Inheritance of hydrocarbons in subspecific big sagebrush (Artemisia tridentata) hybrids

Inheritance of hydrocarbons in subspecific big sagebrush (Artemisia tridentata) hybrids

~ Pergamon Biochemical Sy~tematics and Ecology, Vol. 22, No. 7, pp. 689-697, 1994 Copyright© 1994ElsevierScience Ltd Printed in GreatBritain. All rig...

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~ Pergamon

Biochemical Sy~tematics and Ecology, Vol. 22, No. 7, pp. 689-697, 1994 Copyright© 1994ElsevierScience Ltd Printed in GreatBritain. All rights reserved 0305-1978/94 $7.00+ 0.00

0305-19781941E0040-9

Inheritance of Hydrocarbons in Subspecific Big Sagebrush (Artemisia tridentata) Hybrids D. J. WEBER,*t D. R. GANG,* S. C. HALLS,* B. N. SMITH* and E. D. McARTHUR$ *Department of Botany and Range Science, Brigham Young University, Provo, UT 84602, U.S.A. $Shrub Sciences Laboratory, Intermountain Research Station, Forest Service, U.S. Department of Agriculture, Provo, UT 84606, U.S.A.

Key Word Index--Artemisia tridentata ssp. tridentata; A. t. ssp. vaseyana; Asteraceae; monoterpenoids; methacrolein; hybridization. Abstract--Volatile compounds of the subspecies tridentata and vaseyana of Artemisia tridentata along with their F2 hybrids were characterized and identified. These compounds segregated in the F2s. Methacrolein and thujone characterize ssp. tn'dentata; camphene, camphor, and 1,8-cineole characterize ssp. vaseyana. Results of this study taken together with previous work suggest that low values for the bitter volatile methacrolein might be combined with high biomass and nutritive quality characteristics from hybrid progeny.

Introduction

Big sagebrush (Artemisia tridentata Nutt., Asteraceae) is a widespread, polymorphic, landscape dominant species in western North America. It is the central species of the approximately two dozen taxa of Artemisia subgenus Tridentata (McArthur eta/., 1981, 1988). Artemisia tridentata encompasses five subspecies including basin big sagebrush (A. tridentata ssp. tridentata) and mountain big sagebrush (A. t. ssp. vaseyana) (Goodrich et al., 1985; Rosentreter and Kelsey, 1991). The Tridentatae are believed to be built on a reticulate, hybridizing matrix driven by population migrations in response to past climatic changes and contrasting topography of its habitats (Ward, 1953; McArthur et al., 1981). Artemisia tridentata is an important food and wildlife habitat plant (McArthur, 1983; McArthur and Welch, 1986). Its fat, carbohydrate, protein, fiber, ash, total digestible nutrients, calcium, phosphorus and carotene values have been determined (Kinney and Sugihara, 1943; Welch and McArthur, 1981; Welch, 1989). Feeding trials indicate that A. tridentata is a useful feed for livestock; for mule deer (Odocoileus hernionus) and other wildlife species it is a major food source, especially during the winter (Furbush et al., 1961; Welch and McArthur, 1981, 1986; Welch et al., 1987). Seasonally high monoterpenoid levels in the summer growing season and the availability of alternate succulent foods make A. tridentata less of a preferred feed plant during that period (Kufeld et al., 1973; Kelsey et al., 1982; Cedarleaf et al., 1983). Several accessions of A. tridentata have been found to be preferred by mule deer and/or to be of high nutritive quality (Longhurst et al., 1969; Hanks et al., 1973; School et al., 1977; Welch and McArthur, 1986; Welch eta/., 1986; Bray etal., 1991). Several studies have shown that high levels or composition of monoterpenoids reduce rumen microbial activity of browsing species and affect palatability of A. tridentata (Longhurst et al., 1969; Personius et al., 1987; Bray et al., 1991). Buttkus and tAuthor to whom correspondence should be addressed. (Received 6 December 1993) 689

690

D, J, WEBERETAL.

