Plant Ecol (2009) 204:247–259 DOI 10.1007/s11258-009-9588-1

Native cover crops suppress exotic annuals and favor native perennials in a greenhouse competition experiment Laura G. Perry Æ Spencer A. Cronin Æ Mark W. Paschke

Received: 11 July 2008 / Accepted: 13 February 2009 / Published online: 28 February 2009 Ó Springer Science+Business Media B.V. 2009

Abstract In a greenhouse experiment, we examined the effectiveness of four native cover crops for controlling four exotic, invasive species and increasing success of four western North American grassland species. Planting the annual cover crops, annual ragweed (Ambrosia artemisiifolia) and common sunflower (Helianthus annuus), reduced the biomass of the exotic species cheatgrass (Bromus tectorum), Japanese brome (Bromus japonicus), Canada thistle (Cirsium arvense), and whitetop (Cardaria draba). The annual cover crops also reduced the desired species biomass in competition with the perennial exotics, but either increased or did not affect the desired species biomass in competition with the annual exotics. Planting the perennial cover crops, Canada goldenrod (Solidago canadensis) and littleleaf pussytoes (Antennaria microphylla), rarely inhibited exotic species, but did increase the desired species biomass. Field experiments are needed to test the cover crops under more ecologically relevant conditions, but our results suggested that the annual cover crops may be effective for controlling invasive annuals and for facilitating native perennials.

L. G. Perry
S. A. Cronin
M. W. Paschke (&) Department of Forest, Rangeland, and Watershed Stewardship, Colorado State University, Fort Collins, CO 80523, USA e-mail: [email protected] L. G. Perry e-mail: [email protected]

Keywords Activated carbon
Allelopathy
Invasion
Light competition

Introduction Affordable, long-term methods of weed control are lacking for many of the world’s most problematic exotic, invasive species. Herbicides or mechanical removal can provide a short-term control of invasive species, but are difficult and expensive to apply over large spatial scales, require reapplication for longterm control, and often do not promote establishment of desired vegetation (Sheley and Krueger-Mangold 2003). Planting a cover crop to compete with invasive species has been explored as a potential approach for reducing invasive species success and increasing desired species success in ecological restoration and agriculture (Shirley 1994; Landhausser et al. 1996; Morgan 1997; Perry and Galatowitsch 2003; Singh et al. 2003; Ledgard and Davis 2004; Blackshaw et al. 2006; Sheley et al. 2006). Unfortunately, cover crops often fail to improve the desired species success, in part because they do not act selectively. Cover crops that are strong enough competitors to control the invasive species also tend to strongly suppress the desired species, whereas cover crops that do not strongly suppress the desired species also tend not to suppress the invasive species (Lanini et al.

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1991; Hoffman et al. 1993; De Haan et al. 1994; Perry and Galatowitsch 2003; Ledgard and Davis 2004). For cover crops to act selectively, they must create conditions that the desired species can tolerate better than the invasive species. For example, cover crops that reduce resource availability might favor the desired species over the invasive species when the desired species have lower resource requirements than the invasive species (Perry and Galatowitsch 2006). Low resource availability often favors native species over exotic, invasive species (Daehler 2003). In particular, shade may inhibit the invasive species more than the desired species when species such as invasive annuals are adapted to disturbed environments with high light availability (Bazzaz 1996), more than the desired species. Thus, planting a fastgrowing cover crop that can establish rapidly and produce abundant shade might be expected to favor some desired species over invasive species (Perry and Galatowitsch 2006), especially in disturbed areas with elevated light availability. Allelopathic cover crops also might inhibit some exotic, invasive species more than native, desired species. Allelopathy (i.e., interspecific, chemical interference) is thought to be relatively ineffective in interactions between native species that frequently co-occur, because over time, the species should evolve resistance to effective allelochemicals (Fitter 2003), but allelopathy may be more intense in novel interactions between native and exotic species, because neither the natives nor the exotics have had time to evolve resistance to each other’s allelochemicals (Rabotnov 1982). While this logic is commonly used to explain invasions by exotic, allelopathic species (Callaway and Ridenour 2004), it also suggests that native, allelopathic cover crops may inhibit exotic, invasive species more than native, desired species. Laboratory studies suggest that several North American rangeland species may be allelopathic, including annual ragweed (Ambrosia artemisiifolia; annual Asteraceae) (Jackson and Willemsen 1976; Bruckner 1998; Bruckner et al. 2003; Shetty et al. 2007), common sunflower (Helianthus annuus; annual Asteraceae) (Wilson and Rice 1968; Irons and Burnside 1982; Leather 1983; Morris and Parrish 1992; Macias et al. 1998a, b; Beres and Kazinczi 2000; Maruthi and Sankaran 2001; Ohno et al. 2001;

