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(American Journal of Botany. 2008;95:681-687.) doi: 10.3732/ajb.2007408 © 2008 Botanical Society of America, Inc. |
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Ecology |
2 Biology Department, John Carroll University, University Heights, Ohio 44118-4581 USA 3 USDA-Agricultural Research Service, Eastern Oregon Agricultural Research Center 67826-A Hwy 205, Burns, Oregon 97720 USA
Received for publication 12 December 2007. Accepted for publication 7 April 2008.
ABSTRACT
Understanding the functional traits that allow invasives to outperform natives is a necessary first step in improving our ability to predict and manage the spread of invaders. In nutrient-limited systems, plant competitive ability is expected to be closely tied to the ability of a plant to exploit nutrient-rich microsites and use these captured nutrients efficiently. The broad objective of this work was to compare the ability of native and invasive perennial forbs to acquire and use nutrients from nutrient-rich microsites. We evaluated morphological and physiological responses among four native and four invasive species exposed to heterogeneous (patch) or homogeneous (control) nutrient distribution. Invasives, on average, allocated more biomass to roots and allocated proportionately more root length to nutrient-rich microsites than did natives. Invasives also had higher leaf N, photosynthetic rates, and photosynthetic nitrogen use efficiency than natives, regardless of treatment. While these results suggest multiple traits may contribute to the success of invasive forbs in low-nutrient environments, we also observed large variation in these traits among native forbs. These observations support the idea that functional trait variation in the plant community may be a better predictor of invasion resistance than the functional group composition of the plant community.
Key Words: invasive species • functional traits • root foraging • spotted knapweed • yarrow
Exotic plant invasions pose a serious global ecological and conservation threat to native plant communities (Vitousek, et al., 1996
; Simberloff, 2005) and can induce serious economic costs. For example, in the United States, alone, the annual cost of nonnative plant species was estimated at $34 billion (Pimentel et al., 2005). Because of their potential negative impacts, ecologists and invasion biologists need to understand which traits makes one species more invasive than others. We know that some nonnative species, following their arrival to a new area, simply naturalize and become part of the resident plant community (Richardson et al., 2000). In contrast, other species rapidly expand their range and are considered invasive (Py
ek et al., 2004). Determining which traits contribute most strongly to the competitive ability of a nonnative organism is an essential first step in improving the prediction and management of the spread of invasive species.
In natural ecosystems, plant success depends on a suite of traits related to resource acquisition and use. For example, soil nutrients are heterogeneously distributed both spatially and temporally at the levels of the individual plant and the community (Hodge, 2006). In nutrient-limited systems, the ability of a species to exploit nutrient patches may be important in determining its growth, competitive ability, and survival. At the root-level, plants have developed foraging mechanisms that allow them to alter root architecture, allocation, morphology, and physiology in response to variable resource supply (Drew and Saker, 1975; Jackson et al., 1990; Jackson and Caldwell, 1991; Aanderud et al., 2003; Ivans et al., 2003; Wang et al., 2006). These responses are expected to increase the efficiency and rate of resource capture in heterogeneous environments (Fransen et al., 1999). However, the magnitude of root responses to nutrient patches varies among species (Campbell et al., 1991; Wijesinghe et al., 2001). Differences in foraging ability among species may, in part, contribute to their success in heterogeneous environments, as the ability to exploit patches may influence plant establishment and competitive interactions. For example, under competitive conditions, plants that rapidly proliferate roots into nutrient patches capture more resources than plants that proliferate in patches more slowly (Hodge et al., 1999, 2000; Robinson et al., 1999). Because of the ephemeral nature of nutrient patches (Lamb et al., 2004), the ability to quickly proliferate roots may provide a competitive advantage. Thus, growth rate, root system size, and precision (i.e., the ability to selectively place roots in nutrient patches) together influence a plant’s ability to capture heterogeneous soil resources.
Enhanced allocation to roots can result in greater resource acquisition (Aerts and Chapin, 2000), which in turn influences aboveground processes. For example, in a greenhouse study, grasses with more root biomass also had higher leaf nutrient concentrations (Fransen et al., 1998). As resource acquisition increases, so can photosynthetic rates and biomass accumulation. Photosynthetic rates depend, in part, on leaf N concentration (Field and Mooney, 1986; Evans, 1989), and with increased photosynthetic assimilation, more reduced carbon is available for biomass production. Carbon gain may be enhanced in plants with greater photosynthetic nutrient use efficiencies because higher photosynthetic rates can be obtained for a given unit of nutrient (Lambers et al., 1998).
