Western North American Naturalist

Volume 65 Number 2 Article 14

4-29-2005

Nutrient relationships between fasciculata Nutt. and its host pygmaea Gray in the Uinta Basin of , USA

Jack D. Brotherson Brigham Young University

Brenda T. Simmons Gilbert,

Terry Ball Brigham Young University

W. Ralph Anderson Brigham Young University

Follow this and additional works at: https://scholarsarchive.byu.edu/wnan

Recommended Citation Brotherson, Jack D.; Simmons, Brenda T.; Ball, Terry; and Anderson, W. Ralph (2005) "Nutrient relationships between Nutt. and its host Gray in the Uinta Basin of Utah, USA," Western North American Naturalist: Vol. 65 : No. 2 , Article 14. Available at: https://scholarsarchive.byu.edu/wnan/vol65/iss2/14

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Western North American Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Western North American Naturalist 65(2), © 2005, pp. 242–247

NUTRIENT RELATIONSHIPS BETWEEN OROBANCHE FASCICULATA NUTT. AND ITS HOST ARTEMISIA PYGMAEA GRAY IN THE UINTA BASIN OF UTAH, USA

Jack D. Brotherson1,3, Brenda T. Simmons2, Terry Ball4, and W. Ralph Anderson1

ABSTRACT.—Patterns of mineral nutrient uptake and distribution within the roots, stems, and of Artemisia pyg- maea and in the vascular parasite Orobanche fasciculata were investigated. All nutrients studied were magnified over concentrations found in the soil into the host and parasite. Nitrogen, phosphorus, potassium, and zinc were magnified along the flow gradient of soil-roots-stems-leaves of the host. All others increased in the roots and then decreased in the stems and leaves. Orobanche fasciculata concentrated phosphorus, potassium, and sodium over soil and root concentra- tions while excluding to some degree all others.

Key words: Orobanche fasciculata, Artemisia pygmaea, mineral nutrient uptake, host and parasite interaction.

Orobanche fasciculata Nutt. (clustered can have primary and secondary haustoria, the broomrape or clustered cancerroot) belongs to former located where the shoot of the parasite the or broomrape family, mem- emerges and the latter where the roots from bers of which are parasitic on the roots of the parasite attach to the roots of the host. Par- flowering (Reuter 1986, Welsh et al. 1993, asites that develop more advanced haustoria Wolfe and dePamphilis 1997). The genus have little or no root system. Such is the case Orobanche contains over 100 species (Parker with O. fasciculata (Kuijt 1969). The main pur- and Riches 1993), all of which are annual or pose of the haustorium is uptake of water, monocarpic (Kuijt 1969), obligate, herbaceous organic compounds, and mineral nutrients from parasites (Parker and Riches 1993). Orobanche the host . fasciculata parasitizes a variety of host species, Orobanche species are found in over 58 especially species of Artemisia (Welsh et al. countries, with some species having large pop- 1993). It is purplish to yellowish in color and ulations in areas of intensive agriculture (Jor- grows in a split stem to between 5 cm and 10 dan and Nile River valleys) and other species cm above the soil surface (Welsh et al. 1993). being endemic to small, localized areas (Sauer- Seeds of Orobanche spp. germinate after born 1991). Generally, they grow in infertile being stimulated chemically from 1 to 2 weeks soils, such as the alkaline soils of the Middle by exudates from the host’s root (Sauerborn East. Few Orobanche species grow in acidic 1991, Parker and Riches 1993). Upon germi- soils, as the lower pH causes the seeds to ger- nation Orobanche seed develops a radicle that minate at distances so far from the host that grows in the direction of the chemical stimuli contact between parasite seedling and host of the host’s root. This distance is generally root is not accomplished, thus resulting in the not more than a few centimeters from the seedling’s eventual death (Parker and Riches Orobanche seed. Once the radicle reaches the 1993). Most Orobanche species are found in the host root, a haustorium (that part of the para- Mediterranean region with its characteristic site that grows inside the host) is produced, climate, but are also found in humid, subtropi- which attaches the Orobanche seedling to the cal, arid, semiarid, and temperate climates. They host. The haustorium is also the site where the are associated with both irrigated and nonirri- bud and shoot of the parasite emerge and gated lands (Sauerborn 1991). Orobanche fasci- elongate (Parker and Riches 1993). A parasite culata is endemic to North America, ranging

1Department of Integrative Biology, Brigham Young University, Provo, UT 84602. 2275 West Juniper Avenue #1073, Gilbert, AZ 85233. 3Corresponding author: 435 WIDB, Department of Integrative Biology, Brigham Young University, Provo, UT 84602. 4Department of Ancient Scripture, Brigham Young University, Provo, UT 84602.