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Azania et al. 2003; Gniazdowska et al. 2007; Macias et al. 2008), Canada goldenrod (Solidago canadensis; perennial Asteraceae) (Fisher et al. 1978; Larson and Schwarz 1980; Hanson and Dixon 1985; Tsao and Eto 1996; Butcko and Jensen 2002; Sun et al. 2006; Yang et al. 2007; Zhang et al. 2007), and littleleaf pussytoes (Antennaria microphylla; perennial Asteraceae) (Manners and Galitz 1986; Hogan and Manners 1990; Barkosky et al. 1999; Barkosky et al. 2000). In addition to being putatively allelopathic, annual ragweed and common sunflower are fast-growing annuals, with the potential for rapid shade production in disturbed habitats. Also, annual ragweed, common sunflower, and Canada goldenrod are invasive or naturalized in Eurasia (Weber 2001; Beres et al. 2002; Faure et al. 2002), suggesting that they may be effective competitors against Eurasian species, including those invasive in North America. Littleleaf pussytoes has not been introduced to Eurasia, but is resistant to invasion by the exotic leafy spurge (Euphorbia esula) in North America (Selleck 1972), suggesting that littleleaf pussytoes also may be an effective competitor against other Eurasian, invasive species. We used a greenhouse competition experiment to test the hypotheses that fast-growing and/or allelopathic, native species would (1) reduce exotic, invasive species growth and (2) increase native, desired species growth by freeing desired species from competition with exotic species. In addition, we used activated carbon soil amendments to test (3) whether interactions between the species involved allelopathy. Our broader objective was to identify cover crops with sufficient promise to warrant further examination in long-term field experiments.

Methods We examined the effects of four potential cover crops on interactions between four invasive, exotic species and four native, desired, western North American grassland species. Specifically, we examined the effectiveness of annual ragweed, common sunflower, Canada goldenrod, and littleleaf pussytoes as cover crops (1) to control the exotic species cheatgrass (Bromus tectorum; annual Poaceae), Japanese brome (Bromus japonicus; annual Poaceae), Canada thistle (Cirsium arvense; perennial Asteraceae), and whitetop

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(Cardaria draba; perennial Brassicaceae), and (2) to favor the native species hairy false goldenaster (Heterotheca villosa; perennial Asteraceae), green needlegrass (Nasella viridula; perennial Poaceae), western wheatgrass (Pascopyrum smithii; perennial Poaceae), and upright prairie coneflower (Ratibida columnifera; perennial Asteraceae), in competition with the exotic species. In addition, we used activated carbon, which adsorbs organic compounds in soil (Inderjit and Callaway 2003; Inderjit and Nilsen 2003; Lau et al. 2008), to test the hypothesis that allelochemicals were responsible for effects of the cover crops on the exotic and desired species. We used an additive design competition experiment (Goldberg and Scheiner 2001) to examine the effects of adding cover crops to mixtures of exotic and desired species. The four exotic species were grown in pairwise mixtures with the four desired species to observe effects of the exotic species on the desired species (four exotic species 9 four desired species = 16 exotic 9 desired species combinations). In addition, each exotic species 9 desired species pair was grown with each of the four potential cover crops to determine whether adding the cover crop improved the desired species success in competition with the exotic species (four exotic species 9 four desired species 9 four cover crop species = 64 exotic 9 desired 9 cover crop species combinations). Each of the exotic species also was grown with each cover crop, in the absence of desired species, to examine the effects of the cover crops on the exotic species specifically (four exotic species 9 four cover crops = 16 exotic species 9 cover crop species combinations). Finally, each of the 12 species was grown alone (12 monoculture treatments). All species combinations were grown with and without activated carbon, which adsorbs organic compounds in soil, to test for the role of allelochemicals in the plant interactions. Each of the 216 treatment combinations (two activated carbon treatments 9 [16 ? 64 ? 16 ? 12] species combinations) was replicated ten times. The experiment was arranged in a completely randomized design in a 21–28°C day, 13–21°C night greenhouse lit with high pressure sodium lights for 16-h days, in addition to natural light. Plants were grown in 3.8-cm diameter 9 21-cm deep Ray Leach Cone-tainersTM (Stuewe & Sons, Corvallis, OR, USA) filled with washed quartz sand. We used relatively small growing containers to ensure that

249

competition among the cover crops, exotic species, and desired species would be intense. In half of the tubes, the sand was mixed with 20 mg of activated carbon per 1000 cc of sand in a cement mixer, following Ridenour and Callaway (2001). The sand surface in each tube was covered with 0.5 cm of perlite to retain moisture. Seeds of most study species were germinated in water and grown in fertilized sand for 30 to 38 days before transplanting. False hairy goldenaster, which established more slowly, was grown in sand for 40 to 50 days before transplanting. In January and February 2006, seedlings were transplanted into the cones to create the species treatments, with one seedling per species in each cone. Seedlings were transplanted into the center of the pot for treatments with one individual (i.e., monocultures), into the center of each half of the pot for treatments with two individuals (i.e., exotic 9 desired species mixtures and exotic 9 cover crop species mixtures), and into the center of each third of the pot for treatments with three individuals (i.e., exotic 9 desired 9 cover crop species mixtures). Seedlings were similar in size when transplanted, except that graminoids tended to be taller than forbs. Although cover crops are often seeded prior to desired species in agricultural settings (e.g., Hoffman et al. 1993), cover crops and desired species are often seeded simultaneously in restoration settings (e.g., Ledgard and Davis 2004; Sheley et al. 2006). Therefore, we transplanted all species into each treatment simultaneously. Treatments without cover crops were planted first, 12 to 28 days before treatments with cover crops. The cones were watered as needed to maintain moist soil conditions throughout the experiment. Once transplanting was complete, the cones were fertilized three times weekly with a triple concentrated solution of Peter’s Excel (39-18-39, N–P-K) and once weekly with a 7-day concentration of Peter’s Professional Soluble Trace Element Mix (STEM) (The Scotts Company, Marysville, OH, USA) using a liquid proportioner system (Dosatron, Clearwater, FL, USA) with a 1:100 ratio of fertilizer solution to water. Fertilization rates were based on manufacturer’s recommendations for ‘‘constant feed’’ systems. Plants were lightly rinsed with tap water after fertilizing. Six months after transplanting, aboveground biomass in the cones was harvested, separated among