The broad objective of this research is to quantify a suite of key above- and belowground traits related to resource acquisition and use in native and invasive forbs. We predict that invasive forbs will have a greater ability to forage for heterogeneously distributed nutrients than native forbs. Additionally, we predict that invasive species not only will acquire more resources from patches than native species, but they will produce more biomass, have higher photosynthetic rates, and have higher nutrient use efficiency. Combined, this suite of traits could confer a greater competitive ability in these nonnative species.
MATERIALS AND METHODS
Study species
Four native and four nonnative perennial forbs that cooccur at our study site in eastern Oregon were selected for this experiment (Table 1). All four invasive species are listed as noxious weeds by states in the Intermountain West, and the native species selected are used widely in restoring weed infested areas in this region. Seed for all invasive species and for Erigeron linearis were collected from local populations in eastern Oregon. All other native seeds were purchased from a commercial source (Granite Seed, Lehi, Utah, USA). Prior to planting, seeds were vernalized for 2 weeks at 4°C. Due to its tough seed coat, Sphaeralcea munroana seeds were scarified by poking a small hole in the seed coat with a razor blade.
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) but thereafter were irrigated with tap water 2–3 times per week. While the rate of N release from the slow-release fertilizer is dependent on soil temperature and water, based on pot volume, soil bulk density and initial N concentration of the low N soil media, our N additions were expected to result in an average N supply rate of 0.4 mg•kg–1•d–1. This rate is well within the range of N mineralization rates documented in this system and is threefold lower than N mineralization rates documented following weed invasion in this system (Chen and Stark, 2000; Booth et al., 2003).
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Harvest and measurements
After 12 wk of growth, all aboveground and belowground biomass was harvested. We analyzed 10 leaves from L. lewisii and E. linearis and three leaves from all other species for leaf area using WinRHIZO; this value was divided by their dry mass to determine specific leaf area. For all species, the youngest, fully expanded leaves were collected. Differences in leaf number measured were due to large differences in leaf size; L. lewisii and E. linearis had significantly smaller leaves than the other species. Specific leaf area then was used to determine photosynthetic nutrient use efficiency (described later). Following the harvest, aboveground biomass was triple-rinsed with deionized water, oven-dried at 60°C for 48 h, and then weighed. Belowground biomass was collected from two compartments—within the buried nylon bags and in the remaining portion of the soil column. The buried nylon bags carefully were removed from the surrounding soil, and any roots extending from the bag were cut and added to the remaining belowground biomass. Roots from within the nylon bags were collected and rinsed on a fine sieve (2 mm) and then were stored in deionized water at 4°C until further analysis (described later). After the bags were extracted, the remaining root system was washed gently and recovered over a sieve. Prior to weighing, all root mass was oven-dried for 48 h at 60°C.
Total root length of roots from the buried nylon bags was measured (WinRHIZO). These roots then were oven-dried and weighed to determine specific root length (root length per mass, km•kg–1). Three E. linearis plants (two control replicates and one patch replicate) had so few roots in the nylon bags that reliable masses could not be obtained; these samples were omitted from the statistical analysis for specific root length. Root length density (root length per soil volume, km•m–3) was determined based on total root length and the volume of the nylon bags. Root mass ratio, which indicates the amount of plant biomass allocated to belowground structures, was calculated as the total root mass divided by total plant mass.
Prior to nutrient analyses, all aboveground tissues (consisting almost entirely of leaf tissue) were finely ground. Total nitrogen was determined by micro-Dumas combustion. Samples for total phosphorus were dry-ashed and dissolved in 1 N HCl, then analyzed colorimetrically (Allen, 1989). Photosynthetic nutrient use efficiencies for nitrogen and phosphorus were determined as the photosynthetic assimilation rate per unit nutrient on an area basis (µmol CO2•mol–1 N•s–1 or µmol CO2•mol–1 P•s–1, respectively).
Statistical analysis
Univariate ANOVA was used to compare differences in responses of native and invasive species to resource addition treatments (control vs. patch) (SAS Institute, 2002). Normality and equal variance were assessed using the Shapiro–Wilks test and Levene’s test, respectively. When these assumptions were not met, the data were weighted by the inverse of the variance (Neter et al., 1990).