242 2005] NUTRIENT DYNAMICS BETWEEN OROBANCHE AND ARTEMISIA 243 in distribution from the Yukon Territory, south of Hill Creek. The study site covers 0.8–1.2 ha to Mexico, east to Michigan, and west to Cali- and is located on highly clay loam Green fornia. Within this range, O. fasciculata is asso- River shale soils underlain by fractured sand- ciated with sand dune ecosystems, arid - stone layers called Hill Creek Rock, which has lands and grasslands, pinyon/juniper wood- been mined and used as ornamental building lands, aspen, and fir communities up to 3260 m material. Artemisia pygmaea is the dominant in elevation (Reuter 1986, Welsh et al. 1993). shrub on the site, although its population den- However, O. fasciculata is an uncommon spe- sities are low. Low-growing and grasses cies. As such, several states have listed it as including corymbosum, Elymus spi- rare (Indiana and the province of Ontario), catus, Atriplex confertifolia, Stipa, hymenoides, threatened (Wisconsin and Michigan), and even and Artemisia tridentata dominate areas adja- endangered (Illinois; Sheviak 1978, Bacone cent to the study area (Brotherson 1967). and Hedge 1980, Argus and White 1982, Soils are shallow, sandy clay loams, residual Brynildson and Alverson 1982, Beaman et al. in nature, sandstone based, and rocky. Calcare- 1985). No listing of O. fasciculata as threat- ous and basic, they contain elevated levels of ened or endangered is known in Utah. soluble salts in the upper 46 cm of the soil Other than taxonomic studies, little research profile. Clay increases with depth to 15 cm has been done on O. fasciculata. Reuter (1986) and then decreases. Cation exchange capacity studied the habitat and reproductive ecology ranges from 20 to 25 meq per 100 grams of of O. fasciculata in a sand dune ecosystem in soil and increases with depth. Calcium, potas- Wisconsin. She concluded that O. fasciculata sium, and sodium concentrations decrease with has the ability to reproduce parthenogeneti- depth while magnesium increases (Brotherson cally, that it produces many seeds which dis- 1967). Macronutrient concentrations are low perse across long distances and yet as a species (<215 ppm), with nitrogen, phosphorus, potas- would be considered uncommon, a fact thought sium, and sodium being the lowest. Micro- to be associated with parasite seed dispersal nutrients were more abundant than macro- and host growth dynamics. nutrients. Artemisia pygmaea Gray, or pygmy sage- The area receives between 30 and 40 cm of brush, is found in Arizona, , and Utah rain annually, 10–20 cm falling as snow from growing in shallow, infertile calcareous soils October to April and 10–20 cm from summer (Ward 1953). It has been collected in 13 coun- thunderstorms between May and September. ties from Utah’s desert and mountainous During the winter months temperature lows regions where it grows on clay loam soils asso- average between –18° and –16°C, while mean ciated with Green River shale, igneous and highs range from –2° to 0°C. In the summer calcareous gravels, and dolomitic outcrops or lower temperatures average 9° to 13°C and gravels (Welsh et al. 1993). A dwarf shrub the highs range from 27° to 31°C (Greer et al. (0.5–2 dm tall), A. pygmaea grows in patches 1981). and is not useful as browse (McArthur et al. The study site has had a grazing history of 1979). Welsh et al. (1993) indicate A. pygmaea primarily wild horses, mule deer, and rabbits. is often associated with rare plant species, such Occasional sheep and cattle grazing has also as O. fasciculata. occurred. The purpose of this study is to analyze the host-parasite relationships between A. pygmaea METHODS Gray and O. fasciculata Nutt. regarding nutrient Field Methods uptake and transfer between host and parasite on populations found in the Uinta Basin of Data were taken in August 1986 and 1987. Utah, USA. Data taken during 1986 reflect nutrient flows from the soil to A. pygmaea roots to O. fascicu- STUDY SITE lata. The 1987 samples include data taken to reflect nutrient flows from soil to roots to stems The study site is located 20.5 km (33 miles) and leaves of the host plants along with the south of Ouray, Utah, on the Ute Indian Reser- soil-root-parasite relationship. We collected a vation in Duchesne County. The site is on a total of 20 soil samples, 10 per year. Fifty-eight gentle 2%–3%, west-facing slope on the plateau plant samples were also collected during the 244 WESTERN NORTH AMERICAN NATURALIST [Volume 65