Bose (1977) and Buttkus et aL (1977) identified 28 terpenes in the essential oil of A. tridentata from a British Columbia, Canada location. Camphor, 1,6,6-trimethyl-4ethenyl-exo-oxabicyclo [3.1.0] hexane, 1,8-cineole (eucalyptol), delta-3-carene, santolinyl ester, ~-pinene, camphene, thujone, j]-pinene, 0¢-terpineol, thujyl alcohol, and ~-phlellandrene were present in amounts of 1% or more. Other important volatiles identified in A. tridentata in the Intermountain area of the United States include methacrolein (2-methyl-2-propenal), artole and p~ymene (Scholl et al., 1977; Welch and McArthur 1981; Bray et al., 1991). Methacrolein, an extremely volatile and bitter compound, has, in particular, been suggested as playing an important role in A. tridentata palatability to browsing animals (Scholl et al., 1977; McArthur et al., 1988; Bray et al., 1991). The subspecies tridentata and vaseyana of A. tridentata have different qualitative, quantitative, and seasonal volatile oil profiles (Welch and McArthur, 1981; Kelsey et al., 1982). McArthur et al. (1988) demonstrated that their monoterpenoids of the subspecies tridentata and vaseyana and their natural and F1 artificial hybrids are useful genetic markers. Experimental hybridization between the Dove Creek population of ssp. tridentata (female parent) and the Hobble Creek population of ssp. vaseyana (male parent) was undertaken in an attempt to combine the growth form, palatability, and monoterpenoid characteristics of the male parent with the growth rate and protein content of the female parent (Welch and McArthur, 1986; McArthur et aL, 1988). The purpose of the investigation reported in the study presented here was to evaluate the inheritance of volatile compounds, especially methacrolein, in F2 plants.

Materials and Methods Even-aged plants from parental and F2 populations growing at experimental plots in Hobble Creek Canyon, Utah were used in these studies. These plants were all grown from 1987 seed from populations described by McArthur et al. (1988). Seeds from self-pollination of populations originally from A. tn'dentata ssp. tndentata from Dove Creek, Colorado and A. t. ssp. vaseyana from Hobble Creek, Utah and panmitic seed from F1 experimental plantings resulting from controlled pollination of the ssp. tridentata parent by the ssp. vaseyana parent of McArthur et aL (1988) were germinated and grown in a greenhouse in containers. The container stock was transplanted to the Hobble Creek plots on 27 March, 1989. Leaf and twig samples were collected on 6 July, 1990, placed on ice until they were returned to the laboratory, frozen with liquid nitrogen and ground with a mortar and pestle. The powered tissue was then stored at --20"C until analysis. Chromatographic analyses of the volatile compounds were performed in triplicate for each of three parental plants and for three separate F2 hybrid plants with a 5890 Hewlett Packard gas chromatograph with a flame ionization detector and a Tekmar LC 2000 purge and trap system. Data for parental plants were combined for analysis but the F2s were kept separate. Volatile compounds were separated using a 25 × 0.2 mm × 0.33 p,m capillary column coated with dimethyl polysiloxane. The temperature protocol was a starting temperature 38=C for 4 min with temperature increase programmed at 5°C min -~ to 250°C with the final temperature of 250°C held for 1 min. The injection port was at 250°C and the detector temperature was 310=C. Volatiles were collected by using the Tekmar LC 2000 purge and trap system. Volatile chemical samples (0.5 g) were placed in the purge chamber and purged for 12 min at 50" with helium. Volatile compounds from the samples ware trapped on a Tenax column and subsequently driven off the column by heating for 4 min at 180°C. The compounds were trapped at the beginning of the capillary column by freezing in liquid nitrogen. The sample was injected onto the column by heating the beginning section of the capillary column containing the column for 45 sec at 20(TC. The volatile compounds were identified following the same procedures as described for chromatographic analyses except a Hewlett Packard 5995 capillary gas chromatograph-mass spectrometer with the Tekmar LC 2000 purge and trap system was used. Here the temperature protocol was a starting temperature of 50°C for 4 min with temperature increase programmed at 10°C rain -~ to 250°C with the final temperature of 250°C which was held for 10 min. The injection port was at 200=C, the transfer line at 310°C, and the source temperature at 200°C. The spectra obtained from the monoterpenoids were matched with the computer spectra library of 95,000 spectra and the probability of the match determined. The date were standardized according to Romseburg (1984) and a cluster analysis was performed using the NTSYS-pc computer program (Rohlf, 1993).

