Chemical Characterization of Three Artemisia tridentata Essential Oils and Multivariate Analyses: A Preliminary Investigation

Abstract

Background/Objective: Big sagebrush (Artemisia tridentata Nutt., Asteraceae) is a conspicuous shrub growing in arid and semi-arid regions of intermountain western North America, from eastern Washington and Oregon, through Nevada, Idaho, and Utah, into northern Arizona and New Mexico, and east as far as the western Dakotas, and Colorado. At least three subspecies of A. tridentata have been recognized, including A. tridentata subsp. tridentata Nutt. (basin big sagebrush), A. tridentata subsp. wyomingensis Beetle & A.L.Young (Wyoming big sagebrush), and A. tridentata subsp. vaseyana (Rydb.) Beetle (mountain big sagebrush). Although big sagebrush is an important food source and cover for several animal species, the volatile phytochemistry has shown wide variation in composition. The purpose of this work was to compare and contrast the essential oil compositions of the three subspecies of A. tridentata growing in southwestern Idaho. Methods/Results: Several samples of A. tridentata subsp. wyomingensis and A. tridentata subsp. vaseyana were collected, the essential oils obtained by hydrodistillation using a Likens-Nickerson apparatus in yields of 2.33%-4.45% and 0.90%-1.73%, respectively, and the essential oils analyzed by gas chromatographic techniques. Although A. tridentata shows wide variation in essential oil compositions, multivariate analysis (hierarchical cluster analysis and principal component analysis) indicated A. tridentata subsp. tridentata to be characterized by high concentrations of yomogi alcohol (5.8%-30.8%) and camphor (5.2%-20.1%), while camphor was the defining component in A. tridentata subsp. wyomingensis (10.0%-30.1%) and subsp. vaseyana (16.1%-40.2%). One sample of A. tridentata subsp. vaseyana was dominated by α-thujone (76.1%), however. Conclusion: There is much variation in essential oil compositions of A. tridentata, both within subspecies and between geographical locations; much additional investigation is necessary to more fully characterize the volatile phytochemistry of this plant.

Keywords

big sagebrush basin sagebrush Wyoming sagebrush mountain sagebrush enantiomeric distribution multivariate analysis

Introduction

Big sagebrush, Artemisia tridentata Nutt., Asteraceae, is a conspicuous shrub growing in much of the western United States (Figure 1). The plant is an essential food source and cover for the pygmy rabbit, Brachylagus idahoensis¹; the Gunnison sage-grouse, Centrocercus minimus; and the greater sage-grouse, Centrocercus urophasianus,^2,3 which rely on this plant for up to 99% of their winter forage. In addition, several wild ungulates, including elk, Cervus canadensis; mule deer, Odocoileus hemionus⁴; and pronghorn, Antilocapra americana,⁵ forage on big sagebrush.

Figure 1.

Range of Artemisia tridentata in North America.

The essential oil compositions of A. tridentata have been previously reported,⁶ and the plant has been characterized by the major components camphor (20%-45%), camphene (3%-21%), 1,8-cineole (12%-30%), thujone (6%), and borneol (5%).^7-12 Additionally, a number of irregular monoterpenoids have been isolated and characterized.^13-17 Sesquiterpene lactones have been characterized in the non-volatile extracts of A. tridentata.¹⁸

There is debate regarding the varieties and subspecies of A. tridentata. Nevertheless, there are three widely recognized subspecies: A. tridentata subsp. tridentata Nutt., A. tridentata subsp. wyomingensis Beetle & A.L.Young, and A. tridentata subsp. vaseyana (Rydb.) Beetle.^19,20 It has been observed that the three different sagebrush subspecies have different palatability attributes with respect to herbivory. The vaseyana and wyomingensis subspecies are generally more palatable to herbivores, while the tridentata subspecies is the least preferable.²¹ The chemical constituents of the three subspecies most likely play a role in the observed herbivory.^21-23

To complement our previous examination of A. tridentata subsp. tridentata,⁶ the purpose of this study was to characterize the essential oils of A. tridentata subsp. wyomingensis and A. tridentata subsp. vaseyana growing in southwestern Idaho using gas chromatographic techniques and to compare and contrast the three subspecies using multivariate analyses.

Results and Discussion

Essential Oil Composition

A. tridentata subsp. tridentata

The essential oil composition of A. tridentata subsp. tridentata from southwestern Idaho has been previously reported.⁶ The major components were yomogi alcohol (5.8%-30.8%), santolina epoxide (1.7%-10.5%), camphor (5.2%-20.1%), and (Z)-tagetone (0.9%-8.9%).

A. tridentata subsp. wyomingensis

The aerial parts of A. tridentata subsp. wyomingensis were hydrodistilled to give pale yellow essential oils in 2.34% to 4.45% yield. Gas chromatographic analysis of the six essential oil samples led to identification of a total of 53 compounds, which accounted for 73.4%-84.7% of the total compositions. The essential oil compositions of A. tridentata subsp. wyomingensis are compiled in Table 1.

Table 1.

Chemical Composition (%) of the Essential Oils From the Aerial Parts of Artemisia tridentata subsp. wyomingensis.

