Nitrogen deposition enhances Bromus tectorum invasion: biogeographic differences in growth and competitive ability between China and North America

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1 Ecography 34: , 2011 doi: /j x # 2011 The Authors. Ecography # 2011 Ecography Subject Editor: Francisco Pugnaire. Accepted 22 February 2011 Nitrogen deposition enhances Bromus tectorum invasion: biogeographic differences in growth and competitive ability between China and North America Wei-Ming He, Guo-Lei Yu and Zhen-Kai Sun W.-M. He (weiminghe@ibcas.ac.cn), G.-L. Yu and Z.-K. Sun, State Key Lab of Vegetation and Environmental Change, Inst. of Botany, Chinese Academy of Sciences, PR-Beijing , China. Increased resource supply commonly facilitates invasion by exotic plants, raising concerns over atmospheric nitrogen (N) deposition; fast-growing annual invaders may have exceptional abilities to outperform native perennials in response to N pulses. However, it remains unclear whether this advantage is due to growth differences or to shifts in competitive outcomes, and whether annual invaders are favored by N deposition in their introduced range over native range. We conducted an experiment to compare the growth and competitive ability of Bromus tectorum and its native perennial grasses either at three different N regimes or between China and North America. The soil used in this experiment was from mountain grasslands as a neutral growth medium. The total biomass of three natives from China and North America did not increase along the N deposition gradient. Nitrogen addition enhanced the growth of North American B. tectorum instead of Chinese B. tectorum. Nitrogen addition increased the competitive ability of B. tectorum, but had no effect on that of natives. North American B. tectorum was bigger and had greater competitive ability and root weight ratio than Chinese B. tectorum. In contrast, North American natives were less competitive than Chinese natives. There was a significantly positive correlation between the growth of B. tectorum grown alone and its competitive ability. These findings suggest that N deposition may enhance the B. tectorum invasion through disproportionally increasing the growth and maintaining inherent competitive advantages of North American B. tectorum, further increasing threats to introduced ranges. There were differences in the growth and competitive ability of B. tectorum and natives between China and North America, which explains why B. tectorum is a minor component at home and becomes a successful invader abroad. Soil nitrogen (N) is the most limiting factor for plant growth and productivity in terrestrial ecosystems (Chapin et al. 1986, Elser et al. 2007), and human activity is currently increasing N deposition across the world (Nybakken et al. 2009). Higher rates of N deposition increase soil N availability (Köchy and Wilson 2001, Limpens et al. 2003, Gilliam 2006) which may alleviate soil N limitations (Britton and Fisher 2007, Hwang and Lauenroth 2008), but high concentrations of N can also promote invasions by exotic plants (Maron and Connors 1996, Vitousek et al. 1997, Dukes and Mooney 1999, Brooks 2003, Gilliam 2006). Due to geographic differences of N deposition and invasive plants (Dukes and Mooney 1999), the complex associations between N deposition and plant invasions are likely to vary with regions, and thus increase uncertainty to predict invasion patterns (Bradley et al. 2010). It is already known that some invasive annuals can outperform native perennials under N-poor and N-rich conditions, thus small increases in soil N may cause disproportional effects on invasive annuals and native perennials (James 2008, Mazzola et al. 2008). In other words, resource release may favor invaders over natives (Davis et al. 2000). However, conclusive support for the links of N deposition with invasive and native plants is less common. Bromus tectorum is a successful invader of Eurasian origin, which has conquered North America and posed serious threats to the conservation of ecosystems (Mack 1981, Sperry et al. 2006, Bradley 2009, Griffith 2010). The effects of external factors on B. tectorum invasion have been extensively studied (Chambers et al. 2007, Gundale et al. 2008, James 2008, Griffith 2010, Scott et al. 2010), but the effects of N deposition on B. tectorum invasion remain less understood than others. First, it is not clear mechanistically why B. tectorum should benefit more from higher N supply than natives. Overall good invaders tend to be fast growing species and fast growing species tend to be N-efficient, achieving relatively high carbon gain per unit of N (Feng et al. 2009). If good competitors have disproportionally high resource consumption rates and relative growth rates, then increased soil N may not only increase the growth advantages of invaders, but also disproportionally shift competitive outcomes in favor of invaders. Thus we 1059