2-year study, 20 in 1986 and 38 in 1987. Those the means of each element to identify any that taken in 1986 include 10 of A. pygmaea roots varied significantly in concentration between and 10 of O. fasciculata; the 1987 samples mir- the soil, A. pygmaea plant parts, and O. fascic- rored the 1986 samples with the addition of 9 ulata. The results were then analyzed to deter- stem and 9 samples of A. pygmaea. Plant mine the amount of each element that O. fas- and soil samples were collected as a set, with ciculata was taking from the roots of A. pyg- the plants sampled being randomly selected maea and the concentrations of each nutrient from across the study site with the use of a along the gradient (i.e., from roots to stems to random numbers table. Once the plants to be leaves) of A. pygmaea. Plant nomenclature fol- sampled were selected, a soil sample was col- lows Welch et al. 1993. lected within the root zone and packaged for transport to the laboratory for later analysis to RESULTS AND DISCUSSION determine available nutrients for the plant. Plant samples were divided into roots, stems, Mean ion concentrations (ppm) for each leaves, and associated parasites and were indi- nutrient studied in the soil, in the roots, stems, vidually packaged in air-breathing bags for and leaves of A. pygmaea, and in O. fasciculata transport to the laboratory where they were are found in Table 1. This table shows patterns dried at room temperature (23°C) in a Napco of nutrient enrichment with respect to ion model 630 drying oven. movement from soil to A. pygmaea roots then to stems and leaves, and from soil to A. pyg- Lab and Statistical Methods maea roots to parasite. The soil nutrient con- centration levels (macro- and micronutrients) All soil and plant samples collected from were low, reflecting the poor quality of the the field were analyzed by the Brigham Young soil. Nitrogen, phosphorus, potassium, and zinc University Soil and Plant Analysis Laboratory showed an increase in concentration along the for nutrient content of both macro- and micro- flow gradient in A. pygmaea. Magnesium, iron, nutrients in 1990. Macronutrients analyzed and manganese increased through the stems were nitrogen (N), phosphorus (P), potassium and then decreased in the leaves to concentra- (K), calcium (Ca), sodium (Na), and magnesium tions less than the roots. Such selective exclu- (Mg). Micronutrients were zinc (Zn), iron (Fe), sion of magnesium and iron may be related to manganese (Mn), and copper (Cu). Exchange- high potassium levels in the leaf in that ele- able calcium, magnesium, potassium, and sodi- vated levels of potassium have been shown to um in the soil were extracted using a buffered induce deficiencies in these ions. The low lev- neutral 1.0 normal ammonium acetate solution els of manganese may be due to A. pygmaea’s (Jackson 1958, Hesse 1971, Jones 1973). DTPA selective exclusion of manganese along with a (diethylene-triaminepentaacetic acid) was used decreased capacity to translocate manganese to extract iron, zinc, manganese, and copper from stems to leaves (Treshow 1970). from the soil (Lindsay and Norvell 1969). Soil Calcium and sodium increased from the phosphorus and nitrogen were determined soil to the roots and then decreased or re- using sodium bicarbonate and macro-Kjeldahl mained static, respectively, as they flowed from procedures, respectively (Olsen et al. 1954, the stems to the leaves. Individual element Jackson 1958). uptake can often be inhibited by the presence Individual plant samples were ground and of other elements (Bargagli 1998). The signifi- passed through a 20-mm-mesh screen using a cant decrease of calcium may be due to high Thomas-Wiley mill. Ion concentrations of nitro- potassium levels, which have been shown in gen, phosphorus, potassium, calcium, magne- some plants to impair calcium absorption. The sium, sodium, iron, zinc, manganese, and cop- 2 ions may compete for common transport per in the plant tissue were identified using mechanisms in membranes and on transport procedures described by Graham et al. (1970). proteins (Bargagli 1998). Potassium, which acts Mean concentrations, standard deviations, with sodium or even substitutes for it, may minimums, and maximums were calculated for unbalance calcium to sodium ratios. If ratios of each element analyzed in both the soil and potassium or sodium to calcium are too high, plant material. Tukey’s Honestly Significant calcium deficiency may be induced (Treshow Difference (HSD) tests were conducted on 1970). Copper increased in concentration in 2005] NUTRIENT DYNAMICS BETWEEN OROBANCHE AND ARTEMISIA 245

