromatic industries, foods, and landscaping [3,4]. In Vietnam, there are about 45 species of Piper [5].

Mosquitoes have been and continue to be the deadliest animals on earth and are responsible for several of the world’s deadliest diseases, including malaria, yellow fever, dengue, filariasis, and many others [6]. Mosquito-borne infectious diseases have also been a constant problem in Vietnam. Dengue fever and dengue hemorrhagic fever are especially problematic and chikungunya fever is an emerging threat in the country [7,8]. Aedes aegypti (L.), the yellow fever mosquito, is an important vector of viral diseases including yellow fever [9], dengue [10], chikungunya [11], Zika [12], as well as others. Aedes albopictus (Skuse) (Diptera: Culicidae), the Asian tiger mosquito, is also an important vector of several viral pathogens, including dengue fever virus [13], yellow fever virus [14], chikungunya fever virus [15], and possibly Zika virus [16]. Culex quinquefasciatus Say (Diptera: Culicidae), the southern house mosquito, is a vector of lymphatic filariasis [17] as well as several arboviruses such as West Nile virus and St. Louis encephalitis virus [18], and possibly Zika virus [19].

There is a need for complementary vector control methods for controlling the spread of mosquito-borne diseases; resistance to synthetic insecticides is increasing worldwide [20,21,22,23,24], and the deleterious impacts of synthetic insecticides to the environment have been a major problem for many years [25,26]. Essential oils may provide environmentally safe and renewable alternatives to synthetic insecticides for mosquito control [27,28,29,30,31]. In this work, we present the essential oil compositions and mosquito larvicidal activities of several species of Piper growing wild in central Vietnam [32,33]:

Piper arboricola C. DC. (syn. Piper kadsura (Choisy) Ohwi, Piper futokadsura Siebold, Piper subglaucescens C. DC., local Vietnamese name Tiêu thượng mộc, is an understory liana native to China and Taiwan. In Vietnam, P. arboricola is found in Hà Tĩnh (Vũ Quang National Park), Thừa Thiên Huế Pro (Nam Đông District), and Lâm Đồng Province (Đà Lạt City: Đatanla).

Piper bavinum C. DC., local Vietnamese name Tiêu ba vì, is an understory climber found in China. In Vietnam, P. bavinum is found in Hà Nội City (Ba vì: Cốc Village) and Kon Tum Province.

Piper cambodianum P. Fourn. is found in Vietnam in Nghệ An, Đà Nẵng, and Ninh Thuận Provinces.

Piper caninum C. DC., Vietnamese name Tiêu chó, ranges from India, through Thailand, Malaysia, and Indonesia. In Vietnam, P. caninum is found in Kon Tum Province (Đác Tung).

Piper longum L., Vietnamese names Tiêu lá tím, Tất bạt, Tiêu dài, Tiêu lốt, and Trầu không dại, is an understory liana, which is distributed throughout India, China, Malaysia, Nepal, and Sri Lanka, as well as Vietnam.

Piper mekongense C. DC. (syn. Piper polysyphonum C. DC.), Vietnamese name Tiêu cửu long, is an understory shrub found in Laos, Cambodia, as well as Kon Tum province, Vietnam.

Piper montium C. DC., Vietnamese name Tiêu núi, is an understory climber. In Vietnam, the plant is found in Ninh Bình and Kon Tum provinces.

Piper mutabile C. DC., Vietnamese names Tiêu biến thể, Trầu biến thể, and Mâu linh, is an understory climber that typically grows on slopes in thickets along streams at elevations around 400–600 m. It is found in China as well as Quảng Ninh, Ninh Bình, Thanh Hóa, Nghệ An, and Kon Tum provinces of Vietnam.

Piper nigrum L., Vietnamese names Hồ tiêu and Tiêu, is a widespread liana, believed to have originated in India and Indonesia, but now cultivated throughout the tropics, including Vietnam provinces of Quảng Trị, Quảng Nam, Kon Tum, Đắc Lắc, Lâm Đồng, An Giang (Châu Đốc), and Kiên Giang (Phú Quốc).

Piper politifolium C. DC., Vietnamese name Tiêu lá láng, is native to the Neotropics, but introduced to Vietnam and found in the provinces Kon Tum (Đác Giây, Đác Môn), Gia Lai (An Khê, Kon Hà Nừng), Lâm Đồng (Bảo Lộc), and Đồng Nai.

Piper rubrum C. DC., Vietnamese name Tiêu đỏ, is an understory climber found in China as well as Vietnam, Phú Thọ (Tam Thanh), Ninh Bình, Quảng Nam.

Piper sarmentosum Roxb., Vietnamese names Lốt and Trầu già, is an herb growing in forests and wet places near villages, from sea level to 1000 m. The plant ranges from India and China through Thailand and Malaysia. In Vietnam, P. sarmentosum is found in the provinces of Nghệ An and Đà Nẵng.

Piper umbellatum L. (syn. Piper peltatum Ruiz & Pav., Pothomorphe peltata (L.) Miq., Pothomorphe umbellata (L.) Miq.) is an understory herb, native to the Neotropics, but introduced to Vietnam.

2. Results and Discussion

2.1. Plant Collection and Essential Oils

The plants materials (leaves and/or stems) from 13 Piper species were collected from various sites in Vietnam. The collection sites, plant materials, and essential oil yields for the Piper species are summarized in Table 1.

Table 1.

Collection sites and essential oil yields for Piper essential oils from central Vietnam.

Piper Species Voucher Numbers Collection Site Plant Parts Essential Oil Yield (%) a
Piper arboricola C. DC. LTH 105 Ngoc Linh Nature Reserve-Quang Nam Province (15°50’16.0” N, 107°22’54.7” E, elev. 1341 m) Leaves & stems 0.31
Piper arboricola C. DC. LTH 105 Ngoc Linh Nature Reserve-Quang Nam Province (15°50’16.0” N, 107°22’54.7” E, elev. 1341 m) Leaves 0.32
Piper arboricola C. DC. LTH 105 Ngoc Linh Nature Reserve-Quang Nam Province (15°50’16.0” N, 107°22’54.7” E, elev. 1341 m) Stems 0.12
Piper bavinum C. DC. LTH 107 Ngoc Linh Nature Reserve-Quang Nam Province (15°50’16.0” N, 107°22’54.7” E, elev. 1341 m) Leaves & stems 0.34
Piper cambodianum P. Fourn. LTH 108 Ba Na-Nui Chua Nature Reserve
(16°00′06.6″ N, 108°01′22.1″ E, elev. 791 m)		 Leaves & stems 0.34
Piper caninum C. DC. LTH 112 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.10
Piper longum L. LTH 109 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.15
Piper mekongense C. DC LTH 110 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.32
Piper montium C. DC. LTH 111 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.10
Piper mutabile C. DC. LTH 118 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.38
Piper nigrum L. LTH 113 Hoa Vang district, Da Nang city (16°01’0.6” N, 108°4’25.6” E, elev. 28 m) Leaves & stems 0.39
Piper politifolium C. DC. LTH 114 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.37
Piper rubrum C. DC. LTH 115 Ngoc Linh Nature Reserve-Quang Nam Province (15°50’16.0” N, 107°22’54.7” E, elev. 1341 m) Leaves 0.41
Piper rubrum C. DC. LTH 115 Ngoc Linh Nature Reserve-Quang Nam Province (15°50’16.0” N, 107°22’54.7” E, elev. 1341 m) Stems 0.38
Piper sarmentosum Roxb. LTH 116 Hoa Vang district, Da Nang city (16°01’0.6” N, 108°4’25.6” E, elev. 28 m) Leaves & stems 0.29
Piper umbellatum L. LTH 117 Chu Mom Ray National Park (14°25’33.5” N, 107°43’15.6” E, elev. 672 m) Leaves & stems 0.025
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a Yields are based on mass of fresh plant material.

2.2. Essential Oil Compositions

The Vietnamese Piper species were analyzed by gas chromatography-mass spectrometry (GC-MS). A total of 272 compounds were identified in the Piper essential oils, which are compiled in Table 2. β-Caryophyllene was relatively abundant in all of the Piper essential oils and ranged from 4.0% (P. mekongense) to 44.8% (P. umbellatum). Also found in all of the essential oils were α-pinene (0.2–19.3%), β-pinene (0.1–26.9%), limonene (0.4–23.2%), α-copaene (0.2–13.7%), β-elemene (0.3–3.3%), and α-humulene (0.5–6.1%). β-Bisabolene was particularly abundant in P. sarmentosum (40.3%), P. montium (22.1%), and P. mutabile (12.9%), while decanal was an abundant component of P. rubrum stem essential oil (31.6%), and P. nigrum was rich in δ-elemene (20.4%).

Table 2.

Essential oil compositions (%) of Piper species from central Vietnam.

