Figures
Abstract
The presence of native grasses in communities can suppress native forbs through competition and indirectly benefit these forbs by suppressing the invasion of highly competitive exotic species. We conducted a greenhouse experiment to examine the potential of direct and indirect interactions to influence the aboveground biomass of four native forb species in the presence of the native perennial grass Schizachyrium scoparium and exotic invasive Lespedeza cuneata. We examined patterns of growth for the invasive legume, the perennial grass, and four native species in four scenarios: 1) native species grown with the grass, 2) native species grown with the legume, 3) native species grown with both the grass and legume together, and 4) native species grown alone. Schizachyrium scoparium significantly decreased biomass of all forb species (p<0.05). In contrast, L. cuneata alone only significantly affected biomass of Asclepias tuberosa; L. cuneata increased the biomass of A. tuberosa only when the grass was present. When S. scoparium and L. cuneata were grown together, L. cuneata had significantly lower biomass (p = 0.007) and S. scoparium had significantly greater biomass (p = 0.002) than when each grew alone. These reciprocal effects suggest a potential pathway by which L. cuneata could alter forb diversity in grassland communities In this scenario, L. cuneata facilitates grass growth and competition with other natives. Our results emphasize the importance of monitoring interactions between exotic invasive plant species and dominant native species in grassland communities to understand pathways of plant community change.
Citation: Fill JM, Pearson E, Knight TM, Crandall RM (2019) An invasive legume increases perennial grass biomass: An indirect pathway for plant community change. PLoS ONE 14(1): e0211295. https://doi.org/10.1371/journal.pone.0211295
Editor: Mai-He Li, Eidgenossische Forschungsanstalt fur Wald Schnee und Landschaft Institut fur Schnee- und Lawinenforschung, SWITZERLAND
Received: November 3, 2018; Accepted: January 10, 2019; Published: January 25, 2019
Copyright: © 2019 Fill et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: Funding for this research was provided by the U.S.A. National Science Foundation (DEB 1145274 to T.M.K) and the Washington University Biology Summer Undergraduate Research Fellowship (to E.P.). Support for high school youth in the Tyson Environmental Research Fellowships (TERF) program at Tyson Research Center was provided by a grant to Washington University in St. Louis from the National Science Foundation Advancing Informal STEM Education Program (DRL 0739874). The funders had no role in study design, data collection and analysis, decision to publish,or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Native perennial grasses are a keystone functional group of grassland and savanna communities. They influence fundamental ecosystem processes such as fire regimes and nutrient cycling [1–3] but they also have been shown to increase ecosystem resilience and community resistance to invasion [4–6]. As long-lived individuals that achieve high biomass, native perennial grasses may be particularly influential in competing with other plant species and in determining community invasion dynamics over the long term [7].
Several studies have experimentally demonstrated that native grasses are important in community resistance to invasion. For example, in Kansas tallgrass prairie, native perennial grass biomass had a negative effect on the abundance and richness of exotic plant species after fifteen years [8]. In Wyoming sagebrush-bluebunch wheatgrass communities, perennial grass removal nearly doubled the density and biomass of an invasive grass [9]. Evidence therefore suggests that established perennial grasses are strong competitors and should be considered a focus in perennial grassland restoration efforts [10–11], particularly where remnant grasses are still present [12].
Perennial grasses and invasive plants also affect co-occurring native species’ population dynamics. At intermediate densities, established perennial grasses can increase native plant diversity [5], such as by acting as nurse plants [13], while at high densities they tend to suppress native plant growth by limiting space and resource availability [14]. In a shortgrass steppe community, removal of a dominant native perennial grass resulted in increased densities of native species [15]. Similarly, exotic invasive plants are notorious for their suppression of native plant communities, and their presence has been shown to reduce native species growth, survival, and fecundity [16–17] and native diversity [18–22]. The presence of perennial grasses is expected to have positive effects on native species through their suppression of exotic invasive plants and negative effects through their own direct competition.