TABLE 1. Means (ppm) and significant differences in nutrient concentrations for plant parts and the soil. All values are significantly different (P ≤ 0.05) from each other unless otherwise noted.* Nutrient Soil Root Stems Leaves O. fasciculata Nitrogen 6 7200 8800 12200 4600 Phosphorus 7 400 600 700 1000 Potassium 214 4400 c 8900 cf 12600 f 19600 Calcium 9116 a 28500 g 23100 fg 16700 fi 13300 ai Sodium 30 bj 1000 300 fj 300 bf 1600 Magnesium 900 7400 ec 8800 cf 6000 efi 3600 i Zinc 0.41 24 c 37 cf 33 f 18 Iron 11 2242 c 2834 c 1260 i 1196 i Manganese 11 66 e 101 63 ei 43 i Copper 3 22 15 fh 18 f 13 h Macronutrients* 10300 41400 edg 41200 fgh 35700 efi 38100 dhi Micronutrients 26 2355 g 2977 g 1374 fi 1269 i

*Values are not significantly different between the following: a = soil – Orobanche f = stems – leaves b = soil – roots g = stems – roots c = roots – stems h = stems – Orobanche d = roots – Orobanche i = leaves – Orobanche e = roots – leaves j = stems – soil

TABLE 2. Ratios (ppm plant part/ ppm soil) between each plant part of A. pygmaea compared with the soil for all nutrients. For example, a ratio of 1200 indicates that A. pygmaea roots have that much greater concentration of a nutrient than found in the soil. Nutrient Root O. fasciculata Stem Leaves Nitrogen 1200 767 1467 2033 Phosphorus 57 143 86 100 Potassium 21 92 42 59 Calcium 3 1 3 2 Sodium 33 53 10 10 Magnesium 8 4 10 7 Zinc 59 44 66 80 Iron 204 109 258 115 Manganese 6 4 9 6 Copper 7 4 5 6 Macronutrients 4 4 4 4 Micronutrients 91 49 115 5

the roots, decreased in the stems, and then enhanced when these ions exist in the divalent showed a slight increase again in the leaves. form, a form that allows them to adhere more Table 1 illustrates the relationship between strongly to roots. nutrient concentrations in the soil and corre- Table 2 also shows that although nutrients sponding nutrient concentrations in the roots are higher in O. fasciculata than in the soil, of A. pygmaea and in the parasite O. fascicu- this parasite does exclude some nutrients over lata. As shown, nutrient levels in the plant others. For example, O. fasciculata takes up mirror nutrient levels in the soil. In other calcium on a 1:1 ratio with the soil (Table 2). words, if nutrient concentrations are high in This is probably due to interactions between the soil, they will be correspondingly high in high levels of sodium and potassium, which the plant tissues. This phenomenon, termed have been shown to inhibit calcium absorption luxury consumption, asserts that a plant will in other plants (Boynton and Burrell 1944). absorb and accumulate more nutrients than it Compared with A. pygmaea roots, O. fasci- needs simply because the nutrients are more culata absorbed significantly higher concen- abundant in the soil (Treshow 1970, Brother- trations (x– = 2.83 times) of phosphorus, potas- son 1992). Further, the uptake of the micronu- sium, and sodium. Otherwise, O. fasciculata trients zinc, iron, manganese, and copper is contained the lowest concentrations (x– = 0.59 246 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 3. Ratios (ppm/ppm) of mineral nutrient concentrations in the soil and plant parts according to nutrient flow from the soil to roots to stems to leaves and to Orobanche fasciculata. Nutrient Roots/Soil Stems/Roots Leaves/Stems Orobanche/Roots Nitrogen 1200 1.22 1.39 0.64 Phosphorus 57 1.5 1.17 2.5 Potassium 21 2.02 1.42 4.45 Calcium 3 0.81 0.72 0.47 Sodium 33 0.3 1 1.6 Magnesium 8 1.2 0.68 0.49 Zinc 59 1.13 1.22 0.75 Iron 195 1.26 0.44 0.53 Manganese 6 1.53 0.62 0.65 Copper 8 0.68 1.2 0.59 Macronutrients 4 1 0.87 0.92 Micronutrients 91 1.26 0.05 0.54

