Effects of perennial neighbors and nitrogen pulses on growth and nitrogenuptake by Bromus tectorum

Carolyn Yoder* and Martyn CaldwellDepartment of Rangeland Resources and the Ecology Center, Utah State University, Logan, UT 84322-5205,USA; *Author for correspondence (e-mail: carolyn.yoder@eku.edu; fax: (+1) 859-622-1399)

Received 7 April 2000; accepted in revised form 15 November 2000

Key words: Great Basin vegetation, N uptake, Nutrient pulses

Abstract

An experiment was conducted to determine if growth and biomass responses of the annual grass Bromus tec-torum are affected by the magnitude and timing of nitrogen (N) pulses and if these responses are influenced bydifferent perennial neighbor species. Nitrogen (NH4:NO3) was applied in three pulse treatments of varying in-terpulse length (3-d, 9-d, or 21-d between N additions). The total amount of N added was the same among treat-ments; hence, both the frequency and magnitude of N pulses varied (i.e., the longer the interpulse period, thegreater the amount of N added for a single pulse). Bromus showed little response to the different N-pulse treat-ments. The only characteristic that varied among pulse treatments was specific leaf area (SLA), which was sig-nificantly greater when Bromus was grown under the 21-d N pulse than when grown under the 3-d or 9-d Npulses. Bromus height, leaf and tiller numbers, leaf area and aboveground biomass were not affected by the N-pulse treatments nor were tissue-N contents and concentrations. However, Bromus production and tissue-N weresignificantly different when Bromus was grown with different perennial neighbor species. Tiller production,aboveground biomass, and seed numbers of Bromus were lowest when the perennial neighbor was the tussockgrass Agropyron desertorum, intermediate when the neighbor was the evergreen shrub Artemisia tridentata, andgreatest when the neighbor was the deciduous shrub Chrysothamnus nauseosus. N contents of Bromus leaveswere also lowest when the neighbor was Agropyron. In contrast, root N uptake capacities were greatest for Agro-pyron-Bromus root mixes and lowest for Chrysothamnus-Bromus root mixes. These results suggest that perennialneighbors affect growth, seed production, and N uptake of Bromus to a greater extent than the timing and mag-nitude of N pulses.

Introduction

Plant-available nitrogen (N) most likely occurs inpulses associated with precipitation following dry pe-riods, freeze-thaw events and disturbances such as fireand animal activity that stimulate mineralization orlyses of microbial biomass and consequent release ofN (Bowman 1992; Fisher et al. 1987; DeLuca et al.1992; Lodge et al. 1994). The timing and magnitudeof such N pulses likely have important consequencesfor plant N acquisition, but interactions between thetiming of resource pulses and resource uptake byplants are not well understood (Casper and Jackson1997; Goldberg and Novoplansky 1997). Some recent

studies have investigated plant responses to resourcepulses (e.g., Poorter and Lambers (1986); Crick andGrime (1987); Miao and Bazzaz (1990); Bilbroughand Caldwell (1997)), but none have investigated re-lationships between the timing of resource pulses andthe influence of neighbors on patterns of resource ac-quisition. Here, we report how an exotic annual inva-sive grass in the North American Great Basin, Bro-mus tectorum, responded to N pulses of differentmagnitude and timing while growing with one ofthree native perennial neighbors that have differentlife forms or phenology.

Bromus tectorum was introduced from Eurasia intothe Great Basin of western North America in the late

77Plant Ecology 158: 77–84, 2002.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.

1800’s (Novak et al. 1993) and is now widespread(Daubenmire 1970; Mack 1981, 1986; Novak et al.1993). In a large field study involving controlledpulses of N in sand culture (Bilbrough and Caldwell1997), Bromus and several native Great Basin speciesexhibited greater growth rates and biomass produc-tion when N was supplied in early- and mid-springpulses than when N was supplied in a continuousmanner (control treatment). However, the specieswere grown in monoculture, so the influence of pe-rennial neighbors on the response of Bromus to Npulses was not examined.