Invasive plants, however, can enhance native species’ survival and growth through mechanisms such as habitat modification or competitive release [23]. For example, the biomass of a native perennial grass in Argentina was greater when it was growing near the invasive legume Lotus tenuis (narrowleaf trefoil), presumably due to increased nitrogen levels [24]. Non-native species can serve as nurse plants for regenerating native seedlings by ameliorating otherwise stressful environmental conditions [25–26]. The potential for such facilitative interactions should not be overlooked [27]; both negative and positive interactions among native and invasive species can generate cascading effects on higher trophic levels [23]. We conducted a greenhouse experiment to test the effects of the presence of an exotic invasive legume and an established perennial grass on the aboveground biomass of native forbs, and to examine the reciprocal effects of the invasive legume and perennial grass on each other’s biomass. We examined patterns of growth for the invasive legume, the perennial grass, and four native species in four scenarios: 1) native species were grown with an established native perennial grass, 2) native species were grown with an invasive legume, 3) native species were grown with both the established grass and invasive legume together, and 4) native species were grown alone. We predicted that when grown alone with native species, the dominant perennial grass would increase biomass of co-occurring natives during their early recruitment. We further predicted that when grown alone with native species, the invasive legume should decrease native species’ growth. In pots with both the perennial grass and invasive legume, we predicted that the grass would decrease the growth of the invasive, indirectly resulting in greater growth of co-occurring natives.
Materials and methods
Study species
Lespedeza cuneata (sericea lespedeza) is a legume that invades open roadsides, prairies, and old fields in the Midwestern U.S.A. It was introduced from Asia in the early 1900s primarily to control roadside erosion and provide forage and has since widely invaded pasture and grasslands across the U.S.A. from Kansas to the east coast [28]. Lespedeza cuneata has been shown to directly suppress native forbs by shading them out early in grassland restoration [29]. Reclamation studies also suggest L. cuneata inhibits natural seedling establishment [30].
The native species chosen for this study are typically dominant in remnant prairies and thus often used for prairie restoration [31]. The four focal native species are Monarda fistulosa (wild bergamot), Coreopsis lanceolata (lanceleaf tickseed), Asclepias tuberosa (butterfly milkweed), and Chamaecrista fasiculata (partridge pea). These species relatively common, although given the high diversity in native prairies, one forb species is rarely dominant. All are herbaceous, perennial plants with high germination rates and short time to reproduction. The native grass is Schizachyrium scoparium (little bluestem), a perennial, upright bunchgrass which is ubiquitous in Midwestern U.S.A. prairies [32]. Schizachyrium scoparium was historically one of the dominant grasses of the midwestern tallgrass prairie region and grows in a variety of environments from moist to dry soils [32].
Greenhouse experiment
Seeds of L. cuneata were collected from reproducing plants during November 2013, stored at 3°C for five months, and scarified prior to planting. Native seeds and 2-year old S. scoparium rhizomes (the “established grass” in our experiment) were purchased from Prairie Moon Nursery (https://www.prairiemoon.com/) and Missouri Wildflowers Nursery (http://mowildflowers.net/), respectively. Both companies specialize in native plants for prairie restoration.
During May, rhizomes were planted and seeds were sowed in 5-gallon pots containing Metro-Mix 360. This soil, a combination of Canadian sphagnum peat moss, bark, vermiculite and dolomitic limestone, which has high water retention necessary for germination and seedling success. We set up between four and six replicates of four treatments, haphazardly arranged in five rows to account for spatial variability in greenhouse conditions. The treatments were: 1) grass rhizome and native species; 2) the invasive legume and native species; 3) grass rhizome, the invasive legume, and native species; 4) control (four focal native species). In treatments with S. scoparium, grass rhizomes were planted in the center of each pot. In treatments without S. scoparium, a segment of round PVC 5cm in diameter that extended from bottom of pot to soil surface was inserted in the center of pots to take up approximately the same space as the rhizomes, which have been shown to grow to deep depths in grassland systems [33]. Thus, competition for space should not differ significantly between pots. For each treatment, we planted 20 seeds of the forb species around the rhizome or PVC. In treatments with L. cuneata, we sowed four seeds of the legume and of each native species; in treatments without L. cuneata, we sowed five seeds each native species. The extra individual of each of the four native forbs in treatments without L. cuneata could potentially affect experimental outcomes (e.g., via increased intraspecific competition). However, it is much more likely that overall density (i.e., of all species) at a community level would affect outcomes. We controlled for the density of individuals in our experimental design which ultimately resulted from differences in survival between pots (see Statistical analyses).