RESULTS
Biomass and root morphology measurements
Invasive species, as a group, produced significantly more aboveground and belowground biomass than native species (F1,87 = 45.06, P < 0.001; F1,87 = 73.07, P < 0.001; respectively), but there was no significant main effect of treatment (control or patch) on aboveground (F1,87 = 0.30, P > 0.05) or belowground biomass (F1,87 = 0.04, P > 0.05) or interactive effect of plant origin (native or invasive) and treatment on aboveground (F1,87 = 0.0.24, P > 0.05) or belowground biomass production (F1,87 = 0.10, P > 0.05) (Fig. 2A, B). Additionally, invasive species allocated more of their total biomass belowground, having a significantly higher root mass ratio than did the native species (F1,87 = 32.83, P < 0.001) (Fig. 2C). Again, there was no significant main effect of treatment (F1,87 = 0.00, P > 0.05) or interactive effect of plant origin and treatment (F1,87 = 0.02, P > 0.05). There was, however, large variation in biomass responses among species within a group, with native species having coefficients of variation (CV) greater than 100 in both the control and patch treatments (Table 2). For example, among native species aboveground and belowground biomass varied 43- and 31-fold, respectively. Overall, A. millefolium, and to some extent, S. munroana, behaved more similarly to the invasive species in biomass accumulation than did the other two native species. Because of its low root biomass, L. dalmatica had the lowest root mass ratio of the invasive species, similar in magnitude to that observed in the native species.
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As hypothesized, native and invasive species differed in functional traits related to nutrient acquisition and use. Overall, the suite of invasive species had greater root foraging precision (i.e., greater root length density in resource patches than in control soils) (Fig. 3A), and they invested a substantial portion of their total biomass (>40%) into roots (Fig. 2C). Comparing the mean root mass ratios of the invasive species and the two fast-growing native species (A. millefolium and S. munroana), the invasive species allocated 15% more of their biomass into belowground structures. Although greater root mass ratios often are associated with species adapted to low resource environments, high root allocation also has been observed in fast-growing species from various habitats (e.g., heathlands, grasslands, old fields), potentially increasing nutrient acquisition (Aerts and Chapin, 2000). A comparison of eight herbaceous perennials documented that plants with larger root systems also had a high degree of root foraging precision, and these traits were more common in the introduced, fast-growing species studied (Rajaniemi and Reynolds, 2004). Thus, in both the previous (Rajaniemi and Reynolds, 2004) and current study, species with larger root systems also had higher precision. This combination of traits may enable invasive species to capture more resources disproportionate to their size, potentially promoting size-asymmetric competition belowground.
The greater root foraging precision observed in invasive vs. native species likely is correlated to faster growth rates in the invasive species (James and Drenovsky, 2007). In fact, higher growth rates may underlie fast-growing species’ ability to obtain resources (Kembel and Cahill, 2005). Our data suggest that under competitive conditions the suite of invasive species would be able to preempt resources in nutrient patches because of faster interception (i.e., high relative growth rates and greater root foraging precision). Additionally, when plants are competing for resources, rapid root proliferation is predicted to be more effective than simply increasing uptake rates at the root surface (Robinson, 2001). Thus, the greater or more rapid root foraging ability observed in this study may further contribute to the ability of these invasives to exploit patchy soil resources in an otherwise nutrient-poor environment.
In addition to greater root foraging precision the invasive species were able to maintain higher photosynthetic rates (Fig. 5A) and obtain greater biomass than the native species (Fig. 2A, B), making them more nutrient use efficient (Fig. 5B, C). Higher nutrient use efficiency, in turn, should increase plant performance and, potentially, fitness (Aerts and Chapin, 2000). In a comparison of native and invasive species from low nutrient habitats, higher photosynthetic nutrient use efficiencies were documented in the invasive species, suggesting that greater nutrient use efficiency is one functional trait enhancing their competitive ability and success in these environments (Funk and Vitousek, 2007). Similar results were observed in photosynthetic trait comparisons of native and nonnative Rubus species in the Pacific Northwest (McDowell, 2002) and the evergreen understory species Ilex aquifolium (native) and Rhododendron ponticum (nonnative) at two European sites (Niinemets et al., 2003). Thus, higher photosynthetic nitrogen use efficiency may be an additional key trait allowing these invasives to invade nutrient poor systems (Funk and Vitousek, 2007).
While native and invasive species differed in a number of traits examined, there also was substantial trait variation within a functional group, and in a few instances some native forbs had patterns of root foraging and nutrient use that were comparable to invasives. For example, aboveground and belowground biomass, as well as root length density, varied widely among the native species (Figs. 2A, B, 3A; Table 2), with A. millefolium and S. munroana behaving more similarly to the invasive species than to the other two native species. In contrast, the slow-growing, native species (i.e., E. linearis and L. lewisii) had low root foraging precision (Fig. 3A), photosynthetic rates (Fig. 5A), and shoot and root biomass production (Fig. 2A, B). Under competitive conditions, the potential consequences of this trait variation are large. For the slow-growing species, small root system size decreased their ability to obtain P, a highly immobile soil nutrient (Marschner, 1995); leaf P concentrations declined 15 and 29%, respectively, for E. linearis and L. lewisii in the patch relative to the control treatment (Fig. 4B). Under competitive conditions, these slow-growing species likely would be outcompeted due to resource preemption by their fast-growing, invasive counterparts. In contrast, the faster-growing native species would be more competitive with the invasive species, due to their greater root foraging ability.