RI a Compound P. arboricola P. arboricola P. arboricola P. bavinum P. cambodianum P. caninum P. longum P. mekongense
Leaves & Stems Leaves b Stems b Leaves & Stems Leaves & Stems b Leaves & Stems b Leaves & Stems b Leaves & Stems b
900 Nonane 0.1 --- --- --- --- --- --- ---
919 5,5-Dimethyl-1-vinylbicyclo[2.1.1]hexane --- --- --- --- Tr c --- --- ---
920 Tricyclene --- --- --- --- --- --- --- tr
923 α-Thujene 0.1 tr 0.1 tr tr 0.6 0.3 tr
930 α-Pinene 0.5 6.4 d 19.3 3.3 4.1 6.2 5.1 3.8
945 α-Fenchene --- --- --- --- --- --- --- tr
947 Camphene 0.6 0.6 0.7 0.3 0.1 1.1 1.0 1.4
970 Sabinene 0.7 tr 0.6 0.1 0.2 1.8 0.2 0.1
975 β-Pinene 0.1 0.8 26.9 3.9 4.6 6.8 10.6 5.3
982 6-Methylhept-5-en-2-one --- --- --- --- --- --- --- ---
986 Myrcene 6.6 0.5 1.1 0.2 2.7 0.7 0.8 0.2
997 δ-2-Carene tr --- --- --- --- --- --- tr
1002 p-Mentha-1(7),8-diene --- --- --- --- tr --- --- tr
1003 Octanal --- --- --- --- --- --- --- ---
1004 α-Phellandrene tr 0.1 0.1 0.3 tr 0.1 0.1 tr
1007 δ-3-Carene --- --- --- --- tr --- 0.1 tr
1010 Hexyl acetate --- tr --- --- --- --- --- ---
1015 α-Terpinene --- --- 0.1 --- tr 0.4 0.2 ---
1018 m-Cymene --- --- --- --- --- --- --- ---
1022 p-Cymene 0.2 1.3 0.5 tr tr 0.6 0.6 0.2
1027 Limonene 23.2 2.4 6.8 2.2 7.9 1.6 1.4 0.8
1028 β-Phellandrene 0.1 0.2 0.4 0.2 0.2 3.4 0.1 0.1
1030 1,8-Cineole 0.1 tr 0.2 --- tr 0.4 0.2 0.1
1033 (Z)-β-Ocimene 0.3 0.1 --- 0.3 tr tr 0.1 tr
1035 2-Heptyl acetate --- --- --- --- --- --- --- 0.1
1043 (E)-β-Ocimene 0.1 tr --- 0.2 tr 0.2 1.5 0.1
1047 2,3,6-Trimethylhepta-1,5-diene 0.1 --- --- --- --- --- --- ---
1055 γ-Terpinene --- tr 0.2 0.1 0.2 1.5 1.4 ---
1057 (2E)-Octenal --- --- --- --- --- --- --- ---
1067 cis-Sabinene hydrate --- --- --- --- --- 1.2 --- ---
1079 p-Mentha-2,4(8)-diene --- --- --- --- --- --- --- ---
1083 Terpinolene 0.4 0.1 0.3 0.1 0.1 0.3 0.1 tr
1088 2-Nonanone 0.2 --- --- --- --- --- 0.1 tr
1090 Rosefuran --- --- --- --- --- --- --- ---
1093 α-Pinene oxide --- --- --- --- --- --- --- ---
1097 Linalool 0.8 1.1 0.8 0.3 0.3 10.1 3.4 0.2
1098 trans-Sabinene hydrate --- --- --- --- --- 1.2 --- ---
1098 2-Nonanol tr --- --- --- --- --- --- 0.1
1101 6-Methyl-3,5-heptadien-2-one --- --- --- --- --- --- --- ---
1102 Nonanal 0.2 --- --- --- --- --- --- ---
1103 1-Octen-3-yl acetate tr --- --- --- --- --- --- 0.2
1105 p-Mentha-2-8-dien-1-ol --- --- --- --- --- --- --- tr
1111 4,8-Dimethylnona-1,3,7-triene 0.3 tr --- --- 0.3 --- --- tr
1115 3-Octyl acetate --- --- --- --- --- --- --- tr
1117 trans-p-Mentha-2,8-dien-1-ol 0.1 --- --- --- --- --- --- ---
1122 cis-p-Menth-2-en-1-ol --- --- --- --- --- 0.4 --- ---
1126 allo-Ocimene --- --- --- --- --- --- --- ---
1127 (Z)-Myroxide --- --- --- --- --- --- --- ---
1128 cis-Limonene oxide tr --- --- --- --- --- --- ---
1129 Limona ketone --- --- --- --- --- --- --- ---
1132 cis-p-Mentha-2,8-dien-1-ol 0.1 --- --- --- --- --- --- ---
1133 trans-Limonene oxide tr --- --- --- --- --- --- ---
1135 Nopinone --- --- --- --- --- --- --- tr
1137 (E)-Myroxide 0.1 --- --- --- --- --- --- ---
1138 trans-Pinocarveol --- --- --- --- --- --- --- 0.1
1140 trans-p-Menth-2-en-1-ol --- --- --- --- --- 0.3 --- ---
1143 trans-Verbenol --- --- --- --- --- --- --- tr
1144 Camphor tr 0.1 --- --- --- 0.8 0.4 tr
1152 Camphene hydrate --- --- --- --- --- --- tr tr
1153 Sabina ketone --- --- --- --- --- --- --- tr
1158 Isoborneol 0.1 --- --- --- --- --- --- ---
1159 Pinocarvone --- --- --- --- --- --- --- tr
1167 Rosefuran epoxide --- --- --- --- --- --- --- ---
1167 p-Mentha-1,5-dien-8-ol --- --- --- --- --- --- --- ---
1168 1-Nonanol 0.3 --- --- --- --- --- --- tr
1169 Borneol --- tr --- --- --- 0.1 tr tr
1171 (3E,5E)-Undeca-1,3,5-triene --- --- --- --- --- --- --- ---
1174 Isopinocamphone --- --- --- --- --- --- 0.1 ---
1177 2-Isopropenyl-5-methyl-4-hexenal --- --- --- --- --- --- tr ---
1178 Terpinen-4-ol 0.1 --- 0.1 --- 0.1 7.7 0.2 ---
1182 Naphthalene --- 0.2 --- --- --- 1.2 0.3 ---
1184 p-Cymen-8-ol 0.4 --- --- --- --- --- --- 0.1
1185 Cryptone --- --- --- --- --- --- --- ---
1193 Myrtenal --- --- --- --- --- --- --- 0.1
1193 α-Terpineol --- tr --- 0.1 0.1 0.4 0.2 ---
1199 (3Z)-Octenyl acetate --- --- --- --- --- --- --- ---
1201 cis-Sabinol --- --- --- --- --- --- --- ---
1203 Decanal 6.2 0.6 3.5 0.2 --- --- --- ---
1206 (3E)-Octenyl acetate --- --- --- --- --- --- --- ---
1215 trans-Carveol 0.1 --- --- --- --- --- --- ---
1216 endo-Fenchyl acetate --- --- --- --- --- --- --- ---
1221 2-Hydroxycineole --- --- --- --- --- --- --- ---
1222 Nerol --- --- --- --- tr --- --- ---
1224 Citronellol --- --- --- --- --- --- --- ---
1225 Isobornyl formate --- --- --- --- --- --- --- 0.2
1228 cis-Carveol tr --- --- --- --- --- --- ---
1228 2-Nonyl acetate --- --- --- --- --- --- --- 0.1
1233 Bornyl formate --- --- --- --- --- --- --- 1.6
1237 Ascaridole --- --- --- --- --- 0.7 0.1 ---
1240 Carvone 0.1 --- --- --- --- --- --- ---
1248 Geraniol --- --- --- --- tr --- --- ---
1248 Linalyl acetate --- 0.1 --- --- --- --- --- ---
1256 Methyl citronellate --- --- --- --- --- --- --- ---
1269 1-Decanol 1.1 tr --- --- --- --- --- ---
1271 Methyl hydrocinnamate --- --- --- --- --- --- --- ---
1277 9-Decen-1-ol --- --- --- --- --- --- --- 0.1
1281 Isobornyl acetate --- --- 0.2 --- --- --- 0.1 0.1
1282 Bornyl acetate --- 1.3 --- 0.1 --- 0.7 0.3 0.2
1288 Safrole --- 0.1 --- 0.5 --- --- --- ---
1290 2-Undecanone 0.8 0.1 --- --- tr 0.4 1.7 0.2
1293 Methyl myrtenate --- --- --- --- --- --- tr ---
1299 2-Undecanol --- --- --- --- tr --- tr 0.5
1300 Tridecane --- 0.1 0.4 --- --- 1.2 0.1 ---
1303 Undecanal 0.1 --- --- --- --- --- --- ---
1304 Isoascaridole --- --- --- --- --- 0.5 0.1 ---
1319 Methyl geranate --- --- --- --- --- --- tr ---
1328 Myrtenyl acetate --- tr --- --- --- --- --- ---
1328 Bicycloelemene 0.8 0.3 --- 0.3 0.3 --- tr 0.3
1332 δ-Elemene 0.2 0.1 --- 0.2 0.2 --- tr 0.7
1343 α-Cubebene 0.1 3.0 0.8 0.5 0.4 0.3 0.1 0.2
1344 α-Terpinyl acetate --- --- --- --- --- --- --- ---
1347 Citronellyl acetate --- --- --- --- --- --- --- ---
1358 Decanoic acid 0.1 --- --- --- --- --- --- ---
1364 Cyclosativene --- 0.3 0.1 0.1 tr --- 0.1 0.2
1365 Hydrocinnamyl acetate --- --- --- --- --- --- --- ---
1366 α-Ylangene --- --- --- --- --- --- --- ---
1368 Isoledene --- tr --- 0.2 tr --- tr tr
1372 α-Copaene 0.8 13.7 4.2 3.2 2.1 0.4 0.3 0.7
1375 Geranyl acetate --- 0.1 --- --- --- 0.2 --- ---
1376 (E)-β-Damascenone --- --- --- --- --- --- tr ---
1380 β-Bourbonene 0.3 0.2 --- --- 0.2 0.1 tr 0.1
1384 β-Cubebene 0.2 1.7 0.6 1.6 0.2 --- 0.1 0.5
1385 7-epi-Sesquithujene --- --- --- --- --- --- --- ---
1386 β-Elemene 1.6 0.7 0.4 2.0 1.2 0.4 0.3 2.1
1398 Sesquithujene --- tr 0.1 --- --- --- --- ---
1402 Italicene --- 0.1 --- --- --- --- --- ---
1402 (Z)-Caryophyllene --- --- --- --- 0.4 --- --- ---
1403 α-Gurjunene 0.1 0.3 0.2 1.1 0.2 --- 0.1 0.2
1406 Dodecanal 0.6 0.2 0.3 --- --- 0.2 tr ---
1408 cis-5-Hydroxy-p-menth-6-en-2-one --- --- --- --- --- --- --- ---
1408 β-Maaliene --- --- --- --- --- --- --- 0.2
1409 cis-α-Bergamotene --- 0.3 1.0 0.4 --- 0.2 tr ---
1416 β-Caryophyllene 14.1 9.4 4.9 6.2 19.2 10.3 7.9 4.0
1419 (E)-α-Ionone --- tr --- --- --- --- --- ---
1422 γ-Maaliene tr --- --- --- tr --- --- ---
1423 γ-Elemene --- --- --- --- --- --- --- 0.9
1424 trans-5-Hydroxy-p-menth-6-en-2-one --- --- --- --- --- --- --- ---
1424 β-Gurjunene --- --- --- --- --- --- --- 2.1
1426 β-Copaene 0.3 0.7 0.8 0.4 0.2 0.4 0.1 ---
1430 trans-α-Bergamotene --- 0.1 0.1 0.2 tr 0.1 tr ---
1430 α-Maaliene 0.1 --- --- --- --- --- tr 0.1
1431 α-Guaiene --- 0.7 0.1 0.5 0.3 --- --- ---
1435 Aromadendrene 0.6 0.2 --- 0.1 0.3 0.3 0.1 0.2
1438 (Z)-β-Farnesene --- --- --- --- --- --- --- ---
1439 6,9-Guaiadiene --- --- --- --- --- --- --- ---
1442 Myltayl-4(12)-ene --- --- --- --- --- --- --- 0.2
1443 Selina-5,11-diene --- --- --- --- --- --- tr ---
1445 cis-Muurola-3,5-diene --- 0.9 0.3 --- 0.1 --- tr ---
1445 Geranyl acetone --- --- --- --- --- --- --- ---
1446 trans-Muurola-3,5-diene --- --- --- 1.6 --- --- --- ---
1449 (E)-β-Farnesene --- 0.2 0.3 0.5 tr 1.0 0.4 ---
1450 Valerena-4,7(11)-diene 0.1 --- --- --- --- --- --- ---
1452 α-Humulene 1.1 1.7 0.5 6.1 2.0 1.4 1.4 1.9
1453 Sesquisabinene --- tr 0.2 0.1 --- --- --- ---
1456 allo-Aromadendrene 0.1 0.1 --- 0.2 0.4 0.1 --- ---
1457 Eudesma-1,4(15),11-triene --- --- --- --- --- --- --- ---
1459 cis-Muurola-4(14),5-diene --- --- --- --- --- --- 0.1 ---
1462 cis-Cadina-1(6),4-diene --- --- --- --- tr --- --- ---
1464 Dehydroisolongifolenene --- --- --- --- --- --- --- ---
1467 Selina-4,11-diene --- --- --- --- --- --- --- ---
1467 (2E)-Undecenyl acetate --- --- --- --- --- --- --- ---
1468 trans-Cadina-1(6),4-diene --- 1.1 0.5 --- 0.3 --- 0.1 ---
1470 γ-Gurjunene --- --- --- 1.7 --- --- --- ---
1470 Amorpha-4,7(11)-diene --- --- --- --- --- --- --- ---
1471 γ-Muurolene 0.2 0.4 0.2 0.3 9.6 0.5 0.4 2.2
1472 β-Acoradiene --- --- --- --- --- --- --- ---
1473 γ-Curcumene --- 0.2 2.3 5.8 --- --- --- ---
1475 cis-4,10-epoxy-Amorphane --- --- --- --- 0.6 --- --- ---
1476 α-Amorphene --- tr --- --- --- --- --- ---
1477 Germacrene D 2.8 --- --- 4.7 1.5 --- 1.2 5.2
1477 ar-Curcumene --- 5.5 9.6 --- --- 4.9 --- ---
1480 (Z,Z)-α-Farnesene --- 0.3 0.5 0.3 --- 0.3 tr ---
1480 β-Chamigrene --- --- --- --- 0.9 --- --- 1.3
1480 1-Dodecanol --- --- --- --- --- --- --- ---
1484 δ-Selinene --- tr --- --- --- --- --- ---
1486 trans-Muurola-4(14),5-diene --- 1.6 0.6 1.4 --- --- 0.3 ---
1486 β-Selinene 0.1 0.2 1.1 1.6 0.6 1.4 tr 1.0
1487 Viridiflorene (=Ledene) 0.4 --- --- --- 0.6 --- --- 0.3
1488 Curzerene --- --- --- --- --- --- --- 0.2
1488 α-Zingiberene --- --- --- --- --- 0.8 --- ---
1490 Unidentified sesquiterpenoide --- --- --- --- --- --- 2.3 ---
1492 Asaricin --- --- --- --- --- --- --- ---
1492 Bicyclogermacrene 11.3 7.9 --- 8.9 3.7 --- 1.5 5.6
1492 α-Selinene --- --- --- --- --- 1.1 --- ---
1495 α-Muurolene 0.1 0.9 0.5 0.8 1.3 0.5 0.8 1.1
1495 cis-β-Guaiene --- --- --- --- --- --- --- ---
1497 (Z)-α-Bisabolene --- --- --- --- --- --- 0.1 ---
1499 α-Bulnesene --- 2.5 0.7 3.0 1.2 --- --- ---
1500 δ-Amorphene --- --- --- --- --- --- --- ---
1500 Pentadecane --- --- 0.5 --- --- --- --- ---
1501 (E,E)-α-Farnesene --- --- --- --- --- --- --- ---
1504 β-Bisabolene --- 0.7 0.7 0.7 0.1 8.7 4.5 0.2
1505 β-Curcumene --- 0.1 0.3 1.5 --- --- --- ---
1509 γ-Cadinene 0.1 0.2 --- 0.2 0.5 0.5 1.3 0.6
1511 Cubebol 0.1 1.7 --- 0.7 1.0 0.1 0.3 1.0
1514 δ-Cadinene 0.3 6.0 1.7 4.8 6.1 1.6 3.5 1.8
1515 7-epi-α-Selinene --- --- --- --- --- --- --- 1.4
1518 trans-Calamenene 0.1 8.9 2.4 1.1 0.2 --- --- 0.2
1519 β-Sesquiphellandrene --- --- 0.2 0.2 --- 1.2 --- ---
1520 Zonarene --- --- --- 0.4 0.2 --- --- ---
1523 (E)-γ-Bisabolene --- --- --- 0.2 --- --- --- ---
1526 Kessane --- --- --- --- 0.2 --- --- ---