Plant species respond differently to the timing(Bilbrough and Caldwell 1997) and duration (Camp-bell and Grime 1989) of nutrient pulses, apparentlydue to differences in phenology and growth form andconsequent differences in the timing of demand fornutrients. Therefore, neighbor species may play alarge role in plant response to pulses of available N.Because Bromus responded strongly to N pulses inthe field (Bilbrough and Caldwell 1997), we predictedthat under controlled conditions, Bromus would havegreater biomass and seed production when exposed tolarge, infrequent pulses of N than when exposed tosmaller, frequent pulses (approaching a continuous Nsupply similar to the control in the earlier field ex-periments). We further predicted that the response ofBromus to pulses would be most evident when grow-ing with perennial neighbors that have little spatialand temporal overlap of resource acquisition withBromus and least evident when growing with neigh-bor species that have similar patterns of resource ac-quisition as Bromus. To test these predictions, Bromuswas grown from seed in pots that contained one ofthree perennial species: the perennial tussock grassAgropyron desertorum, which responded strongly toearly- and mid-spring N pulses in the field experi-ments; the evergreen shrub, Artemisia tridentata,which also exhibited a significant growth response topulses, though less pronounced than that of Agropy-ron; or the deciduous shrub Chrysothamnus nauseo-sus, which did not respond to N pulses (Bilbroughand Caldwell 1997). Therefore, when Bromus wasgrowing with these different species as neighbors, weexpected that Bromus would respond most strongly toN pulses when growing next to the drought-decidu-ous shrub Chrysothamnus and least when growingnext to tussock grass Agropyron.

Methods

Study species and growing conditions

In January 1999, 1-yr old seedlings of Artemisia tri-dentata ssp. vaseyana (Rydb.) Beetle (mountain bigsagebrush), and Chrysothamnus nauseosus (Pallas)Britt. (rubber rabbitbrush) were planted in cylindricalpots (0.20 m diameter × 0.4 m tall; 18 pots of eachspecies, one seedling per pot). The seedlings weregrown from seed collected in Sanpete County, Utahand were purchased from a nursery (Plants of theWild, Tekoa, Washington). The seedlings were single-stemmed and were � 18 and 24 cm tall for Artemi-sia and Chrysothamnus, respectively. Chrysothamnushad no leaves at the time of planting; however, leafbuds appeared within ten days and the seedlings werefully leaved ca. three weeks after planting. An addi-tional 18 pots were each planted with seven tillers ofthe perennial grass Agropyron desertorum (Fish. Ex.Link) Schult. (crested wheatgrass). The tillers werecollected from mature tussocks growing in a commongarden located near the campus of Utah State Univer-sity. The pots were filled with a quartz sand (0.35 mmdiameter) and native soil mix in a 3:1 ratio, respec-tively. The sand-soil mix was chosen so that the potswould drain readily, but would not require frequentwatering or fertilization to maintain plant growth. Thenative soil was a fine, loamy, mixed, Xerollic Calcior-thid of the Taylorsflat series and was collected from afield site near Rush Valley, Utah where each of thestudy species is abundant. Concentrations of NO3

−,NH4

+, and P in the sand-soil mix were 2.77, 0.206, and12.7 �g g−1, respectively.

After planting the perennial species centrallywithin each pot, seven seeds of the annual grass Bro-mus tectorum L. (cheatgrass) were planted � 0.5 cmdeep in a circle around the perennial plant. The Bro-mus seeds were collected by hand from plants grow-ing wild near Rush Valley, Utah the previous summer.Once the Bromus plants emerged from the soil andwere 1 to 2 cm tall, densities were thinned to fiveplants per pot. The study was conducted in a glass-house on the campus of Utah State University, Logan,Utah. Day/night temperatures were maintained at21/10 °C, respectively. No supplemental light wasused.

The experimental design was a completely ran-domized three × three factorial with six replications.The treatments consisted of three different perennialneighbor species and three N-pulse treatments, de-

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scribed below. Response variables included Bromusheight, leaf and tiller number, final dry mass, tissue-Ncontent and concentration, and root-N-uptake capac-ity.