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individuals, dried at 60°C to constant mass, and weighed. Plant mortality also was recorded. Belowground biomass was too entangled in the species mixtures to separate individuals and therefore was not harvested. Cones were harvested in the order that they were planted so that they were each maintained for 6 months after transplanting. Statistical analyses were conducted using PROC GLM in SAS version 9.1. Direct effects of activated carbon on aboveground biomass of the 12 species in monoculture were examined using a two-way ANOVA with species and activated carbon as independent variables. Effects of each of the cover crops on exotic species aboveground biomass were examined using separate four-way, full-factorial ANOVAs for each cover crop, with exotic species (Japanese brome, cheatgrass, whitetop, Canada thistle), desired species (none, hairy false goldenaster, green needlegrass, western wheatgrass, upright prairie coneflower), presence of the cover crop (no, yes), and activated carbon (no, yes) as independent variables. Since we conducted separate analyses for each cover crop, we used a Bonferroni adjusted a of 0.0125 to maintain a 5% chance of falsely identifying an effect of any cover crop. Effects of each of the cover crops on desired species aboveground biomass were examined similarly, except that the ANOVAs did not include the ‘‘none’’ desired species treatment level. Because most analyses of exotic species and desired species biomass yielded significant cover crop 9 exotic species interactions, we also conducted separate, post-hoc ANOVAs for each cover crop in combination with each exotic species, with a Bonferroni adjusted a of 0.0031. In some cases, additional post-hoc ANOVAs were conducted to interpret a desired species 9 cover crop interaction within a particular cover crop–exotic species combination, using a Bonferroni adjusted a of 0.0010, 0.0008, or 0.0006 depending on the number of desired species (3–5) examined in the particular analysis. Exotic species biomass and desired species biomass were cube-root transformed and y0.2 transformed, respectively, to correct significant heteroscedasticity. Replicates in which one or more plants died during the course of the experiment were not included in the analyses. Since one or more plants died in all replicates for some species combinations, we were unable to examine the effects of annual ragweed or Canada goldenrod on hairy false goldenaster, the effects of annual ragweed on mixtures of Japanese

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brome and western wheatgrass, or the effects of littleleaf pussytoes on mixtures of cheatgrass and western wheatgrass, cheatgrass and upright prairie coneflower, cheatgrass alone, or Japanese brome and upright prairie coneflower.

Results Annual cover crop species Annual ragweed Annual ragweed tended to reduce exotic species biomass (Fig. 1a), but this effect was more consistent for the exotic annual graminoids than for the exotic perennial forbs, and depended on the presence of the desired species (exotic 9 desired 9 ragweed, Table 1). Annual ragweed reduced cheatgrass biomass across desired species treatments (post-hoc ANOVA, ragweed, F1,102 = 20.65, P \ 0.0001) and reduced Japanese brome biomass without the desired species and with green needlegrass, but not with upright prairie coneflower (post-hoc ANOVA, desired 9 ragweed, F2,73 = 10.58, P \ 0.0001). In contrast, annual ragweed reduced Canada thistle and whitetop biomass only in the absence of the desired species (post-hoc ANOVAs, desired 9 ragweed, F3,116 = 33.38, P \ 0.0001 and F3,126 = 9.59, P \ 0.0001, respectively). Annual ragweed rarely reduced exotic species survival, but did cause 100% Japanese brome mortality in mixtures with western wheatgrass and 20–60% Japanese brome mortality in mixtures with hairy false goldenaster and upright prairie coneflower (data not shown). Annual ragweed tended to increase desired species biomass in mixtures with the exotic annual graminoids and decrease desired species biomass in mixtures with the exotic perennial forbs (exotic 9 ragweed, Table 2) (Fig. 2a), but these effects also varied among the desired species (desired 9 ragweed, Table 2). In mixtures with cheatgrass or Japanese brome, annual ragweed tended to increase desired species biomass, although this effect was significant only for cheatgrass (post-hoc ANOVA, ragweed, F1,68 = 41.11, P \ 0.0001). In contrast, in mixtures with Canada thistle or whitetop, annual ragweed tended to reduce desired species biomass, although this was significant only for western wheatgrass and for green needlegrass

Plant Ecol (2009) 204:247–259

4

251

Ragweed cover crop

Sunflower cover crop

(a)

(b)

3

Exotic species biomass (g)

**(i) 2

**(i)

**(i) **(i)

**

**

1

**(i)

**(i) 0 4

Goldenrod cover crop

Pussytoes cover crop

(c)

(d)