ARTEMISlA HYDROCARBONS

691

Results and Discussion Gas chromatography More compounds were detected using this method than with the gas chromatograph-mass spectrometer because this method recorded compounds that were too low in concentration to be analyzed by the mass spectrometer. Twenty-five and 18 compounds were separated by capillary gas chromatography for A. tridentata ssp. tridentata and for A. t. ssp. vaseyana, respectively. The retention time and average concentration for each compound in ppm and percent is given in Table 1. The F2 hybrids were variable both in the number of compounds detected (22, 27, 37) and the concentration of those compounds (Table 2). Such results would be expected from the principles of genetic recombination. The extra compounds and higher concentrations of compounds found in the F2s over the parents may result from metabolic heterosis (Grant 1975). McArthur et al. (1988) reported a high value as compared to the parents for an unknown monoterpenoid in the F2 hybrids that produced the F2s of the current study. As shown in Fig. 1 there are 37 compounds in the comparison between ssp. tridentata and ssp, vaseyana; 19 of these are shared by both taxa, 17 are unique to ssp. tridentata, and one is unique to ssp. vaseyana. When a similar comparison is made between ssp. tridentata and the F2 hybrid there are 43 compounds in the comparison; 27 of these are shared, eight are unique to ssp. tridentata and eight are unique to the F2. The comparison between ssp. vaseyana and the F2 gives 20 shared

TABLE 1. RETENTION TIME, COMPOUND CONCENTRATION AND PERCENTAGE TOTAL VOLATILE COMPOUNDS FROM ARTEMISlA TRIDENTATA SSP. TRIDENTATA AND A. TRIDENTATA SSP. VASEYANA SEPARATED BY CAPILLARY GAS CHROMATOGRAPHY

Artemisia tridentata ssp. tridentata Concentration Ret time fresh wt. (min) (ppm)

(%)

Artemisia tridentata ssp. vaseyana Concentration Ret. time fresh wt. (rain) (ppm)

(%) 1.5 0.3 0.7 0.7 6.0 1.0 1.9 2.3 8.9 15.1 3.3 2.6 1.1 4.5 30.2 11.8 0.7 7.3

7.47 9.97 10.04 12.38 12.88 14.87 17.04 17.54 18.69 21.71 23.34 23.99 27.81 28.86 29.65 30.51 31.69 32.56

0.5 0.2 0.6 0.2 5.4 0.3 0.2 0.2 4.4 0.1 0.2 0.2 0.2 0.2 2.1 0.1 0.3 0.4

0.5 0.2 0.6 0.2 5.2 0.3 0.2 0.2 4.4 0.1 0.2 0.2 0.2 0.2 2.0 0.1 0.3 0.4

7.42 8.71 9.94 12.87 23.86 27.07 28.73 30.96 31.55 32.44 33.31 33.69 35.06 35.66 36.04 36.04 38.17 41.34

33.08 33.41 35.49 36.20 36.74 37.7 40.84

0.4 0.6 1.5 3.2 79.1 1.1 1.1

0.4 0.5 1.4 3.1 76.9 1.1 1.1

Total

Total

102.9

0.4 0.1 0.2 0.2 1.7 0.3 0.5 0.6 2.5 4.2 0.9 0.7 0.3 1.2 8.4 3.3 0.2 2

27.7

D.J. WEBER ETAL.

