plasticity in low resource environments
High phenotypic plasticity has long been thought to be a characteristic of invasive species (Baker 1965; Marshall & Jain 1968) but few studies have properly evaluated this claim by comparing plasticity among invasives and phylogenetically related natives or introduced non-invasive species (Williams & Black 1994; Gerlach & Rice 2003; Burns & Winn 2006). In a recent review of the existing literature, Richards et al. (2006) concluded that the ability to capitalize on increased resource availability is a prevalent trait among invasive species. This conclusion concurs with predictions of the fluctuating resource hypothesis (Davis et al. 2000), which states that a community becomes more susceptible to invasion when resource availability is increased. Thus, as habitats experience alterations in the availability and timing of resources due to changing climate and anthropogenic disturbance, increased resource acquisition by invaders may alter competitive outcomes between invaders and natives. But should we extend this theory to low resource systems where species are thought to display low trait plasticity?
Working in a nutrient-poor environment, I found the magnitude of plasticity for leaf-level (PIV = 0.06–0.57) and plant-level (PIV = 0.19–0.66) traits across a suite of native and invasive species to be comparable to that found in species occupying higher resource habitats. In response to variation in light availability, Niinemets et al. (2003) found a PIV range of 0.18–0.59 for leaf-level traits in two evergreen shrubs occurring in a nutrient-rich site in Belgium (30–45 kg N ha−1 yr−1 via atmospheric deposition). Other studies in low resource systems, including a phosphorus-deficient, arid Mediterranean systems, found similar plasticity ranges for a diverse set of leaf- and plant-level traits (PIV = 0–0.80; Balaguer et al. 2001). The observation of considerable trait plasticity in species adapted to nutrient-poor environments runs counter to the argument that plasticity is too costly in stressful environments (e.g. Grime et al. 1986). However, the degree of plasticity in any environment will depend on the traits being examined. In a series of studies, Valladares et al. (2000, 2002) found that shade-tolerant species have low physiological plasticity and high morphological plasticity, while the reverse is true for shade-intolerant species.
species differences in trait plasticity
Invaders generally displayed higher trait plasticity than natives in response to altered nutrient availability while trait plasticity did not differ among native and invasive species in response to light availability. As all five pairs occur in nitrogen-poor soils (while only two of the five pairs also occur in light-limited forests), invaders in these habitats may benefit from the ability to respond to increased nutrient availability. Invasive species displayed trait plasticity consistent with success in nutrient-rich habitats. First, invasive species increased above-ground allocation (lower RWR, R/S) under high nutrient conditions, which concurs with expectations that plants will optimally partition biomass to maximize the capture of limiting resources (Bloom et al. 1985). Second, invasive species responded to increased nutrient availability with increased leaf N content (Narea) and photochemical function (Vmax, ΦPSII). Over time, these changes may lead to increased photosynthetic rate and growth under high nutrient conditions, but this effect was not observed here.
As a consequence of indeterminate growth, plants are inherently plastic; but not all trait plasticity is adaptive (Sultan 1995). Thus, for trait plasticity to contribute to plant invasiveness, it must be correlated with plant performance. As I used biomass instead of reproductive measures to assess plant performance, my data do not directly address adaptive plasticity. However, correlations of traits with biomass across the environmental gradient suggested that several plant- and leaf-level traits correlate strongly with plant fitness.
While light use efficiency (ΦPSII) correlated strongly with biomass in two native and three invasive species, the functional significance of several other traits varied among the two species groups. Asat and Narea showed strong correlations with biomass in four invasive but only one native species, while LMA correlated strongly with biomass in three native but only one invasive species. However, a complete understanding of the functional significance of trait plasticity may be especially difficult in low resource environments where plants display long leaf lifespan, high concentrations of defense compounds, low tissue nutrient content, and thicker leaves, all of which may result in reduced rates of photosynthesis and growth (Coley et al. 1985). While advantageous on long timescales (e.g. generation), these resource conservation traits (e.g. WUE, PNUE, LMA, leaf lifespan) may not correlate with fitness measures on short timescales (e.g. 1-year study), which may explain the insignificant correlations between many traits and plant biomass observed here.
While a few native species maintained thick leaves (LMA) and high light use efficiency (ΦPSII) relative to paired invasive species, native species as a group did not display higher resource-use efficiency than invasive species. These data support the conclusion from a recent field survey that invasive species may succeed in low resource systems by employing resource conservation traits similar to the native species adapted to these systems (Funk & Vitousek 2007). The observation that invaders displayed high trait plasticity and resource conservation contradicts the idea that there exists a trade-off between these two strategies (Grime et al. 1986). In fact, I observed no correlation among species PIV and any measure of resource-use efficiency. However, this assessment was limited to just ten species and does not provide a robust examination of this trade-off.
Several traits which showed low plasticity (e.g. Fv/Fm, Chl a/b) correlated strongly (P < 0.01) with biomass in some species while other traits (e.g. RWR, R/S, Nmass) showed high plasticity but did not correlate strongly with biomass. Although I did not directly assess adaptive plasticity, these data support the idea that small differences in the plasticity of some traits can have profound fitness consequences (Givnish 2002; Heschel et al. 2004; Funk et al. 2007). This result highlights the importance of exploring the functional significance of traits (rather than simply quantifying the amount of plasticity) in both genotypic- and species-level studies.
In conclusion, my data support the general paradigm that invasive species display high trait plasticity. The few studies that previously examined trait plasticity in invasive and native or non-invasive species in low resource environments found mixed support for higher trait plasticity in invasives (Williams & Black 1994; Padgett & Allen 1999; Weber & D’Antonio 1999; Cordell et al. 2002). However, this uncertainty may stem from the different types of traits (morphological, physiological, reproductive) measured across studies. As plant traits vary substantially in PIV (0.06–0.66, this study), studies examining only a handful of leaf-level or plant-level traits may not accurately represent differences in plasticity among native and invasive species.
Differences in phenotypic plasticity between native and invasive species will influence how these species will respond to changing environmental conditions. While low resource systems generally experience low levels of invasion (Burke & Grime 1996; Daehler 2003), these systems may become more susceptible to invasion as environmental conditions change and propagule pressure increases. Invasive species displayed high plasticity for traits (Narea, Vmax, ΦPSII) that correlated strongly with biomass across several species, which suggests that invaders in these low resource systems will benefit from N enrichment. Future work should focus on understanding plasticity in environments where plant productivity is limited by multiple interacting factors. As a large proportion of low resource environments are water limited, the influence of water availability on plasticity may be particularly important.