Fig. 1. Ratio of nutrients in Orobanche fasciculata compared with nutrient levels in Artemisia pygmaea roots. times) of all other macro- and micronutrients important to Orobanche’s physiology. Phos- (N, Ca, Mg, Zn, Fe, Mn, and Cu; Table 3). phorus, for example, is a major component of Concentrations of all nutrients were signifi- adenosine triphosphate (ATP), which must be cantly different (P < 0.05) between roots of A. present in high amounts to provide energy for pygmaea and O. fasciculata. Differences be- nutrient uptake. Potassium and sodium would tween nutrient concentrations in O. fascicu- likely be absorbed in high quantities because lata and other plant organs also existed. How- they act in osmotic regulation of cellular fluids ever, such differences appear to be of little and produce an osmotic potential in the body value in explaining patterns of nutrient uptake of the parasite that when in combination with in the parasite since it parasitizes roots only. the parasite’s production of mannitol will aid Table 3 presents the nutrient concentration in the uptake of all other needed nutrients gradients (i.e., parasites to root, stem to root, (Parker and Riches 1993). Without such en- and leaf to stem ratios) of A. pygmaea and O. hancement of the parasite’s osmotic potential, fasciculata according to the path of nutrient the parasite would be unable to take up enough flow. All nutrient concentration gradients show nutrients for its survival. In contrast to A. pyg- a negative relationship (<1.0) between host maea, O. fasciculata is very selective in its roots and parasite except for phosphorus, nutrient uptake, as is illustrated by its exclud- potassium, and sodium (Table 3). Magnifica- ing or reducing uptake of major quantities of tion of these nutrients by the parasite may be most of the sampled nutrients in the study luxury consumption or it may be that they are (Fig. 1). 2005] NUTRIENT DYNAMICS BETWEEN OROBANCHE AND ARTEMISIA 247

