Plant Soil DOI 10.1007/s11104-015-2498-1

REGULAR ARTICLE

Soil conditioning effects of native and exotic grassland perennials on the establishment of native and exotic plants Stefanie N. Vink & Nicholas R. Jordan & Sheri C. Huerd & Craig C. Shaeffer & Linda L. Kinkel & Laura Aldrich-Wolfe

Received: 7 October 2014 / Accepted: 27 April 2015 # Springer International Publishing Switzerland 2015

Abstract Background and Aims Semi-natural grasslands can combine biomass production with provision of multiple ecosystem services. Unfortunately, grassland establishment can be unpredictable and vulnerable to exotic plant invasion, potentially due to soil legacies from previous cultivation. Native plants could mitigate these legacies by changing soil attributes and facilitating other native grassland species. However, facilitation may be affected by nitrogen (N) fertilization, added during and after establishment. Methods We conditioned soils in a former maizesoybean field for 3 years using multiple native or exotic perennial species or a maize-soybean rotation. Half of each plot received N fertilizer. Native and exotic grassland perennials were grown on these conditioned soils in

Responsible Editor: Gera Hol . Electronic supplementary material The online version of this article (doi:10.1007/s11104-015-2498-1) contains supplementary material, which is available to authorized users. S. N. Vink (*) : N. R. Jordan : S. C. Huerd : C. C. Shaeffer Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN 55108, USA e-mail: [email protected] L. L. Kinkel Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, USA L. Aldrich-Wolfe Biology Department, Concordia College, Moorhead, MN 56562, USA

the greenhouse, with N added to half of the pots, and biomass was measured. Results Consistent facilitation of native species by other natives was not observed, nor did invasive species facilitate other invasives. Soil conditioning affected individual plant species’ biomass in several instances. Field N addition had little effect on plant biomass, while greenhouse N addition increased native more than exotic plant biomass, but did not alter the overall pattern of facilitation. Conclusions Native plants failed to facilitate native prairie establishment in this work, suggesting resistance to conditioning on former intensive, high-input agricultural soils. Keywords Soil conditioning . Diversified biofuel grassland . Facilitation . Invasion ecology . Native nurseplants . Nitrogen

Introduction In central North America, semi-natural grasslands, comprising diverse mixes of native perennial prairie grassland species, are exciting interest from a wide range of stakeholder groups as attractive options for sustainable production of biomass feedstocks for biofuels (Williams et al. 2013). However, poor native establishment, potentially as a consequence of soil legacies from previous land use, is limiting the wider uptake of these diversified grasslands.

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These grassland production systems have the potential for equal or higher biomass yield than maize (Nichols et al. 2014; Zhou et al. 2009), currently the dominant biofuel crop in the US (U.S. Department of Energy 2011). In addition, they can be integrated within highly multi-functional agroecosystems that combine biomass production with provision of other ecosystem services related to native biodiversity, such as habitat creation (Fletcher et al. 2011; Gardiner et al. 2010), control of weedy species (Török et al. 2012), and increases in carbon sequestration, water quality and resilience to variations in rainfall (Boody et al. 2005; Schulte et al. 2006; Tilman et al. 2006). Diversity and functional composition of native plants are important for diversified grasslands because it enables the maintenance of ecosystem services and functioning (Hector and Bagchi 2007; Isbell et al. 2011; Naeem et al. 1996; Zavaleta et al. 2010) whilst increasing the level and stability of productivity (Jarchow et al. 2012; Tilman et al. 2006). Establishment of diversified grassland production systems can be problematic, due in part to low seedling germination rates and survivorship of certain species (Hillhouse and Zedler 2011). An additional problem is that poor native plant establishment creates an opportunity for invasion by exotic weedy perennials (Allison 2011), further excluding native species and potentially resulting in biodiversity loss (Hejda et al. 2009; Wilcove et al. 1998) and altering ecosystem properties and functioning (D’Antonio and Vitousek 1992; Ehrenfeld 2003). One potential cause of poor establishment is the presence of persistent soil legacies from previous plant communities (Corbin and D’Antonio 2012; Ehrenfeld et al. 2005). Annual field crops and perennial weeds can produce strong and persistent microbial (Jordan et al. 2008; Kulmatiski and Beard 2008) or abiotic (Inderjit and van der Putten 2010) legacies in soils, and conversely, soil microbes can strongly affect the dynamics of plant communities and weed invasion (Inderjit and van der Putten 2010; Klironomos 2002; Suding et al. 2013). Therefore, microbial and abiotic legacies of annual crop cultivation may interfere with establishment of diversified biofuel grasslands if these legacies specifically inhibit germination, growth or reproduction of native perennial species while exotics are either less negatively affected or unaffected by these soil legacies. Cultivation of facilitative native species in the initial phase of conversion may remediate detrimental legacies of crop production. While the term ‘nurse-species’ is