RI_calc	RI_db	Compound^a	Atw#1	Atw#2	Atw#3	Atw#4	Atw#5	Atw#6
888	888	Ethyl pent-4-enoate	1.6	0.4	0.8	0.3	0.3	0.5
901	902	Santolina triene	6.2	1.8	5.1	4.7	5.1	12.6
902	909	2-Acetylfuran	1.9	1.4	1.1	-	1.2	-
922	922	Artemisia triene	0.2	0.1	-	0.2	0.1	0.1
932	933	α-Pinene	-	-	-	0.3	0.1	0.2
932	-	Unidentified (932)^b	-	4.0	-	-	-	-
946	944	4,4-Dimethyl-2-buten-4-olide	-	8.4	0.2	-	-	-
950	954	Camphene	0.3	-	1.3	4.7	1.4	0.4
974	971	Artemiseole	2.9	4.8	7.9	9.9	16.6	3.1
980	978	β-Pinene	-	-	-	0.4	-	-
990	990	Dehydro-1,8-cineole	-	-	-	-	-	0.2
995	996	Yomogi alcohol	7.8	3.5	5.3	2.8	0.9	6.6
1008	1008	Isomaltol	-	-	-	0.2	-	-
1009	1003	Isobutyl 2-methylbutanoate	1.2	0.9	1.0	0.3	0.5	0.2
1025	1025	p-Cymene	0.9	0.4	0.2	0.3	0.3	1.0
1028	-	Unidentified (1028)^c	1.0	0.6	1.4	1.4	1.5	1.4
1031	1031	Santolina alcohol	0.3	0.2	0.2	0.2	0.3	0.3
1033	1032	1,8-Cineole	6.3	7.2	1.8	4.5	4.9	11.1
1039	1035	γ-Valerolactone	-	1.7	-	-	-	-
1047	1047	Santolina epoxide	5.9	3.6	4.2	1.5	1.5	7.1
1051	1049	cis-Arbusculone	0.2	1.1	0.6	0.6	1.1	0.6
1052	1049	o-Cresol	0.2	0.3	0.2	0.1	0.2	-
1054	1053	epi-Isolyratol	0.6	1.0	0.8	0.7	0.8	1.0
1058	1058	γ-Terpinene	-	0.3	-	-	-	0.3
1068	1070	Isolyratol	1.5	2.3	2.2	1.9	2.1	2.6
1072	1072	α-Santolina alcohol	3.3	2.0	2.4	0.8	1.0	2.2
1074	1075	epi-α-Santolina alcohol	1.6	1.2	1.3	0.6	0.9	1.0
1080	1079	Artemisia alcohol	8.6	1.4	2.3	0.8	0.4	2.0
1110	-	Unidentified (1110)^d	2.4	1.4	1.8	0.7	0.9	1.6
1116	1115	3-Methyl-3-vinylcyclohexanone	0.5	0.7	0.7	0.5	0.8	0.4
1133	1129	Methyl santolinate	2.6	5.0	6.6	6.9	13.6	2.6
1141	-	Unidentified (1141)^e	1.2	1.7	1.9	1.3	2.6	1.5
1150	1149	Camphor	10.0	13.4	13.4	30.1	14.0	10.5
1166	1164	β-Artemisyl acetate	3.4	5.2	6.2	5.6	0.8	10.0
1174	1173	Borneol	-	-	1.2	0.4	0.2	0.1
1181	1180	Terpinen-4-ol	0.6	0.6	0.2	0.4	0.4	0.8
1187	1188	p-Cymen-8-ol	0.3	0.4	0.3	0.2	-	0.4
1199	1197	Myrtenal	-	-	-	0.4	-	-
1211	1208	Verbenone	-	-	-	0.3	-	-
1234	-	Unidentified (1234)^f	7.3	5.2	6.2	2.5	4.3	5.4
1241	-	Unidentified (1241)^g	0.3	-	1.1	0.8	1.5	-
1251	1253	trans-Chrysanthenyl acetate	0.5	0.4	1.4	0.8	1.3	0.2
1257	1255	Geraniol	0.7	0.4	0.5	0.2	0.2	0.4
1261	1258	Santolinolide B'	1.4	1.7	0.2	0.8	1.3	0.8
1265	1259	Santolinolide B	-	0.7	0.6	0.6	1.3	0.2
1269	1266	cis-Chrysanthenyl acetate	1.2	0.6	1.6	0.8	1.0	0.2
1293	1292	Santolinolide C	0.6	0.5	0.4	-	0.2	0.3
1367	-	Unidentified (1367)^h	1.3	1.5	1.9	0.4	0.6	0.3
1396	1396	(2E)-13,7-Trimethyl-2,6-octadienyl acetate	0.2	-	-	-	-	-
1419	1424	(E)-β-Caryophyllene	0.4	0.4	0.1	0.2	0.2	0.2
1439	-	Verbenyl 2-methylpropionate	0.6	0.5	0.4	0.3	0.5	0.4
1481	1480	Germacrene D	0.3	0.3	0.2	0.2	0.2	0.2
1555	-	Unidentified (1555)ⁱ	2.3	0.7	1.3	1.3	1.9	0.6
1562	1562	(E)-Nerolidol	-	0.3	-	-	-	-
1584	1587	Caryophyllene oxide	0.4	0.6	0.2	0.2	-	0.6
1639	1636	Caryophylla-4(12),8(13)-dien-5β-ol	-	0.4	0.2	0.2	0.4	0.5
1645	1647	Methyl (Z)-jasmonate	0.5	0.3	0.5	0.3	0.4	0.5
1657	1655	α-Bisabolol oxide B	-	-	-	-	-	0.3
1676	1676	Methyl epi-(E)-jasmonate	0.2	-	-	-	-	-
1686	1683	Germacra-4(15),5,10(14)-trien-1α-ol	-	-	-	-	-	0.2
1805	-	Unidentified (1805)^j	1.1	1.0	1.5	1.2	1.0	1.2
2045	2045	Kaurene	0.1	0.1	0.1	0.1	0.1	0.1
		Monoterpene hydrocarbons	9.1	4.5	8.9	12.1	9.1	16.9
		Oxygenated monoterpenoids	59.2	54.2	58.6	69.5	61.6	61.5
		Sesquiterpene hydrocarbons	0.7	0.7	0.3	0.4	0.4	0.4
		Oxygenated sesquiterpenoids	0.4	1.3	0.4	0.4	0.4	1.5
		Benzenoid aromatics	0.2	0.3	0.2	0.1	0.2	0.0
		Diterpenoids	0.1	0.1	0.1	0.1	0.1	0.1
		Others	6.4	14.9	5.0	2.3	4.2	2.2
		Total identified	76.2	76.0	73.4	84.7	76.0	82.6
		Number identified	38	41	39	42	38	42

Abbreviations: RI_calc, retention index determined with respect to a homologous series of n-alkanes on a ZB-5ms column using the linear equation of van den Dool and Kratz²⁴; RI_db, reference retention index obtained from the databases.^25-28

^aMass spectra of unidentified components are available as a supplementary figure (Figure S1).

^bMS(EI): 136(2%), 113(47%), 93(32%), 71(99%), 67(100%), 55(40%), 43(63%), 41(35%).

^cMS(EI): 135(3%), 107(5%), 94(5%), 79(9%), 69(100%), 53(8%), 41(84%).

