Centaurea solstitialis Invasion Success Is Influenced by pulchra Size Kimberly J. Reever Morghan1,2 and Kevin J. Rice3

Abstract We allowed C. solstitialis seed to fall naturally into plots Replacement of perennial grasses with non-native annual containing N. pulchra . For each plot, we measured grasses in ’s Central Valley and foot- the number of C. solstitialis seedlings and mature plants, as hills has increased deep soil water availability. Yellow well as C. solstitialis biomass and seedhead production. In starthistle (Centaurea solstitialis), a deep-rooted invasive both years of the study, C. solstitialis number, biomass, and thistle, can use this water to invade annual grasslands. seedhead production declined significantly as N. pulchra Native perennial bunchgrasses, such as Purple needlegrass size increased. However, even C. solstitialis grown with (), also use deep soil water, so there is an the largest N. pulchra plants produced some seed, espe- overlap in resource use between N. pulchra and C. solsti- cially during the higher rainfall year. We conclude that tialis. Restoration of N. pulchra to annual grasslands restoration plantings with larger, established N. pulchra could result in strong competitive interactions between plants will be more resistant to invasion by C. solstitialis N. pulchra and C. solstitialis, which may reduce survival, than young N. pulchra plantings, but site management growth, and reproduction of the invader. The strength of must continue as long as a C. solstitialis seed source is this competitive interaction can increase as N. pulchra present. plants mature, increase in size, and develop more exten- sive root systems. We studied how the size of N. pulchra Key words: Centaurea solstitialis, restoration, affected the success of C. solstitialis invasion over 2 years. invasion, Nassella pulchra.

Introduction Valley, where changing soil moisture levels resulting from Perennial bunchgrasses were once an important com- the invasion of annual grasses appears to have facilitated ponent of the native vegetation of California’s Central invasion by the deep-rooted annual thistle, Yellow star- Valley, and Purple needlegrass (Nassella pulchra) was thistle (Centaurea solstitialis). considered one of the dominant grasses (Clements 1934; Non-native annual grasses that dominate grasslands in Bartolome et al. 1986; Heady 1988, though different argu- California only reduce soil moisture to a depth of about ments are offered by Hamilton 1997; Holstein 2001). How- 30 cm and leave deep soil water relatively untouched ever, the combined effects of invasion by exotic species, (Holmes & Rice 1996). Centaurea solstitialis is a more drought, overgrazing, and agriculture resulted in replace- recent invader and uses the deep soil moisture left ment of most of the perennial grasses with non-native by annual grasses to invade many California grasslands annual grasses (Dasmann 1973; Heady 1988; Menke 1989; (Borman et al. 1992). Studies have shown a positive corre- Gerlach et al. 1998). lation between C. solstitialis invasion success and soil In fact, the grasslands of California’s Central Valley water availability during late spring and summer (Dukes may be experiencing an ‘‘invasional meltdown’’ where the 2001). Unfortunately, C. solstitialis is one of the most seri- initial invasion by one group of non-native species in- ous invasive weeds in the western and cov- creases the likelihood that other non-native species will ers an estimated 10–22 million acres in California (White invade. When describing the concept of invasion melt- 1999; DiTomaso 2000; DiTomaso et al. 2000). Thus, the down, Simberloff and Von Holle (1999) give as an ex- conversion from perennial grasslands to annual grasslands ample the modification of habitat by a non-native has increased deep soil moisture availability and facili- that facilitates establishment by another non-native plant. tated invasion by an even more problematic invader. We propose that this is happening in California’s Central Restoring native perennial grasses to California grass- lands may slow this invasional meltdown, especially if native grasses preempt resources that C. solstitialis requires for 1 USDA/Agricultural Research Service, 67826-A, Hwy 205, Burns, OR 97720, successful establishment and reproduction. Centaurea sol- U.S.A. 2 stitialis is deeply rooted and has a long growing season; Address correspondence to K. J. Reever Morghan, email morghan@ rocketmail.com native perennial grasses may create an effective barrier 3 Department of Plant Sciences and Center for Population Biology, University to invasion if the grasses compete with C. solstitialis for of California, Davis, Davis, CA 95616, U.S.A. above- and belowground resources, especially deep soil Ó 2005 Society for Ecological Restoration International moisture. Centaurea solstitialis allocates much of its early