generally applied to plant species that have a direct facilitative effect on other species by ameliorating poor conditions for establishment (Callaway and Lawrence 1997), it can also be used to describe indirect facilitative effects through changes in soil community composition (Jordan et al. 2008). Utilizing native nurse-plants to change soil attributes so as to specifically favor native grassland species in the initial stages of conversion could improve the overall establishment of diversified semi-natural grasslands (Eviner and Hawkes 2012; Jordan et al. 2008). High levels of soil nitrogen (N) due to soil type and prior cropping practices may interfere with or override facilitative effects of nurse-species. Residual N in soils transitioning from annual field crops to perennial grasslands can be high as a consequence of fertilization of previous crops. In prairie grasslands increased levels of N in soils can benefit invasive species more than natives (Rothrock and Squiers 2003; Vinton and Goergen 2006) and can also modify soil microbial community composition and function, e.g., by altering arbuscular mycorrhizal fungal (AMF) communities and relations between AMF and their plant hosts (Egerton-Warburton et al. 2001; 2007; Johnson et al. 2003), or by delaying nodulation and limiting nitrogen fixation in legumes (Chen and Phillips 1977; Hirsch 1996; Nutman 1956). Thus, N fertilization may interfere with conditioning by native nurse-species by altering the soil dynamics that create specific facilitative effects, or may override these effects during subsequent seedling establishment of native species, by stimulating exotic plant growth. Taken together, evidence suggests that soil legacies and N fertilization may strongly affect the establishment and growth of native and exotic perennials during establishment of diversified grasslands on soils previously used for annual crop production, but these effects, their relative impacts on native and exotic species, and their interactions are poorly known. Here we describe the results of a study evaluating the short-term legacy effects of potential native nurse-species, exotic perennial species and a long established maize-soybean cropping system on growth of three native and three exotic plant species. We additionally determined how nitrogen fertilization treatments may interact with these legacy effects. In our experiment we focus on so-called ‘heterospecific’ soil feedbacks (Perkins and Nowak 2013), whereby the soil legacy of one species affects the performance of a different species, in contrast to the

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more common conspecific feedback examined in the majority of plant-soil feedback experiments. We conducted our experiment on a soil that was previously subjected to high intensity cropping, which is likely to have reduced levels of beneficial soil organisms (Oehl et al. 2003) and increased resource availability (Matson et al. 1997). These conditions favor invasion by exotic plants (Kulmatiski et al. 2006) because these species tend to be less reliant on mutualists. Once exotic invasive plants are established, their populations are maintained through the creation of positive conspecific and heterospecific soil feedbacks (Callaway et al. 2004; Jordan et al. 2008; Klironomos 2002; Kulmatiski 2006; Reinhart and Callaway 2006). In contrast, conditioning by native plants generally leads to negative conspecific feedbacks, due to a build-up of hostspecific pathogens (Bever et al. 2012). However, positive heterospecific effects have been observed in a range of studies (Bever 2002; Suding et al. 2013), particularly when in mid- to late successional species are used for conditioning (Kardol et al. 2006), as was the case for most of the species in our study. These positive feedbacks can occur through increases in the diversity and abundance of beneficial soil organisms such as AM fungi during soil conditioning (Bever et al. 2012; Fitzsimons and Miller 2010; Jordan et al. 2012). We tested the following hypotheses: 1. Soil conditioning treatments will affect exotics and natives differently. Exotic conditioning treatments will create positive feedback effects on exotic species, with neutral or negative effects on native species (Jordan et al. 2008), while native conditioning treatments will have positive feedback effects on other native species. Additionally, maize-soybean conditioning treatments will benefit exotic plants but not natives. We expect community level effects (i.e., native, exotic and maize-soybean) but also heterogeneity of these effects from and on individual species. 2. Indirect (field) and direct (greenhouse) N fertilization will alter the effect of soil conditioning. Specifically, we expect field N fertilization to affect native response plants negatively, by disturbing the relationship between conditioning species and AMF (Egerton-Warburton et al. 2007; Johnson et al. 2003) and thereby reducing the beneficial effects of soil conditioning by native plants on native plants. N fertilization of soils in the greenhouse

phase of our study is expected to promote growth of both native and exotic plants. However, we expect that exotic plants will be able to utilize this better, potentially increasing the positive feedback of exotics on exotic growth even further.

Material and methods This experiment is part of a larger study examining the effect of soil conditioning by a range of native prairie, crop and exotic perennial species on soil communities in the establishment of semi-natural prairie grasslands. Our experiment consisted of two separate phases: an initial soil conditioning field treatment (field conditioning) in a field with a long-term history of rotational maizesoybean cropping, and a subsequent greenhouse study to evaluate the legacy effects from each field conditioning treatment on the biomass of a variety of native and exotic plants (greenhouse response). Field experiment: soil conditioning treatments Soil conditioning treatments were initiated on 24 June 2010 at the University of Minnesota Outreach and Research Experiment Station (UMORE Park; 44°42′41″ N, 93°6′51″ W) and maintained until November 2012. The study site has a field history of maize (Zea mays L.) - soybean (Glycine max (L.) Merr.) rotations (1 year maize followed by 1 year soybean) on a Waukegan silt loam soil (well-drained, mesic Typic Hapludoll). The experiment was set up in a randomized block design, with 4 replicate blocks and 6 treatment plots. The plots of 3×15 m (crop plots were 3.5×15 m) were sown with one of six conditioning treatments: two native perennial prairie species, one mixture of native prairie species, two exotic perennial species, and a maize-soybean rotation. Soil from each of these treatments was used in two separate greenhouse experiments to assess the effect of conditioning on the subsequent growth of native and exotic response plants. The three native conditioning treatments were big bluestem (Andropogon gerardii Vitman.; hereafter species will be referred to by genus after their first mention), Canada wild rye (Elymus canadensis L.) or a polyculture mix consisting of eight native species (see Table S1 in the Supplementary Material for a full list of the species and seed sources used in the conditioning

