Functional Ecology 2014, 28, 1266–1273
doi: 10.1111/1365-2435.12277
Decreased root heterogeneity and increased root length following grassland invasion Brenda M. Vaness1, Scott D. Wilson*,1 and Andrew S. MacDougall2 1
Department of Biology, University of Regina, Regina, SK S4S 0A2, Canada; and 2Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada
Summary 1. Plant invasions can be promoted by environmental heterogeneity, but the opposite effect, the impact of plant invasion on heterogeneity, has received little attention. Grassland invasions might contribute to decreased spatial heterogeneity because invaders tend to be larger than native vegetation. Lowered heterogeneity may contribute to the low diversity of invaded communities, as well as to the persistence of invasive populations. 2. We compared the spatial heterogeneity of roots and resources in uninvaded native grassland and in stands invaded by a relatively large exotic grass (Agropyron cristatum), in four combinations of mowing and nitrogen (N) addition. We focused on roots because they account for the majority of primary production in grasslands. 3. The spatial heterogeneity of root length (m root m2 rhizotron image) and root production was significantly lower beneath A. cristatum than uninvaded grassland. This result was consistent in all combinations of mowing and N addition. 4. Beneath the invader, root length was significantly greater, and the proportion of samples that contained roots was significantly higher. This suggests that the invader decreased spatial heterogeneity by more completely filling the soil volume with roots. 5. Resource heterogeneity varied significantly between vegetation types in just one of four cases examined, suggesting that invader effects on resource heterogeneity were small relative to its effects on root heterogeneity. 6. These results suggest a novel mechanism promoting invader success and persistence: high root heterogeneity, lower root length and empty soil volumes in native grassland may make it relatively vulnerable to invasion, while reduced heterogeneity and greater root length in invaded grasslands may sustain stable, low-diversity communities dominated by the invader. Lowered heterogeneity accompanying invasion may partly account for the wide-spread occurrence of low-diversity, invader-dominated grasslands in North America. Key-words: Agropyron cristatum, grass, mowing, nitrogen, patch, root length, root mortality, root production, soil
Introduction Plant invasions may be promoted when environmental heterogeneity – spatially or temporally – provides opportunities for invader establishment (Davis & Pelsor 2001; Brandt & Seabloom 2011). In contrast, the opposite effect, the impact of plant invasion on heterogeneity, has received little attention (Levine et al. 2003; Melbourne et al. 2007), even though it may have significant implications for understanding invader impact and persistence. Here, we ask whether the magnitude of spatial heterogeneity *Correspondence author. E-mail:
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below-ground in a grassland is changed by an invading plant. We also examine differences in mean values. Invaders of grasslands might reduce the magnitude of spatial heterogeneity because they are typically larger than native species (Reed, Seastedt & Blair 2005; Kempel et al. 2013). Large invaders are often associated with increases in community productivity (Rout & Callaway 2009; Wilsey et al. 2009; Wolkovich et al. 2010). Large size may allow invaders to access resource-rich soil patches, as well as resource-poor patches, facilitating invasion into heterogeneous environments (Grime 1994; Rajaniemi & Reynolds 2004; P€ artel, Laanisto & Wilson 2008; Eilts et al. 2011). Once established, relatively large invaders might reduce
© 2014 The Authors. Functional Ecology © 2014 British Ecological Society
Invasion and root heterogeneity spatial heterogeneity if their resource uptake and resource deposition (litterfall or root exudates) homogenizes abiotic spatial variability. A recent review includes several examples of animal invasions increasing spatial heterogeneity but none for plants (Melbourne et al. 2007). Another review of >100 studies of the impacts of invasive plant species does not mention heterogeneity (Levine et al. 2003). Subsequent studies of the effects of grassland invasion on heterogeneity report both positive and negative effects (Crooks 2002; Lane & BassiriRad 2005; P€artel, Laanisto & Wilson 2008). Heterogeneity is likely to influence interspecific competition (Mommer et al. 2012) and ecosystem responses to global change (Garcia-Palacios et al. 2012). Reductions in spatial heterogeneity following invasion may have two consequences. First, species diversity in general decreases both with invasions (Levine et al. 2003; Melbourne et al. 2007) and with decreasing environmental heterogeneity (Hutchings, John & Stewart 2000; Questad & Foster 2008, but see Fridley et al. 2007; Lundholm 2009; Reynolds & Haubensak 2009). Reductions in heterogeneity following invasion could partly explain the often-observed correlation between invasion and lowered diversity. On the other hand, a greater competitive ability on the part of invaders could also contribute to lower diversity (Crooks 2002). Secondly, because heterogeneity can facilitate invasion (Davis & Pelsor 2001; Schoolmaster & Snyder 2007), a community with invader-driven heterogeneity reduction should be less susceptible to subsequent invasions, including the potential re-establishment of displaced native