N-pulse treatments

Nitrogen (NH4:NO3) was applied in three pulse treat-ments of varying interpulse length (3-d, 9-d, or 21-d)from January 25 – June 4, 1999. The total amount ofN added (117 mg pot−1) was the same among treat-ments. Hence, both the frequency and the magnitudeof N pulses varied among treatments; i.e., the 3-dpulse treatment consisted of 43 applications of 2.72mg N applied every 3rd d, the 9-d pulse treatmentconsisted of 15 applications of 7.8 mg N applied ev-ery 9th d, and the 21-d pulse treatment consisted of 7applications of 16.71 mg N applied every 21st d. TheN pulses were delivered in 270 mL of water. Thisvolume of water was adequate for recharging potmoisture to a depth of 0.35 m but was not largeenough to result in drainage of liquid from the pots.Regardless of the pulse treatment, all pots receivedthe same quantity of water with equal frequency (i.e.,250 mL of water + 20 mL of N solution or 270 mLof N-free water every three days). Soil water content(SWC, g water g−1 soil) was measured periodicallyfrom soil samples collected from each pot three timesduring the experiment at two soil depths (0.10 m and0.30 m). The soil samples were collected three daysafter the first, middle, and last pulse for each treat-ment.

At the end of the experiment, June 4, 1999, plantN-uptake capacity was assessed for Bromus and theassociated perennial species by applying 23 mg of99.8 atom % 15NH4:15NO3 (Isotech, Inc., Miamis-burg, OH, USA) in 250 ml H2O. This date was cho-sen because the Bromus plants were nearing maturityand N uptake capacities were expected to be nearmaximum. Some, but not all, Bromus had flowered bythis time. We did not wait for all Bromus to flowerbecause senesence occurs soon after anthesis, and inthis experiment we were most interested in root-N-uptake capacity. The 15N-solution was allowed to re-main for 30 minutes before Bromus and the perennialplants were removed from the pots. Roots from eachpot were washed through a fine mesh screen (0.6mm), dried in a convection oven at 65 °C to constantmass and weighed to obtain dry mass. Because theBromus roots were very fine and completely inter-twined with the perennial plant roots, Bromus roots

were not separated from the perennial plant roots;rather, whole-pot root mass values were obtained.Root and shoot tissue N concentration and 15N-en-richment were measured by continuous-flow directcombustion and mass spectrometry using an ANCA2020 system (Europa Scientific, Cheshire, UK). TotalN content (mg) was calculated by multiplying totalbiomass by tissue N concentrations.

Plant growth, leaf area and biomass measurements

Prior to the initiation of N-treatments, initial peren-nial plant sizes were recorded (height and width forArtemisia and Chrysothamnus, number of tillers andleaves and maximum height for Agropyron). Peren-nial plant sizes were then measured monthly through-out the experiment. Bromus height and number ofleaves were recorded bi- or tri-weekly throughout theexperiment on two individuals per pot. Phenologicalstages of Bromus and the perennial species were alsorecorded throughout the experiment. At final harvest,total numbers of tillers and leaves were counted forthe two individuals per pot that had been monitoredthroughout the experiment for leaf number andheight. Leaf areas for these same individuals weremeasured with a Li-3100 leaf area meter (LiCor, Lin-coln, NE, USA). Specific leaf area (SLA) was deter-mined by dividing the leaf area by the dry mass ofthe sample. All remaining aboveground Bromus tis-sues were dried in a convection oven at 65 °C to aconstant mass. Perennial aboveground tissues werealso dried and weighed to obtain total abovegroundbiomass.

Statistical analysis

Statistical analyses were performed with SAS soft-ware (SAS institute, Inc., Cary, NC, USA). Repeatedmeasures analysis of variance (ANOVA) was used totest for significant differences (P � 0.05) in Bromusheight and number of leaves through time. Main ef-fects were perennial neighbor and N-pulse treatments;plants within pots were treated as subsamples. Re-maining variables (i.e., final dry mass, tissue-N, N-uptake capacity, etc.) were analyzed as a two-factorANOVA in a completely randomized design. Whereappropriate, means were separated using the Dun-can’s New Multiple Range Test (Snedecor and Co-chran 1980). Plots of residuals against predicted val-ues as well as normality curves were used to test theassumptions of equal variance and normality. Data

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were transformed as needed until the Shapiro-Wilktest statistic, normal probability plots, and stem leafplots (Cody and Smith 1991) indicated normally dis-tributed data.