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treatments). The remaining conditioning treatments were planted with one of two exotic invasive species, either smooth brome (Bromus inermis Leyss. ssp. inermis) or crested wheatgrass (Agropyron cristatum (L.) Gaertn.), both of which were originally introduced for forage production and can be highly invasive in prairie ecosystems (Ortega and Pearson 2005), or with a maize-soybean rotation (maize in 2010 and 2012 and soybean in 2011). Prior to seeding of the conditioning species, the soil was cultivated, harrowed and rolled; pure live seed (Supplementary Material) was applied at a rate of 10 g m−2 and raked into the soil. Legume seeds were treated with appropriate rhizobium inoculum supplied with the seed. Maize and soybean were seeded using a garden seeder (1001-B, Earthway Products Inc., Bristol, Indiana) in rows that were 76 cm apart. Due to poor establishment, Bromus was reseeded with new seed at 5 g m−2 in July 2010; in 2012, maize was subject to severe seedling mortality and plots were reseeded once in June where necessary. All plots, except the maize plots, were mown once each month in July and August 2010 using a sickle mower (Jari Sickle Mower, Jari Mowers, Mankato, Minnesota) to reduce the establishment of weeds from the seed bank. In 2011 and 2012 all plots were hand weeded as necessary. Plots were irrigated twice in 2010 due to drought conditions. The maizesoybean plots were re-established yearly in May using a hand rototiller (Horse tiller, Troy-Bilt, Valley City, Ohio) and the same seeding method as in 2010. In early June 2011, one half of each treatment plot was randomly assigned to receive 6.7 g m−2 NH4NO3 in a single dose (Field N+) while the other half received no additional N (Field N−). This treatment was repeated at the end of May 2012 for the same half of each plot as in 2011. Maize Field N+ plots received double the amount of N (13.4 g m−2) each year due to the known high N use of this crop. At the start of June 2011, K2O fertilizer was applied at a rate of 7.8 g m−2 on all plots as levels were found to be below recommended field levels for maize and native plantings (Kaiser et al. 2011). At the end of each growing season, maize-soybean plots were harvested by hand for grain. Maize and soybean residues were shredded and incorporated into the soil prior to planting the following year. On November 1 2012, after three conditioning growing seasons, approximately 75 L of soil were extracted from each of the 12 plots in each of the four blocks (48 plots in total). Specifically, a six meter long, 13 cm wide

and 13 cm deep trench of soil was extracted from the central axis of each 3×7.5 m plot. Soils from each trench were put into separate containers, covered to prevent drying and moved to the University of Minnesota, St. Paul. Containers were enclosed by a waterproof covering and remained outdoors at ambient conditions (predominantly below 0 °C), for 17 and 25 weeks until the start of greenhouse experiments 1 and 2, respectively. Soil abiotic analysis Samples for soil abiotic analysis were collected from each field plot at the end of September 2012, prior to soil collection for the greenhouse experiment. 15–20 cores (1.9 cm diameter×15 cm deep) were taken from within 5 cm of treatment plants, yielding approximately 250 g of soil from each conditioning treatment and replicate, and air-dried. Soil nitrate (NO3−-N), ammonium (NH4+N), phosphate (Bray P1), potassium (K), pH, water content and organic matter (OM) analysis was conducted at the UMN Research Analysis Laboratory (Frank et al. 1998; Henriksen and Selmer-Olsen 1970; Keeney and Nelson 1982; Warncke and Brown 1998; Watson and Brown 1998). Soil microbial carbon (MBC) and microbial N (MBN) content were assessed on 3 g of soil using the methods of Vance et al. (1987) and Brookes et al. (1985) respectively. C:N ratios were calculated from total carbon (TC) and total N (TN), analysis was performed by dry combustion GC analysis (ECS 4010, Costech analytical, Valencia, California, http://www. costechanalytical.com/products/ecs4010_principle. aspx) at the Ecosystems Analysis Lab, University of Nebraska following the manufacturer’s protocol. Greenhouse experiments: plant growth in conditioned soils Two similar greenhouse experiments were conducted (with minor differences in protocol and study species as noted below). Experiment 1 ran from March 12 to July 1 2013 and experiment 2, which was a component of a larger study, from May 29 to August 2 2013. Six days prior to the start of each experiment soils were brought into the greenhouse (approx. 21 °C) to warm up and sieved (0.5 cm mesh size) into clean containers, keeping soil from each field plot separate. Some soils were too wet to sieve initially; these were covered and dried on greenhouse benches until friable. 600 ml of soil was added to 60 (Experiment 1) or 24 (Experiment 2) D40 Deepots