692

TABLE 2. RETENTION TIME, COMPOUND CONCENTRATION AND PERCENTAGE TOTAL VOLATILE COMPOUNDS FROM F2 HYBRIDS OF ARTEMISIA TRIDENTATA SSP. TRIDENTATA AND A. TRIDENTATA SSP. VASEYANA SEPARATED BY CAPILLARY GAS CHROMATOGRAPHY

Hybrid A Ret. time (min)

Hybrid B Concentration fresh wt, (ppm)

(%)

Ret. time (rain)

7.27 8.78 9.76 10.91 12.25 12.76 13.54 14.02 15.08 15.68 18.12 18.59 23.87 24.38 25.37 26.65 27.16 28.76 29.57 30.42 31.00 31.60 32.40 33.00 33,30 33.67 34.43

4.7 0.7 1.7 0.1 0.1 18.4 0.2 0.9 0.4 0.2 0.5 1.7 0.3 0.8 1.8 1.0 6.7 2.5 10.2 0.7 1.2 1.1 1.0 0.3 2.4 2.1 0.6

3.4 0.5 1.2 0.0 0.1 13.4 0.1 0.7 0.3 0.1 0.4 1.3 0.3 0.6 1.3 0.8 4.9 1.8 7.5 0.5 0.9 0.8 0.7 0.2 1.8 1.5 0.5

35.43 36.29 37.29 37.57 38.24 39.74 40.27 40.59 40.73 41.44

1.0 62.1 3.3 3.5 0.4 0,3 0.1 0.5 2.7 0.6

0.7 45.4 2,4 2.5 0.3 0.2 0.1 0.4 2.0 0.4

Total

136.1

Hybrid C Concentration fresh wt. (ppm)

(%)

7.33 8.84 9.82 10.95 11,44 12.79 14.06 18.14 18.63 23.92 25.43 28.80 29.61 30.46 31.04 31.64 32.54 33.35 33.70 34.48 36.33 37.32 37.62 39.78 40.31 40.77 41.5

2.9 0.3 0.9 0,3 0.1 10.0 0.6 0.7 0.7 0.2 0.8 1.3 7.8 0.6 0.9 0.7 0.6 1.5 1.4 0.5 4.7 2.1 2.6 0,2 1.1 0.2 0.4

6.6 0.7 2.1 0.7 0.3 22.6 1.4 1.7 1.7 0.4 1.9 3.0 17.6 1.3 2.1 1.6 1.3 3.5 3.2 1.1 10.5 4,8 5.8 0.5 2.5 0.4 1.0

Total

44.4

Ret. time (rain)

Concentration fresh wt. (ppm)

(%)

7.33 8.83 9.82 12.78 13.57 14.05 18.15 18.70 23.92 28.80 29.60 30.46 31.04 31.64 32.54 33.35 33.7 36.29 37.31 37.62 40.32 40.77

1.5 0.2 1.1 6.8 0.1 0.4 0.5 0.3 0.2 1.2 3.2 0.5 0.3 0.3 0.3 0.8 0.8 20.2 1.0 0.2 0.6 1.1

3.5 0.4 2.6 16.4 0.3 1.0 1.1 0.8 0.5 2.8 7.6 1.1 0.7 0.8 0.8 1.9 1.8 48.7 2,4 0.4 1.5 2.8

Total

41.5

compounds, none unique to ssp. vaseyana, and 15 unique to the F2. When this data is subjected to cluster analysis each group clusters clearly (Fig. 2). The F2 hybrids are slightly closer to ssp. tridentata, the female parent in the initial hybridization.