3

**(i) 2 1

**

**

br om C an e ad a th is tle wh ite to p

gr as s

es e

at

an

ch e

Ja p

ch

ea tg Ja ra pa ss ne se br om C an e ad a th is tle wh ite to p

0

Exotic species without cover crop

with cover crop

Fig. 1 Aboveground biomass of the exotic weeds, grown alone and in mixture with the desired species, with and without the cover crops: a Annual ragweed. b Common sunflower. c Canada goldenrod. d Littleleaf pussytoes. The means shown are averaged across desired species and activated carbon treatments. Significant cover crop effects are shown for each cover crop 9 exotic species combination (Bonferroni-adjusted a = 0.0031; ** P \ 0.0001, * P \ a, (i): significant cover crop 9 desired species interaction). For cheatgrass with the sunflower cover crop, there was also a significant cover crop 9 desired species 9 activated carbon interaction. Exotic species biomass was cube-root transformed for analysis. Backtransformed statistics are shown. Error bars are 1 SEM

in mixtures with whitetop (post-hoc ANOVAs, desired 9 ragweed, F2,83 = 12.44, P \ 0.0001 and F2,93 = 6.52, P = 0.0022, respectively). Annual ragweed rarely influenced desired species survival, but did cause nearly 100% mortality in hairy false goldenaster across exotic species mixtures (data not shown).

depended on the presence of the desired species (exotic 9 desired 9 sunflower, Table 1). With regard to the exotic annual graminoids, common sunflower reduced Japanese brome biomass across desired species treatments (post-hoc ANOVA, sunflower, F1,156 = 112.80, P \ 0.0001) and reduced cheatgrass biomass without the desired species, and with false hairy goldenaster, western wheatgrass, and upright prairie coneflower, but not with green needlegrass (post-hoc ANOVA, desired 9 sunflower, F1,144 = 17.90, P \ 0.0001). With regard to the exotic perennial forbs, common sunflower reduced Canada thistle biomass without the desired species and with false hairy goldenaster and western wheatgrass but not with green needlegrass or upright prairie coneflower (post-hoc ANOVA, desired 9 sunflower, F4,169 = 5.73, P = 0.0002). Further, common sunflower reduced whitetop biomass without the desired species and with false hairy goldenaster, but not with green needlegrass, western wheatgrass, or upright prairie coneflower (post-hoc ANOVA, desired 9 sunflower, F4,164 = 12.94, P \ 0.0001). Common sunflower, like annual ragweed, also tended to increase desired species biomass in mixtures with the exotic annual graminoids and decrease desired species biomass in mixtures with the exotic perennial forbs (Fig. 2b), but these effects also varied among the desired species (exotic 9 desired 9 sunflower, Table 2). In mixtures with cheatgrass or Japanese brome, common sunflower tended to increase desired species biomass, but this was significant only for upright prairie coneflower in mixture with Japanese brome (post-hoc ANOVA, desired 9 sunflower, F3,120 = 6.74, P = 0.0003). In contrast, in mixtures with Canada thistle and whitetop, common sunflower reduced desired species biomass (post-hoc ANOVAs, sunflower, F1,130 = 44.53, P \ 0.0001 and F1,130 = 44.53, P \ 0.0001, respectively).

Perennial cover crop species Canada goldenrod

Common sunflower Common sunflower, like annual ragweed, tended to reduce exotic species biomass (Fig. 1b), but again this effect was more consistent for the exotic annual graminoids than for the exotic perennial forbs, and

Canada goldenrod reduced biomass of only some exotic species (exotic 9 goldenrod, Table 1), and only in the presence of some desired species (desired 9 goldenrod, Table 1) (Fig. 1c). Canada goldenrod did not influence cheatgrass or Canada

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Table 1 ANOVA results for effects of each of the four potential cover crops on biomass of the four exotic species in mixtures with the desired, native species, and with and without activated carbon Annual ragweed e