Plants were grown in the greenhouse at Washington University in St. Louis for 14 weeks. Pots were watered daily with 1500 mL of water and ladybugs were released on plants, as needed, to control aphids. During this time, there were some reproducing individuals of three species: S. scoparium, A. tuberosa, and C. fasiculata. At 14 weeks, individual plants were harvested. Plants were clipped at soil level, dried in an oven for 48 hours or until completely dry at 40 °C, and weighed to quantify aboveground biomass for each individual (see S1 Appendix for sample sizes). It was not possible to quantify belowground biomass because the roots of all species were so entangled that we could not separate them and differentiate between species.
Statistical analyses
We ran all analyses in R 3.4.3, R Core Development Team, 2017. We conducted four two-way ANOVAs to examine the effects of L. cuneata and S. scoparium on the aboveground biomass of each of the four forb species. Our main factors were the independent and interactive effects of grass and invasive presence/absence. We included the number of forb individuals (excluding the grass) that survived in each pot as a random effect (plant density) to control for differences in the number of individuals per pot. We conducted two Welch’s two-sample t-tests to compare S. scoparium aboveground biomass between pots with and without L. cuneata, and to compare L. cuneata aboveground biomass between pots with and without S. scoparium.
Results
Native perennial grass and invasive legume presence had different effects on the growth of native grassland forbs. The perennial grass alone significantly decreased the aboveground biomass of all native forbs (Table 1; Fig 1). In contrast, the invasive legume alone only significantly affected biomass of A. tuberosa (Table 1). When the grass was absent, A. tuberosa biomass was higher when growing with the invasive (Fig 1). When the grass was present, A. tuberosa biomass was not affected by the presence or absence of the invasive (Fig 1). None of the forb species were significantly affected by plant density (Table 1).
Aboveground biomass (mean ± standard error) for four forb species grown in pots with and without the native grass, Schizachyrium scoparium, and the invasive legume, Lespedeza cuneata.
The native grass and invasive legume each had different effects on each other’s growth. When L. cuneata grew with S. scoparium, the aboveground biomass of L. cuneata was significantly lower relative to pots in which L. cuneata grew with only native species (Fig 2A). In contrast, S. scoparium had significantly greater biomass when grown with L cuneata plus the native species than when grown with only the native species (Fig 2B).
(a) Aboveground biomass of invasive Lespedeza cuneata when grown in pots with and without the native grass, Schizachyrium scoparium (P = 0.007) (b) Aboveground biomass of Schizachyrium scoparium when grown in pots with and without Lespedeza cuneata (P = 0.002). In all pots, four species of native, perennial forbs were present.
Discussion
When grown separately, the native perennial grass, but not the invasive legume, suppressed native species’ aboveground biomass. Native forbs grown with S. scoparium had lower biomass than those grown alone, but counter to our hypothesis, native forbs were generally not affected by the invasive legume. The exception to this result was Asclepias tuberosa, which had more biomass where L. cuneata was present and the grass was absent. Although light limitation is a mechanism by which both L. cuneata and perennial grasses can negatively affect co-occurring native species [29, 34], this type of competition was unlikely in our study. The four native forbs are relatively tall-statured species that quickly exceeded the height of S. scoparium. It is possible that belowground interactions have a greater effect on growth. Lespedeza cuneata is a nitrogen-fixer and increased nitrogen in pots with L. cuneata might have ameliorated any negative direct effects of competition between L. cuneata and natives, and even facilitated growth (e.g., A. tuberosa). Lespedeza cuneata is also known to alter soil bacterial and fungal community composition [35, 36] which may have differentially influenced forb growth.