For example, Orobanche species are lim- GRAHAM, R.D., C. LLANO, AND A. ULRICO. 1970. Rapid ited in their use of inorganic nitrogen (NO ) preparation of plant samples for cation analysis. 3 Communications in Soil Science and Plant Analysis because they do not synthesize nitrate reduc- 1:373–382. tase (Parker and Riches 1993). Instead, O. fas- GREER, D.C., K.D. GURGEL, H.A. CHRISTY, AND G.B. PETER- ciculata and other Orobanche spp. utilize SON. 1981. Atlas of Utah. Weber State College, Ogden, ammonium nitrogen, which can be metabo- UT, and Brigham Young University Press, Provo, UT. lized with glutamine synthetase in the GS1 300 pp. HESSE, P.R. 1971. Textbook of soil chemical analysis. form. It is also presumed that these parasites William Clowes and Sons, Ltd., London. 520 pp. can obtain their necessary amino acids directly JACKSON, M.L. 1958. Soil chemical analysis. Prentice-Hall, from the host’s xylem and phloem (Parker and Inc., Englewood Cliffs, NJ. 498 pp. Riches 1993). The nitrogen balance between JONES, J.B. 1973. Soil testing in the United States. Com- munications in Soil Science and Plant Analysis 4: A. pygmaea and O. fasciculata is delicate as 307–322. increased nitrogen levels in the host plant KUIJT, J. 1969. The biology of parasitic flowering plants. would allow the host to reverse the osmotic University of California Press, Berkeley and Los potential in favor of itself, thus decreasing the Angeles. 246 pp. vigor and even killing the parasite (Sauerborn LINDSAY, W.L., AND W.A. NORVELL. 1969. Equilibrium relationships of Zn2+, Fe3+, Ca2+ and H+ with 1991). EDTA and ETPA in soil. Soil Society of America Host plants can be damaged or even killed Proceedings 33:62–68. when parasitized by Orobanche spp. When MCARTHUR, E.D., A.C. BLAUER, A.P. PLUMMER, AND R. heavily parasitized, host plant growth declines STEVENS. 1979. Characteristics and hybridization of important Intermountain shrubs. III. Sunflower fam- or even stops and severe wilting occurs in some ily. Research Paper INT-220, USDA Forest Service, instances (Sauerborn 1991). Biomass produc- Intermountain Forest and Range Experiment Sta- tion has been shown to be severely reduced or tion, Ogden, UT. 82 pp. even eliminated in crop plants when heavily OLSEN, S.R., C.V. COLE, F.S. WATANABE, AND L.A. DEAN. parasitized by Orobanche (Sauerborn 1991). 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939. LITERATURE CITED PARKER, C., AND C.R. RICHES. 1993. Parasitic weeds of the world: biology and control. CAB International, Wall- ARGUS, G.W., AND D.W. WHITE. 1982. The rare vascular ingford, Oxon, UK. plants of Ontario. Syllogeus series 14. Botany Divi- REUTER, B.C. 1986. The habitat, reproductive ecology and sion, National Museum of Natural Sciences, Ottawa, host relations of Orobanche fasciculata Nutt. (Oro- Canada. 63 pp. banchaceae) in Wisconsin. Bulletin of the Torrey BACONE, J.A., AND C.L. HEDGE. 1980. A preliminary list Botanical Club 113:110–117. of endangered and threatened plants in Indiana. SAUERBORN, J. 1991. Parasitic flowering plants: ecology Proceedings of the Indiana Academy of Science 89: and management. Margraf Scientific Books, Weiker- 359–371. sheim, Germany. 127 pp. BARGAGLI, R. 1998. Trace elements in terrestrial plants: an SHEVIAK, C.J. 1978. Proposed list for state endangered/ ecophysiological approach to biomonitoring and threatened status plants. Natural Land Institute, biorecovery. Springer-Verlag, Georgetown, TX. 324 Rockford, IL. pp. TRESHOW, M. 1970. Environment and plant response. BEAMAN, J.H., E.A. BOURDO, F.W. CASE, S.R. CRISPIN, D. McGraw-Hill Book Company, New York. 422 pp. HENSON, R.W. PIPPEN, A.A. REZNICEK, ET AL. 1985. WARD, G.H. 1953. Artemisia, section Seriphidium, in North Endangered and threatened vascular plants in Michi- America: a cytotaxonomic study. Contributions from gan. II. Third biennial review proposed list. Michigan the Dudley Herbarium 4:155–205. Botany 24:99–116. WELSH, S.L., N.D. ATWOOD, S. GOODRICH, AND L.C. HIG- BOYNTON, D., AND A.B. BURRELL. 1944. Potassium-induced GINS. 1993. A Utah flora. Brigham Young University magnesium deficiency in the McIntosh apple tree. Press, Provo, UT. 986 pp. Soil Science. 58:441–454. WOLFE, A.D., AND C.W. DEPAMPHILIS. 1997. Alternate BROTHERSON, J.D. 1967. A study of certain community re- paths of evolution for the photosynthetic gene rbsL lationships of Eriogonum corymbosum Benth. in DC in four nonphotosynthetic species of Orobanche. in the Uinta Basin, Utah. Unpublished master’s the- Plant Molecular Biology 33:965–977. sis, Brigham Young University, Provo, UT. ______. 1992. Mineral-nutrient concentrations in the Received 5 February 2002 mountain mahogany species Cercocarpus montanus Accepted 20 August 2004 and Cercocarpus intricatus and in their associated soils. Journal of Plant Nutrition 15:49–67. BRYNILDSON, I., AND B. ALVERSON. 1982. Wisconsin’s en- dangered flora. Department of Natural Resources, Office of Endangered and Nongame Species. 47 pp.