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(6.4 cm diameter×25 cm deep, Stuewe & Sons, Tangent, Oregon) per soil conditioning treatment, yielding a total of 2880 (Experiment 1) or 1152 (Experiment 2) pots. Soils from each conditioning treatment were planted with one of six plant species. These included three native species Andropogon, switchgrass (Panicum virgatum L.) and Canada milkvetch (Astragalus canadensis L.) and three exotic species Bromus, bird’sfoot trefoil (Lotus corniculatus L.) and spotted knapweed (Centaurea stoebe ssp. micranthos (S.G. Gmel. ex Gugler) Hayek). In experiment 2, Agropyron was used instead of Centaurea as not enough seeds of the latter were available for a full planting. Seeds (10–25 per species) were scattered over the surface of each Deepot and covered with 50 mL of sterile vermiculite to prevent water splash and contamination. Species specific Rhizobium inoculum supplied with the seed was added to Astragalus and Lotus seeds at sowing (Supplementary Material). Seedlings were thinned to two seedlings per pot 2 weeks after planting and weeding continued throughout the experiments to maintain initial plant densities. The Deepots were placed in a randomized complete block design in the greenhouse: six response species monocultures by two N treatments by 48 conditioned soils (i.e., six conditioning treatments × two field N treatments × four field blocks) in each of five (Experiment 1) or two blocks (Experiment 2). The greenhouse N treatment was applied at week 9 (experiment 1) or 4 (experiment 2) with a single application of inorganic NH4NO3 at a rate of 6.7 g m−2 in solution to a random selection of half of the pots (Greenhouse N+ or Greenhouse N−) of each treatment in each block. Plants were grown in natural light in the greenhouse, supplemented with 400-W high-pressure sodium lamps when light intensity was less than 400 W m−2 within a 16 h day. Temperatures were set at 20 °C night and 22 °C day, and all pots were watered daily. After 13 to 16 (experiment 1) or nine (experiment 2) weeks plants were harvested per greenhouse block. Entire plants were separated from soil and dried at 60 °C for 3 days. Shoots were separated from roots and shoots were weighed to obtain aboveground biomass. If more than two plants were recorded for a pot, the data for the entire pot was removed from the dataset; this occurred in <6 % of pots. Statistical analysis Since the two experiments differed in response species and duration, we analyzed the data from the two

experiments separately. Linear mixed models were used to assess the effect of the treatments on shoot biomass using the lmer function of the lmerTest package (Kuznetsova et al. 2014) in R v. 3.0.2 (R Core Team 2013). Prior to analysis, data were log transformed to meet assumptions of normality. We were interested in contrasting effects of conditioning treatments (native, exotic and maize-soybean) on native and exotic plant growth. Additionally we sought to assess the degree of heterogeneity among individual soil conditioning and response species; therefore we conducted two separate analyses for each experiment. The first analysis evaluated the effects of conditioning on plant biomass at a group level by placing species into either native, exotic or maize-soybean conditioning groups and either native or exotic groups for greenhouse response (see Supplementary Material for species and group information). In the second analysis we assessed variation in biomass of the six individual greenhouse plants in response to soil conditioning by the six individual conditioning treatments. Each model initially included all four treatment factors: Field N, Conditioning Group or Species, Greenhouse N, and Greenhouse Response Group or Species as fixed effects in a full factorial design. In addition, due to their low sample size and because they were not randomly selected, Field Block and Greenhouse Block were also included (additively) as fixed effects, while Field Plot was included as a random effect since it had a larger sample size (>4) and it was randomly selected within each block (Zuur et al. 2007). In the models where plant group data was used, Greenhouse Response and Conditioning Species were also included (additively) as random effects, to take the inherent differences in conditioning and growth between different species into account. Each full model was subsequently simplified by automatic backward elimination using the step function in lmerTest package to remove any nonsignificant effects. ANOVA, type 3 with p-values calculated based on Satterthwaite’s approximation, was subsequently carried out on each simplified model. To assess the effect of conditioning on abiotic factors, linear mixed models (and subsequent ANOVA, as above) were used incorporating Field N and Conditioning Group or Species interactively as fixed effects. Additionally, Field Block was included additively as a fixed effect and Field Plot as a random effect. When Conditioning Group was used in the model Conditioning Species was included as a random effect.

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To ascertain whether soil abiotic factors could explain variation in plant biomass we ran separate multiple regression models (function lm in R) for each Greenhouse Response Species, initially incorporating all abiotic factors. Each model was simplified by backward elimination using the stepAIC function from the MASS package (Venables and Ripley 2002). To assess how much of the variation in our data could be explained by abiotic factors, we calculated the proportion of variance for each simplified model using the function calc.relimp from the relaimpo package (Grömping 2006).