Although the perennial grass did reduce the growth of L. cuneata as we hypothesized, it was surprising that L. cuneata significantly increased perennial grass aboveground biomass in our study. [36] also found that Sorghastrum nutans biomass was higher when grown with L. cuneata than with a conspecific. Conversely, [37] found that the native grass Panicum virgatum had reduced growth in soil conditioned by L. cuneata, which has been shown to disrupt the mychorrhizal fungal communities associated with P. virgatum [38]. These outcomes suggest that nutrient levels or microbial communities could also be mediating grass-legume interactions. Schizachyrium scoparium has shown an ability to take advantage of nutrient pulses [39] and may have therefore gained a competitive edge over the invasive due to increased nitrogen levels. Lespedeza cuneata might also have disrupted soil microbial communities in a manner favorable to the perennial grass.
Our results suggest a potential pathway by which L. cuneata could alter biodiversity in grassland communities. Given S. scoparium’s negative effect on forb aboveground biomass, we suggest that L. cuneata facilitates competition of S. scoparium with co-occurring natives (Fig 3). In this scenario (Fig 3), Lespedeza cuneata initially establishes in an area of low bunchgrass density. By increasing nitrogen levels or altering microbial communities, it increases grass growth, thereby enhancing the competitive advantage of the grass over native forbs. Despite experiencing suppression from the grass, if L. cuneata persists until high grass density limits grass growth [40] it could have a dominant effect on grassland communities.
Arrows and signs show interactions among an invasive legume (Lespedeza cuneata), perennial grass (Schizachyrium scoparium) and co-occurring native perennial forbs.
There are many mechanisms that could affect the ability of L. cuneata to eventually become dominant in the community besides the interactions that we investigated here. Initial interactions between the grass and legume could change over time. Although initial interactions might be dominated by the nitrogen supply to the grass, after the legume has increased in biomass and density it might compete the grass for other resources (e.g., water or sunlight; [41]). Lespedeza cuneata might also be developing feedbacks with soil microbial communities that would eventually favor its own growth [42] and generate other mechanisms for community change. Alternatively, ecological processes could limit L. cuneata invasion. Prolific seed production is an attribute that increases L. cuneata’s invasiveness [43–44]. Lespedeza cuneata adults are susceptible to herbivory and fire [45–46]; disturbances such as herbivory or grazing and fire could limit the species’ population growth via effects on seed production.
Our results emphasize the importance of considering interactions between exotic invasive plant species and dominant native grasses to understand pathways of native plant suppression. An invasive plant might appear to have no direct effect on biodiversity, but when interactions with the dominant native grasses are involved, the results become more complex. Studies of interactions among invasive and dominant native species should prevent unexpected outcomes in invasive species management and promote more appropriate and effective management strategies for biodiversity.
Acknowledgments
Mike Dyer, Darlene Branson and Jeanne Cablish helped water and care for plants in the greenhouse. Tom Collins, George Garner, Andrew Feltmann and Emily Wen helped collect data.
References
- 1. Wedin DA, Tilman D. Species effects on nitrogen cycling: a test with perennial grasses. Oecologia 1990;84: 433–441. pmid:28312957
- 2. Snyman HA, Ingram LJ, Kirkman KP. Themeda triandra: a keystone grass species. Afr J Range For Sci 2013;30: 99–125.
- 3. Fill JM, Moule B, Varner JM, Mousseau TA. Flammability of the keystone savanna bunchgrass Aristida stricta. Plant Ecol. 2016;217: 331–342.