P

Common sunflower

Canada goldenrod

Littleleaf pussytoes

df

df

F

df

F

df

F

F

P

P

P

Exotic (e)a

3;417

462.53

\0.001

3;633

760.91

\0.001

3;512

756.56

\0.001

3;434

682.41

\0.001

Desired (d)b

3;417

5.38

0.001

4;633

21.37

\0.001

4;512

43.39

\0.001

4;434

23.57

\0.001

e9d

8;417

3.66

\0.001

12;633

3.41

\0.001

9;512

9.78

\0.001

8;434

4.69

\0.001

Cover (c)c

1;417

113.21

\0.001

1;633

318.91

\0.001

1;512

11.17

\0.001

1;434

2.51

ns

e9c

3;417

4.03

0.007

3;633

8.48

\0.001

3;512

12.90

\0.001

3;434

4.21

0.006

d9c

3;417

35.87

\0.001

4;633

7.36

\0.001

4;512

8.48

\0.001

4;434

0.69

ns

e9d9c

8;417

13.92

\0.001

12;633

6.53

\0.001

9;512

2.32

ns

8;434

1.15

ns

Activ. carb. (ac)d

1;417

3.75

nsf

1;633

4.87

ns

1;512

5.17

ns

1;434

1.68

ns

e 9 ac

3;417

3.98

0.008

3;633

0.90

ns

3;512

1.42

ns

3;434

0.46

ns

d 9 ac

3;417

1.63

ns

4;633

3.17

ns

4;512

7.04

\0.001

4;434

3.42

0.009

e 9 d 9 ac c 9 ac

8;417 1;417

0.95 1.80

ns ns

12;633 1;633

1.47 2.85

ns ns

9;512 1;512

2.49 2.63

0.009 ns

8;434 1;434

1.00 0.67

ns ns

e 9 c 9 ac

3;417

4.87

0.002

3;633

1.24

ns

3;512

1.93

ns

3;434

0.28

ns

d 9 c 9 ac

3;417

2.54

ns

4;633

1.03

ns

4;512

0.93

ns

4;434

1.39

ns

e 9 d 9 c 9 ac

6;417

1.75

ns

12;633

1.78

ns

9;512

1.69

ns

8;434

0.79

ns

a

Exotic species = cheatgrass, Japanese brome, Canada thistle, whitetop

b

Desired species = none, hairy false goldenaster, green needlegrass, western wheatgrass, upright prairie coneflower. Because of mortality in all or most replicates for some treatment combinations, analyses for annual ragweed did not include hairy false goldenaster or combinations of Japanese brome and western wheatgrass, analyses for Canada goldenrod did not include hairy false goldenaster, and analyses for littleleaf pussytoes did not include cheatgrass grown without a desired species or combinations of cheatgrass with western wheatgrass, cheatgrass with upright prairie coneflower, and Japanese brome with upright prairie coneflower

c

Cover crop = present, absent

d

Activated carbon = present, absent

e

Degrees of freedom presented are: numerator; denominator

f

ns indicates P [ 0.0125 (Bonferonni corrected a)

thistle biomass. Canada goldenrod reduced Japanese brome biomass in mixtures with green needlegrass and upright prairie coneflower, but not without the desired species or in mixtures with western wheatgrass (post-hoc ANOVA, desired 9 goldenrod, F3,115 = 9.65, P \ 0.0001). Canada goldenrod reduced whitetop biomass across desired species treatments (post-hoc ANOVA, goldenrod, F1,128 = 16.25, P \ 0.0001). Canada goldenrod tended to increase desired species biomass (Fig. 2c), but the significance of this effect depended on the desired species 9 exotic species combination (desired 9 exotic 9 goldenrod, Table 2). In mixtures with cheatgrass, Canada goldenrod increased the biomass of upright prairie coneflower but not green needlegrass or western wheatgrass (post-hoc ANOVA, desired 9 goldenrod,

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F2,101 = 10.91, P \ 0.0001). In mixtures with Japanese brome, Canada goldenrod increased biomass of green needlegrass and upright prairie coneflower but not western wheatgrass (post-hoc ANOVA, desired 9 goldenrod, F2,79 = 21.82, P \ 0.0001). In mixtures with Canada thistle, Canada goldenrod increased the biomass of all desired species (post-hoc ANOVA, goldenrod, F1,96 = 9.29, P = 0.0030). Finally, in mixtures with whitetop, Canada goldenrod increased the biomass of western wheatgrass and upright prairie coneflower but not green needlegrass (post-hoc ANOVA, desired 9 goldenrod, F2,95 = 6.75, P = 0.0018). Canada goldenrod rarely influenced desired species survival, but did cause nearly 100% mortality for hairy false goldenaster across exotic species mixtures (data not shown).

Plant Ecol (2009) 204:247–259

253

Table 2 ANOVA results for effects of each of the four potential cover crops on biomass of the four desired species in mixtures with the exotic species, and with and without activated carbon Annual ragweed df