^dMS(EI): 134(3%), 121(45%), 107(14%), 105(15%), 93(58%), 91(44%), 79(100%), 77(42%), 43(21%), 41(29%).

^eMS(EI): 137(9%), 123(26%), 119(100%), 105(28%), 95(35%), 93(35%), 91(93%), 79(64%), 77(46%), 67(60%), 55(42%), 43(40%), 41(68%).

^fMS(EI): 139(6%), 121(4%), 96(94%), 81(100%), 75(62%), 57(61%), 43(63%).

^gMS(EI): 137(9%), 123(26%), 119(100%), 105(28%), 95(35%), 93(35%), 91(93%), 79(64%), 77(46%), 67(60%), 55(42%), 43(40%), 41(68%).

^hMS(EI): 139(3%), 117(37%), 96(30%), 81(30%), 75(30%), 67(9%), 55(9%), 43(100%).

ⁱMS(EI): 150(16%), 149(25%), 134(10%), 107(12%), 91(11%), 79(10%), 43(100%).

^jMS(EI): 192(3%), 179(3%), 151(8%), 141(27%), 123(14%), 108(67%), 80(19%), 79(19%), 69(100%), 55(10%), 43(29%), 41(59%).

The major components found in the essential oil of A. tridentata subsp. wyomingensis were camphor (10.0%-30.1%), artemiseole (2.9%-16.6%), methyl santolinate (2.6%-13.6%), 1,8-cineole (1.8%-11.1%), santolina triene (1.8%-12.6%), β-artemisyl acetate (0.8%-10.0%), and an unidentified component (retention index [RI] = 1234, 2.5%-7.3%).

A. tridentata subsp. vaseyana

Hydrodistillation of A. tridentata subsp. vaseyana gave yellow essential oils (0.89%-1.73% yield). An aqueous leaf extract of each A. tridentata subsp. vaseyana sample gave a bright blue-white fluorescence under illumination with UV light indicating the presence of coumarins (eg, isoscopoletin, scopoletin, and esculetin) in the leaves.⁹ Coumarins are known to be abundant in A. tridentata subsp. vaseyana, but are present in only trace amounts in subsp. tridentata or subsp. wyomingensis.¹⁹ The chemical components of A. tridentata subsp. vaseyana essential oils are listed in Table 2.

Table 2.

Chemical Composition (%) of the Essential Oils From the Aerial Parts of Artemisia tridentata subsp. vaseyana.