Gas chromatography-mass spectrometry The major volatile compounds identified from A. tridentata ssp. tridentata are listed in Table 3; those for A. t. ssp. vaseyana are listed in Table 4. The major compounds of the F2s are listed in Table 5. Here, as in the capillary gas chromatograph results there were more compounds identified from ssp. tridentata than from ssp. vaseyana. Major compounds of the F2s included compounds that characterized both parental species as well as some that were either missing or only occurred as minor constituents in the

ARTEMISlA HYDROCARBONS

693

A rternisia tridentata ssp tridentata

Hybrid cross o f tridentata and vasevana

A rtemisia triden[ata ssp vaseyana FIG. 1. GC CHROMATOGRAMS OF VOLATILE COMPOUNDS OF ARTEMISIA TRIDENTATASSP. TRIDENTATA,ARTEMISlA TRIDENTATASSP. VASEYANAAND F2 HYBRID BETWEEN THOSE PARENTALSUBSPECIES. Open peaks are shared compounds, double diamond hatched peaks show differences between ssp. tridentata and ssp. vaseyana, single diamond hatch peaks show F2 hybrid differences from parents.

2.0 i

1.6 i

1.2 i

0.8 i

0.4 i

I

1. Artemisia tridentata ssp vaseyana 2. Artemisia tridentata ssp vaseyana 3. Artemisia tridentata ssp vaseyana

l J " I

1. Artemisia tridentata ssp tridentata 2. Artemisia tridentata ssp tridentata 3. Artemisia tridentata ssp tridentata

[

I

"

1. F2 hybrid of tridentata and vaseyana 2. F2 hybrid of tridentata and vaseyana L 3. F2 hybrid of tridentata and vaseyana

FIG. 2. CLUSTER ANALYSIS PLOT OF VOLATILE COMPOUNDS OF ARTEM/SlA TRIDENTATA SSP. VASEYANA, ARTEMISlA TRIDENTATASSP. TRIDENTATA,AND F2 HYBRIDS BETWEEN THOSE ENTITIES.

parental species. McArthur et al. (1988) reported a similar phenomenon in the F1 population that produced the F2s. Several of these compounds are similar in structure and may be derivative compounds produced in collection and processing, e.g. the compounds (3), (5) and (6) of Fig. 3. Again, as in the results for the capillary gas chromatography without mass spectrometry there was the expected genetic segregation in the F2s.

694

D. J. WEBER ETAL. TABLE 3. RETENTION TIME, NAME, PROBABILITY, MOLECULAR WEIGHT, FORMULA OF VOLATILE COMPOUNDS FROM ARTEMISlA TRIDENTATA SSP. TRIDENTATA SEPARATED AND IDENTIFIED BY CAPILLARY GAS CHROMATOGRAPH-MASS SPECTROMETRY Ret. time (min)

Name

Prob.

Molecular wt.

Formula

1.36 1.53 1.58 1.62 2.04 2.30 4.69 6.74 8.68 9.45 10.18 10.84 11.16 12.92

1-butene, 3-methyl2-propanone 2-propanal, 2-methyl 2-butenal 1-propanal, 2-methyl 2-hexenal 2-hexanol trans-ocimene 0c-pinene, (-)1-phellandrene 1,8-cineole l~-thujone Camphor 2(3H)-furanone, dihydro-5-(2-octenyl)-

86 70 70 60 87 50 50 28 70 89 92 81 70 51

70 58 70 70 74 98 102 136 136 136 154 152 152 167

C~H~o C3H60 C4H60 C4H6 C4H~oO C6H~oO C6H~40 CloH16 C~oH~6 C~oH~6 C~oH~80 C~oH160 C~oH160 C12H2oO2

TABLE 4. RETENTION TIME, NAME, PROBABILITY, MOLECULAR WEIGHT AND FORMULA OF VOLATILE COMPOUNDS FROM ARTEMISIA TRIDENTATA SSP. VASEYANA SEPARATED AND IDENTIFIED BY CAPILLARY GAS CHROMATOGRAPHMASS SPECTROMETRY Ret. time (rain)

Name

Prob.

Molecular wt.