Results Soil conditioning effects on native and exotic plants We found no evidence that soil conditioning by native or exotic species differentially affected plant growth of native or exotic species overall (Fig. 1; non-significant Conditioning Group × Greenhouse Response Group interaction in Table 1). Thus, we found no evidence that native conditioning specifically benefited natives, nor that exotic conditioning specifically benefited exotics. Moreover, neither native nor exotic soil conditioning affected plant biomass of natives and exotics differently than soil conditioning by the maize-soybean rotation. N fertilization during the soil conditioning phase differentially affected both conditioning and response factors (significant Conditioning Group × Field N) and significant Greenhouse Response Group × Field N Fig. 1 Response of native and exotic greenhouse response plants to native, exotic and maizesoybean conditioning in Experiment 1 (Conditioning group × Greenhouse response group, n.s.). Untransformed shoot biomass, averaged across nitrogen treatments and species per group, and standard errors are shown. Native conditioning group: Andropogon, Elymus and native plant mixture; exotic conditioning group: Agropyron and Bromus. Native greenhouse response group: Andropogon, Astragalus and Panicum; exotic greenhouse response group: Bromus, Centaurea and Lotus

interactions respectively in Table 1), but the difference in biomass was small (Fig. S1 and S2 in the Supplementary Material) compared to that of greenhouse N addition. Moreover, field N fertilization did not alter the overall effect of native, exotic or maizesoybean conditioning on native or exotic plant biomass (Conditioning Group × Greenhouse Response Group × Field N interaction not significant and dropped during backward selection of model). Residual soil N levels were low after the 3 years of conditioning (Table 2); we measured no differences in NH4+-N for any of the treatments, and small differences in soil NO3−-N between N fertilized and unfertilized treatments in the maize-soybean and native conditioned soil and no change for exotic soils. Therefore field N addition was unlikely to have a large direct impact on plant growth in the greenhouse (i.e., an effect mediated by soil residual N levels). While greenhouse N fertilization had a large impact on biomass of both natives and exotics, native biomass increased relatively more than that of exotics (significant Greenhouse Response Group × Greenhouse N interaction in Table 1). We had hypothesized that N fertilization in the feedback phase might increase the positive feedback effect of exotic conditioning on exotic growth, but we did not find that such feedback effects occurred. We observed a significant interaction between conditioning groups, greenhouse response groups, and greenhouse N (Fig. 2; significant Conditioning Group × Greenhouse Response Group × Greenhouse N interaction in Table 1), but these N additions did not

Plant Soil Table 1 Results of ANOVA for comparisons between conditioning, greenhouse response, field N and greenhouse N additions in experiments 1 and 2. F values and corresponding P values and degrees of freedom (numerator, approximate denominator) of conditioning and greenhouse response species

(top) and groups (bottom) and field and greenhouse N fertilization are shown. Only significant interactions are shown for species level responses. For group level responses, only main effects and interactions involving conditioning or greenhouse response groups are shown

Experiment 1 d.f.

Experiment 2 F

P

d.f.

F

P

Conditioning species (CS)

5,18

8.4

<0.001

5,18

13.7

<0.001

Greenhouse response species (GS)

5,2396

428.8

<0.001

5800

275.2

<0.001

Field N fertilization (FN)

1,2398

16.4

<0.001

1797

21.9

<0.001

Greenhouse N fertilization (GN)

1,2397

1830.9

<0.001

1794

118.3

<0.001

CS × GS

25,2396

1.6

0.037

25,800

1.6

0.027

CS × FN

5,2398

3.0

0.010

GS × FN

5,2397

3.0

0.011

GS × GN

5,2396

34.8

<0.001

5794

2.3

0.042

FN × GN

1,2396

22.3

<0.001

1794

6.3

0.012

CS × GS × FN

25,2397

2.4

<0.001

CS × GS × GN

25,2396

1.7

0.014

n.a.

Conditioning group (CG)

2,3

1.5

n.s.

n.a.

Greenhouse response group (GG)

1,4

0.3

n.s.

CG × GG

2,2481

1.3

n.s.

CG × FN

2,2482

3.2

0.040

n.a.

CG × GN

2,2481

2.3.

n.s.

n.a.

GG × FN

1,2481

4.5

0.034

GG × GN

1,2481

17.8

<0.001

CG × GG × GN

2,2481

3.2

0.042

n.a. n.a.

n.a.

1,4

2.0

n.s. n.a.

n.a. 1823

4.2

0.042 n.a.

n.s. not significant, n.a. backward eliminated and not included in the final model

substantially alter the relative performance of native and exotic plants within any soil treatment, i.e., native plants remained larger than exotic plants irrespective of soil conditioning or greenhouse N addition. Therefore, we found that soil conditioning effects were essentially unaffected by greenhouse N additions, despite the large biomass responses that were observed in response to these N additions. Soil conditioning and response of individual species Although the growth responses of native and exotic groups did not differ across native, exotic and maizesoybean group conditioning, we did observe heterogeneity in growth responses among the individual plant species across the individual soil conditioning treatments (Fig. 3; Conditioning Species × Greenhouse

Response Species interaction in Table 1). Most conditioning treatments were broadly similar in their effects on plant growth, but Andropogon, Elymus and Agropyron conditioning produced distinctive effects. In both experiments, Andropogon-conditioned soils were consistently associated with relatively low plant biomass in most species; mean response species biomass was lower on Andropogon-conditioned soil than on any of the other soils. Conversely, Agropyron-conditioned soils were associated with relatively high plant biomass in most species in experiment 1, while in experiment 2 soils conditioned by Elymus led to higher biomass for most response plants. However, the effects of Agropyron and Elymus conditioning were not as consistent as that of Andropogon. Contrary to our expectations, maize-soybean soil conditioning did not have a distinctive effect on plant growth.