RI_calc	RI_db	Compound^a	Atv#1	Atv#2	Atv#3	Atv#4
900	902	Santolina triene	-	-	4.5	4.0
910	912	2,5-Diethenyl-2-methyltetrahydrofuran	-	-	0.1	-
920	926	Tricyclene	0.2	tr	0.3	0.2
922	927	α-Thujene	0.1	0.1	tr	-
931	932	α-Pinene	2.0	0.5	2.1	0.6
941	943	Thuja-2,4(10)-diene	tr	tr	-	-
946	942	4,4-Dimethyl-2-butenolide	-	-	0.7	5.1
949	953	Camphene	5.3	tr	7.6	1.9
972	972	Sabinene	2.3	1.1	0.2	-
973	971	Artemiseole	-	-	4.4	9.2
978	978	β-Pinene	1.2	0.3	1.1	0.5
989	990	Dehydro-1,8-cineole	0.5	0.3	-	0.2
990	991	Myrcene	0.2	0.3	2.6	0.1
994	996	Yomogi alcohol	-	-	-	0.1
1006	1007	α-Phellandrene	-	-	-	0.1
1016	1018	α-Terpinene	0.3	0.2	-	-
1023	1025	p-Cymene	0.2	0.2	0.2	0.5
1026	1026	2-Acetyl-3-methylfuran	tr	tr	0.1	-
1029	1030	Limonene	0.3	0.1	0.3	0.2
1031	1031	β-Phellandrene	-	0.1	-	-
1031	1031	Santolina alcohol	-	-	-	0.1
1033	1032	1,8-Cineole	24.6	10.4	1.0	7.0
1035	1035	γ-Valerolactone	-	-	0.1	0.4
1044	1045	Benzene acetaldehyde	0.1	tr	-	-
1045	1047	Santolina epoxide	-	-	2.2	0.6
1050	1049	cis-Arbusculone	-	-	-	4.2
1052	-	Unidentified (1052)^b	-	-	-	3.9
1053	1053	epi-Isolyratol	-	-	0.1	0.1
1058	1058	γ-Terpinene	0.6	0.4	-	0.1
1067	1070	Isolyratol	-	-	0.3	0.3
1068	1068	trans-Arbusculone	-	-	0.1	2.3
1070	1069	cis-Sabinene hydrate	0.5	0.4	-	0.3
1070	1072	α-Santolina alcohol	-	-	0.1	0.3
1072	1075	epi-α-Santolina alcohol	-	-	0.1	-
1080	1079	Artemisia alcohol	-	-	tr	0.1
1086	1086	Terpinolene	0.1	0.1	-	tr
1101	1101	Linalool	0.2	-	0.1	0.1
1102	1101	trans-Sabinene hydrate	0.3	-	-	0.1
1108	1105	α-Thujone	16.3	76.1	1.9	0.1
1113	1113	Phenethyl alcohol	-	-	-	tr
1118	1118	β-Thujone	1.5	3.5	0.1	-
1121	1122	Dehydrosabina ketone	0.1	tr	-	-
1122	1122	Chrysanthenone	tr	tr	0.1	0.3
1123	1122	trans-p-Mentha-2,8-dien-1-ol	0.1	0.1	-	-
1126	1124	cis-p-Menth-2-en-1-ol	0.1	-	-	-
1127	1126	α-Campholenal	tr	-	-	-
1127	-	Unidentified (1127)^c	-	-	1.3	-
1133	1129	Methyl santolinate	-	-	0.2	1.1
1139	1144	trans-Tagetone	-	0.1	0.4	1.4
1140	1138	cis-p-Mentha-2,8-dien-1-ol	0.1	-	-	-
1140	1140	exo-Isocitral	0.1	-	-	-
1141	1138	trans-Sabinol	-	0.3	-	-
1143	1141	trans-Pinocarveol	0.7	0.1	-	-
1144	1142	trans-p-Menth-2-en-1-ol	0.1	tr	-	-
1144	1145	trans-Verbenol	-	tr	0.9	0.9
1144	1141	trans-Pinocarveol	-	-	-	0.1
1148	-	Unidentified (1148)^d	-	-	1.0	-
1149	1149	Camphor	28.7	0.1	40.2	16.1
1153	1152	Nerol oxide	-	-	0.3	0.2
1154	1153	neo-Thujol	-	0.2	-	-
1156	1156	β-Pinene oxide	0.1	0.1	-	-
1158	1157	Sabina ketone	tr	-	-	-
1164	1164	Pinocarvone	0.7	0.2	-	-
1164	1164	Lyratol	-	-	0.7	0.7
1170	1168	α-Phellandrene epoxide	0.1	-	-	-
1171	1169	Thujol	-	0.3	-	-
1172	1170	δ-Terpineol	0.3	0.1	-	0.1
1174	1173	Borneol	2.2	-	1.9	0.9
1182	1180	Terpinen-4-ol	1.9	1.4	0.4	0.6
1184	1184	Thuj-3-en-10-al	0.1	tr	-	-
1189	1187	trans-p-Mentha-1(7),8-dien-2-ol	0.1	-	-	-
1189	1186	p-Cymen-8-ol	-	0.1	-	-
1193	1202	Myrtenol	0.1	-	-	-
1197	1195	α-Terpineol	2.0	0.9	0.3	0.9
1200	1198	cis-Dihydrocarvone	0.1	tr	0.3	-
1203	1213	4-Hydroxy-α-thujone	-	tr	-	-
1205	1202	cis-Sabinol	-	tr	-	-
1220	1218	trans-Carveol	0.1	tr	0.1	-
1226	1229	Nerol	0.3	0.1	0.1	0.2
1228	1232	Citronellol	-	-	0.2	-
1231	1230	cis-p-Mentha-1(7),8-dien-2-ol	0.1	-	-	-
1234	1232	cis-Carveol	tr	tr	tr	-
1239	1238	Neral	0.1	tr	-	-
1244	1242	Cuminal	tr	tr	-	-
1249	1253	trans-Chrysanthenyl acetate	-	-	1.2	2.2
1251	1249	Geraniol	tr	tr	-	-
1255	-	Unidentified (1255)^e	-	-	0.6	1.3
1267	1266	cis-Chrysanthenyl acetate	-	-	0.4	0.5
1269	1268	Geranial	0.1	tr	0.1	-
1285	1284	Lavandulyl acetate	-	-	0.2	0.3
1286	1285	Bornyl acetate	0.3	-	0.3	0.1
1291	1291	trans-Sabinyl acetate	-	tr	-	-
1293	1298	Thujyl acetate	-	tr	-	-
1294	1291	p-Cymen-7-ol	-	tr	-	-
1320	1326	Myrtenyl acetate	-	tr	-	-
1349	1349	α-Terpinyl acetate	0.5	tr	0.1	-
1352	1350	Citronellyl acetate	-	tr	0.1	-
1361	1361	Neryl acetate	1.2	0.5	2.5	2.8
1367	-	Unidentified (1367)^f	-	-	0.4	1.0
1380	1380	Geranyl acetate	0.1	0.1	0.5	0.3
1424	1424	(E)-β-Caryophyllene	0.8	0.3	0.6	0.2
1447	1448	Neryl propionate	tr	tr	-	-
1456	1453	α-Humulene	0.1	tr	-	-
1478	1482	γ-Curcumene	0.1	tr	-	-
1482	1483	Germacrene D	0.2	0.2	-	0.3
1483	1483	Davana ether 1	-	-	-	2.9
1484	1485	Neryl isobutyrate	0.1	tr	-	-
1492	1500	trans-Chrysanthenyl 2-methylbutanoate	-	-	0.2	-
1497	1497	Bicyclogermacrene	0.1	0.1	-	-
1504	1502	Davana ether 2	-	-	-	8.9
1505	1504	Davana ether 3	-	-	-	1.4
1520	1520	δ-Cadinene	tr	tr	-	-
1523	1521	Davana ether 4	-	-	-	4.7
1529	1529	Artedouglasia oxide A	-	-	0.1	-
1551	1557	Davanone B	-	-	0.1	-
1561	1562	(E)-Nerolidol	-	-	-	1.0
1572	1582	Neryl isovalerate	0.1	0.1	-	-
1579	1578	Spathulenol	-	0.1	-	-
1583	1582	Davanone D	-	-	8.5	0.3
1585	1587	Caryophyllene oxide	0.1	tr	0.7	-
1638	1632	Caryophylla-4(12),8(13)-dien-5α-ol	tr	-	0.1	-
1641	1636	Caryophylla-4(12),8(13)-dien-5β-ol	0.1	tr	0.5	-
1644	1642	Methyl (Z)-jasmonate	0.3	0.2	0.3	0.3
1659	1655	α-Eudesmol	0.1	0.1	0.1	-
1676	1673	Methyl epi-(E)-jasmonate	0.1	tr	0.1	0.2
1714	1718	β-Davanon-2-ol	-	-	0.2	-
		Monoterpene hydrocarbons	12.6	3.2	18.6	8.0
		Oxygenated monoterpenoids	84.5	95.2	62.0	48.2
		Sesquiterpene hydrocarbons	1.2	0.6	0.6	0.4
		Oxygenated sesquiterpenoids	0.3	0.1	10.3	19.2
		Benzenoid aromatics	0.1	traces	0.0	traces
		Others	0.7	0.2	1.7	12.7
		Total identified	99.5	99.4	93.3	88.5
		Number identified	60	39	59	57

^aMass spectra of unidentified components are available as a supplementary figure (Figure S2).

^bMS(EI): 137(30%), 107(26%), 95(100%), 79(32%), 67(88%), 57(27%), 41(44%).

^cMS(EI): 135(19%), 81(70%), 79(31%), 69(56%), 53(16%), 41(100%).

^dMS(EI): 119(4%), 105(2%), 84(100%), 83(31%), 69(15%), 56(14%), 43(26%), 41(24%).

^eMS(EI): 136(8%), 121(22%), 95(100%), 93(16%), 79(10%), 67(38%), 55(15%), 43(41%), 41(14%).