524 Restoration Ecology Vol. 13, No. 3, pp. 524–528 SEPTEMBER 2005 Nassella pulchra Effect on Centaurea solstitialis photosynthate to creation of a deep taproot to access deep mixed, nonacid, thermic Mollic Xerofluvents) (Huntington reserves of soil moisture (Thomsen et al. 1989; Roche´ et al. 1981). The mean annual precipitation for Davis et al. 1994; Gerlach et al. 1998). Although lacking a taproot, is 418 mm, and precipitation occurs primarily between the extensive fibrous root systems of perennial grasses can October and April, so plant growth relies mostly on stored also access moisture deep in the soil profile (Holmes & soil moisture between April and September (Major 1988). Rice 1996; Dyer & Rice 1999). For example, N. pulchra is Rainfall during the period of this study was 373 mm, or able to significantly reduce soil moisture at 60- to 150-cm 89% of normal, for the 2001–2002 growing season and soil depths (Dyer & Rice 1999). As a result, perennial 523 mm, or 125% of normal, for the 2002–2003 growing grasses extract at least as much deep soil water as C. solsti- season (California Irrigation Management Information tialis, and mature, well-established perennial grasses can System). The dominant vegetation in the site is a mixture extract even more (Borman et al. 1992; Gerlach 2004). of introduced annual grasses and forbs, including Bromus Deep soil water depletion under stands of cool-season diandrus, Bromus hordeaceus, Hordeum murinum, Avena perennial grasses creates summer water stress, which lim- fatua, and Centaurea solstitialis. its the success of C. solstitialis invasion (Borman et al. Each competition plot was a tube constructed from 1992; Roche´ et al. 1994). Competition with perennial a 30-cm-diameter by 100-cm-long section of polyvinyl grasses for light also negatively impacts C. solstitialis; chloride pipe. Tubes were set into 100-cm-deep holes, so shading by perennial grasses decreases root length, above- tops were flush with the soil surface and were refilled with ground biomass, and seedhead production of C. solstitialis soil from the site. Tubes were arranged in a grid with 1-m (Roche´ et al. 1994). Thus, restoring perennial grasses to spacing. The bottom of each tube was open, so rooting annual grass sites can potentially create an environment depth was not limited, but belowground competition could much more resistant to C. solstitialis invasion. only occur between plants rooted in the tubes (hereafter If restoration projects are to have long-term success, referred to as plots). Soil was not fertilized, and soil nutri- control of invaders is critical. There has been much interest ent levels are very similar between the tubes and adjacent in restoring sites in California using native perennial soil at the site. grasses, and researchers hope that these restored sites will We planted a single Nassella pulchra seedling in the be able to resist invasion (Bugg et al. 1991; Stromberg & center of each plot in December 1998. This site has been Kephart 1996). The maturity of a restoration project can used for C. solstitialis research in the past, and the plots influence the strength of competitive interactions between are located within a large patch of C. solstitialis, which perennial grasses and invaders because older perennial provides a regular seed rain. Half the N. pulchra plants grasses develop more extensive root systems. Dukes (2002) were grown with competition from C. solstitialis every found that monocultures containing seedling N. pulchra year, and the other half were grown alone. This was done were the most easily invaded communities by C. solstitialis, by allowing C. solstitialis seeds to naturally germinate in but those containing 1-year-old N. pulchra were among the the plots and subsequently removing all vegetation from least invasible communities. As a result, we would expect around the N. pulchra plants in the control plots and all a stronger negative impact of larger, more established but two of the C. solstitialis seedlings on either side of the N. pulchra plants on C. solstitialis invasion. N. pulchra in the competition plots. The N. pulchra that In this study we measured how the size of established were grown with competition were smaller, and there N. pulchra plants in a plot impacts invasion by C. solstitialis. was also individual variation in plant size. Thus, though The likelihood of invasion by C. solstitialis into restored N. pulchra plants were all 4 years old at the start of the sites is high, so restoration practitioners will benefit from experiment, there was variation in N. pulchra size. The ex- an understanding of how N. pulchra impacts C. solstitialis. isting population of C. solstitialis at the site was allowed to We predicted that larger N. pulchra plants would more form a dense stand in 2001, and natural C. solstitialis seed strongly resist invasion of C. solstitialis into adjacent soil rain was allowed to occur in the plots in the fall. We than small N. pulchra plants. This reduction of invasion weeded all species other than C. solstitialis and N. pulchra success will be indicated by decreased numbers of C. sol- from inside the plots throughout the experiment and kept stitialis at the end of the growing season and reduced seed- the area around each plot clear of aboveground com- head production by C. solstitialis in plots containing larger petition from plants rooted outside of the plots. N. pulchra plants. To measure N. pulchra size, we used digital calipers to measure the basal diameter along two perpendicular axes and then averaged these measurements to obtain mean Methods N. pulchra basal diameter. These measurements were made each May, when N. pulchra reached maximum size Study Site for the season. Basal diameter of N. pulchra is strongly The study was conducted at the Agronomy Farm on the related to harvested biomass (r2 ¼ 0.83, p ¼ 0.002; Reever campus of the University of California at Davis (lat Morghan, unpublished data), so use of basal diameter pro- 38°339N, long 121°489W, elevation 15 m). The soil at the vides a reasonable surrogate for bunchgrass size without site is a deep, well-drained Yolo loam soil series (fine-silty, destroying the production of the measured plants.