Plant Soil n=4 or 12 for species or group level respectively. P (mean 17.6 μg/ g±0.7 SE), NH4+-N (mean 3.5 μg/g±0.1 SE), OM (mean 4.5 %± 0 SE) and C:N ratios (mean 11.2±0 SE) were not significantly different in any of the treatments (n=48)

Table 2 Abiotic soil values (top) and ANOVA significance levels (bottom) per conditioning treatment prior to the greenhouse experiment from field samples taken at the end year 3 of soil conditioning. Means and standard errors of the mean are shown, NO3−-N (μg/g)

K (μg/g)

Acidity (pH)

H2O (%)

MBC (μg/g)

MBN (μg/g)

Conditioning Species/ Group

N fertilization

Andropogon

−

0.4 (0)

125.5 (1.7)

6.5 (0.1)

18.9 (0.4)

56.2 (2.3)

12.3 (1)

+

0.6 (0.1)

122 (5.6)

6.4 (0.1)

18.8 (0.3)

44.3 (4.1)

12.4 (1.9)

Elymus Native mix Agropyron Bromus Zea Native mean

−

0.8 (0.1)

118 (5.4)

6.6 (0.1)

20.2 (0.2)

32.6 (3.5)

12.9 (0.8)

+

1.2 (0.1)

119.8 (4)

6.6 (0.1)

19.1 (0.6)

39 (6.7)

16.9 (3.3)

−

0.6 (0.1)

134 (3.6)

6.5 (0.1)

17.7 (0.6)

56.6 (5)

14.9 (2)

+

0.6 (0.1)

136.8 (6.2)

6.5 (0.1)

14.9 (0.6)

65.2 (6.4)

13.5 (0.7)

−

0.9 (0.1)

138.3 (9)

6.7 (0.1)

19.5 (0.5)

46.5 (2.4)

19.7 (1)

+

0.8 (0.1)

124.3 (7.4)

6.6 (0)

17.4 (0.6)

52 (4.4)

17 (1.6)

−

0.7 (0.1)

130.8 (4.7)

6.8 (0.2)

16.4 (1.5)

43.4 (5)

14.3 (1.8)

+

0.7 (0.1)

131 (1.2)

6.7 (0.1)

15.2 (1)

50.4 (7.3)

12.8 (1)

−

0.9 (0.2)

105.3 (4.6)

6.7 (0.1)

16.5 (0.7)

40.1 (4.2)

10.7 (1.2)

+

1.5 (0.2)

100.5 (2.3)

6.8 (0.1)

14.3 (0.9)

43.2 (5.1)

14.1 (0.9)

−

0.6 (0.1)

125.8 (2.8)

6.5 (0)

18.9 (0.4)

48.5 (3.9)

13.4 (0.8)

+

0.8 (0.1)

126.2 (3.6)

6.5 (0.1)

17.6 (0.6)

49.5 (4.6)

14.3 (1.3)

−

0.8 (0.1)

134.5 (5.0)

6.7 (0.1)

17.9 (0.7)

45.0 (2.6)

17.0 (1.4)

+

0.8 (0.1)

127.6 (3.7)

6.7 (0.1)

16.3 (0.6)

51.2 (4.0)

14.9 (1.2)

Conditioning Species (CS)

**

***

***

***

**

**

Conditioning Group (CG)

n.s.

n.s.

n.s.

n.s.

n.s.

n.s.

Field N Fertilization (FN)

***

n.s.

n.s.

***

n.s.

n.s.

CS × FN

***

n.s.

n.s.

n.s.

n.s.

n.s.

CG × FN

***

n.s.

n.s.

n.s.

n.s.

n.s.

Exotic mean

***P<0.001, **P<0.01, *P<0.05 n.s. not significant

Fig. 2 The effect of greenhouse N fertilization on plant biomass for native and exotic greenhouse response plants grown in soils conditioned by natives, exotics or maize-soybean in Experiment 1 (Conditioning group × Greenhouse response group × Greenhouse N, F=3.2 , p<0.05). Untransformed shoot biomass, averaged across species per group, and standard errors are shown. Native conditioning group: Andropogon, Elymus and native plant mixture; exotic conditioning group: Agropyron and Bromus. Native greenhouse response group: Andropogon, Astragalus and Panicum; exotic greenhouse response group: Bromus, Centaurea and Lotus

Plant Soil

Fig. 3 Effect of conditioning species on greenhouse response plant biomass in Experiment 1 (Conditioning species × Greenhouse response species, F=1.6, p<0.05) and Experiment 2 (Conditioning species × Greenhouse response species, F=1.6, p<0.05). Untransformed mean shoot biomass, averaged across greenhouse

nitrogen treatments, and standard errors are shown. In both graphs, the first three species are native and the last three are exotics for both conditioning and greenhouse response treatments. ^ Note the substitution of Agropyron for Centaurea in Experiment 2