Formula

4.88 7.58 8.07 9.89 10.41 12.40

1-octene =-pinene, (-)camphene 2-J}-pinene 1,8-cineole camphor

90 93 97 95 91 94

112 136 136 136 154 152

C8H1~ C~oH~6 C~oH16 C~oH~6 C~oH~80 CloH160

TABLE 5. RETENTION TIME, NAME, PROBABILITY, MOLECULAR WEIGHT AND FORMULA OF VOLATILE COMPOUNDS FROM F2 HYBRIDS BETWEEN ARTEMISIA TRIDENTATA SSP. TRIDENTATA AND A. TRIDENTATA SSP. VASEYANA SEPARATED AND IDENTIFIED BY CAPILLARY GAS CHROMATOGRAPHMASS SPECTROMETRY Ret. time (rain)

Name

Prob.

Molecular wt.

Formula

Hybrid A 1.27 1.50 5.36 7.53 8.59 9.32 10.61 11.08 11.34 13.01

butane 2-propenal, 2-methyl 2-hexano~ trans-ocimene camphene ~-thujone 1,8-cineole ~-thujone fenchone ethanone, 1-(1-hydroxycyclopentyl)-

60 70 50 59 95 55 89 51 70 42

58 70 102 136 136 152 154 152 152 128

C4H~o C4H80 C6H140 CloH~e CloH~6 CloHlsO CloH180 CloH~sO CloH160 C~H1202

ARTEMISIA HYDROCARBONS

695

TABLE 5-- CONTINUED Ret. time (min)

Name

Prob.

Molecular wt.

Formula

1.39 1.53 6.52 7.93 8.62 10.06 10.53 10.61 10.96 12.31 12.83

2-propanone 2-propenal, 2-methyl trans-ocimene camphene ~thujone 1,8-cineole ~-thujone similar to thujone fenchone camphor 2(3H)-furanone, dihydm-5-(2-octenyl)-

76 70 59 95 60 89 52 40 70 79 53

58 70 136 136 152 154 152 152 152 152 196

C3H60 C4HsO CloH,6 C~oH,6 CloH~80 CloH,80 C10H~eO C~oH,60 C10Hl~O C~0H~O C~2H2oO2

Hybrid C 1.47 1.70 7.21 8.33 9.00 10.32 10.90 11.19 11.45 12.98

2 propanone 2-propenal, 2-methyt trans-ocimene camphene similar to thujone 1,8-cineole ~-thujone c¢-thujone 2-pyrrolidone camphor

70 70 59 96 42 91 65 52 42 70

58 70 136 136 152 154 152 152 85 152

C3HsO C4HsO C10H~ C10Hlo C10H~60 C~0H~80 C10H~60 C,0H~oO C4HTNO C~0H~60

Hybrid B

O

I

/ ~ / ~ [11

H

[2]

C

O

.j~...c=o

~

[3]

[4]

~

o. [5]

o

[6]

CH2--CHCH 2CH2CH2CHzCH2CH]

[7]

O

O [8]

[121

[9]

[13]

~ [191

[141

[11]

[i0]

[151

[16]

[171

[18]

0

[20]

[21]

FIG. 3. CHEMICAL STRUCTURES OF VOLATILE CHEMICALS IDENTIFIED IN THIS STUDY (molecular weights and formulae are in Tables 3-5). (1) Butane; (2) 2-proponone; (3) 3-methyl-l-butene; (4) 2-butenal, (5) 2-methyl-2-propenal (methacmlein); (6) 2-methyl-2-propenal; (7) 2-pyrolidone; (8) 2-hexenal; (9) 2-hexanol; (10) 1-octene; (11) 1-(1-hydroxycyclopentyl)-ethanone; (12) camphene; (13) trans-ocimene; (14) 0c-pinene; (15) ~-pinene; (16) 1-phellandrene; (17) camphor; (18) thujone; (19) fenchone; (20) 1,8-cineole; (21) dihydro-5-(2-octenyl)-2(3H)-furanone.

696

D.J. WEBERETAL.