1527 Nootkatene --- 0.1 --- --- --- --- --- ---
1529 trans-Cadina-1,4-diene --- 0.8 0.3 0.9 0.7 --- 0.1 ---
1533 α-Cadinene --- tr --- --- 0.1 --- 0.3 0.2
1537 cis-Cadinene ether --- tr --- --- --- --- --- ---
1538 (E)-α-Bisabolene --- --- --- --- --- --- 0.2 ---
1538 α-Calacorene --- 0.4 --- --- 0.1 --- --- 0.2
1542 trans-Cadinene ether --- 0.5 --- --- --- --- 0.2 ---
1544 Unidentified sesquiterpenoid f 0.3 --- --- --- --- --- 1.3 ---
1545 α-Elemol --- --- --- --- 0.1 --- --- 0.3
1554 Germacrene B 0.1 --- --- --- --- --- --- 2.0
1557 (E)-Nerolidol 1.7 0.4 --- 0.2 1.6 2.3 8.1 0.9
1558 β-Calacorene --- 0.1 --- --- --- --- --- 0.2
1565 Maaliol --- --- --- --- --- --- --- 13.8
1565 Palustrol --- --- --- 1.1 0.1 --- --- ---
1566 Dendrolasin --- --- --- --- --- --- --- ---
1573 Spathulenol 8.3 0.6 --- 0.4 1.3 1.2 0.7 6.4
1574 Germacra-1(10),5-dien-4β-ol --- --- --- --- --- --- 0.6 ---
1578 Caryophyllene oxide 3.3 0.4 --- 0.2 1.6 3.1 0.8 1.3
1582 Globulol 0.6 0.4 --- 0.8 0.3 0.5 --- 2.2
1583 Gleenol --- 0.3 --- --- --- --- --- ---
1586 Unidentified sesquiterpenoid g --- 0.1 --- --- 0.1 --- --- ---
1590 Viridiflorol 1.2 0.5 --- 1.0 6.5 0.5 --- 1.4
1593 Cubeban-11-ol --- 0.1 --- 0.2 --- --- --- ---
1595 Humulene epoxide I --- --- --- --- --- --- --- ---
1597 Curzerenone --- --- --- --- --- --- --- ---
1600 Rosifoliol --- --- --- 0.1 --- --- --- 0.1
1600 Guaiol --- --- --- --- 0.8 --- --- ---
1601 Ledol --- 0.1 --- 0.9 0.3 --- --- ---
1601 β-Oplopenone --- --- --- --- --- --- 0.5 ---
1605 β-Atlantol --- --- --- --- --- --- --- ---
1606 Humulene epoxide II 0.2 0.1 --- --- 0.1 0.3 --- 0.3
1606 Tetradecanal --- --- --- --- --- --- --- ---
1609 Unidentified sesquiterpenoid h --- --- --- --- --- --- --- ---
1612 1,10-di-epi-Cubenol --- --- --- --- 0.1 --- 0.1 ---
1613 α-Corocalene --- 0.1 --- --- --- --- --- ---
1616 Junenol --- --- --- --- --- --- --- ---
1623 Selina-6-en-4β-ol --- --- --- --- --- --- --- ---
1624 1-epi-Cubenol 0.1 2.1 0.3 2.6 0.7 --- 0.3 ---
1626 iso-Spathulenol 0.7 --- --- --- 0.3 --- --- 1.3
1628 Caryophylla-4(12),8(13)-dien-5α-ol --- --- --- --- --- --- --- ---
1633 Caryophylla-4(12),8(13)-dien-5β-ol --- --- --- --- 0.2 --- --- ---
1636 allo-Aromadendrene epoxide --- --- --- --- --- --- --- ---
1638 τ-Cadinol --- --- --- --- 0.9 0.4 2.2 1.1
1640 τ-Muurolol 0.2 --- --- 0.6 0.6 0.5 2.0 2.9
1640 Cubenol --- 1.4 --- 1.7 --- --- --- ---
1643 α-Muurolol (= δ-Cadinol) 0.1 0.4 --- 0.7 2.4 0.5 1.2 0.8
1648 Unidentified sesquiterpenoid i --- --- --- 1.6 --- --- --- 1.3
1651 α-Eudesmol --- --- --- --- --- --- --- ---
1652 α-Cadinol --- 0.2 --- 1.2 1.8 0.8 4.9 3.6
1654 Selin-11-en-4α-ol --- --- --- 0.4 --- --- --- 0.9
1655 Pogostol --- 0.4 --- 0.4 0.2 --- --- ---
1656 Unidentified fatty acid derivative j 0.2 --- --- --- --- --- --- ---
1658 ar-Turmerone --- 0.2 --- --- --- --- --- ---
1658 9-Methoxycalamenene --- --- --- --- --- --- --- 0.3
1661 Intermedeol --- --- --- --- --- --- --- ---
1661 Bulnesol --- --- --- --- 0.3 --- --- ---
1663 (6Z)-Pentadecen-2-one --- --- --- --- --- --- --- ---
1664 (2E,6Z)-Farnesol --- --- --- --- --- --- --- ---
1666 14-Hydroxy-9-epi-(E)-caryophyllene --- --- --- --- 0.1 --- --- ---
1670 Cadalene --- 0.1 --- --- --- --- --- ---
1680 Unidentified sesquiterpenoid k --- --- --- --- --- --- 5.7 ---
1680 Germacra-4(15),5,10(14)-trien-1α-ol --- --- --- --- tr --- --- ---
1681 epi-α-Bisabolol --- --- --- --- --- 2.4
1684 α-Bisabolol --- --- --- --- --- --- --- ---
1686 (2Z,6Z)-Farnesol --- --- --- --- --- --- --- ---
1690 Shyobunol --- --- --- --- 1.5 --- --- ---
1690 2-Pentadecanone --- --- --- --- --- --- --- ---
1700 Heptadecane --- --- --- --- --- --- --- ---
1710 Unidentified sesquiterpenoidl --- --- --- --- --- --- 11.9 ---
1711 (2E,6Z)-Farnesol --- --- --- --- --- --- --- ---
1722 Cryptomerione --- --- --- --- --- --- --- ---
1725 Zerumbone --- --- --- --- --- --- --- ---
1747 Cyclocolorenone 0.5 0.1 0.1 7.9 --- --- --- ---
1763 Benzyl benzoate --- --- --- --- 0.1 --- --- ---
1798 Curzerenone B --- --- --- --- --- --- --- ---
1809 Hexadecanal --- --- --- --- --- --- --- ---
1828 (2Z,6E)-Farnesyl acetate --- --- --- --- --- --- --- ---
2017 (E,E)-Geranyl linalool --- --- --- --- --- --- --- ---
2103 (E)-Phytol --- --- --- --- --- --- --- ---
Monoterpene hydrocarbons 33.0 12.5 57.2 11.0 20.0 25.3 23.7 11.9
Oxygenated monoterpenoids 1.8 2.7 1.3 0.5 0.4 24.6 5.1 2.6
Sesquiterpene hydrocarbons 35.9 73.0 36.3 64.1 55.2 36.5 25.3 38.4
Oxygenated sesquiterpenoids 17.0 9.7 0.4 20.9 23.4 10.1 21.9 41.0
Diterpenoids 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Benzenoids 0.0 0.1 0.0 0.5 0.1 0.0 0.0 0.0
Others 9.9 1.1 4.8 0.2 0.3 3.0 2.1 1.3
Total identified 97.6 99.0 100.0 97.1 99.5 99.4 78.2 95.2
RI a Compound P. montium P. mutabile P. nigrum P. politifolium P. rubrum P. rubrum P. sarmentosum P. umbellatum
Leaves & Stems b Leaves & Stems b Leaves & Stems b Leaves & Stems Leaves b Stems b Leaves & Stems b Leaves & Stems
900 Nonane --- --- --- --- --- --- --- ---
919 5,5-Dimethyl-1-vinylbicyclo[2.1.1]hexane --- --- --- --- --- --- --- ---
920 Tricyclene --- --- --- tr c --- --- tr ---
923 α-Thujene tr --- tr 0.8 tr 0.1 0.1 ---
930 α-Pinene 0.2 3.1 0.8 12.9 d 0.9 0.5 2.3 0.4
945 α-Fenchene --- --- tr --- --- --- tr ---
947 Camphene tr 1.0 tr 3.2 0.2 0.8 2.0 0.1
970 Sabinene --- --- tr 1.7 0.2 2.1 0.1 0.1
975 β-Pinene 0.2 5.5 1.3 7.1 0.1 0.3 5.5 0.8
982 6-Methylhept-5-en-2-one --- --- --- --- --- --- tr ---
986 Myrcene tr 0.2 0.5 1.6 4.1 0.9 0.4 0.3
997 δ-2-Carene --- --- --- --- tr --- --- ---
1002 p-Mentha-1(7),8-diene --- --- --- --- --- --- --- tr
1003 Octanal 0.1 --- --- --- --- --- --- ---
1004 α-Phellandrene 0.2 --- 1.0 0.4 --- 0.1 --- tr
1007 δ-3-Carene --- 0.2 4.6 2.3 --- --- --- tr
1010 Hexyl acetate --- --- --- --- --- --- --- ---
1015 α-Terpinene tr --- tr 0.4 --- 0.1 --- ---
1018 m-Cymene --- --- tr --- --- --- --- ---
1022 p-Cymene 0.2 --- 0.1 0.3 0.2 0.2 0.1 tr
1027 Limonene 0.4 3.8 2.4 2.6 7.0 9.3 1.3 0.9
1028 β-Phellandrene 0.2 0.4 0.1 1.4 tr 0.8 tr 0.5
1030 1,8-Cineole 0.2 0.2 --- --- --- --- 0.5 ---
1033 (Z)-β-Ocimene tr --- tr 0.4 0.2 tr 0.3 4.3
1035 2-Heptyl acetate --- --- --- --- --- --- 0.1 ---
1043 (E)-β-Ocimene tr 0.2 0.2 2.8 tr 0.1 1.3 1.0
1047 2,3,6-Trimethylhepta-1,5-diene --- --- --- --- --- --- --- ---
1055 γ-Terpinene 0.1 --- 0.1 0.6 --- 0.1 --- tr
1057 (2E)-Octenal 0.2 --- --- --- --- --- --- ---
1067 cis-Sabinene hydrate tr --- --- --- --- --- --- ---
1079 p-Mentha-2,4(8)-diene --- --- 0.1 --- --- --- --- ---
1083 Terpinolene tr 0.2 0.2 5.7 0.1 0.6 --- tr
1088 2-Nonanone --- --- --- --- --- 0.2 0.1 ---
1090 Rosefuran --- --- --- --- --- --- 0.1 ---
1093 α-Pinene oxide --- --- --- --- --- --- 0.1 ---
1097 Linalool 2.1 3.7 0.8 0.8 0.4 0.3 0.4 0.5
1098 trans-Sabinene hydrate --- --- --- --- --- --- --- ---
1098 2-Nonanol --- --- --- --- --- 0.1 --- ---
1101 6-Methyl-3,5-heptadien-2-one --- --- --- --- --- --- 0.2 ---
1102 Nonanal --- --- --- --- 0.1 0.3 --- ---
1103 1-Octen-3-yl acetate --- --- --- --- --- --- --- 0.4
1105 p-Mentha-2-8-dien-1-ol --- --- --- --- --- --- --- ---
1111 4,8-Dimethylnona-1,3,7-triene --- --- --- --- 0.7 0.5 tr tr
1115 3-Octyl acetate --- --- --- --- --- --- --- 0.1
1117 trans-p-Mentha-2,8-dien-1-ol --- --- --- --- --- --- --- tr
1122 cis-p-Menth-2-en-1-ol --- --- --- --- --- --- --- ---
1126 allo-Ocimene --- --- --- --- --- --- tr 0.2
1127 (Z)-Myroxide --- --- --- --- --- --- tr ---
1128 cis-Limonene oxide --- --- --- --- --- --- --- ---
1129 Limona ketone --- --- --- --- --- --- tr ---
1132 cis-p-Mentha-2,8-dien-1-ol --- --- --- --- --- --- --- ---
1133 trans-Limonene oxide --- --- --- --- --- --- --- ---
1135 Nopinone --- --- --- --- --- --- --- ---
1137 (E)-Myroxide --- --- --- --- --- --- 0.1 ---
1138 trans-Pinocarveol --- --- --- --- --- --- 0.1 ---
1140 trans-p-Menth-2-en-1-ol --- --- --- --- --- --- --- ---
1143 trans-Verbenol --- --- --- --- --- --- tr ---
1144 Camphor tr 1.0 --- --- --- --- tr ---
1152 Camphene hydrate --- --- --- --- --- --- --- ---
1153 Sabina ketone --- --- --- --- --- --- --- ---
1158 Isoborneol --- --- --- --- --- --- --- ---
1159 Pinocarvone --- --- --- --- --- --- tr ---
1167 Rosefuran epoxide --- --- --- --- --- --- tr ---
1167 p-Mentha-1,5-dien-8-ol --- --- --- --- --- --- --- tr
1168 1-Nonanol --- --- --- --- 0.1 0.2 --- ---
1169 Borneol --- 0.1 --- --- --- --- 0.1 ---
1171 (3E,5E)-Undeca-1,3,5-triene --- --- --- --- --- --- --- tr
1174 Isopinocamphone --- --- --- --- --- --- --- ---
1177 2-Isopropenyl-5-methyl-4-hexenal --- 0.2 --- --- --- --- --- ---
1178 Terpinen-4-ol 0.8 0.3 --- 0.4 --- 0.1 tr ---
1182 Naphthalene 0.8 2.3 --- --- --- 0.3 --- 0.2
1184 p-Cymen-8-ol --- --- --- 0.1 0.2 0.2 tr ---
1185 Cryptone --- --- --- --- --- --- tr ---
1193 Myrtenal --- --- --- --- --- --- 0.2 ---
1193 α-Terpineol 0.1 0.3 tr 0.1 --- --- --- ---
1199 (3Z)-Octenyl acetate --- --- --- --- --- --- tr 0.1
1201 cis-Sabinol --- --- --- --- --- --- --- ---
1203 Decanal --- --- --- --- 1.3 31.6 --- ---
1206 (3E)-Octenyl acetate --- --- --- --- --- --- 0.1 0.1
1215 trans-Carveol --- --- --- --- --- --- --- ---
1216 endo-Fenchyl acetate --- --- --- --- --- --- 0.1 ---
1221 2-Hydroxycineole --- --- --- --- --- --- --- ---
1222 Nerol --- --- --- --- --- --- --- ---
1224 Citronellol --- --- tr --- --- --- --- ---
1225 Isobornyl formate --- --- --- --- --- --- --- ---
1228 cis-Carveol --- --- --- --- --- --- --- ---
1228 2-Nonyl acetate --- --- --- --- --- --- --- ---
1233 Bornyl formate --- --- --- --- --- --- --- tr
1237 Ascaridole --- --- --- --- --- --- --- ---
1240 Carvone --- --- --- --- --- --- --- ---
1248 Geraniol --- --- --- --- --- --- --- ---
1248 Linalyl acetate --- --- 0.1 --- --- --- --- ---
1256 Methyl citronellate --- --- 0.5 --- --- --- --- ---
1269 1-Decanol 0.2 --- --- --- 0.1 3.4 --- ---
1271 Methyl hydrocinnamate --- --- --- --- --- --- 0.1 ---
1277 9-Decen-1-ol --- --- --- --- --- --- --- ---
1281 Isobornyl acetate 0.1 --- --- --- --- --- 1.6 0.2
1282 Bornyl acetate --- --- --- 0.1 0.1 --- 0.1 tr
1288 Safrole --- --- --- 2.7 --- --- --- 0.1
1290 2-Undecanone 0.1 --- 0.2 1.6 0.2 2.3 0.3 tr
1293 Methyl myrtenate --- --- --- --- --- --- --- ---
1299 2-Undecanol --- --- tr --- --- 0.1 --- tr
1300 Tridecane 2.8 1.9 --- --- --- 0.5 --- ---
1303 Undecanal --- --- --- --- --- 0.1 --- ---
1304 Isoascaridole --- --- --- --- --- --- --- ---
1319 Methyl geranate --- --- 0.1 --- --- --- --- ---
1328 Myrtenyl acetate 0.1 --- --- --- --- --- --- ---
1328 Bicycloelemene --- --- 1.6 0.4 1.1 0.3 --- 0.9
1332 δ-Elemene 0.1 0.2 20.4 0.2 0.1 0.1 0.4 9.2
1343 α-Cubebene 0.2 0.1 1.1 0.1 0.4 0.1 --- 0.1
1344 α-Terpinyl acetate --- --- --- --- --- --- 0.3 ---
1347 Citronellyl acetate --- --- 0.1 --- --- --- --- ---
1358 Decanoic acid --- --- --- --- --- 0.4 --- ---