Field N fertilization resulted in only small increases in plant biomass in the greenhouse (mean increase 6 %), and while it did affect the interaction between response and conditioning species (Fig. S3 in the Supplementary Material; Conditioning Species × Greenhouse Response Species × Field N in Table 1), the effect was highly idiosyncratic and no clear pattern was observed. In contrast, greenhouse N addition altered the biomass of individual species markedly (Fig. 4). The strength of

this effect varied between greenhouse response and conditioning species (Conditioning Species × Greenhouse Response Species × Greenhouse N interaction in Table 1), with in particular Panicum profiting from fertilization at the greenhouse response phase (mean increase 157 %) while the two leguminous species Astragalus and Lotus responded relatively weakly to N fertilization. However, greenhouse N addition did not markedly alter the effect of conditioning on individual

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Fig. 4 The effect of greenhouse N addition on plant biomass per conditioning species and greenhouse response species in Experiment 1 (Conditioning species × Greenhouse response species × Greenhouse N, F=1.7, p<0.05). Untransformed mean shoot biomass, averaged across field N, and standard errors are shown. The

top three graphs show native and the bottom three show exotic greenhouse response species. In all graphs, the first three conditioning species (Andropogon, Elymus and native mix) are native, while the fourth and fifth (Agropyron and Bromus) are exotic conditioning species

species. In particular, it did not result in individual exotic species benefiting more than natives.

attributes among conditioning and fertilization treatments was large enough to have any observable effects on seedling growth. Most observed differences were among soils from different conditioning species, rather than between the groups of species or N fertilization levels. Soil NO3−-N differed between different conditioning species and fertilization generally increased soil NO3−-N, but levels were very low in all treatments at the end of growing season. Overall, K and P levels were comparable to that of medium to high fertility agricultural sites in the region (University of Minnesota Extension, http://www. extension.umn.edu/agriculture/nutrient-management). Soil P levels did not differ between any of the treatments and soil K levels were different only at the species level. Soil acidity levels ranged from 6.4 to 6.8 and were

Effects of conditioning on soil abiotic factors After 3 years of conditioning in the field, we observed statistically significant differences among conditioning species and N fertilization treatments in certain soil abiotic attributes (Table 2), but these effects were modest in magnitude. Moreover, multiple linear regression did not reveal any meaningful relationships between these abiotic attributes and the biomass of each greenhouse response species; the proportion of variation in plant biomass explained by each model ranged from 1.6 % for Lotus to 6.6 % for Andropogon. Therefore, we consider it unlikely that the difference in abiotic soil

Plant Soil

marginally lower in the soils conditioned by the three native species. Soil moisture content was affected by species identity and by fertilization. Microbial C and N measures differed between conditioning treatments; in particular Elymus had a lower MBC content, while MBN was highest in the Agropyron plots. No differences among treatments were observed for NH4+N, OM or soil C:N ratios.

Discussion We found no evidence of community level feedbacks for native or exotic grassland perennials. Thus, our findings do not support the hypothesis that native species can act as facilitative nurse-plants for the native species studied here, nor that soil conditioning by exotic species specifically facilitated growth of exotic plants. Moreover, the biomass of native and exotic plants grown on soils that had been conditioned by native and exotic species for 3 years was very similar to that of plants grown in soils with a continuous history of conditioning by a maize-soybean rotation. This is in contrast to a number of studies that show evidence of community level plant-soil feedbacks for both natives and exotics (Klironomos 2002; Perkins and Nowak 2013; Baxendale et al. 2014). In a meta- analysis of native-exotic pairwise feedback experiments, Suding et al. (2013) found consistent growth increases for natives grown on soil conditioned by natives while exotic responses were more idiosyncratic. Similarly, Jordan et al. (2011) found AMF mediated effects of soil conditioning that led to different growth patterns of native and exotic response plants. In theory, the difference in life forms of the species that comprised our native and exotic groups could have led to a lack of response to soil conditioning. However, we used predominantly grasses in both native and exotic groups, and these have been found to be affected more strongly by conditioning than forbs (Kulmatiski et al. 2008) and therefore, the selection of these species should have led to a stronger community level response to conditioning. While we did not find differences in conditioning effects of natives, exotics and annual crops at the community level, we did find differences among individual species in their effects on plant biomass. For example, conditioning by the native prairie grass Andropogon and the exotic grass Agropyron led to strongly different effects, with Andropogon conditioning resulting in

consistently lower biomass across all response plants, while Agropyron conditioning resulted in the opposite. Since Andropogon is highly reliant on AMF, we had expected it to generate positive con- and heterospecific feedbacks, rather than the observed broad negative effects. However, Andropogon has been found to be affected by an AMF-mediated conspecific negative feedback response (Casper and Castelli 2007; Castelli and Casper 2003). Its broad negative effects demonstrate that certain native plants may hinder establishment of semi-natural grasslands on soils with a history of annual agriculture, and the use of such species should probably be avoided. Interestingly, we observed only a small soilmediated facilitative effect in Elymus in experiment 2 and none in experiment 1. In the region where we conducted our study, Elymus is frequently used in prairie restorations because of its rapid and reliable establishment and growth and it is widely viewed by US grassland restoration practitioners as facilitating establishment of native species. Although it is only weakly reliant on AM fungi (Wilson and Hartnett 1998), it has been postulated to have the ability to increase mycorrhizal inoculum potential (Noyd et al. 1995) thus potentially facilitating establishment of highly AMFdependent native grassland species. If indeed Elymus would be tolerant of depauperate AMF soil communities while altering those communities to facilitate other natives, the species would exemplify an ideal nursespecies, as envisioned by Eviner and Hawkes (2012). However, in our study, we found little evidence that Elymus conditioning provided consistent or strong facilitative effects on plant growth for any species. We also found little evidence that N fertilization during the soil conditioning phase differentially affected soil conditioning effects of native and exotic species. Growers could be motivated to supply N in early stages of seminatural grassland establishment to increase biomass production. We expected that additional N would reduce facilitative effects of native species, because high levels of N can disrupt associations with mutualistic soil organisms, including AMF (Corkidi et al. 2002; EgertonWarburton et al. 2001; Johnson et al. 2003) and Nfixing bacteria (Chen and Phillips 1977; Nutman 1956). Moreover, nitrogen supply, by stimulating greater belowground plant biomass accumulation, might additionally modify rhizosphere community composition and function. Possibly the long history of N fertilization associated with maize-soybean production might have reduced the abundance of soil organisms that are specifically