2 hypothesized that N deposition might simultaneously enhance the growth and competitive advantages of B. tectorum against native plants. A second unexplored aspect of the effects of N deposition on B. tectorum invasion is how N deposition affects its growth and competitive potential between home range and introduced range. Bromus tectorum has invaded North America for over 200 yr (cf. Valliant et al. 2007). Due to natural enemy release and new selection pressures, B. tectorum populations have shown dramatic genetic variation and rapid evolution (Novak and Mack 1993, Bartlett et al. 2002, Valliant et al. 2007, Leger et al. 2009, Scott et al. 2010). Thus it is most likely that B. tectorum populations from China (home range) and North America (introduced range) exhibit contrasting growth potential and competitive ability. Here we hypothesized that there might exist geographical differences in the growth and competitive ability of B. tectorum between China and North America. Additionally, biogeographic comparisons can also provide evidence for evolution of increased competitive ability (EICA, Blossey and Nötzold 1995). The EICA is the most common context in which successful invasion is often attributed to the evolution of an introduced species. In this case, release from natural enemies is thought to result in genotypes that evolve to allocate less to herbivore defense (Janzen 1975), and then to reallocate the freed energy and resources to growth (Blossey and Nötzold 1995). Greater growth could make these new genotypes more competitive than their predecessors in the native range and lead to invasive success. However, conclusive support for the full causal process proposed for EICA is less common (He et al. 2009). Thus, the final purpose of this study is to test the EICA hypothesis in the context of N deposition. Methods Bromus tectorum (hereafter Bromus) is a fast-growing annual grass, native in temperate regions through much of Eurasia and northern Africa (cf. Valliant et al. 2007). Bromus was first detected in North America in about 1790 in Lancaster Co., Pennsylvania, USA, but was rarely collected before 1860 (cf. Valliant et al. 2007). To date Bromus has invaded perennial grasslands and forestlands of the western USA (Mack 1981, Bradley 2009, Bradley and Wilcove 2009). To compare the biogeographic effects of N deposition, seeds of Bromus were collected from Montana State in western USA and Gansu Province in western China. More specifically, we chose at least 30 Bromus individuals with 2 m apart and then collected seeds from them. Thus this approach, to some extent, allowed the seeds collected from both continents to represent native and introduced populations of Bromus. Due to biogeographic differences between China and North America, we were not able to find the same species or congeners that dominate local grasslands in two continents simultaneously. In nature Bromus can invade perennial grasslands and natively occurs in grasslands where perennial grasses dominate (unpubl.), thus we chose perennial grasses as target competitors only. We chose three native North American perennial grasses (i.e. Poa pratensis, P. secunda, and Stipa comata) and three native Chinese perennial grasses (Bromus inermis, Phleum pratense, Roegneria kokonorica) that are widely distributed in North America and China, and that are dominant components in local grasslands. These species also occupy the same regions as Bromus populations. Accordingly, the seeds of native perennial grasses were collected from Montana and Gansu, respectively. We conducted an experiment in which plants from the Chinese and North American populations of Bromus were each planted in competition with each of the three native Chinese and North American species, testing interspecific competition. Specifically, two plants in a pot were 2 3 cm apart each other. Plants from Bromus populations and all native species were also grown alone as controls. For each speciespopulation pair the replication was 10. Since our goal was to contrast the growth and competitive ability of Bromus and native species at different N deposition regimes, we repeated this entire design three times, once for ambient N concentrations, which consisted of neutral soil from Beijing mountain grasslands, again for low deposition rates (1 g N m 2 yr 1 ), and a third time for high deposition rates (4 g N m 2 yr 1 ). We note that mountain grassland soil was chosen because it was neutral to all species used in this study and provided the same soil environment for them. If we chose soils from Montan or Gansu, then biological factors in the soils would disproportionally affect the experimental results. The total replication for all N treatments and species combinations was 600. According to the National Atmospheric Deposition Program/National Trends Network (NADP/NTN, < current N deposition ranges between 0.1 and 2.0 g N m 2 yr 1 across the United States. Thus we chose 1 g N m 2 yr 1 as a low deposition rate. Based on the previous experiments and predictions for future deposition rates (van de Wal et al. 2003, Galloway et al. 2004, Pregitzer et al. 2008), we used 4gNm 2 yr 1 as a high deposition rate. In our study we chose a greenhouse (not a common garden) as experimental space because in the common garden soil nutrients are most likely to lose due to rainfall pulses and atmospheric N pulses also occur but these potential noises can be ruled out in the greenhouse. In a search of the literature, 55% of the previous studies we found used ammonium nitrate (NH 4 NO 3 ) for simulating N deposition. Thus we simulated N deposition by adding NH 4 NO 3. Nitrogen was applied as a solution of NH 4 NO 3 in deionized water. During the course of the experiment, all plants were watered every 23 d, depending on how fast the soil dried. All plants were grown from seed and grown in 1250 cm 3 pots filled with soil. Abiotic conditions were controlled so that growing conditions were identical for all plants, thus allowing us to rule out phenotypic plasticity. Greenhouse temperatures and relative humidity were maintained between 20308C and 5060%, respectively. Natural light in the greenhouses was supplemented by metal halide bulbs, and total photosynthetically active radiation during the day remained above 1200 mmol m 2 s 1. This experiment lasted for four months from 15 November 2009 through 18 March At the end of the experiment, all plants were harvested and separated into shoots and roots. Plants were dried at 758C for 48 h and weighed. Root weight ratio was determined as the ratio of root biomass to the total biomass of plants. To quantify the 1060