1364 Cyclosativene 0.2 0.3 0.1 --- 0.1 --- --- tr
1365 Hydrocinnamyl acetate --- --- --- --- --- --- 0.5 ---
1366 α-Ylangene 0.1 --- 0.1 --- --- --- --- ---
1368 Isoledene --- --- 0.3 --- 0.1 --- --- ---
1372 α-Copaene 0.7 1.3 3.5 1.1 7.1 1.7 0.2 0.4
1375 Geranyl acetate 0.2 --- --- --- --- --- --- ---
1376 (E)-β-Damascenone --- --- --- --- --- --- --- ---
1380 β-Bourbonene 0.1 --- 0.1 0.1 0.4 0.1 0.1 tr
1384 β-Cubebene --- --- --- 0.2 0.4 0.2 --- 0.1
1385 7-epi-Sesquithujene --- --- --- --- --- --- 0.1 ---
1386 β-Elemene 1.2 0.4 3.3 0.6 2.8 0.5 2.0 0.6
1398 Sesquithujene --- --- --- --- --- --- --- ---
1402 Italicene --- --- --- --- --- --- --- ---
1402 (Z)-Caryophyllene --- --- tr --- --- --- --- tr
1403 α-Gurjunene tr 0.2 2.2 0.1 0.2 0.1 --- 0.1
1406 Dodecanal 0.1 --- --- --- 0.3 5.0 --- ---
1408 cis-5-Hydroxy-p-menth-6-en-2-one --- --- --- --- --- --- --- ---
1408 β-Maaliene --- --- 0.4 --- --- --- --- ---
1409 cis-α-Bergamotene 0.4 0.2 --- --- 0.1 --- 0.1 ---
1416 β-Caryophyllene 19.2 16.5 7.7 6.5 22.9 9.7 5.5 44.8
1419 (E)-α-Ionone --- --- --- --- --- --- --- ---
1422 γ-Maaliene --- --- tr --- 0.1 --- --- tr
1423 γ-Elemene --- --- 0.2 --- --- --- --- 0.2
1424 trans-5-Hydroxy-p-menth-6-en-2-one --- --- --- --- --- --- --- ---
1424 β-Gurjunene --- --- --- --- --- --- --- ---
1426 β-Copaene 0.6 0.9 --- 0.2 0.5 0.2 0.1 0.3
1430 trans-α-Bergamotene 0.2 0.2 --- 0.1 --- --- 0.1 tr
1430 α-Maaliene --- --- --- --- 0.1 --- --- tr
1431 α-Guaiene --- --- --- 0.2 --- --- --- ---
1435 Aromadendrene 0.2 0.4 0.9 0.1 1.3 0.2 0.1 0.1
1438 (Z)-β-Farnesene --- --- --- --- --- --- 0.1 ---
1439 6,9-Guaiadiene --- --- 0.5 --- --- --- --- 0.2
1442 Myltayl-4(12)-ene --- 0.1 --- --- 0.1 --- --- tr
1443 Selina-5,11-diene --- --- --- --- --- --- --- ---
1445 cis-Muurola-3,5-diene 0.1 0.1 0.1 --- --- --- --- 0.2
1445 Geranyl acetone --- --- 0.4 --- --- --- --- 0.4
1446 trans-Muurola-3,5-diene --- --- --- --- --- --- --- ---
1449 (E)-β-Farnesene 1.6 1.1 --- --- --- --- 2.2 0.1
1450 Valerena-4,7(11)-diene --- --- tr --- 0.1 --- --- ---
1452 α-Humulene 1.6 2.1 2.7 3.2 1.9 0.8 1.2 3.8
1453 Sesquisabinene --- --- --- --- --- --- --- ---
1456 allo-Aromadendrene 0.1 --- --- --- 0.2 --- --- 0.1
1457 Eudesma-1,4(15),11-triene --- --- 0.6 --- --- --- --- ---
1459 cis-Muurola-4(14),5-diene --- --- --- --- --- --- --- 0.1
1462 cis-Cadina-1(6),4-diene --- --- 0.4 --- --- --- --- ---
1464 Dehydroisolongifolenene --- --- --- --- --- --- --- 0.1
1467 Selina-4,11-diene --- --- --- --- --- --- --- 0.1
1467 (2E)-Undecenyl acetate --- --- --- --- --- --- 0.1 ---
1468 trans-Cadina-1(6),4-diene 0.2 --- --- --- --- --- --- ---
1470 γ-Gurjunene --- --- 0.6 --- 0.1 --- --- ---
1470 Amorpha-4,7(11)-diene --- --- --- --- --- --- --- 1.7
1471 γ-Muurolene 1.0 1.0 3.6 0.1 0.2 0.3 --- 0.4
1472 β-Acoradiene --- --- --- --- --- --- 0.7 ---
1473 γ-Curcumene --- --- --- --- --- --- --- ---
1475 cis-4,10-epoxy-Amorphane --- --- --- --- --- --- --- ---
1476 α-Amorphene --- 0.2 0.2 --- --- --- --- ---
1477 Germacrene D --- --- 1.1 5.1 2.9 1.8 --- 1.8
1477 ar-Curcumene 15.1 8.2 --- --- --- --- 1.8 ---
1480 (Z,Z)-α-Farnesene 0.8 0.7 --- --- --- --- 0.5 ---
1480 β-Chamigrene --- --- --- --- 0.1 --- --- ---
1480 1-Dodecanol --- --- --- --- --- 0.5 --- ---
1484 δ-Selinene --- --- 2.2 --- --- --- --- 1.3
1486 trans-Muurola-4(14),5-diene 0.4 0.3 2.0 --- --- --- --- 0.2
1486 β-Selinene 1.4 0.7 5.1 0.6 0.3 0.1 4.4 0.3
1487 Viridiflorene (=Ledene) --- --- 2.5 0.1 0.9 0.3 --- ---
1488 Curzerene --- --- --- --- --- --- --- ---
1488 α-Zingiberene 3.1 2.2 --- --- --- --- --- ---
1490 Unidentified sesquiterpenoid e --- --- --- --- --- --- --- ---
1492 Asaricin --- 3.2 --- 18.7 --- --- --- ---
1492 Bicyclogermacrene --- --- --- --- 15.7 3.5 --- 1.6
1492 α-Selinene 0.9 --- 4.3 --- --- --- 3.2 ---
1495 α-Muurolene 1.5 1.1 0.2 0.3 0.3 0.1 0.1 0.3
1495 cis-β-Guaiene --- --- --- --- --- --- --- 0.2
1497 (Z)-α-Bisabolene --- --- --- --- --- --- 0.1 ---
1499 α-Bulnesene --- --- --- --- 0.1 --- --- ---
1500 δ-Amorphene --- --- 0.2 --- --- --- --- ---
1500 Pentadecane --- --- --- --- 0.2 5.3 --- ---
1501 (E,E)-α-Farnesene --- --- 0.4 0.1 --- --- --- ---
1504 β-Bisabolene 22.1 12.9 0.3 0.1 0.1 --- 40.3 0.6
1505 β-Curcumene --- --- --- --- --- --- --- ---
1509 γ-Cadinene 0.6 0.7 0.2 0.1 0.1 --- --- 0.4
1511 Cubebol 0.1 --- 0.2 0.1 0.1 0.1 --- 0.2
1514 δ-Cadinene 2.1 2.8 1.4 1.5 0.9 0.5 --- 1.2
1515 7-epi-α-Selinene --- --- --- --- --- --- 0.2 ---
1518 trans-Calamenene 0.3 0.4 0.2 tr 1.1 0.2 --- 0.5
1519 β-Sesquiphellandrene 2.9 2.1 --- 0.1 --- --- 0.2 0.1
1520 Zonarene --- --- --- --- --- --- --- ---
1523 (E)-γ-Bisabolene 0.2 0.1 --- --- --- --- --- ---
1526 Kessane --- --- --- --- --- --- --- ---
1527 Nootkatene --- --- --- --- --- --- --- ---
1529 trans-Cadina-1,4-diene 0.2 0.2 0.7 --- --- --- --- 0.1
1533 α-Cadinene 0.2 0.2 0.1 --- --- --- --- 0.2
1537 cis-Cadinene ether --- --- --- --- --- --- --- ---
1538 (E)-α-Bisabolene --- --- --- --- --- --- 0.5 ---
1538 α-Calacorene 0.3 0.3 0.1 --- --- --- --- 0.2
1542 trans-Cadinene ether --- --- --- --- --- --- --- ---
1544 Unidentified sesquiterpenoid f --- --- --- --- --- --- --- ---
1545 α-Elemol 0.1 --- 0.1 --- --- --- 0.2 ---
1554 Germacrene B --- --- 0.2 0.1 --- --- --- 0.2
1557 (E)-Nerolidol --- --- 0.2 0.7 2.6 4.7 0.7 4.1
1558 β-Calacorene --- --- --- --- --- --- --- ---
1565 Maaliol --- 0.3 --- 0.2 --- --- --- 1.0
1565 Palustrol --- --- 0.1 0.1 --- --- --- ---
1566 Dendrolasin --- --- --- --- --- --- tr ---
1573 Spathulenol 0.5 1.0 0.3 1.0 8.6 1.1 1.3 ---
1574 Germacra-1(10),5-dien-4β-ol --- --- --- --- --- --- --- 0.9
1578 Caryophyllene oxide 3.1 3.5 0.2 0.5 3.8 1.3 5.1 2.5
1582 Globulol 0.2 0.4 0.3 0.2 0.5 --- 0.1 0.3
1583 Gleenol --- --- --- --- --- --- --- ---
1586 Unidentified sesquiterpenoid g --- --- 3.2 --- --- --- --- 0.1
1590 Viridiflorol 0.2 0.2 0.1 0.2 1.0 0.2 tr 0.2
1593 Cubeban-11-ol --- --- --- --- --- --- --- ---
1595 Humulene epoxide I --- --- --- --- --- --- tr ---
1597 Curzerenone 0.4 --- --- --- --- --- --- ---
1600 Rosifoliol --- --- --- tr --- --- --- tr
1600 Guaiol --- --- 0.1 --- --- --- --- tr
1601 Ledol --- --- --- 0.1 --- --- --- ---
1601 β-Oplopenone --- --- --- --- --- --- --- ---
1605 β-Atlantol --- --- 0.5 --- --- --- --- ---
1606 Humulene epoxide II 0.2 0.2 --- 0.1 0.2 0.1 0.8 0.1
1606 Tetradecanal --- --- --- --- --- 0.4 --- ---
1609 Unidentified sesquiterpenoid h --- 2.8 --- --- --- --- --- ---
1612 1,10-di-epi-Cubenol --- --- --- --- --- --- --- ---
1613 α-Corocalene --- --- --- --- --- --- --- ---
1616 Junenol --- --- --- --- --- --- --- ---
1623 Selina-6-en-4β-ol --- --- 0.7 --- --- --- --- 0.9
1624 1-epi-Cubenol 0.5 0.4 --- 0.1 0.2 0.3 --- ---
1626 iso-Spathulenol --- --- 3.9 --- 0.5 0.1 0.5 2.5
1628 Caryophylla-4(12),8(13)-dien-5α-ol --- --- --- --- --- --- 0.4 ---
1633 Caryophylla-4(12),8(13)-dien-5β-ol --- --- --- --- --- --- 0.2 0.2
1636 allo-Aromadendrene epoxide --- --- --- --- --- --- --- ---
1638 τ-Cadinol 0.4 0.3 --- 0.1 --- 0.2 --- 0.4
1640 τ-Muurolol 0.8 1.2 --- 0.1 --- 0.1 --- 0.5
1640 Cubenol --- --- --- --- 0.3 --- --- ---
1643 α-Muurolol (= δ-Cadinol) 0.9 1.3 --- 0.2 0.2 0.3 0.2 0.1
1648 Unidentified sesquiterpenoid i --- --- --- 0.1 --- --- --- ---
1651 α-Eudesmol --- --- --- --- --- --- 0.2 ---
1652 α-Cadinol 1.6 1.2 0.3 0.3 --- 0.3 --- 0.7
1654 Selin-11-en-4α-ol --- --- 0.1 --- --- 0.3 --- ---
1655 Pogostol 0.5 --- --- --- --- --- 0.3 ---
1656 Unidentified fatty acid derivativej --- 1.0 --- 3.9 --- --- --- ---
1658 ar-Turmerone --- --- --- --- --- 0.1 --- ---
1658 9-Methoxycalamenene --- --- --- --- --- --- --- ---
1661 Intermedeol --- --- tr --- --- --- 0.2 ---
1661 Bulnesol --- --- --- --- --- --- --- ---
1663 (6Z)-Pentadecen-2-one --- --- --- 0.2 --- 0.4 --- ---
1664 (2E,6Z)-Farnesol --- --- --- --- --- --- --- 0.2
1666 14-Hydroxy-9-epi-(E)-caryophyllene --- --- --- --- --- --- --- ---
1670 Cadalene --- --- --- --- --- --- --- ---
1680 Unidentified sesquiterpenoid k --- --- --- --- 0.2 --- --- ---
1680 Germacra-4(15),5,10(14)-trien-1α-ol --- --- --- --- --- --- --- ---
1681 epi-α-Bisabolol --- --- --- --- --- --- 0.1 ---
1684 α-Bisabolol --- --- --- --- --- --- 0.2 0.2
1686 (2Z,6Z)-Farnesol --- --- --- --- --- --- 0.3 ---
1690 Shyobunol --- --- --- --- --- --- --- ---
1690 2-Pentadecanone --- --- --- 0.1 --- 0.3 --- ---
1700 Heptadecane --- --- --- --- --- 0.3 --- ---
1710 Unidentified sesquiterpenoid l --- --- --- --- --- --- --- ---
1711 (2E,6Z)-Farnesol --- --- 0.2 --- --- --- 0.2 ---
1722 Cryptomerione --- --- --- --- --- --- 0.3 ---
1725 Zerumbone --- --- --- --- --- --- 0.1 ---
1747 Cyclocolorenone --- --- --- 0.5 tr 0.1 --- ---
1763 Benzyl benzoate --- --- --- --- --- --- --- ---
1798 Curzerenone B 0.3 --- --- --- --- --- --- ---
1809 Hexadecanal --- --- --- --- --- 0.2 --- ---
1828 (2Z,6E)-Farnesyl acetate --- --- 0.1 --- --- --- 0.1 ---
2017 (E,E)-Geranyl linalool --- --- --- --- --- --- 0.1 ---
2103 (E)-Phytol --- --- 0.1 --- --- --- 0.3 0.9
Monoterpene hydrocarbons 1.5 14.6 11.4 44.3 13.0 15.9 13.2 8.5
Oxygenated monoterenoids 3.5 5.9 1.5 1.4 0.6 0.6 3.6 0.7
Sesquiterpene hydrocarbons 79.9 58.2 71.9 21.4 62.9 20.9 64.1 72.6
Oxygenated sesquiterpenoids 10.0 10.1 7.4 4.5 18.1 9.3 11.3 15.0
Diterpenoids 0.0 0.0 0.1 0.0 0.0 0.0 0.4 0.9
Benzenoids 0.0 3.2 0.0 21.4 0.0 0.0 0.6 0.1
Others 4.3 4.2 0.5 1.9 2.9 52.4 0.9 1.3
Total identified 99.2 96.2 92.8 94.8 97.5 99.0 94.2 99.0
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a RI = “Retention Index” determined in reference to a homologous series of n-alkanes. b Essential oil was used for larvicidal activity screening. c tr = “trace” (<0.05%). d Major essential oil components (>5%) are highlighted in blue bold font. e MS(EI): 202(45%), 187(18%), 159(70%), 145(47%), 131(58%), 119(60%), 117(60%), 105(71%), 91(100%), 81(55%), 43(100%). f MS(EI): 218(8%), 176(13%), 161(17%), 134(32%), 119(100%), 105(48%), 91(38%), 77(18%), 55(16%), 41(27%). g MS(EI): 220(11%), 205(10%), 187(9%), 162(63%), 147(65%), 134(41%), 119(100%), 107(42%), 105(53%), 93(67%), 91(58%), 79(29%), 69(18%), 55(21%), 43(100%), 41(28%). h MS(EI): 204(56%), 161(30%), 148(18%), 135(25%), 131(100%), 122(14%), 117(18%), 115(19%), 103(34%), 91(11%), 77(23%), 51(11%), 41(7%). i MS(EI): 223(8%), 162(97%), 147(67%), 133(65%), 119(60%), 105(100%), 94(81%), 91(68%), 81(52%), 67(25%), 59(88%), 43(34%), 41(33%). j MS(EI): 164(13%), 95(20%), 94(21%), 93(28%), 91(21%), 81(38%), 80(65%), 79(100%), 67(56%), 55(27%), 54(18%), 43(98%), 41(38%). k MS(EI): 218(51%), 190(14%), 175(30%), 161(79%), 147(49%), 134(87%), 119(100%), 105(53%), 91(49%), 77(21%), 55(17%), 41(34%). l MS(EI): 218(6%), 203(8%), 176(40%), 161(100%), 147(28%), 124(65%), 121(26%), 119(27%), 105(31%), 95(44%), 91(30%), 77(20%), 67(31%), 55(17%), 41(37%).