Plant Soil

mutualistic with native species, in which case the additional N fertilization treatments we imposed would have had no effect. The soil in our experimental site is a silt loam soil with high organic matter, and our results contrast with those of a similar study on a less fertile sandy loam without a history of high-input annual crop production where N inputs strongly affected soil conditioning effects of individual species (Manning et al. 2008). We also found no evidence that N addition during the greenhouse phase selectively promoted plant growth of the exotic species in this study. Since we observed no facilitative effects of native soil conditioning, we were therefore unable to assess the impact of N fertilization on native conditioning effects. However, among the native and exotic species that we examined, N fertilization in the greenhouse did not selectively promote growth of exotic species; rather, the opposite was observed. Plants of the native species Panicum showed the greatest response to N fertilization, but all species, apart from the two legumes, were very responsive to N addition. More broadly, while greenhouse N addition benefitted natives more than exotics, the overall pattern of plant growth associated with each field soil conditioning treatment did not change qualitatively, indicating that N fertilization did not substantially change the effect of the soil conditioning treatments and suggests that ongoing N fertilization once grasslands are established may affect plants less than anticipated. Of course, as is the case for N fertilization during the initial stages of grassland establishment, ongoing fertilization may affect plant communities by other mechanisms, such as changes in resource competition among associated plant species with increased biomass from fertilization. Our results are similar to the results of Lowe et al. (2002) who found that there was no clear differential response between native and exotic plants to N addition. Our study is among the first to assess interspecific variation in soil conditioning effects by perennial species in a soil with a long history of intensive, high-input annual crop production. We found only modest interspecific differentiation in these effects. Notably, we did not find that the maize-soybean treatment was different from any of the native and exotic conditioning treatments despite the fact that the former received higher levels of N fertilization and was tilled yearly. Distinctive and persistent soil biotic communities can develop in annual crop agroecosystems in response to high levels of nutrient inputs and disturbance, producing biotic and

abiotic soil legacies (Adl et al. 2006; Buckley and Schmidt 2001; Elgersma et al. 2011) that are difficult to overcome (Jiang et al. 2010; Morris 2012) and can be maintained long after cessation of management (Buckley and Schmidt 2003; Steenwerth 2003). Our results suggests that the 3 year soil conditioning period in our experiment was insufficient to overcome the legacies of cultivation and produce large changes to abiotic or biotic factors in these soils. The possibility of such persistent legacies is supported by an analysis of soils from our study after 3 year of conditioning, which found no differences in density of pathogen-suppressive Streptomyces for any of the conditioning treatments in our study site (Felice et al. 2015). Although the weak conditioning effects in our study could also be due to other factors, such as the short time frame or the growth of plants in a greenhouse setting, other studies have found strong effects of soil conditioning on plants in exactly these situations (see Kulmatiski et al. 2008 for an overview). However, we cannot rule out that conditioning may have led to changes in other plant characteristics, such as altering the interspecific competitiveness of native and exotic plants (Blank 2010; Casper and Castelli 2007; Hol et al. 2013; Marler et al. 1999; Perkins and Nowak 2012; Shannon et al. 2012; Smith and Reynolds 2012) which we did not measure, nor that the use of different species than we selected might have resulted in stronger conditioning effects or responsiveness. Our study indicates that establishment of seminatural grasslands on soils with long histories of intensive, high-input annual crop production may be affected only to a small degree by several years of soil conditioning, whether by native species established with the intent of providing nurse-plant effects, or by exotic species that may become established during the initial conversion from annual crop production. Our findings contrast with studies that have detected rapid and significant effects of soil conditioning. However, most of these studies have been conducted in non-agricultural ecosystems and it may be that soils from high input, intensive annual production systems are relatively slow to respond to soil occupancy by different species, potentially limiting the use of nurse-plants for diversified grassland establishment on former agricultural land. Acknowledgments We thank our field, lab and greenhouse assistants; M. Bezener at the UMN Statistical Consulting Service for statistical advice; J. Larson for agricultural advice; L. Felice for

Plant Soil significant contributions to our research and review of this manuscript and two anonymous referees for helpful suggestions on improving the manuscript. This work was supported by Agriculture and Food Research Initiative grant nr 2010-85320-20565 from the United States Department of Agriculture.

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