3 effects of N deposition on the growth of Bromus populations, the increase in biomass (IB) was calculated as the following: IB(B n B c )/B c 100%, where B n is the biomass of plants grown alone but subjected to N addition (i.e. low and high N deposition) and B c is the biomass of plants grown alone but subjected to no N addition. To quantify the effects of N deposition on competitive ability, relative interaction intensity (RII; Armas et al. 2004), was calculated. RII indicates the competitive ability of a target plant against its neighbour; RII has values ranging from 1 to 1, and is negative for competition and positive for facilitation (Armas et al. 2004). We used a three-way ANOVA, with N deposition, Bromus source, and competitor source as fixed factors, to test their effects on the competitive effects of Bromus on native perennial grasses, indicated by relative interaction intensity (RII). We used a two-way ANOVA, with N deposition and Bromus source or competitor source as fixed factors, to test their effects on the growth and RII of Bromus populations and Chinese or North American natives. Additionally, a one-way ANOVA also was used to test whether the growth and RII of Bromus or native plants differ between China and North America. In order to more directly compare growth responses to RII (competitive effects), we regressed mean growth responses to N for Bromus populations against mean RII of Bromus populations under two levels of N deposition. All statistical analyses were carried out with SPSS 13.0 (SPSS, Chicago). Results When all three native Chinese species were considered together, their total biomass did not significantly increase along the N gradient (Fig. 1; F1.497, p0.231). Nor did the total biomass of three native North American plants as a whole increase along the N gradient (Fig. 1; F0.302, p0.740). Thus, N deposition did not exhibit beneficial effects on the growth of native species from two continents. Nitrogen addition dramatically enhanced the growth of North American Bromus grown alone, and its total biomass monotonically increased with soil N availability (Fig. 2A; F , p B0.0001). In contrast, N addition increased the total biomass of Chinese Bromus marginally (Fig. 2A; F 2.684, p 0.075). The growth of North American Bromus was significantly greater than that of Chinese Bromus (Fig. 2A; p 0.014, p 0.002, pb for the control, low N deposition, and high N deposition). Most importantly, N addition significantly favored the growth of North American Bromus ( %) over Chinese Bromus ( %) across two levels of N deposition (Fig. 2A; p0.002). Root weight ratio (RWR) of North American Bromus decreased with N addition (F 6.730, p0.002), but RWR of Chinese Bromus was not affected by N addition (F0.786, p 0.460) (Fig. 2B). RWR was much smaller in Chinese Bromus than North American Bromus (p B0.0001), and this effect was heavily dependent upon N addition (P Bromus sourcen deposition 0.005) (Fig. 2B). Nitrogen addition increased the competitive effects, indicated by relative interaction intensity (RII), of Bromus on native species, particularly in high rates of N deposition Figure 1. Mean biomass along the N deposition gradient for three native perennial grasses grown alone, which were from China and North America. We note that all the three natives per continent were considered together. Data are means1 SE(n30). The bars sharing the same letters within a continent are not significantly different. (Table 1, effect of N deposition; Fig. 3). The competitive effect of North American Bromus was greater ( ) than that of Chinese Bromus ( ) (Table 1, effect of Bromus source). The competitive effect of Bromus was much greater on North American natives ( ) than on Chinese natives ( ) (Table 1, effect of competitor source). This ability of Bromus heavily depended on N deposition (effect of N B) and competitor source (effect of BC) (Table 1). The differences in competitive effects of Chinese Bromus on Chinese versus North American natives increased along the N deposition gradient and the reverse was the case for North American Bromus (Fig. 3A, B, C). The competitive effects of natives were insensitive to N addition in China (Fig. 4A; F2.211, p0.067) and in North America (Fig. 4B; F 1.187, p0.308). The competitive effects of Chinese natives were greater on Chinese Bromus than North American Bromus (Fig. 4A; F 6.016, p0.015) but the competitive effects of North American natives were smaller on Chinese Bromus than North American Bromus (Fig. 4B; F , p 0.001). Chinese natives had much greater competitive effects than North American natives, regardless of on Chinese Bromus ( vs ) or on North American Bromus ( vs ) (Fig. 4A, B). The mean RII values (competitive effects) of Bromus populations were negatively associated with the mean increases in biomass of Bromus populations (Fig. 5; r0.929, p0.035), and the regression equation was: RII0.0023increased growth (R ). Thus, the competitive ability of Bromus populations was dependent upon its growth potential, that is, greater growth higher competitive ability. 1061