TABLE 6. PERCENTAGEOF TOTALIDENTIFIEDVOLATILECOMPOUNDSAS INDICATORSOF ARTEMISIA TRIDENTATASSP. TRIDENTATAAND A. TRIDENTATASSP. VASEYANAOBTAINEDFROMGC-MS ANALYSIS(see McArthur et al., 1988). Compound

tridentata

tridentata indicators 2-propenal,2-methyl (methacrolein) ~z-and ~]-thujone

31.6 30.6

vaseyanaindicators camphene camphor 1,8-cineole

0.0 3.3 11.4

vaseyana

Hybrid A

Hybrid B

Hybrid C

0.0 0.0

14.3 29.0

30.8 21.4

18.0 44.6

11.6 7.9 57.8

5.8 0.0 22.9

6.1 3.1 13.7

2.0 7.7 13.1

Table 6 presents the quantity of indicator compounds in the two parental subspecies and F2 samples. Methacrolein and thujone are characteristic for ssp. tridentata whereas camphene, camphor, and 1,8-cineole characterize ssp. vaseyana. The F2s vary widely in their content of these characterizing compounds. Previous studies have shown that ssp. tridentata individual plants are characterized by the presence of methacrolein (Welch and McArthur 1981; McArthur et al., 1988). Means of individual parental populations may vary but those populations had tight means with low standard deviations values (McArthur et al., 1988). Consequently in our current study, we pooled the values of the parental plants. Of particular interest in the current study is the reduced amount of the bitter methacrolein in some of the F2s. Lowering methacrolein in hybrid selections while maintaining the desirable biomass, palatability, and protein values of one or the other parental species in those hybrid lines gives promise to the possibility of selection for A. tridentata for particular rangeland purposes (McArthur eta/., 1992; McArthur in press; unpublished). Acknowledgements--This research was supported by Cooperative Agreement INT-88364 between Brigham Young University and the Intermountain Research Station, U.S.D.A. Forest Service; by U.S.D.A. Cooperative State Research Service Competitive Grant 91-383300-6157; and by Pittman Robertson Wildlife Habitat Project W82R (Utah Division of Wildlife Resources and Intermountain Research Station, cooperating).

References Bray, R. O., Wambolt, C. L. and Kelsey, R. G. (1991) Influence of sagebrush terpenoids on mule deer preference. J. Chem. EcoL 17, 2053-2062. Buttkus, H. and Bose, R. J. (1977) Characterization of a monoterpenoid ether from the essential oil of sagebrush (Artemisia tridentata). J. Am. Oil Chem. Soc. 54, 212-214. Buttkus, H. A., Bose, R. J. and Shearer, D. A. (1977) Terpenes in the essential oil of sagebrush (Artemisia tridentata). J. Agtic. Food Chem. 25, 288-291. Cedarleaf, J. D., Welch, B. L. and Brotherson, J. D. (1983) Seasonal variation of monoterpenoids in big sagebrush (Artemisia tridentata). J. Range Manage. 36, 492--494. Furbush, P. B., Carlson, C. E. and Dal Porto, N. J. (1961) Palatability of sagebrush to livestock. Western Livestock J. 39, 115-119. Goodrich, S., McArthur, E. D. and Winward, A. H. (1985) A new combination and a new variety in Artemisia tridentata. Great Basin Nat. 45, 99-104. Grant, V. (1975) GeneEcs of FIowenng Plants. Columbia University Press, New York. Hanks, D. L., McArthur, E. D., Stevens, R. and Plummer, A. P. (1973) Chromatographic Characteristics and Phylogenetic Relationships of Artemisia, section Tridentatae. U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station Res. Pap. INT-141, Ogden, Utah. Kelsey, R. G., Stephens, J. R. and Shafizadeh, R. (1982). The chemical constituents of sagebrush foliage and their isolation. J. Range. Manage. 35, 617-622. Kinney, C. R. and Sugihara, J. (1943) Constituents of Artemisia tridentata (American sage brush). II. J. Org. Chem. 8, 290-294. Kufeld, R. C., Wallmo, O. C. and Feddema, C. (1973) Foods of the Rode/Mountain Mule Deer. U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station Res. Pap. RM-111, Ft. Collins, Colorado.

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