e

Common sunflower

Canada goldenrod

P

df

F

P

df

F

F

Littleleaf pussytoes P

df

F

P

Desired (d)a

2;289

58.79

\0.001

3;488

67.25

\0.001

2;371

40.94

\0.001

3;345

106.37

\0.001

Exotic (e)b

3;289

92.96

\0.001

3;488

258.94

\0.001

3;371

296.49

\0.001

3;345

129.84

\0.001

d9e

5;289

22.67

\0.001

9;488

4.69

\0.001

6;371

2.45

ns

6;345

2.98

0.008

Cover (c)c

1;289

0.41

nsf

1;488

6.90

0.009

1;371

145.32

\0.001

1;345

5.75

ns

d9c

2;289

8.01

\0.001

3;488

9.06

\0.001

2;371

23.54

\0.001

3;345

11.84

\0.001

e9c

3;289

3.95

0.009

3;488

18.79

\0.001

3;371

5.88

\0.001

3;345

1.08

ns

d9e9c

5;289

1.18

ns

9;488

2.53

0.008

6;371

4.65

\0.001

6;345

1.15

ns

Activ. carb. (ac)d

1;289

1.32

ns

1;488

15.07

\0.001

1;371

0.04

d 9 ac

2;289

4.80

0.009

3;488

14.57

\0.001

2;371

14.94

e 9 ac

3;289

1.03

ns

3;488

0.71

ns

3;371

d 9 e 9 ac c 9 ac

5;289 1;289

2.68 0.25

ns ns

9;488 1;488

1.05 3.64

ns ns

d 9 c 9 ac

2;289

0.72

ns

3;488

1.78

e 9 c 9 ac

3;289

1.94

ns

3;488

3.17

d 9 e 9 c 9 ac

3;289

1.91

ns

9;488

0.53

ns

1;345

0.58

\0.001

3;345

16.75

\0.001

ns

3.45

ns

3;345

3.91

0.009

6;371 1;371

1.15 5.30

ns ns

6;345 1;345

2.86 8.50

0.010 0.004

ns

2;371

2.15

ns

3;345

0.36

ns

ns

3;371

2.56

ns

3;345

0.79

ns

ns

6;371

2.18

ns

6;345

2.90

0.009

a

Desired species = hairy false goldenaster, green needlegrass, western wheatgrass, upright prairie coneflower. Because of mortality in all or most replicates for some treatment combinations, analyses for annual ragweed did not include hairy false goldenaster or combinations of Japanese brome and western wheatgrass, analyses for Canada goldenrod did not include hairy false goldenaster, and analyses for littleleaf pussytoes did not include cheatgrass grown without a desired species or combinations of cheatgrass with western wheatgrass, cheatgrass with upright prairie coneflower, and Japanese brome with upright prairie coneflower

b

Exotic species = cheatgrass, Japanese brome, Canada thistle, whitetop

c

Cover crop = present, absent

d

Activated carbon = present, absent

e

Degrees of freedom presented are: numerator; denominator

f

ns indicates P [ 0.0125

Littleleaf pussytoes Littleleaf pussytoes reduced the biomass of only one exotic species, whitetop (post-hoc ANOVA, pussytoes, F1,160 = 15.51, P = 0.0001) (exotic 9 pussytoes, Table 1) (Fig. 1d). Effects of littleleaf pussytoes on exotic species biomass did not depend on whether or which desired species were present. Cheatgrass and Japanese brome caused high littleleaf pussytoes mortality (82 and 65%, respectively) (data not shown). Littleleaf pussytoes, like Canada goldenrod, tended to increase desired species biomass, but the significance of this effect depended on the desired species (desired 9 pussytoes, Table 2) and not on the exotic species (Fig. 2d). Littleleaf pussytoes increased the biomass of green needlegrass and upright prairie coneflower (post-hoc ANOVAs, pussytoes, F1,116 =

11.84, P = 0.0008 and F1,59 = 13.64, P = 0.0005, respectively), but not hairy false goldenaster or western wheatgrass (Fig. 2d inset). Activated carbon Activated carbon did not influence the biomass of the 12 study species when grown individually in monocultures (ac, F1,349 = 0.49, P = 0.48; ac 9 species, F11,349 = 0.42, P = 0.95). Activated carbon did influence growth of some desired species grown in mixtures with exotic species (desired 9 ac, Table 2), but these effects did not depend on the identity of the exotic species or the presence of cover crops and therefore do not suggest allelopathic interactions. Activated carbon only rarely influenced cover crop effects on exotic or desired species. Specifically, activated carbon reduced

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2.5

Sunflower cover crop

Ragweed cover crop

(a)

(b)

2.0 **(i) ** **(i)

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coneflower

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needlegrass

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wheatgrass

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th a

br C

an

ad

se ne

is tle wh ite to p

e om

s gr as at pa Ja

ch e

ch ea Ja tg ra pa ss ne se br om C an e ad a th is tle wh ite to p

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Exotic species competitor without cover crop

with cover crop

Fig. 2 Aboveground biomass of desired species, grown in mixture with each of the exotic species, with and without the cover crops: a Annual ragweed. b Common sunflower. c Canada goldenrod. d Littleleaf pussytoes. The means shown are averaged across the desired species and activated carbon treatments (except in the inset in d). The inset in d shows aboveground biomass of the desired species grown with and without littleleaf pussytoes, averaged across the exotic species and activated carbon, and is provided because the desired species 9 littleleaf pussytoes interaction, and not the exotic species 9 littleleaf pussytoes interaction, was significant for desired species biomass (Table 2). Significant cover crop effects are shown for each cover crop 9 exotic species combination (Bonferroni-adjusted a = 0.0031; ** P \ 0.0001, * P \ a, (i): significant cover crop 9 desired species interaction). In the inset in d, significant effects of littleleaf pussytoes are shown for each desired species (Bonferroni-adjusted a = 0.0031; ** P \ 0.0001, * P \ a). Exotic species biomass was y0.2 transformed for analysis. Back-transformed statistics are shown. Error bars are 1 SEM

the negative effect of annual ragweed on Canada thistle biomass (exotic 9 ragweed 9 ac, Table 1) and reduced the negative effect of common sunflower on cheatgrass in mixtures with western wheatgrass (posthoc ANOVA, sunflower 9 ac, F1,33 = 14.93, P = 0.0005) (post-hoc ANOVA, desired 9 sunflower 9 ac, F4,144 = 8.55, P \ 0.0001). Activated carbon also increased the negative effect of common sunflower on cheatgrass in mixtures with green needlegrass

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(post-hoc ANOVA, sunflower 9 ac, F1,32 = 20.93, P \ 0.0001) (post-hoc ANOVA, desired 9 sunflower 9 ac, F4,144 = 8.55, P \ 0.0001), and reduced the positive effect of littleleaf pussytoes on green needlegrass in mixtures with Canada thistle (posthoc ANOVA, desired 9 pussytoes 9 ac, F3,140 = 5.65, P = 0.0012) (exotic 9 desired 9 pussytoes 9 ac, Table 2).