plants, due to a reduction in available niche space (Davis, Grime & Thompson 2000). Evidence for this comes from the difficulty of restoring higher levels of species richness in lowdiversity stands of invasive grasses (MacDougall, Wilson & Bakker 2008; Foster et al. 2009; Rowe 2010; Wilson & Pinno 2013). We measured the spatial heterogeneity of roots and soil resources in North American grasslands that were dominated either by native species or by the invasive perennial C3 grass Agropyron cristatum (L.) Gaertn (crested wheatgrass). A. cristatum has established on >10 million ha of the Great Plains of North America and readily invades native grassland in the northern Great Plains (Heidinga & Wilson 2002; Henderson & Naeth 2005). A. cristatum stands have double the standing crop (Christian & Wilson 1999) and root length (m root per sample; MacDougall & Wilson 2011) of native grassland. Richness and diversity is significantly lower (c. 40%) in A. cristatum stands than in native grassland (Christian & Wilson 1999; Heidinga & Wilson 2002; Henderson & Naeth 2005), and A. cristatum is a typical grassland invader in its negative effect on diversity (Walker & Smith 1996; Otfinowski, Kenkel & Catling 2007). We focused on root heterogeneity because 50–90% of temperate grassland productivity occurs below-ground (Steinaker & Wilson 2005; Mokany, Raison & Prokushkin 2006) and because grassland competition is dominated by
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below-ground interactions (Peltzer, Wilson & Gerry 1998; Dornbush & Wilsey 2010). We tested whether differences in heterogeneity between native and invaded vegetation are influenced by two management practices widely used in grasslands: mowing and nitrogen (N) addition. Mowing strongly influences grassland species composition (Williams, Jackson & Smith 2007; Foster et al. 2009) and decreases the cover of A. cristatum (Wilson & P€ artel 2003). We also consider mowing as a surrogate for grazing because of the difficulty of applying real grazing evenly to small experimental areas. Mowing and grazing have been reported both to decrease (Wijesinghe, John & Hutchings 2005) and increase (Schlesinger et al. 1990) soil resource heterogeneity. N limits production in temperate grasslands, and higher nutrient availability promotes grassland invasions (Foster et al. 2009; James et al. 2011; Wilson & Pinno 2013). Increased N availability may increase plant size and thus the scale at which individual plants forage for soil resources, and possibly decrease the spatial heterogeneity of soil resources (Grime 1994). Here, we test whether A. cristatum decreases spatial heterogeneity against a backdrop of mowing and N availability. Specifically, we tested the hypothesis that the spatial heterogeneity of roots (length, production, and mortality) and resources (soil water and available N) was lower in invaded than native grassland, and whether this difference varied with mowing and N availability. Differences in mean values were also examined.
Materials and methods We worked at Medicine Lake National Wildlife Refuge in northeastern Montana (48°280 16″ N, 104°220 16″ W). Native grassland was dominated by the C4 grass Bouteloua gracilis (H.B.K.) Lag. Ex Steud. (blue grama) and Selaginella densa (Rydberg) (spikemoss). Covers of these species in nearby grassland are c. 18% and 25%, respectively (Christian & Wilson 1999). Average annual precipitation is 33 cm, the average July temperature is 199 °C, and the average January temperature is 131 °C (NOAA-Western Regional Climate Center, http://www.wrcc.dri.edu/). Soils are well-drained loam (A-horizon, 0–15 cm) over clay loam (B-horizon, 15–100 cm), >200 cm above the water-table (http://websoil survey.nrcs.usda.gov). Agropyron cristatum was planted on a fireguard adjacent to our study site during 1940–1960 (J. Rodriguez, unpublished data). Since then, A. cristatum has invaded from the fireguard into the adjacent uncultivated native grassland of our study site. The uncultivated nature of the invaded grassland is shown by the absence of plow lines in aerial images (e.g. http://websoilsurvey. nrcs.usda.gov) and the presence of native vegetation in patches where A. cristatum is absent. The total study area was about 1 km parallel to the fireguard (SW-NE axis) and up to 300 m away from the fireguard (SE-NW axis). The study area was within a single management area that had received occasional light-moderate grazing in previous decades (J. Rodriguez, unpublished data) and was not grazed during our study. Twenty plots were randomly located in stands of non-invaded native grassland further away from the fireguard that had no A. cristatum. Twenty other plots were randomly located in stands closer to the fireguard that had c. 100% cover of A. cristatum. Plots were 5 m in diameter and >10 m apart. Each plot was randomly assigned to one of four
© 2014 The Authors. Functional Ecology © 2014 British Ecological Society, Functional Ecology, 28, 1266–1273
1268 B. M. Vaness et al. treatments: mowing, nutrient addition, mowing and nutrient addition, or no treatment. There were five replicates of each treatment combination in each vegetation type. Treatments were administered in late May and early July of 2006 and 2007, during peak production of roots and shoots (Steinaker & Wilson 2008). Mowed plots were cut to about 5 cm, and clippings were removed to mimic biomass removal by grazing. We added nitrogen (N) as N is often the limiting nutrient in these grasslands (K€ ochy & Wilson 2001). N was broadcast (by hand in equal portions