^fMS(EI): 139(3%), 117(35%), 96(29%), 81(30%), 77(28%), 67(8%), 55(8%), 43(100%).

The essential oils of A. tridentata subsp. vaseyana showed wide variation in composition, but major components included α-thujone (0.1%-76.1%), camphor (0.1%-40.2%), and 1,8-cineole (1.0%-24.6%).

Multivariate Analysis

To provide insight into possible chemical differentiation between the three subspecies of A. tridentata collected in southwestern Idaho, both agglomerative hierarchical cluster analysis (HCA) and principal component analysis (PCA) were carried out using the percent compositions of the major components. The compositions of A. tridentata subsp. tridentata⁶ are also included in the analyses. The HCA is shown in Figure 2, and the PCA is shown in Figure 3.

Figure 2.

Dendrogram based on hierarchical cluster analysis of Artemisia tridentata chemical compositions.

Figure 3.

Biplot based on principal component analysis of Artemisia tridentata chemical compositions.

The HCA revealed three well-defined clusters: (a) A cluster defined by relatively high concentrations of yomogi alcohol and camphor and made up of the three A. tridentata subsp. tridentata samples,⁶ (b) a cluster dominated by camphor and comprised of all six A. tridentata subsp. wyomingensis samples as well as three A. tridentata subsp. vaseyana samples, and (c) a single A. tridentata subsp. vaseyana sample dominated by α-thujone. The PCA corroborates the HCA with the A. tridentata subsp. tridentata group positively correlating with yomogi alcohol and camphor. There is large grouping that strongly correlates with camphor and corresponds to the camphor-rich cluster from the HCA. Finally, A. tridentata subsp. vaseyana sample #2 strongly correlates with α-thujone.

To further probe the volatile components that differentiate the three A. tridentata subspecies, an analysis of variance (ANOVA) was carried out on each of the major components in A. tridentata essential oils. The chemical components that exhibited statistical differences between the subspecies are illustrated in Figure 4.

Figure 4.

Percentage differences of volatile chemical components in the essential oils of three subspecies of Artemisia tridentata from Southwest Idaho, USA. Bars with same letter are not significantly different at P ≤ 0.05.

As observed in the HCA and PCA, the high concentration of yomogi alcohol in A. tridentata subsp. tridentata differentiates that subspecies from the wyomingensis and vaseyana subspecies. Furthermore, the (Z)-tagetone concentration differentiates A. t. tridentata from A. t. wyomingensis and A. t. vaseyana. On the other hand, the concentration of unidentified component (RI = 1234) in A. t. wyomingensis is significantly higher than those in A. t. tridentata or A. t. vaseyana. At this point, it is difficult to explain the chemical differences between the subspecies. There are likely genetic differences, but the collection sites were also different, so there may be environmental effects.

The essential oils of A. tridentata subsp. tridentata, A. tridentata subsp. wyomingensis, and A. tridentata subsp. vaseyana from Wyoming have been published.²³ A comparison of the major components of A. tridentata subsp. wyomingensis and A. tridentata subsp. vaseyana from Idaho and from Wyoming is summarized in Table 3.

Table 3.

Major Essential oil Components of Artemisia tridentata Subsp. wyomingensis and Artemisia tridentata Subsp. vaseyana from Southwestern Idaho and North-Central (Bighorn Mountains) Wyoming.

Compound	Artemisia tridentata subsp. wyomingensis				Artemisia tridentata subsp. vaseyana
	Idaho		Wyoming ²³		Idaho		Wyoming ²³
	Range (n = 6)	Ave	Range (n = 3)	Ave	Range (n = 4)	Ave	Range (n = 12)	Ave
Santolina triene	1.8-12.6	5.9	4.5-6.0	5.3	0.0-4.5	2.1	0.0-2.5	0.5
α-Pinene	0.0-0.3	0.1	1.1-4.0	2.6^a	0.5-2.1	1.3	0.0-35.5	7.4
Camphene	0.0-4.7	1.4	6.6-8.0	7.3^a	0.0-7.6	3.7	0.0-13.8	5.1
Artemiseole	2.9-16.6	7.5	17.4-20.2	18.8^a	0.0-9.2	3.4	0.0-13.0	1.7
Yomogi alcohol	0.9-7.8	4.5^b	nd	-	0.0-0.1	0.0	0.0-0.2	0.1
1,8-Cineole	1.8-11.1	6.0	12.4-13.0	12.7^a	1.0-24.6	10.7	0.0-17.9	7.2
cis-Arbusculone	0.2-1.1	0.7	1.0-5.6	3.3^a	0.0-4.2	1.0	0.0-0.2	0.0
Santolina epoxide	1.5-7.1	4.0^b	nd	-	0.0-2.2	0.7^b	0.0-0.3	0.0
trans-Arbusculone	nd	-	5.1-8.6	6.8^a	0.0-2.3	0.6	0.0-2.0	0.4
α-Santolina alcohol	0.8-3.3	2.0	13.0-14.8	13.9^a	0.0-0.3	0.1	0.0-9.7	1.1
Artemisia alcohol	0.4-8.6	2.6	nd	-	0.0-0.1	0.0	0.0-0.2	0.0
α-Thujone	nd	-	nd	-	0.1-76.1	23.6^b	0.0-7.5	1.0
Methyl santolinate	2.6-13.6	6.2^b	nd	-	0.0-1.1	0.3^b	nd	-
Chrysanthenone	nd	-	1.0-6.4	3.7^a	0.0-0.3	0.1	0.0-18.0	3.1
Camphor	10.0-30.1	15.2	20.6-21.7	21.1	0.1-40.2	21.3	0.0-45.4	15.4
Borneol	0.0-1.2	0.3	1.2-7.2	4.2^a	0.0-2.2	1.3	0.0-2.0	0.6
β-Artemisyl acetate	0.8-10.0	5.2^b	nd	-	nd	-	nd	-
Fragranol	nd	-	nd	-	nd	-	0.0-20.3	5.8
trans-α-Necrodyl acetate	nd	-	nd	-	nd	-	0.0-45.2	11.5
Grandisol	nd	-	nd	-	nd	-	0.0-36.2	10.0

Abbreviation: nd, not detected.

^aThe concentrations were significantly greater (ANOVA, P < 0.05) in the Wyoming samples than the Idaho samples.