Results

Growth responses

Bromus growth (as measured by increase in height)was not significantly different among N-pulse or pe-rennial-neighbor treatments (Figure 1). Bromus leafproduction was also not affected by the N-pulse treat-ments (Figure 1). However, Bromus leaf productionwas significantly lower when the perennial neighborwas Agropyron than when the neighbor wasChrysothamnus or Artemisia (Figure 1).

Growth of perennial shrubs (as measured by in-crease in canopy height and width) was also not af-fected by the N-pulse treatments (data not shown).However, the tussock grass, Agropyron, grew signifi-cantly more leaves (P = 0.02) under the 3-d N pulsethan when experiencing 9-d or 21-d N pulses (mean± SE = 55.5 ± 5.4; 43.5 ± 3.5; 46.5 ± 3.6 for the 3-d,9-d, and 21-d N pulses, respectively).

Total production at final harvest

At final harvest, Bromus leaf and tiller numbers werenot different among N-pulse treatments. However,Bromus produced significantly fewer tillers when the

neighbor species was Agropyron than when the neigh-bor species was Artemisia or Chrysothamnus (Fig-ure 2). In addition, Bromus produced fewer leaveswhen the neighbor was Agropyron or Chrysothamnusthan when the neighbor was Artemisia (Figure 2).Leaf area of Bromus was not significantly differentamong the N-pulse treatments or the species of pe-rennial neighbors (Figure 2). However, specific leafarea (SLA) was significantly greater for Bromusgrown under the 21-d N pulse than when Bromus wasgrown under the 3-d or the 9-d N-pulse treatments(Figure 2). Final aboveground biomass of Bromuswas not affected by the N-pulse treatments, but wassignificantly different among perennial-neighbortreatments; Bromus neighboring Chrysothamnus hadsignificantly greater aboveground biomass than Bro-mus neighboring Agropyron or Artemisia (Figure 3).For the perennial species, aboveground biomass wasgreatest for Agropyron, intermediate for Artemisia,and lowest for Chrysothamnus (Figure 3). In contrast,the total pot belowground biomass was not signifi-cantly different among perennial-species or N-pulsetreatments (Figure 3). The perennial-neighbor × N-pulse interaction term was not significant for any ofthe biomass variables.

Bromus seed production at final harvest was con-siderably lower for plants neighboring Agropyron

Figure 1. Mean height and number of leaves (left and right pan-els, respectively) for Bromus tectorum on eight sample dates withassociated analysis of variance P-values. The Bromus was exposedto N pulses of different magnitude and frequency (see text) andgrown in pots with one of three perennial neighbors: Agropyrondesertorum, Artemisia tridentata, or Chrysothamnus nauseosus. Er-ror bars represent the standard error of the mean.

Figure 2. Mean tiller number (a), leaf number (b), leaf area (c),and specific leaf area (d) for Bromus tectorum at final harvest withassociated analysis of variance P-values (n = 12; 6 pots x 2 sub-samples). Species names on the X-axes indicate the perennialneighbor species grown with the Bromus. Error bars represent ofthe standard error of the mean.

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than for Bromus neighboring Chrysothamnus or Arte-misia (Table 1). Across perennial-neighbor treat-ments, seed production of Bromus grown under the9-d N pulse was greater than seed production ofplants grown under the 3-d or 21-d N pulses (Ta-ble 1). However, at the time of harvest only 7 % ofthe total 270 Bromus plants (54 pots × 5 Bromus perpot) had gone to seed. Therefore, the data do not lendthemselves to statistical analyses. Further, we do notknow if total seed production among treatmentswould have differed if all Bromus had completed theirlife cycle by the harvest date. However, rates of seedproduction were lowest for Bromus associated withAgropyron.

Plant tissue-N and N-uptake capacity

Neither Bromus nor perennial plant tissue-N contents(mg) were affected by the N-pulse treatments (Fig-ure 4). However, the N content of Bromus leaveswhose neighbor was Agropyron was significantlylower than the N content of Bromus leaves neighbor-ing Artemisia or Chrysothamnus (Figure 4). For theperennial species, the N content of the aboveground

tissue of Chrysothamnus was significantly lower thanthe N contents of aboveground tissues of Agropyronor Artemisia (Figure 4). The N content of roots (Bro-mus roots and perennial roots combined) was alsosignificantly lower for pots containing Chrysotham-nus than for pots containing Bromus with Agropyronor Artemisia (Figure 4).