Interestingly, many Piper essential oils are rich in phenylpropanoids [2], particularly Pipers from the Neotropics [34,35]. In this current study, however, phenylpropanoids were generally found to be lacking, with the exception of P. politifolium, which had asaricin (18.7%) and safrole (2.7%). As far as we are aware, there have been no previous studies on the essential oils of P. arboricola, P. cambodianum, P. caninum, P. mekongense, P. montium, P. mutabile, P. politifolium, or P. rubrum.

The essential oil from the leaves and stems of P. bavinum, collected in Hainan, China, was found to be rich in spathulenol (8.0%), caryophyllene oxide (7.8%), propiopiperone (7.8%), and 2,4,6-trimethylbenzenepropanol (26.9%) [36]. The identification of 2,4,6-trimethylbenzenepropanol is doubtful, however; the identification was based only on the mass spectrum (retention indices not reported) and the compound is not found in the Dictionary of Natural Products [37]. In contrast, the essential oil of P. bavinum from Huong Son, Ha Tinh Province, Vietnam, was composed largely of bicyclogermacrene (10.6%), globulol (5.7%), viridiflorene (5.1%), α-pinene (4.4%), viridiflorol (3.5%), terpinen-4-ol (3.2%), and α-gurjunene (3.0%) [38]. The major components in P. bavinum essential oil in this study were bicyclogermacrene (8.9%), cyclocolorenone (7.9%), β-caryophyllene (6.2%), α-humulene (6.1%), γ-curcumene (5.8%), as well as α-pinene (3.3%), α-gurjunene (1.1%), and viridiflorol (1.0%). Thus, there are qualitative similarities between the two Vietnamese P. bavinum samples.