^bThe concentrations were significantly greater (ANOVA, P < 0.05) in the Idaho samples than the Wyoming samples.

There are some notable differences between the concentrations of the major components of the samples from Idaho and the samples from Wyoming. A perusal of Table 3 reveals that both the Idaho samples and the Wyoming samples of A. tridentata subsp. wyomingensis were rich in santolina triene, artemiseole, 1,8-cineole, and camphor. However, the Wyoming samples had significantly higher concentrations of artemiseole and 1,8-cineole. The camphor concentrations were statistically comparable. In addition, the Wyoming samples of A. tridentata subsp. wyomingensis showed significantly higher percentages of α-pinene, camphene, cis-arbusculone, trans-arbusculone, chrysanthenone, and borneol. Conversely, the concentrations of yomogi alcohol, santolina epoxide, methyl santolinate, and β-artemisyl acetate were significantly higher in the Idaho samples.

There are wide variations in the concentrations of the major components in A. tridentata subsp. vaseyana, in both the samples from Idaho and the samples from Wyoming. Nevertheless, the concentrations of 1,8-cineole and camphor were generally high in samples from both locations. α-Thujone was particularly abundant in A. tridentata subsp. vaseyana from Idaho, while significantly lower in samples from Wyoming. In addition, santolina epoxide and methyl santolinate concentrations were significantly higher in the A. tridentata subsp. vaseyana samples from Idaho. In a common garden experiment, Welch and McArthur⁹ found α-thujone content to be significantly higher in A. tridentata susbp. vaseyana while camphor concentration was higher in A. tridentata subsp. tridentata. There were, however, large variations in monoterpenoid concentrations.

Interestingly, there were three compounds that were found in high concentrations in several samples of A. tridentata subsp. vaseyana from Wyoming²³ that were not detected in this subspecies from Idaho: Fragranol, trans-α-necrodyl acetate, and grandisol. Fragranol was first isolated and characterized from Artemisia fragrans.²⁹ It has been subsequently identified in several essential oils of the Asteraceae, including Tanacetum dumosum,³⁰ Achillea falcata,³¹ Achillea ligustica,³² and Achillea lingulata.³³ trans-α-Necrodyl acetate is a major component of Lavandula luisieri,^34,35 but it has also been found in the essential oils of Cladanthus mixtus (Asteraceae)³⁶ and Achillea ageratifolia (Asteraceae).³⁷ Grandisol is a sex pheromone of the boll weevil (Anthonomus grandis) and the pine weevil (Pissodes castaneus).¹⁸ It was also found in high concentration in Achillea falcata (Asteraceae)³¹ and Artemisia vestita (Asteraceae).³⁸

Terpenoid Enantiomeric Distributions

To further characterize the volatile phytochemistry of A. tridentata, chiral GC-MS was carried out on the essential oils of A. t. tridentata,⁶ A. t. wyomingensis, and A. t. vaseyana (see Table 4).

Table 4.

Enantiomeric Distribution of Chiral Terpenoid Components (Percentage of Each Enantiomer) in Artemisia tridentata Essential Oils.

Compound	RT (min)^a	A.t.t. #1^b	A.t.t. #2^b	A.t.t. #3^b	A.t.w. #1	A.t.w. #2	A.t.w. #3	A.t.w. #4	A.t.w. #5	A.t.w. #6	A.t.v. #1	A.t.v. #2	A.t.v. #3	A.t.v. #4
(+)-α-Thujene	13.92	nd^c	nd	nd	nd	nd	nd	nd	nd	nd	15.0	nd	nd	nd
(–)-α-Thujene	13.99	nd^c	nd	nd	nd	nd	nd	nd	nd	nd	85.0	nd	nd	nd
(–)-α-Pinene	15.92	0.0	0.0	0.0	52.7	89.1	73.9	84.8	27.8	49.4	88.1	48.9	87.1	78.3
(+)-α-Pinene	16.40	100.0	100.0	100.0	47.3	10.9	26.1	15.2	72.2	50.6	11.9	51.1	12.9	21.7
(–)-Camphene	17.73	82.6	32.2	3.9	60.6	98.8	99.2	99.5	78.0	17.2	99.6	nd	100.0	99.6
(+)-Camphene	18.30	17.4	67.8	96.1	39.4	1.2	0.8	0.5	22.0	82.8	0.4	nd	0.0	0.4
(+)-Sabinene	19.74	nd	nd	nd	nd	nd	nd	nd	nd	nd	45.3	67.5	28.5	15.0
(–)-Sabinene	20.60	nd	nd	nd	nd	nd	nd	nd	nd	nd	54.7	32.5	71.5	85.0
(+)-β-Pinene	20.27	100.0	100.0	nd	nd	nd	nd	nd	nd	nd	8.6	13.7	10.4	64.0
(–)-β-Pinene	20.62	0.0	0.0	nd	nd	nd	nd	nd	nd	nd	91.4	86.3	89.6	36.0
(–)-α-Phellandrene	22.59	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd	0.0
(+)-α-Phellandrene	22.81	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd	100.0
(–)-Limonene	25.06	nd	nd	nd	nd	nd	nd	nd	nd	nd	89.8	nd	92.8	92.2
(+)-Limonene	25.99	nd	nd	nd	nd	nd	nd	nd	nd	nd	10.2	nd	7.2	7.8
(–)-β-Phellandrene	26.15	nd	nd	nd	nd	nd	nd	nd	nd	nd	100.0	nd	nd	nd
(+)-β-Phellandrene	26.88	nd	nd	nd	nd	nd	nd	nd	nd	nd	0.0	nd	nd	nd
(+)-cis-Sabinene hydrate	40.70	nd	nd	nd	nd	nd	nd	nd	nd	nd	21.4	31.0	nd	nd
(–)-cis-Sabinene hydrate	41.25	nd	nd	nd	nd	nd	nd	nd	nd	nd	78.6	69.0	nd	nd
(+)-α-Thujone	43.32	nd	nd	nd	nd	nd	nd	nd	nd	nd	100.0	100.0	100.0	nd
(–)-α-Thujone	44.88	nd	nd	nd	nd	nd	nd	nd	nd	nd	0.0	0.0	0.0	nd
(+)-β-Thujone	46.06	nd	nd	nd	nd	nd	nd	nd	nd	nd	100.0	100.0	nd	nd
(–)-β-Thujone	^d	nd	nd	nd	nd	nd	nd	nd	nd	nd	0.0	0.0	nd	nd
(+)-trans-Sabinene hydrate	46.15	nd	nd	nd	nd	nd	nd	nd	nd	nd	22.6	nd	nd	nd
(–)-trans-Sabinene hydrate	46.84	nd	nd	nd	nd	nd	nd	nd	nd	nd	77.4	nd	nd	nd
(–)-Camphor	49.31	59.0	8.4	0.0^e	38.8	0.0^e	0.0^e	0.0^e	44.8	4.0	0.0^e	nd	0.0^e	0.0^e
(+)-Camphor	50.12	41.0	91.6	100.0	61.2	100.0	100.0	100.0	55.2	96.0	100.0	nd	100.0	100.0
(+)-Terpinen-4-ol	54.64	27.7	29.8	25.7	100.0	100.0	nd	nd	nd	100.0	30.5	44.4	27.2	22.1
(–)-Terpinen-4-ol	54.93	72.3	70.2	74.3	0.0	0.0	nd	nd	nd	0.0	69.5	55.6	72.8	77.9
(–)-Borneol	58.59	90.4	22.3	0.0	nd	nd	100.0	100.0	100.0	nd	100.0	nd	100.0	100.0
(+)-Borneol	59.11	9.6	77.7	100.0	nd	nd	0.0	0.0	0.0	nd	0.0	nd	0.0	0.0
(–)-Bornyl acetate	59.46	100.0	100.0	nd	nd	nd	100.0	100.0	nd	nd	100.0	nd	100.0	100.0
(+)-Bornyl acetate	^f	0.0	0.0	nd	nd	nd	0.0	0.0	nd	nd	0.0	nd	0.0	0.0
(–)-α-Terpineol	59.73	nd	nd	nd	nd	nd	nd	nd	nd	nd	88.3	75.2	100.0	100.0
(+)-α-Terpineol	60.58	nd	nd	nd	nd	nd	nd	nd	nd	nd	11.7	24.8	0.0	0.0
(–)-Verbenone	61.70	0.0	0.0	0.0	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd
(+)-Verbenone	62.73	100.0	100.0	100.0	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd
(–)-(E)-β-Caryophyllene	69.33	nd	nd	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0
(+)-(E)-β-Caryophyllene	g	nd	nd	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0
(+)-Germacrene D	73.48	nd	nd	nd	nd	nd	nd	nd	nd	nd	0.0	0.0	nd	0.0
(–)-Germacrene D	73.73	nd	nd	nd	nd	nd	nd	nd	nd	nd	100.0	100.0	nd	100.0
(–)-δ-Cadinene	76.50	100.0	100.0	100.0	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd
(+)-δ-Cadinene	77.33	0.0	0.0	0.0	nd	nd	nd	nd	nd	nd	nd	nd	nd	nd
(+)-(E)-Nerolidol	83.40	nd	8.1	7.9	nd	0.0	nd	nd	nd	nd	nd	nd	nd	0.0
(–)-(E)-Nerolidol	83.59	nd	91.9	92.1	nd	100.0	nd	nd	nd	nd	nd	nd	nd	100.0