- 4. Prober SM, Lunt ID. Restoration of Themeda australis swards suppresses soil nitrate and enhances ecological resistance to invasion by exotic annuals. Biol Inv. 2009;11: 171–181.
- 5. Sasaki T, Lauenroth WK. Dominant species, rather than diversity, regulates temporal stability of plant communities. Oecologia 2011;166: 761–768. pmid:21279386
- 6. Hoover DL, Knapp AK, Smith MD. Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 2014;95: 2646–2656.
- 7. D’Antonio CM, Flory SL. Long-term dynamics and impacts of plant invasions. J Ecol. 2017;105: 1459–1461.
- 8. Smith MD, Knapp AK. Exotic plant species in a C4-dominated grassland: invasibility, disturbance, and community structure. Oecologia 1999;120: 605–612. pmid:28308312
- 9. Sheley RL, James J. Resistance of native plant functional groups to invasion by medusahead (Taeniatherum caput-medusae). Inv Plant Sci Manage. 2010;3: 294–300.
- 10. Prober SM, Thiele KR. Restoring Australia’s temperate grasslands and grassy woodlands: integrating function and diversity. Ecol Manage Restor. 2005;6: 16–27.
- 11. Vaughn KJ, Young TP.Short-term priority over exotic annuals increases the initial density and longer-term cover of native perennial grasses. Ecol Appl 2015;25: 791–799. pmid:26214923
- 12. Davies KW, Sheley RL. Promoting native vegetation and diversity in exotic annual grass infestations. Restoration Ecol. 2011;19: 159–165.
- 13. Pugnaire FI, Haase P, Puigdefabregas J. Facilitation between higher plant species in a semiarid environment. Ecology 1996;77: 1420–1426.
- 14. McCain KNS, Baer SG, Blair JM, Wilson GWT. Dominant grasses suppress local diversity in restored tallgrass prairie. Restoration Ecol. 2010;18: 40–49.
- 15. Munson SM, Lauenroth WK. Plant population and community responses to removal of dominant species in the shortgrass steppe. J Veg Sci. 2009;20: 224–232.
- 16. Gould AM, Gorchov DL. Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals. Am Mid Nat. 2000;144: 36–50.
- 17. Lloydi A, Donath TW, Eckstein RL, Otte A. Non-native species litter reduces germination and growth of resident forbs and grasses: allelopathic, osmotic or mechanical effects? Biol Inv. 2015;17: 581–595.
- 18. Hejda M, Pysek P, Vojtech J. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol. 2009;97: 393–403.
- 19. Flory SL, Clay K. Non-native grass invasion alters native plant composition in experimental communities. Biol Inv. 2010;12: 1285–1294.
- 20. Davies KW. Plant community diversity and native plant abundance decline with increasing abundance of an exotic annual grass. Oecologia 2011;167: 481–491. pmid:21509533
- 21. Vila M, Espinar JL, Hejda M, Hulme PE, Jarosik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pysek P. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett. 2011;14: 702–708. pmid:21592274
- 22. Powell KI, Chase JM, Knight TM. Invasive plants have scale-dependent effects on diversity by altering species-area relationships. Science 2013;339: 316–318. pmid:23329045
- 23. Rodriguez LF. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Inv. 2006;8: 927–939.
- 24. Quinos PM, Insausti P, Soriano A. Facilitative effect of Lotus tenuis on Paspalum dilatatum in a lowland grassland of Argentina. Oecologia 1998;114: 427–431. pmid:28307787
- 25. Becerra PI, Montenegro G. The widely invasive tree Pinus radiata facilitates regeneration of native woody species in a semi-arid ecosystem. Appl Veg Sci. 2013;16: 173–183.
- 26. Svriz M, Damascos MA, Zimmermann H, Hensen I. The exotic shrub Rosa rubiginosa as a nurse plant: implications for the restoration of disturbed temperate forests in Patagonia, Argentina. For Ecol Manage. 2013;289: 234–242.