One major hypothesis of invasion resistance is similarity in functional grouping between the biomass dominant and the invader (Emery, 2007). However, support for this hypothesis is mixed (Symstad, 2000; Dukes, 2001; Pokorny et al., 2005; Emery, 2007). Much of this inconsistency may be related to the manner in which species are categorized into functional groups. Recent evidence suggests that categorizing species based on coarse differences in morphology or taxonomy may not adequately predict species effects on ecosystem processes (Wright et al., 2006). In support, our study suggests large trait variation may limit the ability to use conventional functional groupings to predict invasion resistance.
One limitation of our study was that we were unable to distinguish between traits of introduced, noninvasive species and traits of introduced, invasive species. Simple comparisons of native and invasive species cannot predict which characteristics are associated with invasiveness, per se, because species native to one area may become invasive in other areas if introduced (Burns, 2004). Although comparing invasive and noninvasive introduced species is a powerful comparison, this suite of species is not commonly found in the Great Basin. Namely, noninvasive, nonnative forbs do not tend to establish stable populations in the Great Basin. But given the inclusion of A. millefolium, an invasive weed in parts of the southern hemisphere (Pickering and Hill, 2007), we can make some inferences about the value of observed resource use and acquisition traits for an invader. As stated, A. millefolium behaved more similarly to the invasive species included in the experiment than to the other native species. This observation suggests that the measured resource use and acquisition traits are good indicators of invasibility and not just traits of nonnative species.
Overall, the ability of a species to capture N and P was influenced little by the different treatments. One interpretation of these results is that the patch treatments were potentially ineffective as a result of substantial nutrient movement out of the patches during the duration of the experiment. Such a scenario would have made the soils in the patch treatment relatively homogenous. This scenario is a possibility because there likely was some degree of nutrient diffusion and mass flow out of the patches. However, two lines of reasoning suggest nutrient movement from the patches was not a likely factor in our lack of treatment effect on plant nutrient capture. First, most species produced more root length in enriched patches compared to control patches, suggesting soil conditions in the two treatments differed enough to drive different root responses. Second, it has been fairly well demonstrated that the benefit of root proliferation in terms of plant biomass production and total nutrient capture is typically observed to the greatest degree when plants are in competition (e.g., Robinson et al., 1999).
Concluding remarks
Although as a group the native species had smaller root systems and lower root foraging precision, the responses among these native species were highly variable. Linum lewisii and E. linearis produced very little biomass and ineffectively foraged for nutrients, but the other two native species (A. millefolium and S. munroana) had biomass and root foraging traits more similar to the invasive species than to their native counterparts. Previous work has documented similar, and rapid, growth rates among A. millefolium and S. munroana and the suite of invasive species studied here (James and Drenovsky, 2007). Thus, although previous research has suggested native species of the same functional group as the introduced species may be more effective at resisting invasion (e.g., Pokorny et al., 2005), our data suggest that species from the same functional group may not share physiological and/or morphological traits. In fact, important functional traits were more variable within than between groups of native and nonnative species. Recent research has suggested that the ability to link plant community composition to ecosystem function may depend heavily on understanding patterns of functional trait variation in plant assemblages and not simply how functional group diversity or composition is distributed in the plant community (Wright et al., 2006; Lavorel and Garnier, 2002). From a management perspective, focusing on native species with similar traits, rather than functional groups, as nonnative species may improve the ability to establish and maintain communities more resistant to invasion. Seed mixtures used to restore degraded or weed-infested communities typically are designed with the intent to maximize species diversity with the expectation that establishing diverse communities will maximize weed resistance. Results from this study and the ideas developed by Wright et al. (2006) and Lavorel and Garnier (2002) suggest restoration practitioners could gain more economic and ecological return on purchased seeds by designing species mixtures based on specific desired traits and not based solely on species diversity per se.
FOOTNOTES
1 The authors thank C. Sheil and N. Pietrasiak for help installing the experiment and C. Sheil for illustrating Fig. 1. Comments from R. B. Pratt, J. L. Funk, and an anonymous reviewer significantly improved the manuscript. A Franklin Research Grant from the American Philosophical Society (R.E.D.) and a Summer Research Fellowship from the Huntington-Codrington Foundation (C.E.M.) helped support this work. 
4 Author for correspondence (e-mail: rdrenovsky{at}jcu.edu)
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