Discussion Effects of the cover crops on exotic and desired species Our hypotheses that native cover crops would reduce exotic species growth and increase desired species growth in competition with exotic species were partially supported. In particular, annual ragweed and common sunflower appeared to improve desired species biomass by reducing competition from some of the exotic species. Annual ragweed and common sunflower reduced cheatgrass and Japanese brome biomass both with and without the desired species (Fig. 1a, b). When both exotic and desired species were present, the reduction in cheatgrass and Japanese brome biomass corresponded to increased desired species biomass, although this increase was only sometimes significant (Fig. 2a, b). Among the effects of annual ragweed and common sunflower, the most consistent were that annual ragweed reduced cheatgrass biomass (Fig. 1a) and concurrently increased biomass of desired species (Fig. 2a). Annual ragweed and common sunflower also reduced Canada thistle and whitetop biomass (Fig. 1a, b), but mainly in the absence of desired species (data not shown). Perhaps consequently, annual ragweed and common sunflower tended to reduce, rather than increase, desired species biomass in mixtures with Canada thistle and whitetop (Fig. 2a, b). The Canada goldenrod and littleleaf pussytoes cover crops also reduced the biomass of some exotic species (Fig. 1c, d), and increased the biomass of some desired species in competition with the exotic species (Fig. 2c, d). However, the connection between the negative effects of Canada goldenrod and littleleaf pussytoes on the exotic species and their positive effects on the desired species was less clear. While Canada goldenrod and littleleaf pussytoes

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reduced the biomass of only some of the exotic species, they increased biomass of the desired species similarly across exotic species treatments. Thus, some other mechanism besides competition with the exotic species must explain at least some of the positive effects of Canada goldenrod and littleleaf pussytoes on the desired species. In a few cases, facilitation by Canada goldenrod and littleleaf pussytoes increased desired species biomass in mixtures with exotic species to competition-free levels (data not shown). Limited evidence for a role of allelopathy Our hypothesis that the cover crops would inhibit exotic species via allelopathy was not supported. In most cases, activated carbon did not influence the effects of the cover crops on the exotic species or the desired species, suggesting that organic compounds did not have a role in those interactions. In only two cases, the activated carbon treatment suggested that organic compounds may have been responsible for negative effects of cover crops on exotic species: effects of annual ragweed on Canada thistle and effects of common sunflower on cheatgrass in the presence of western wheatgrass. Conversely, the activated carbon treatment also suggested that organic compounds may have moderated the negative effect of common sunflower on cheatgrass in the presence of green needlegrass. Activated carbon did not influence biomass in the species monocultures, indicating that the effects of activated carbon on species interactions were not caused or masked by the direct effects of activated carbon on other environmental conditions besides allelochemicals (Lau et al. 2008). Thus, our results suggest that allelopathic effects of the cover crops were rare in our experiment and strongly depend on target species identity and community composition. Possible roles of resource competition Cover crop effects on resource availability, rather than allelopathy, may explain the negative effects of annual ragweed and common sunflower on the exotic species, and their positive effects on the desired species. Plants in our experiment probably competed primarily for light, since the experiment was wellwatered and well-fertilized. Annual plants tend to be faster-growing (Grime 1974; Muller and Garnier

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1990) and have greater specific leaf area than perennials (Garnier 1992), which may allow them to produce shade more quickly and compete more effectively for light. The annual cover crops, annual ragweed and common sunflower, grew substantially larger than the perennial cover crops, Canada goldenrod and littleleaf pussytoes (data not shown), and probably produced much greater shade. This may explain why they reduced exotic species growth more consistently than Canada goldenrod and littleleaf pussytoes in our light-limited experiment (Fig. 1). By reducing exotic species growth, annual ragweed and common sunflower may have reduced the competitive effects of the exotic species on the desired species. The cover crops also almost certainly competed directly with the desired species, but the negative effects of cover crop competition sometimes may have been offset by positive effects of reduced exotic species competition, leading to a net increase or lack of effect on desired species growth. This pattern appeared to occur in mixtures with the annual exotic species, cheatgrass and Japanese brome, but not with the perennial exotic species, Canada thistle and whitetop (Fig. 2a, b). Shade from annual ragweed and common sunflower may have favored the desired species over the annual exotic species because the annuals were less shade-tolerant than the perennial desired species (Perry and Galatowitsch 2006). Annual plants are adapted to environments with high light availability (Bazzaz 1996) and tend to be less shade tolerant than perennial plants (Sutherland 2004). By the same logic, shade from annual ragweed and common sunflower may not have favored the desired species over the perennial exotic species because the perennial exotics were similarly or more shade tolerant than the desired species. Instead, the desired species appeared to be effective competitors against Canada thistle and whitetop in the absence of cover crop shade; the desired species alone reduced Canada thistle and whitetop biomass (data not shown), and grew substantially larger in mixtures with Canada thistle or whitetop than in mixtures with cheatgrass or Japanese brome (Fig. 2). Potential mechanisms are less apparent to explain the positive effects of the Canada goldenrod and littleleaf pussytoes cover crops on desired species biomass (Fig. 2c, d), which did not coincide with the negative effects on exotic species biomass (Fig. 1c, d). Facilitation in plant interactions has been attributed to