4 Figure 2. Total biomass (A) and root weight ratio (B) along the N deposition gradient for Bromus tectorum grown alone, which was from China and North America. NANorth American. Data are means1 SE(n10). The bars sharing the same letters within a continent are not significantly different. Discussion Results were from a controlled greenhouse experiment lasting for four months, but this study does provide evidence for the effects of N deposition on the growth and competitive ability of Bromus, and also should provide a basis for further research to test whether N deposition enhances or decreases the risk of invasive plants. In the real world Bromus always grows with native plants of various ages. Thus our findings cannot be simply extrapolated into the field because the growth and competitive outcomes may be different when Bromus and native plant species grow under contrasting biotic and/or abiotic conditions (conditionality of experiments). Nitrogen deposition enhanced the growth of the North American invader Bromus grown alone but not the growth of three native North American perennials when they were considered together, indicating that the sensitivity in response to N pulses differs between Bromus and natives; higher concentrations of N maintained the strong competitive advantages that Bromus had inherently in the no N- addition conditions. These findings suggest that N deposition may enhance the Bromus invasion through increasing its growth advantages and maintaining its inherent competitive advantages, and in part support the first hypothesis that N deposition may simultaneously enhance the growth and competitive advantages of B. tectorum against native plants. In addition, our findings also support the notion that N deposition gives advantages to exotic invaders and disadvantages to native species simultaneously (Dukes and Mooney 1999, Gilliam 2006). Previous studies have shown that increased soil N facilitates plant invasions either through increasing the supply of unused resources for invaders (Davis et al. 2000) or increasing the relative competitive ability of invasive species under conditions with high resource availability (Shea and Chesson 2002). Bromus is highly sensitive to soil N availability (Lowe et al. 2003, Gundale et al. 2008), which can be explained using the following possibilities. Nitrate reductase activity usually is higher in invasive species than native species (Kourtev et al. 1999); soil N mobilization increases the growth of Bromus (Mazzola et al. 2008, Perry et al. 2010); Bromus has greater N-uptake activity than the perennials (MacKown et al. 2009), which is linked to root weight ratio and leaf N productivity (James 2008); the rapid establishment of an extensive root system of Bromus by early spring renders resources unavailable to native plants that initiate growth at warmer temperatures (Sperry et al. 2006). Competitive outcomes commonly drive invasion dynamics (Seabloom et al. 2003). Bromus is a good competitor because it is able to co-opt nutrients in the rooting zone of the natives, thus gains a competitive advantage (Blank 2010). In our study, North American Bromus had about 5-fold greater competitive effects than native North American perennials. More importantly, this competitive advantage remained unchanged along the N deposition gradient. Thus the competitive outcomes may favor Bromus over native North American grasses under changing N levels, and thus allow Bromus to maintain high invasiveness. Recent studies have shown that low N levels decrease competitive interactions between invaders and natives (Lowe et al. 2003, Vasquez et al. 2008, Hebel et al. 2009) and high N levels increase the growth and competitive advantages of invaders Table 1. ANOVA of relative interaction intensity of Bromus tectorum populations on native perennial grasses as affected by N deposition (N), Bromus source (B), competitor source (C), and their interactions. Values of pb0.05 are in bold. Source Type III sum of squares DF F p N deposition (N) Bromus source (B) Competitor source (C) B0.000 NB NC BC B0.000 NBC

5 Figure 3. Competitive effects, indicated by relative interaction intensity, of Bromus tectorum populations from China and North America on Chinese and North American natives under three different N regimes. NANorth American. Data are means1 SE (n30). The bars sharing the same letters within a continent are not significantly different. over natives (Huenneke et al. 1990, Milchunas and Lauenroth 1995, Lowe et al. 2003, van de Wal et al. 2003, Vasquez et al. 2008, Hebel et al. 2009). Thomsen et al. (2006) pointed out that elevated soil N did not influence competition among invasive and native perennials based on an experiment with three invasive perennial grasses and three native perennial grasses, which is inconsistent with our findings. If there are other limiting factors like precipitation and phosphorus, plants may not respond to increased N availability (Tomassen et al. 2003, 2004, Bradley et al. 2010). Similarly, if water is the limiting factor in western USA, Bromus may not respond to N deposition significantly; otherwise the effects of N deposition would be significant. This experiment suggests that N deposition may benefit the competitive advantage of Chinese Bromus more than North American Bromus, and there are biogeographic differences in the growth and competitive ability