SEPTEMBER 2005 Restoration Ecology 525 Nassella pulchra Effect on Centaurea solstitialis

The number of C. solstitialis was counted in three differ- There was a significant negative relationship between ent ways. First, we counted the number of C. solstitialis the three remaining C. solstitialis response variables and seedlings as they emerged in the fall of 2001 and 2002; this N. pulchra size in both years of the study. The number of was recorded as ‘‘total C. solstitialis seedlings.’’ Second, in surviving C. solstitialis plants was negatively related to the fall of 2002 and 2003, after C. solstitialis matured and N. pulchra size in 2002 and 2003 (n ¼ 45, p ¼ 0.0003 and dropped some of its seeds, we harvested and counted all n ¼ 45, p ¼ 0.0023, respectively; Fig. 1A), as was the num- C. solstitialis plants in a plot, which we refer to as ‘‘number ber of C. solstitialis plants that flowered (n ¼ 39, p ¼ of surviving C. solstitialis.’’ Third, because not all the 0.0046 and n ¼ 39, p ¼ 0.0074, respectively; Fig. 1B). C. solstitialis plants that were alive at the end of the season There was also a significant negative relationship between produced flowers, we recorded the number of C. solstitialis N. pulchra size and C. solstitialis biomass in 2002 and 2003 plants that flowered and refer to this number as ‘‘num- (n ¼ 39, p ¼ 0.0033 and n ¼ 39, p ¼ 0.0013, respectively; ber of flowering C. solstitialis.’’ In addition, we oven-dried Fig. 1C) and C. solstitialis seedhead production (n ¼ 36, the harvested C. solstitialis at 60°C to a constant mass p ¼ 0.0023 and n ¼ 37, p ¼ 0.0048, respectively; Fig. 1D). and recorded the biomass of C. solstitialis for each plot. The ANCOVA showed that, overall, C. solstitialis vigor Finally, we counted all the seedheads on the plants in each was greater during the second year of the study. In 2003, plot to get a measure of C. solstitialis seedhead production there was a greater number of surviving plants (n ¼ 90, per plot. F[1,87] ¼ 27.93, p < 0.0001), a greater number flowering We used linear regression to test the relationships (n ¼ 78, F[1,75] ¼ 34.50, p < 0.0001), larger biomass (n ¼ between C. solstitialis life history data and N. pulchra size. 78, F[1,75] ¼ 12.52, p ¼ 0.0007), and greater seedhead pro- All C. solstitialis measurements were natural log(x 1 1) duction (n ¼ 73, F[1,70] ¼ 19.94, p < 0.0001) in each plot transformed prior to regression analysis to conform to as- at the end of the season. The regression slopes relating sumptions of parametric analyses. Plots without surviving N. pulchra size to C. solstitialis measurements did not dif- C. solstitialis plants were not used in the analyses of num- fer between years: surviving (n ¼ 90, t ¼ 0.55, p ¼ 0.58), ber of flowering C. solstitialis or biomass, and plots with flowering (n ¼ 78, t ¼ 0.61, p ¼ 0.55), biomass (n ¼ 78, t ¼ no surviving or flowering C. solstitialis were not used in 0.20, p ¼ 0.85), and seedheads (n ¼ 73, t ¼ 0.27, p ¼ 0.79). the analysis of seedhead production. In addition, we used analysis of covariance (ANCOVA) to test the difference in C. solstitialis responses between the 2 years to see if higher rainfall had a significant effect Discussion on C. solstitialis numbers, biomass, and reproduction. As predicted, established Nassella pulchra plants had We also used t tests to test whether the slopes relating a negative impact on Centaurea solstitialis during the N. pulchra