The phytochemistry of P. longum has been reviewed [2,39,40]. The leaf essential oil of P. longum from the Western Ghats region of Kerala, India, had elemol (22.5%), β-caryophyllene (16.8%), and α-humulene (5.8%) as the major components, while the stem essential oil was dominated by β-pinene (34.8%), α-pinene (14.0%), limonene (10.3%), and β-caryophyllene (9.3%) [41]. A report on the leaf essential oil of P. longum from Nghệ An Province, Vietnam showed the major components to be fonenol (40.5%) and elemol (8.2%) [42], and is, therefore, remarkably different from the P. longum essential oil in this present study, which was composed largely of α-pinene (5.1%), β-pinene (10.6%), β-caryophyllene (7.9%), (E)-nerolidol (8.1%), and two unidentified sesquiterpenoids (5.7% and 11.9%).

The major components in the essential oil from the leaves and stems of P. nigrum from Vietnam in this study were δ-elemene (20.4%), β-caryophyllene (7.7%), and β-selinene (5.1%). There have been numerous studies on the essential oils of P. nigrum, mostly on the fruit essential oils, but the leaves and stems have also been studied [2]. There are large variations in the leaf essential oil compositions of P. nigrum from India depending on the geographical location [43] and the particular cultivar [44]. Indian P. nigrum leaf oils are generally dominated by (E)-nerolidol, β-caryophyllene, germacrene D, and elemol, but show wide variation in concentrations [43,44]. In contrast, the leaf essential oil of P. nigrum “Bragantina”, cultivated in Belém, Pará State, Brazil, showed cubenol (14.6–21.5%), δ-cadinene (2.7–5.5%), bicyclogermacrene (6.4–8.2%), β-selinene (4.1–6.2%), α-copaene (3.5–5.2%), and α-gurjunene (3.5–5.1%) as the major components [45], while the essential oil from Hainan, China, was rich in β-caryophyllene (13.8%), spathulenol (6.2%), and caryophyllene oxide (6.0%) [36].