Plant N concentrations (mg g−1 dry mass) werealso not significantly affected by the N-pulse treat-ments (Figure 4). However, the N concentration ofBromus grown with Artemisia was significantly lowerthan the N concentration of Bromus grown with Agro-pyron or Chrysothamnus (Figure 4). For the perennialspecies, the N concentration of Agropyron above-ground tissue was significantly lower than that of Ar-temisia or Chrysothamnus. For combined perennialand Bromus roots, N concentration was significantlylower for pots containing Chrysothamnus than forpots containing Agropyron or Artemisia (Figure 4).

The N-uptake capacity of roots (perennial com-bined with Bromus) was not significantly differentamong N-pulse treatments, but was significantly dif-ferent among perennial-species treatments (Figure 5).Root N-uptake capacity was greatest for the Bromus-Agropyron root combination and lowest for the Bro-mus-Chrysothamnus root combination (Figure 5).

Discussion

Bromus showed little response to the timing and mag-nitude of N pulses. The only characteristic that dif-fered significantly with pulse treatments was specificleaf area (SLA), which was greater for Bromus grownunder the 21-d N pulse than when grown under the3-d or 9-d N pulses. Because there is a strong, posi-tive correlation between SLA and photosynthetic N-use efficiency (PNUE) in many species (e.g., Poorterand Evans (1998)), Bromus grown under the 21-d Npulse may have had greater PNUE than Bromusgrown under the 3-d or 9-d N pulses. However, nosignificant differences in N-uptake capacity, tissue-Ncontent, tissue-N concentration, or final dry mass ofBromus occurred among N- pulse treatments. There-fore, no advantage was apparent for Bromus grownunder the 21-d N pulse compared to those given themore frequent pulses.

The perennial-neighbor species also failed to re-spond differently to the N-pulse treatments. These re-sults are inconsistent with earlier field experiments(Bilbrough and Caldwell 1997) where Bromus, Agro-

Figure 3. Mean dry mass of plant tissue at final harvest with as-sociated analysis of variance P-values (n = 6). Species names onthe X-axis indicate the perennial neighbor species grown with theBromus. Error bars represent the standard error of the mean.

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pyron, and the evergreen shrub Artemisia tridentataresponded to early- and mid-spring N pulses with in-creased growth rates and biomass production relativeto a continuous N supply. The inconsistency in plantresponse to N pulses between these studies may bedue, in part, to differences in the implementation ofthe pulse treatment. In the Bilbrough & Caldwell fieldstudy (Bilbrough and Caldwell 1997), each N pulsewas delivered over a four-day period that was fol-lowed by a heavy watering treatment to flush the Nbelow the root zone. In our study, the N added in thepulse treatments was not flushed. Therefore, ratherthan experiencing ephemeral pulses of N for a rela-tively short duration, the plants in our study receivedN pulses of different magnitude and frequency thatwere allowed to remain in the soil. This pulse regimemay more closely represent natural conditions sinceit is unlikely that N pulses would be removed so rap-idly by plant uptake or microbial immobilization.

In contrast to the N-pulse treatments, growth ratesand primary production of Bromus were significantlydifferent among perennial-neighbor treatments.

Growth rates of Bromus were lower when the peren-nial neighbor was Agropyron than when the neighborwas either Artemisia or Chrysothamnus. Furthermore,at final harvest, aboveground dry mass of Bromusgrown with Chrysothamnus or Artemisia was ca. 1.5and 1.3 times greater, respectively, than abovegrounddry mass of Bromus grown with Agropyron. Seed pro-duction rate of Bromus was also greater when grown

Table 1. Number of seeds produced by Bromus tectorum when grown in pots with different perennial species and exposed to N pulses ofdifferent frequency and magnitude (see text). The number of individuals that produced seed at the time of harvest is in parentheses.