size to C. solstitialis responses differed between growing season in both years of the study, and the strength years. of the interaction was dependent on N. pulchra size. The larger N. pulchra plants were much more successful at lim- iting the invasion success of C. solstitialis. The stronger impact seen in plots with larger N. pulchra agrees with Results other researchers’ findings that C. solstitialis survival, bio- During the winter of 2001–2002, the number of Centaurea mass, and flower production is decreased by perennial solstitialis seedlings emerging in each plot was highly vari- grasses, and this decrease is stronger in plots containing able and had no linear relationship to Nassella pulchra size perennial grasses with greater aboveground biomass in the 2 years (May 2001: n ¼ 39, r2 ¼ 0.002, p ¼ 0.91; May (Larson & McInnis 1989). Although the number, size, and 2002: n ¼ 39, r2 ¼ 0.003, p ¼ 0.88). During the winter of reproductive output of C. solstitialis increased in the sec- 2002–2003, however, there was a significant negative linear ond year of our study in response to higher rainfall, there relationship between initial C. solstitialis seedling number was no change in the strength of the overall interaction and the size of N. pulchra (n ¼ 40, r2 ¼ 0.16, p ¼ 0.011). between N. pulchra and C. solstitialis. Thus, the relative The percentage of C. solstitialis seedlings that died be- effect of N. pulchra competition on C. solstitialis does not tween emergence and the end of the season ranged from appear to change from a somewhat low-rainfall year to 0 to 100% and was significantly higher in plots containing a somewhat high-rainfall year. larger N. pulchra plants (n ¼ 44, r2 ¼ 0.33, p < 0.0001). Our experiment did not allow us to determine whether There was little change in mean size of N. pulchra over adult N. pulchra had a competitive effect on seedling the 2 years of the study. In the spring of 2002, N. pulchra C. solstitialis.IfN. pulchra competes directly with em- basal diameter ranged from 9.2 to 123.9 mm, with a mean erging seedlings, then seedling density would relate to of 85.2 ± 4.0 mm (X ± SE). In the spring of 2003, N. pul- N. pulchra size. We saw this negative relationship between chra basal diameter ranged from 21.1 to 127.4 mm, with N. pulchra size and initial number of C. solstitialis in the a mean of 88.6 ± 4.0 mm. Three N. pulchra plants died second year of the study but not in the first year. There during the summer of 2002, all of which were at the small were more C. solstitialis plants surrounding the plots in the end of the size distribution in the spring of 2002. first year than in the second because of the need to

526 Restoration Ecology SEPTEMBER 2005 Nassella pulchra Effect on Centaurea solstitialis

8 2 A 2002: r = 0.27, p = 0.0003 B 2002: r2 = 0.20, p = 0.0046 2 6 2 2003: r = 0.20, p = 0.0023 ) 2003: r = 0.18, p = 0.0074

) 6

4 4 C. solstitialis C. solstitialis 2 2

Log (Total 0 0 Log (Flowering

0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 Nassella pulchra basal diameter Nassella pulchra basal diameter

8 2 C 2002: r2 = 0.21, p = 0.0033 D 2002: r = 0.24, p = 0.0023 2 8 2 2003: r = 0.25, p = 0.0013 2003: r = 0.21, p = 0.0048 6

6

4 seedheads) biomass) (g)

4 2 C. solstitialis C. solstitialis 2 0 Log ( Log (

0 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 Nassella pulchra basal diameter Nassella pulchra basal diameter