^aA.t.t., Artemisia tridentata subsp. tridentata; A.t.w., Artemisia tridentata subsp. wyomingensis; A.t.v., Artemisia tridentata subsp. vaseyana; RT, retention time in minutes.

^bThe data for Artemisia tridentata subsp. Tridentata has been previously published⁶ but included here for comparison.

^cnd, compound not detected.

^dReference enantiomer not available; according to the Dictionary of Natural Products,¹⁸ (+)-β-thujone is a “constituent of many essential oils,” but (–)-β-thujone is not.

^eThe peak for camphor is very broad; it is uncertain whether there is (–)-camphor in the sample.

^fReference enantiomer not available; only (–)-borneol reported in the Dictionary of Natural Products.¹⁸

^gReference enantiomer not available; apparently only (–)-(E)-β caryophyllene seen in higher plants, but (+)-(E)-β caryophyllene has been found in some liverworts.¹⁸

A perusal of Table 4 reveals a few trends in enantiomeric distribution of terpenoids in A. tridentata essential oils, so differentiation between subspecies based on enantiomers does not seem possible. (+)-α-Pinene was the exclusive enantiomer in A. tridentata subsp. tridentata, but the enantiomeric distribution varied widely in the wyomingensis and vaseyana subspecies. The enantiomeric distribution of camphene varied widely within subspecies. Sabinene was only detected in A. tridentata subsp. vaseyana, but the enantiomeric distribution was variable. Limonene was only detected in A. tridentata subsp. vaseyana and (–)-limonene was the major enantiomer. Only the (+)-enantiomers of α- and β-thujone were observed in A. tridentata subsp. vaseyana. (+)-Camphor generally dominated the essential oils of A. tridentata. (–)-Terpinen-4-ol was the major enantiomer in A. tridentata subsp. tridentata and A. tridentata subsp. vaseyana. When observed, only (+)-terpinen-4-ol was found in A. tridentata subsp. wyomingensis. (–)-Borneol was the major enantiomer in A. tridentata subsp. wyomingensis and A. tridentata subsp. vaseyana. Only (–)-bornyl acetate was found in A. tridentata essential oils. α-Terpineol was only found in A. tridentata subsp. vaseyana and the (–)-enantiomer predominated. Only (–)-(E)-β-caryophyllene was detected in A. tridentata essential oils.

Conclusions

The essential oil compositions of three subspecies of big sagebrush, A. tridentata subsp. tridentata, A. tridentata subsp. wyomingensis, and A. tridentata subsp. vaseyana have shown chemical profiles that may be useful in differentiating these subspecies. However, there is much variation in essential oil compositions both within subspecies and between geographical locations. In this work, the essential oils were examined in different stages of development, which likely affects the compositions. It is apparent that much additional investigation is necessary to more fully characterize the volatile phytochemistry of A. tridentata, and we plan future studies to include collections in the same calendar year, at several different months, and different geographical locations, to examine seasonal and geographical variations as well as subspecies variations.