of plants from China and North America, thereby completely supporting the second hypothesis. For example, North American Bromus populations were much bigger and had higher competitive ability than Chinese Bromus populations across three N levels. Second, North American Bromus populations allocated more biomass to roots than Chinese counterparts, which allows them to have a higher capacity to absorb soil resources such as water and nutrients. This allocation strategy is highly beneficial to help North American Bromus populations effectively deal with the shortages of soil water and nutrients in the western USA, which in turn renders their growth and competitive advantages (James 2008). Additionally, native North American perennials exhibited much smaller competitive effects on Bromus populations than native Chinese perennials, which decreases the competitive effects of native North American grasses on Bromus in North America and increases the competitive effects of native Chinese grasses on Bromus in China. These biogeographic differences can to some extent explain why Bromus is a minor component in its home range but dominates where introduced. Our findings strongly support the EICA hypothesis (Blossey and Nötzold 1995) but decline the hypothesis of decreased competitive ability (Bossdorf et al. 2004). The key assumption of the EICA hypothesis is that those plants with greater growth have higher competitive ability (i.e. greater growth higher competitive ability) (Blossey and Nötzold 1995). However, this assumption has rarely been tested directly. Our findings demonstrate that Bromus has greater growth and higher competitive ability simultaneously. In contrast, our recent research suggests that the growth response of the perennial invader Centaurea maculosa to N deposition does not predict its competitive ability (He and Callaway unpubl.). Thus, growth and competitive ability need to be considered simultaneously in related studies. The EICA hypothesis predicts that differences among native and introduced phenotypes are due to evolutionary responses within the introduced range (Blossey and Nötzold 1995), which is supported by recent studies. The above biogeographic differences indicate that genetic differentiation is likely to occur in Bromus populations from two continents. This case study did not provide direct evidence for genetic differentiation, but this differentiation has been detected between home and introduced ranges in previous research (see below). Rapid evolution of local adaptation within the introduced range is essential for invasion success and invasive spread commonly involves rapid evolutionary change (Bartlett et al. 2002, Valliant et al. 2007, Leger et al. 2009, Scott et al. 2010). There were genetic differences between native and introduced Bromus populations, Eurasian populations had greater genetic differentiation than North American populations, and populations from southwest Asia were the most genetically differentiated; these genetic differences stem from the reduction in genetic variability across populations produced by founder effects combined with an increase in the within-population component of genetic variation from multiple introductions (Novak and Mack 1993). Interestingly, different North American Bromus populations share similar net photosynthesis and water-use efficiency, but differ in 1063

6 Figure 4. Changes in mean competitive effects, indicated by relative interaction intensity, along the N deposition gradient of three native perennial grasses from China and North America on two Bromus tectorum populations. Narrow bars are means and 1 SE (n30) for each N regime. Wide bars are means and 1 SE (n90) for across three N levels. The bars sharing the same letters within a continent are not significantly different. Figure 5. The relationship between competitive effects, indicated by relative interaction intensity, of Bromus tectorum populations and increases in biomass of B. tectorum populations with N deposition when grown alone. Each point denotes mean values of competitive effects and increased growth for each B. tectorum population grown in either low or high N deposition. biomass allocation (Rice et al. 1992). Higher biomass allocation to shoot growth allows plants to reach reproductive size more rapidly and set seed before moisture becomes limiting by late spring in North America. In summary, our findings suggest that atmospheric N deposition is likely to increase the prevalence of Bromus and the threats to introduced ranges. Specifically, N deposition may help Bromus invade some new terrains where soil N was extremely poor previously through shifting infertile soils into fertile soils (i.e. increased invasibility). Second, N deposition may increase the fire risk of Bromus-dominated communities because N deposition can increase their cover and productivity. Once Bromus-dominated communities are established, they result in more frequent wildfires, leading to a Bromus-wildfire cycle in which fire promotes Bromus and Bromus promotes fire (Link et al. 2006, Chambers et al. 2007, Gundale et al. 2008). Additionally, if Chinese Bromus invades North America, it may confer more serious consequences to introduced ecosystems compared to those established North American Bromus because Chinese Bromus populations are a much stronger competitor against North American natives compared to North American counterparts. The implications of this case study 1064

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