Perennial species association 3-d N pulse 9-d N pulse 21-d N pulse Species Total

Agropyron desertorum 119 (2) 173 (2) 0 292 (4)

Artemisia tridentata 171 (3) 143 (2) 163 (3) 477 (8)

Chrysothamnus nauseosus 70 (1) 236 (5) 227 (2) 533 (8)

N pulse Total 360 (6) 552 (9) 390 (5) 1302 (20)

Figure 4. Mean tissue N contents (left panels) and concentrations(right panels) with associated analysis of variance P-values (n =6). Species names on the X-axes indicate the perennial neighborspecies grown with the Bromus. Error bars represent the standarderror of the mean.

Figure 5. Mean root nitrogen uptake capacities (g−1dry mass) forroot mixtures of Bromus tectorum and one of three perennial spe-cies: Agropyron desertorum, Artemisia tridentata, or Chrysotham-nus nauseosus with associated analysis of variance P-values (n =6). Species names on the X-axes indicate the perennial neighborspecies grown with Bromus. Error bars represent the standard errorof the mean.

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with Chrysothamnus or Artemisia than when grownwith Agropyron. Because the pots were watered fre-quently in order to maintain high soil water contentand soil water content did not differ significantlyamong pots with different perennial neighborsthroughout the experiment, lower Bromus productionin the Agropyron pots did not likely result from lowersoil water availability. Instead, differences in Bromusgrowth and production apparently occurred due todifferences in nutrient acquisition by the perennialspecies.

Because Bromus was not grown in monoculture inthis experiment, we cannot quantify competitive re-sponses between Bromus and the perennial species.However, differences in growth rates and biomassproduction of Bromus when grown with differentneighbor species, as well as root-N-uptake capacities(Figure 5), suggest that competition for N was great-est between Bromus and Agropyron and least betweenBromus and Chrysothamnus. Because Bromus rootswere extremely fine and thoroughly interwoven withroots of the perennial species, the roots of Bromus andthe perennial species could not be separated. There-fore, root-N-uptake rates in (Figure 5) are rates ofcombined perennial and Bromus roots. Subsequently,we do not know if root mass and root uptake capac-ity of Bromus were influenced differently by the spe-cies of perennial neighbor. However, root N uptakecapacities were greatest for the Bromus-Agropyronroot mixtures and the N content of aboveground pe-rennial tissue was also greatest for Agropyron. In con-trast, N contents of Bromus leaves were lower whengrown in pots with Agropyron than when grown inpots with either Artemisia or Chrysothamnus. Theseresults suggest that the greater N-uptake rates of theBromus-Agropyron root mixtures were largely due toAgropyron roots.

In summary, growth rates and primary productionof Bromus were not affected by the magnitude andfrequency of N pulses. Therefore, we were unable totest our predictions regarding the relative responsesof Bromus to N pulses when growing next to peren-nial neighbors of different life form or phenology.However, growth rates and production of Bromuswere influenced strongly by perennial neighbors.Tiller production, aboveground biomass, rates of seedproduction, and N-uptake capacity suggested thatcompetition for N was greatest between Bromus andthe tussock grass, Agropyron, and least between Bro-mus and the deciduous shrub Chrysothamnus. Theseresults are consistent with a field study (Bilbrough

and Caldwell 1997), which indicated that Agropyron,Artemisia and Bromus exhibit similar temporal pat-terns of resource acquisition, whereas Chrysothamnusexhibits later phenological development and largelyavoids competition. In our study, Agropyron beganproducing reproductive tillers shortly ( � 2 weeks)after transplanting vegetative tillers into the green-house and Artemisia began reproductive growth� 15 weeks after the seedlings were planted. In con-trast, Chrysothamnus did not initiate reproductivegrowth during the course of this experiment. The re-sults of our study indicate that perennial species as-sociations affect growth and seed production of Bro-mus to a greater extent than the timing and magnitudeof N additions.

Acknowledgements

Authors thank Amy Stevenson, Usha Spaulding, AnnMull, Lori Bently, Mayme Seng and Brent Binghamfor assistance in the greenhouse and with measuring,harvesting, grinding, and weighing plant tissue. Thisresearch was supported by the National ScienceFoundation (grant # DEB-9807097) and the Utah Ag-ricultural Experiment Station.

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