Materials and Methods

Plant Material

Aerial parts from six individuals of A. tridentata subsp. wyomingensis were collected on August 1, 2022 (flowering stage) from the Snake River Birds of Prey National Conservation Area, Idaho (see Table 5). Hydrodistillation of A. tridentata subsp. wyomingensis gave pale-yellow essential oils (Table 5). Note that an aqueous leaf extract of A. tridentata subsp. wyomingensis was not fluorescent under UV light, indicating the absence of coumarins.

Table 5.

Artemisia tridentata Collection and Hydrodistillation Details.

Plant	Sample number	Location	Mass aerial parts (g)	Yield essential oil (g)
A. tridentata subsp. wyomingensis	Atw#1	43°18′52″ N, 116°25′26″ W, 853 m elevation	49.37	1.8361
	Atw#2	43°18′58″ N, 116°27′12″ W, 845 m elevation	43.81	1.1579
	Atw#3	43°18′58″ N, 116°27′14″ W, 844 m elevation	37.33	1.6610
	Atw#4	43°18′5″ N, 116°23′19″ W, 869 m elevation	28.02	1.1661
	Atw#5	43°18′5″ N, 116°23′19″ W, 869 m elevation	35.10	0.8203
	Atw#6	43°18′21″ N, 116°22′50″ W, 875 m elevation	29.44	0.8195
A. tridentata subsp. vaseyana	Atv#1	43°24′21″ N, 115°17′33″ W, 1423 m elevation	106.35	1.8424
	Atv#2	43°24′21″ N, 115°17′33″ W, 1423 m elevation	157.36	2.4966
	Atv#3	43°43′58″ N, 116°7′42″ W, 1673 m elevation	81.11	0.7190
	Atv#4	43°43′34” N, 116°9′28” W, 1481 m elevation	61.57	0.5896

Two individuals of A. tridentata subsp. vaseyana were collected near Pine, Idaho on June 28, 2022 (pre-flowering) and two individuals were collected near Bogus Basin Ski Resort, Idaho on July 7, 2022 (pre-flowering) (see Table 5). Hydrodistillation of the four samples gave yellow essential oils. Note that aqueous leaf extracts of each A. tridentata subsp. vaseyana showed bright blue-white fluorescence under UV light, indicating the presence of coumarins.

Plants were identified by Setzer by consulting the botanical descriptions,^21,39 and by comparison with samples from the New York Botanical Garden Virtual Herbarium (https://sweetgum.nybg.org/science/vh/, accessed on August 1, 2022). Voucher specimens (WNS-Atw-5745, WNS-Atv-5680, and WNS-Atv-5714) have been deposited in the University of Alabama in Huntsville herbarium. For each specimen, the aerial parts were fresh frozen and stored at −20 °C until distilled. The plant material was hydrodistilled using a Likens-Nickerson apparatus for 4 h to give the essential oils (Table 5).

Gas Chromatography Coupled with Flame Ionization Detection and Gas Chromatography–Mass Spectrometry Analyses

The essential oils of A. tridentata subsp. wyomingensis and A. tridentata subsp. vaseyana were analyzed by gas chromatography coupled with flame ionization detection, gas chromatography–mass spectrometry (GC/MS), and chiral GC/MS as previously described.⁶ The essential oil components were identified by comparison of the mass spectral fragmentation patters and by comparison of RI values available in the Adams,²⁵ FFNSC 3,²⁶ NIST20,²⁷ and our own in-house database.²⁸ The identification of enantiomers was determined by the comparison of retention times with authentic samples obtained from Sigma-Aldrich (Milwaukee, WI, USA).

Statistical Analysis

For the HCA, the 13 A. tridentata essential oil compositions were treated as operational taxonomic units, and the percentages of the 22 most abundant essential oil components, namely, santolina triene, 4,4-dimethyl-2-buten-4-olide, camphene, artemiseole, yomogi alcohol, 1,8-cineole, santolina epoxide, cis-arbusculone, artemisia ketone, trans-arbusculone, α-santolina alcohol, artemisia alcohol, α-thujone, methyl santolinate, camphor, (Z)-tagetone, β-artemisyl acetate, unidentified (1234), davana ether 2, davana ether 4, unidentified (1554), and davanone D, were used to delineate the chemical associations between the A. tridentata essential oil samples. Pearson correlation was used to measure similarity, and the unweighted pair group method with arithmetic average was used for cluster definition. PCA was performed for the visual verification of the essential oil interrelationships of the different A. tridentata subspecies using the 13 major components as variables with a Pearson correlation matrix. The HCA and PCA analyses were performed using XLSTAT v. 2018.1.1.62926 (Addinsoft, Paris, France). ANOVA was conducted by one-way ANOVA followed by the Tukey test using Minitab® 18 (Minitab Inc., State College, PA, USA). Differences at P < 0.05 were considered to be statistically significant.

Supplemental Material

sj-docx-1-npx-10.1177_1934578X231154965 - Supplemental material for Chemical Characterization of Three Artemisia tridentata Essential Oils and Multivariate Analyses: A Preliminary Investigation

Supplemental material, sj-docx-1-npx-10.1177_1934578X231154965 for Chemical Characterization of Three Artemisia tridentata Essential Oils and Multivariate Analyses: A Preliminary Investigation by Kathy Swor, Prabodh Satyal, Ambika Poudel and William N Setzer in Natural Product Communications

Supplemental Material

sj-docx-2-npx-10.1177_1934578X231154965 - Supplemental material for Chemical Characterization of Three Artemisia tridentata Essential Oils and Multivariate Analyses: A Preliminary Investigation

Supplemental material, sj-docx-2-npx-10.1177_1934578X231154965 for Chemical Characterization of Three Artemisia tridentata Essential Oils and Multivariate Analyses: A Preliminary Investigation by Kathy Swor, Prabodh Satyal, Ambika Poudel and William N Setzer in Natural Product Communications

Footnotes

Acknowledgement

This work was carried out as a part of the activities of the Aromatic Plant Research Center (https://aromaticplant.org/).

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval

Ethical approval is not applicable for this article.

Data Availability Statement

The data presented in this study are available upon reasonable request from the corresponding author.

Statement of Human and Animal Rights

This article does not contain any studies with human or animal subjects.

Statement of Informed Consent

There are no human subjects in this article, and informed consent is not applicable.

ORCID iD

William N Setzer

Supplemental Material

Supplemental material for this article is available online.

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