The phytochemistry of P. sarmentosum has also been reviewed [2,46]. The essential oils of P. sarmentosum have shown great variation, depending on geographical location. The essential oil from the leaves and stems of P. sarmentosum collected in Guangzhou, China, had asaricin (54.5%) and palmitic acid (8.2%) as major components [36]. On the other hand, the leaf essential oil of P. sarmentosum from Kuching, Sarawak, Malaysia, was composed largely of spathulenol (21.0%), myristicin (18.8%), β-caryophyllene (18.2%), and (E,E)-farnesol (10.5%) [47]. Furthermore, the essential oil from leaves and stems of P. sarmentosum from China (location not provided) was dominated by myristicin (65.2%) and β-caryophyllene (13.9%) [48]. The leaf essential oil of P. sarmentosum from Bạch Mã National Park, central Vietnam, was made up largely of benzenoids, benzyl benzoate (49.1%), benzyl alcohol (17.9%), benzyl salicylate (10.0%), and (2E)-butenylbenzene [49]. In complete contrast to these previous studies, the essential oil composition of P. sarmentosum essential oil from Da Nang, Vietnam, in this study, was composed of β-bisabolene (40.3%), β-pinene (5.5%), β-caryophyllene (5.5%), and caryophyllene oxide (5.1%) as the major components; neither asaricin, palmitic acid, myristicin, nor benzyl derivatives were observed in the present Vietnamese sample.

P. umbellatum, native to the Neotropics, has been investigated from several geographical locations, including Belém, Pará State, Brazil [50]; Campinas, São Paulo State, Brazil [51]; Araraquara, São Paulo State, Brazil [52]; Monteverde, Costa Rica [53]; and Topes de Collantes, Cuba [54]. The major components of P. umbellatum essential oils are summarized in Table 3. A cluster analysis based on the concentrations of the major components reveals two clearly defined groups. The P. umbellatum essential oil fits into a cluster along with essential oils from Monteverde, Costa Rica, and Belém, Brazil (Figure 1).

Table 3.

Major essential oil components (%) of Piper umbellatum.

Vietnam Belém-1 Belém-2 Belém-3 Belém-4 Campinas Monteverde Cuba Araraquara
Compound This work [50] [50] [50] [50] [51] [53] [54] [52]
Camphor 0.0 0.0 0.3 4.2 0.0 0.0 0.0 9.6 0.0
Safrole 0.1 0.0 0.0 0.0 0.0 0.0 0.0 26.4 0.0
δ-Elemene 9.2 0.0 0.0 0.0 0.0 1.5 1.4 0.0 0.0
β-Elemene 0.6 0.0 0.0 0.0 0.0 0.0 6.9 0.0 0.0
β-Caryophyllene 44.8 68.0 39.1 39.5 64.8 6.3 28.3 6.6 3.0
α-Humulene 3.8 5.9 4.0 2.1 6.5 0.7 2.2 0.0 1.1
γ-Muurolene 0.4 0.0 0.0 0.0 0.0 0.5 0.0 0.5 8.9
Germacrene D 1.8 6.2 13.3 12.7 8.7 55.8 16.7 3.7 34.2
Bicyclogermacrene 1.6 2.2 5.8 4.3 3.2 11.8 6.6 0.5 9.0
γ-Cadinene 0.4 0.4 1.4 2.1 0.0 1.4 0.0 0.0 5.9
δ-Cadinene 1.2 1.0 3.8 2.2 1.0 2.0 0.2 2.0 15.0
(E)-Nerolidol 4.1 4.9 4.8 11.1 7.5 0.4 4.4 4.9 4.4
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Figure 1.

Figure 1

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Agglomerative hierarchical cluster analysis based on the major components in Piper umbellatum essential oils.

2.3. Larvicidal Activities

Several of the Piper essential oils, depending on essential oil availability and availability of mosquito larvae, were screened for larvicidal activity against Aedes aegypti, and, when available, Aedes albopictus and Culex quinquefasciatus. The larvicidal activities are summarized in Table 4. According to a review by Dias and co-authors, plant essential oils are considered to have Ae. aegypti larvicidal activity if the LC50 values are less than 100 µg/mL [55]. Based on this criterion, all of the Piper essential oils in this investigation are active against larvae of this mosquito. Furthermore, four of the Piper essential oils showed outstanding larvicidal activity against Ae. aegypti, namely P. caninum, P. longum, P. montium, and P. mutabile, which had LC50 and LC90 values less than 10 µg/mL. In addition, P. nigrum essential oil had LC50 < 10 µg/mL and LC90 < 20 µg/mL. Although P. cambodianum had LC50 less than 10 µg/mL, the LC90 values were greater than 30 µg/mL.

Table 4.

Larvicidal activities (LC50 and LC90, μg/mL) of Piper essential oils from central Vietnam.

Mosquito Species Piper species
P. arboricola P. arboricola P. cambodianum P. caninum P. longum P. mekongense P. montium
Leaves Stems Leaves & Stems Leaves & Stems Leaves & Stems Leaves & Stems Leaves & Stems
Aedes aegypti
24-h LC50 (95% confidence) 26.85 (24.55–29.52) 28.45 (26.54–30.77) 8.861 (7.012–10.650) 1.376 (1.252–1.513) 5.342 (4.950–5.757) 40.16 (37.09–42.88) 1.964 (1.778–2.169)
24-h LC90 (95% confidence) 47.83 (37.83–71.41) 41.88 (37.37–49.09) 36.42 (29.16–49.60) 2.419 (2.126–2.887) 7.730 (7.006–8.955) 52.66 (49.13–57.71) 3.743 (3.273–4.472)
48-h LC50 (95% confidence) 15.59 (12.46–18.32) 26.60 (24.51–28.97) 6.773 (4.957–8.467) 1.304 (1.183–1.437) 4.979 (4.608–5.377) 36.91 (34.35–39.56) 1.533 (1.376–1.703)
48-h LC90 (95% confidence) 46.24 (40.60–55.31) 39.79 (35.89–46.73) 30.62 (24.39–42.18) 2.351 (2.060–2.822) 7.354 (6.659–8.469) 50.00 (46.18–55.42) 3.127 (2.714–3.773)
Aedes albopictus
24-h LC50 (95% confidence) N.T. N.T. 34.20 (31.90–36.73) N.T. N.T. N.T. N.T.
24-h LC90 (95% confidence) N.T. N.T. 45.98 (42.28–51.38) N.T. N.T. N.T. N.T.
48-h LC50 (95% confidence) N.T. N.T. 31.13 (29.15–33.70) N.T. N.T. N.T. N.T.
48-h LC90 (95% confidence) N.T. N.T. 40.82 (37.09–47.24) N.T. N.T. N.T. N.T.
Culex quinquefasciatus
24-h LC50 (95% confidence) N.T. N.T. 56.16 (51.10–61.54) N.T. N.T. N.T. N.T.
24-h LC90 (95% confidence) N.T. N.T. 104.7 (93.0–121.7) N.T. N.T. N.T. N.T.
48-h LC50 (95% confidence) N.T. N.T. 51.21 (46.52–56.27) N.T. N.T. N.T. N.T.
48-h LC90 (95% confidence) N.T. N.T. 97.91 (86.55–114.54) N.T. N.T. N.T. N.T.
Mosquito Species Piper species Permethrin
P. montium P. mutabile P. nigrum P. rubrum P. rubrum P. sarmentosum
Leaves & Stems Leaves & Stems Leaves & Stems Leaves Stems Leaves & Stems
Aedes aegypti
24-h LC50 (95% confidence) 1.925 (1.771–2.092) 1.850 (1.715–1.997) 8.805 (7.905–9.811) 24.98 (22.74–27.48) 30.87 (28.66–33.32) 22.82 (17.73–27.91) 6.4 × 10−4 (5.5 × 10−4–7.5 × 10−4)
24-h LC90 (95% confidence) 3.180 (2.784–3.793) 2.696 (2.442–3.108) 18.83 (16.15–23.13) 43.70 (38.35–52.39) 45.54 (40.14–54.01) 130.6 (88.7–256.8) 2.5 × 10−3 (1.9 × 10−3–3.44 × 10−3)
48-h LC50 (95% confidence) 1.691 (1.531–1.867) 1.695 (1.544–1.842) 6.909 (6.149–7.720) 22.15 (20.19–24.25) 26.09 (23.83–28.63) 18.42 (12.97–23.48) N.T.
48-h LC90 (95% confidence) 3.024 (2.714–3.509) 2.641 (2.367–3.122) 15.49 (13.28–19.03) 37.18 (32.97–43.97) 44.80 (40.63–51.40) 126.8 (90.1–220.9) N.T.
Aedes albopictus
24-h LC50 (95% confidence) N.T. N.T. 43.92 (40.18–47.95) N.T. N.T. 49.24 (44.72–53.99) 2.3 × 10−3 (2.1 × 10−3–2.6 × 10−3)
24-h LC90 (95% confidence) N.T. N.T. 74.25 (66.15–86.73) N.T. N.T. 90.30 (80.19–105.31) 4.2 × 10−3 (3.8 × 10−3–4.9 × 10−3)
48-h LC50 (95% confidence) N.T. N.T. 39.19 (35.75–42.86) N.T. N.T. 38.33 (33.62–42.97) N.T.
48-h LC90 (95% confidence) N.T. N.T. 67.14 (59.57–79.16) N.T. N.T. 86.32 (74.63–104.92) N.T.
Culex quinquefasciatus
24-h LC50 (95% confidence) N.T. N.T. N.T. N.T. N.T. N.T. 1.7 × 10−2 (1.5 × 10−2–1.8 × 10−2)
24-h LC90 (95% confidence) N.T. N.T. N.T. N.T. N.T. N.T. 2.9 × 10−2 (2.7 × 10−2–3.3 × 10−2)
48-h LC50 (95% confidence) N.T. N.T. N.T. N.T. N.T. N.T. N.T.
48-h LC90 (95% confidence) N.T. N.T. N.T. N.T. N.T. N.T. N.T.
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N.T. = Not tested.