Figure 1. Per plot relationship between Nassella pulchra basal diameter and Centaurea solstitialis measurements: (A) number of surviving C. solstitialis (n ¼ 45), (B) number of flowering C. solstitialis (n ¼ 39), (C) biomass (n ¼ 39), and (D) seedhead production (2002: n ¼ 36, 2003: n ¼ 37). Closed circles show 2002 data points, whereas open circles show 2003 data points. All C. solstitialis measurements are natural log(x 1 1) transformed. eliminate shading of plants in the plots by outside vegeta- ever, it can reduce C. solstitialis density and make C. sol- tion. As a result, C. solstitialis seed in the second year may stitialis more vulnerable to other factors. Even in plots have been largely from C. solstitialis plants flowering in the with the largest N. pulchra plants (basal diameter > 105 plots during the previous year. Thus, if N. pulchra size mm), we saw an average of five C. solstitialis seedheads reduced C. solstitialis seedhead production in the first year, produced in 2002 and 35 seedheads in 2003. Centaurea sol- then the seed availability in that plot could be lower the stitialis seedheads contained between 8 and 22 seeds each, following year, and seed availability would have a large so even C. solstitialis grown with large N. pulchra still pro- effect on seedling number. duced more than enough seed to replace the stand and Competition for light between N. pulchra and C. solstitia- increase in number. lis later in the season may have constrained C. solstitialis A limitation of our study is that all the N. pulchra plants survival, growth, and reproduction. Roche´ et al. (1994) in this study were of the same age and the variation in size found that C. solstitialis plants produced shorter roots, lower was created, at least in part, by whether or not they aboveground biomass, and fewer seedheads, and failed to received competition with C. solstitialis during the first 3 flower more frequently when grown in lower light environ- years after planting. As a result, our experiment may bet- ments under perennial grasses. Also, shade may slow C. sol- ter answer the question whether N. pulchra that estab- stitialis root growth (DiTomaso et al. 2003). Thus, lower lishes without competition can more strongly resist later survival and growth of C. solstitialis is expected if shading invasion than N. pulchra exposed to competition during by N. pulchra impairs root growth and reduces the ability of establishment. Callaway and Aschehoug (2000) found that C. solstitialis to reach deep soil moisture. Centaurea diffusa root exudates impair native grass It is important to emphasize that use of N. pulchra growth and resource uptake. If C. solstitialis has similar alone will not entirely stop C. solstitialis invasion; how- effects, then our smaller N. pulchra plants may have been

SEPTEMBER 2005 Restoration Ecology 527 Nassella pulchra Effect on Centaurea solstitialis even less resistant to C. solstitialis invasion than stands of Dukes, J. S. 2001. Biodiversity and invasibility in grassland microcosms. small N. pulchra growing in a site without C. solstitialis. Oecologia 126:563–568. We conclude that if C. solstitialis is controlled in the ini- Dukes, J. S. 2002. Species composition and diversity affect grassland sus- ceptibility and response to invasion. Ecological Applications tial years of a restoration project to enable establishment 12:602–617. of the native grasses, then these mature grasses may resist Dyer, A. R., and K. J. Rice. 1999. Effects of competition on resource later C. solstitialis invasion by reducing number, size, and availability and growth of a California bunchgrass. Ecology seedhead production of nearby C. solstitialis plants. How- 80:2697–2710. ever, C. solstitialis can produce seed even around the larg- Gerlach, J. D. Jr. 2004. The impacts of serial land-use changes and biolog- est N. pulchra plants, so competitive plantings alone will ical invasions on soil water resources in California, USA. Journal of not likely stop C. solstitialis invasion entirely. Arid Environments 57:365–379. Gerlach, J., A. Dyer, and K. Rice. 1998. Grassland and foothill woodland ecosystems of the Central Valley. Fremontia 26:39–43. Acknowledgments Hamilton, J. G. 1997. Changing perceptions of pre-European grasslands in California. Madron˜ o 44:311–333. Funding for this research was provided by the National Heady, H. F. 1988. Valley grassland. Pages 491–514 in M. G. Barbour, Science Foundation’s Graduate Research Fellowship pro- and J. Major, editors. Terrestrial vegetation of California. Special gram. In addition, we thank Jim Richards, Truman Young, Publication 9. California Native Plant Society, Sacramento, and two reviewers for their valuable comments on earlier California. versions of this manuscript. Holmes, T. H. and K. J. 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