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(1) moderation of temperature extremes, (2) moderation of water stress, (3) increased nutrient availability via nitrogen fixation, increased atmospheric nitrogen deposition, or nutrient ‘‘pumping’’ by deep roots, (4) oxygenation of water-logged soils, (5) modification of substrate characteristics including bulk density, stability, and coarse organic matter, (6) protection from herbivores, (7) attraction of pollinators, (8) spatial concentration of propagules, and (9) altered soil microbial community composition and behavior (Callaway 1995). These factors seem unlikely to have been important in our short-term, well-watered, well-fertilized, well-drained, temperature-controlled greenhouse experiment. Canada goldenrod and littleleaf pussytoes may have increased desired species biomass via another, as yet unrecognized mechanism of facilitation. Methodological limitations Several aspects of our methods limit our ability to draw firm conclusions about the effects of the cover crops on the desired and exotic species. First, although all treatments were grown for the same total amount of time, the treatments with cover crops present were planted and harvested later (by 12–28 days) than the corresponding treatments with cover crops absent. The treatments planted later may have been exposed to more light, both because they grew later in the spring and because the canopy may have become more open at the end of the experiment as neighboring cones were harvested. Consequently, greater desired species biomass when some cover crops were present may have been due to the later transplant date rather than the presence of the cover crop per se. However, the fact that the cover crop treatments affected the exotic species differently from the desired species suggests that any effects of transplant date would have to be species-specific to explain the results. Second, we could not measure belowground biomass, and therefore, could not distinguish between the effects of the cover crops on total biomass and effects on biomass allocation. Shade production and light competition may have stimulated allocation to aboveground biomass relative to belowground biomass in the species mixtures, thus increasing aboveground biomass even if total biomass was reduced (Shipley and Meziane 2002). If so, this might explain the greater aboveground biomass of the desired species in

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the presence of some cover crops. It would not, however, explain the lower aboveground biomass of the desired species in mixtures with other cover crops and exotic species, or the lower aboveground biomass of the exotic species in mixtures with the cover crops and the desired species. Finally, the experiment was conducted under relatively unrealistic conditions. For one, cheatgrass and Japanese brome, which are winter annuals, were planted simultaneously with the other species, which probably gave them a disadvantage in competition with the cover crops compared to if they had established in the preceding autumn as they do in nature (Sheley and Larson 1994). If so, annual ragweed and common sunflower may be less effective against cheatgrass and Japanese brome in the field than they were in our experiment. Also, the experiment was well-watered, well-fertilized, and relatively brief, which may have given an advantage to the annual cover crops and annual exotic species over the perennials. If soil resources had been more limited, or if the experiment had been conducted over multiple growing seasons, the perennial cover crops might have been more effective competitors, particularly against the annual exotic species. Further, the annual cover crops might have been less effective, particularly against the perennial exotic species. Also, we might have observed more evidence of allelopathy, since allelopathic plants may produce more phytotoxins and target species may be more sensitive to allelochemicals when resources are scarce (Graneli and Johansson 2003; Fistarol et al. 2005).

Conclusions Our results suggest that annual cover crops should be examined as an approach for controlling invasive annuals and facilitating restoration of western North American grasslands. Specifically, planting annual ragweed and common sunflower as cover crops in western grassland restorations may reduce cheatgrass, Japanese brome, Canada thistle, and whitetop invasion and may improve desired species growth in competition with cheatgrass and Japanese brome, although not in competition with Canada thistle and whitetop. Planting Canada goldenrod and littleleaf pussytoes as cover crops also may improve desired

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species success, but is unlikely to inhibit exotic species. Annual ragweed and common sunflower may have favored the desired species over cheatgrass and Japanese brome by reducing light availability, which may have inhibited growth of the less shade-tolerant, annual exotic species more than the more shadetolerant, perennial desired species. The mechanisms behind the positive effects of Canada goldenrod and littleleaf pussytoes on the desired species are less clear. Although the four cover crops we examined are thought to be allelopathic, we found only limited support for the role of allelopathy. The success of the annual cover crops for favoring the perennial desired species over the annual exotic species in our light-limited experiment suggests that cover crops may be most effective when they are functionally similar to the exotic species of interest and not to the desired species, perhaps especially with regard to their requirements for the limiting resources in the site. Further research is needed to test the long-term efficacy of these cover crops for controlling invasion and encouraging the desired native species under more ecologically-relevant conditions in the field. Acknowledgements The Wyoming Abandoned Coal Mine Land Research Program and USDOD-SERDP-SI1388 provided funding for this research. Two anonymous reviewers provided useful comments on earlier versions of the paper. E´lan Alford, Lauren Alleman, Ma´tya´s Csa´nyi, Natasha Davis, Joshua Eldridge, Lilly Hines, Timothy Hoelzle, Erica Ontl, and Julie Rieder assisted with transplanting, harvesting, and daily maintenance of the experiment.

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