- 27. Crandall R, Knight TM. Positive frequency dependence undermines the success of restoration using historical disturbance regimes. Ecol Lett. 2015;18: 883–891. pmid:26147188
- 28.
Ohlenbusch PD, Bidwell T. Sericea lespedeza: history, characteristics and identification. Kansas State University Agricultural Experiment Station and Cooperative Extension Service MF-2408: 2001.
- 29. Brandon AL, Gibson DJ, Middleton BA. Mechanisms for dominance in an early successional old field by the invasive non-native Lespedeza cuneata (Dum. Cours.) G. Don. Biol Inv. 2004;6: 483–493.
- 30. Holl KD, Cairns J Jr. Vegetational community development on reclaimed coal surface mines in Virginia. Bull Torrey Bot Club 1994;121: 327–337.
- 31. Foster BL, Dickson TL. Grassland diversity and productivity: the interplay of resource availability and propagule pools. Ecology 2004;85: 1541–1547.
- 32.
Nelson PW. The terrestrial natural communities of Missouri. Missouri Natural Areas Committee: 2010.
- 33. Craine JM, Wedin DA, Chapin FS, Reich PB. Relationship between the structure of root systems and resource use for 11 North American grassland plants. Plant Ecology 2003;165: 85–100.
- 34. Hautier Y, Niklaus PA, Hector A. Competition for light causes plant biodiversity loss after eutrophication. Science 2009;324: 636–638. pmid:19407202
- 35. Yannarell AC, Busby RR, Denight ML, Gebhart DL, Taylor SJ. Soil bacteria and fungi respond on different spatial scales to invasion by the legume Lespedeza cuneata. Front Microbiol 2011;2: 127. pmid:21687434
- 36. Coykendall KE, Houseman GR. Lespedeza cuneata invasion alters soils facilitating its own growth. Biol Inv. 2014;16: 1735–1742.
- 37.
Andrews R. Invasive Chinese lespedeza (Lespedeza cuneata [Dum.-Course.] G. Don) alters the root and rhizosphere fungal communities of switchgrass (Panicum virgatum L.) in northern Virginia. M. Sc. Thesis, George Mason University. 2011.
- 38.
Beck AM. Invasive lespedeza cuneata and its relationship to soil microbes and plant-soil feedback. Ph.D Thesis, University of Illinois at Urbana-Champaign. 2017.
- 39.
West JB. The effects of dominant bunchgrass species on sandhill longleaf pine savanna ecosystem function: a comparison of wiregrass to the bluestems. Ph.D Dissertation, University of Georgia. 2002.
- 40. Briske DD, Butler JL. Density-dependent regulation of ramet populations within the bunchgrass Schizachyrium scoparium: interclonal versus intraclonal interference. J Ecol 1989;77: 963–974.
- 41. Dostal P et al. 2013 Ecology letters 16: 1277
- 42. Crawford KM, Knight TM. Competition overwhelms the positive plant-soil feedback generated by an invasive plant. Oecologia 2017;183: 211–220. pmid:27796508
- 43. Burns JH, Pardini EA, Schutzenhofer MR, Chung YA, Seidler KJ, Knight TM. Greater sexual reproduction contributes to differences in demography of invasive plants and their noninvasive relatives. Ecology 2013;94 995–1004. pmid:23858640
- 44. Woods TM, Hartnett DC, Ferguson CJ. High propagule production and reproductive fitness homeostasis contribute to the invasiveness of Lespedeza cuneata (Fabaceae). Biological Invasions 2009;11: 1913–1927.
- 45. Schutzenhofer MR, Knight TM. Population-level effects of augmented herbivory on Lespedeza cuneata: Implications for biological control. Ecological Applications 2007;17: 965–971. pmid:17555210
- 46. Schutzenhofer MR, Valone TJ, Knight TM. Herbivory and population dynamics of invasive and native Lespedeza. Oecologia 2009;161: 57–66. pmid:19444475