In order to provide insight into the components responsible for the larvicidal activity, a multivariate analysis, agglomerative hierarchical cluster (AHC), and principal component analysis (PCA) were carried out to correlate composition with activity. The cluster analysis revealed two clearly defined clusters, one cluster with excellent larvicidal activity (P. mutabile, P. caninum, P. montium, P. longum, and P. nigrum) and another cluster of Piper essential oils with good larvicidal activity (Figure 2).

Figure 2.

Figure 2

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Agglomerative hierarchical cluster analysis based on the major components of the Piper essential oils from central Vietnam along with larvicidal activities (LC50 and LC90) against Aedes aegypti.

The principal component analysis indicates a positive correlation between Ae. aegypti larvicidal activity (LC50 and LC90) and concentrations of β-caryophyllene, β-bisabolene, α-pinene, and β-pinene (Figure 3). In addition, P. caninum, P. montium, and P. mutabile essential oils had relatively high concentrations of ar-curcumene; P. caninum, P. longum, P. montium, and P. mutabile had relatively high concentrations of linalool; and P. nigrum essential oil was rich in δ-elemene.

Figure 3.

Figure 3

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Principal component biplot of PC1 and PC2 scores and loadings indicating the correlation of chemical components of Piper essential oils from central Vietnam and Aedes aegypti larvicidal activity.

Several Piper essential oils had previously demonstrated larvicidal activity against Ae. aegypti [55,56,57]. The fruit essential oil of P. aduncum from northeastern Brazil was found to be rich in both β-pinene (32.7%) and β-caryophyllene (17.1%) and showed larvicidal activity with LC50 of 30.2 µg/mL [58]. Similarly, P. nigrum fruit essential oil with β-caryophyllene (24.2%) and β-pinene (5.4%) had LC50 of 75.8 µg/mL [58]. The phenylpropanoid-rich essential oils of P. permucronatum and P. hostmanianum showed larvicidal activity against Ae. aegypti of 36 and 54 µg/mL, respectively [56]. Furthermore, P. sarmentosum essential oil from Thailand, dominated by croweacin (71.0%) and β-caryophyllene (7.4%), showed very good mosquito larvicidal activity against Anopheles cracens [59]. In addition, α-pinene, β-pinene [60], linalool [61], and β-caryophyllene [62] had previously shown Ae. aegypti larvicidal activities with LC50 of 15.4, 12.1, 38.6, and 88.3 µg/mL, respectively.

3. Materials and Methods

3.1. Plant Material

Piper plant material (leaves and stems) was collected from several different locations in central Vietnam (Table 1). The plants were identified by Dr. Do Ngoc Dai, and voucher specimens (see Table 1) have been deposited in the Pedagogical Institute of Science, Vinh University. The fresh plant materials (2.0 kg each) were shredded and hydrodistilled for 4 h using a Clevenger type apparatus (Witeg Labortechnik, Wertheim, Germany). Essential oil yields are summarized in Table 1.

3.2. Gas Chromatographic-Mass Spectral Analysis

Each of the Piper essential oils was analyzed by gas chromatography–mass spectrometry (GC-MS) as previously described [63]: Shimadzu GCMS-QP2010 Ultra (Shimadzu Scientific Instruments, Columbia, MD, USA), electron impact (EI) mode (electron energy = 70 eV), scan range = 40–400 atomic mass units, scan rate = 3.0 scans/s, and GC–MS solution software. The GC column was a ZB-5 fused silica capillary column (30 m length × 0.25 mm internal diameter) with a (5% phenyl)-polymethylsiloxane stationary phase and a film thickness of 0.25 μm; He carrier gas with a column head pressure of 552 kPa and flow rate of 1.37 mL/min; injector temperature = 250 °C, ion source temperature = 200 °C. The GC oven temperature program was programmed to have an initial temperature of 50 °C, and the temperature increased at a rate of 2 °C/min to 260 °C. A 5% w/v solution of the sample in CH2Cl2 was prepared, and 0.1 μL was injected with a splitting mode (30:1). Identification of the oil components was based on their retention indices determined by reference to a homologous series of n-alkanes, and by comparison of their mass spectral fragmentation patterns with those reported in the databases [64,65,66,67]. The percentages of each component in the essential oils are reported as raw percentages based on total ion current without standardization. Gas chromatograms for the Piper essential oils are available as supplementary material.

3.3. Mosquito Larvicidal Assay

Eggs of Ae. aegypti were purchased from Institute of Biotechnology, Vietnam Academy of Science and Technology, and maintained at the Laboratory of Department of Pharmacy of Duy Tan University, Da Nang, Vietnam. For the assay, aliquots of the essential oils of Piper species, dissolved in DMSO (1% stock solution), was placed in a 500-mL beaker and added to water that contained 20 larvae (third and early fourth instar). With each experiment, a set of controls using DMSO was also run for comparison. Mortality was recorded after 24 h and again after 48 h of exposure during which no nutritional supplement was added. The experiments were carried out 25 ± 2 °C. Each test was conducted with four replicates with several concentrations (100, 50, 25, 12.5, 6.0, 3.0, 1.5, and 0.7 μg/mL). Larvicidal activities against Ae. albopictus and Culex quinquefasciatus (reared from wild populations) were determined similarly with concentrations of 150, 100, 50, 25, and 12.5 μg/mL. Permethrin was used as a positive control.

3.4. Statistical Analysis

Mosquito larvicidal activities (LC50 and LC90) were determined by log-probit analysis using XLSTAT v. 2018.5 (Addinsoft, Paris, France). The chemical compositions of the Piper essential oils were used in the multivariate analyses. The essential oil compositions were treated as operational taxonomic units (OTUs), and the concentrations (percentages) of 29 major essential oil components and the 24-h LC50 and LC90 larvicidal activity data were used to determine the associations between the Piper essential oils using agglomerative hierarchical cluster (AHC) analysis using XLSTAT Premium, version 2018.5 (Addinsoft, Paris, France). Dissimilarity was determined using Euclidean distance, and clustering was defined using Ward’s method. For the principal component analysis (PCA), the 29 major components and the larvicidal data were taken as variables using a Pearson correlation matrix using XLSTAT Premium, version 2018.5 (Addinsoft, Paris, France). A total of 414 data (31 variables × 12 samples) were used for the PCA.

4. Conclusions

Plant materials from 13 species of Piper, growing in central Vietnam were collected and the essential oils obtained and chemically analyzed. Larvicidal activity assays indicated that five Piper species (P. nigrum, P. mutabile, P. longum, P. montium, and P. caninum) showed excellent larvicidal activities with LC50 and LC90 values < 10 μg/mL, and that the larvicidal activities are correlated with concentrations of β-caryophyllene, β-bisabolene, β-pinene, and α-pinene. These Piper essential oils deserve consideration for future applications as natural, sustainable alternatives to synthetic pesticides for mosquito control.

Acknowledgments

P.S. and W.N.S. participated in this work as part of the activities of the Aromatic Plant Research Center (APRC, https://aromaticplant.org/).

Supplementary Materials

The following are available, Figures S1–S16: Total Ion Chromatograms of Essential Oils of Piper Species from Central Vietnam.

Click here for additional data file. (3.8MB, pdf)

Author Contributions

Conceptualization, L.T.H. and P.S.; Data curation, W.N.S.; Formal analysis, W.N.S.; Funding acquisition, N.H.H.; Investigation, L.T.H., N.H.H., D.N.D., T.A.T., and V.T.H.; Methodology, L.T.H., N.H.H., and P.S.; Project administration, N.H.H.; Resources, L.T.H., N.H.H., D.N.D., and P.S.; Software, P.S.; Supervision, N.H.H. and W.N.S.; Validation, L.T.H., N.H.H., P.S., and W.N.S.; Visualization, W.N.S.; Writing—original draft, W.N.S.; Writing—review and editing, L.T.H., N.H.H., D.N.D., P.S., and W.N.S.

Funding

This research was funded by Duy Tan University.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Sample Availability: Essential oil samples are not currently available.

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