Trait Values, Not Trait Plasticity, Best Explain Invasive Species' Performance in a Changing Environment

<div><p>The question of why some introduced species become invasive and others do not is the central puzzle of invasion biology. Two of the principal explanations for this phenomenon concern functional traits: invasive species may have higher values of competitively advantageous traits than non-invasive species, or they may have greater phenotypic plasticity in traits that permits them to survive the colonization period and spread to a broad range of environments. Although there is a large body of evidence for superiority in particular traits among invasive plants, when compared to phylogenetically related non-invasive plants, it is less clear if invasive plants are more phenotypically plastic, and whether this plasticity confers a fitness advantage. In this study, I used a model group of 10 closely related <em>Pinus</em> species whose invader or non-invader status has been reliably characterized to test the relative contribution of high trait values and high trait plasticity to relative growth rate, a performance measure standing in as a proxy for fitness. When grown at higher nitrogen supply, invaders had a plastic RGR response, increasing their RGR to a much greater extent than non-invaders. However, invasive species did not exhibit significantly more phenotypic plasticity than non-invasive species for any of 17 functional traits, and trait plasticity indices were generally weakly correlated with RGR. Conversely, invasive species had higher values than non-invaders for 13 of the 17 traits, including higher leaf area ratio, photosynthetic capacity, photosynthetic nutrient-use efficiency, and nutrient uptake rates, and these traits were also strongly correlated with performance. I conclude that, in responding to higher N supply, superior trait values coupled with a moderate degree of trait variation explain invasive species' superior performance better than plasticity per se.</p> </div

Correlation of trait values and plasticity indices with performance.

<p>Trait abbreviations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048821#pone-0048821-t001" target="_blank">Table 1</a>. Pearson product-moment correlations (r) and p-values (p) for the relationship between mean trait values or mean plasticity index and mean RGR. Mean values are the average of the two nutrient treatments. The bottom three rows represent correlations between mean RGR and a combined plasticity index drawn from several traits (see text). Boldface denotes p-values less than.05; § denotes p-values significant at α = .05 when corrected for 17 multiple comparisons by the Benjamini-Hochberg procedure for individual traits or indices, and for 3 multiple comparisons for grouped plasticity indices. After elimination of an outlier for SMR plasticity (see text), the correlation coefficient r = .76557 and p = .0448 (non-significant).</p

Plasticity indices (PI_v) for invasive and non-invasive species.

<p>Trait abbreviations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048821#pone-0048821-t001" target="_blank">Table 1</a>. Test statistics (t) and p-values (p) are from Student's t-test for unequal variances; p-values in boldface are <.05. The bottom three rows represent mean values for combined indices with several traits' plasticity indices averaged together by species (see also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048821#pone-0048821-g003" target="_blank">Figure 3</a>). No plasticity indices for individual traits were significantly different between invasive and non-invasive groups after Benjamini-Hochberg correction for 17 trait comparisons, nor were grouped indices significantly different after correction for three comparisons. Means, standard errors, and test statistics were calculated using the PI_v, which represents the absolute value of the change in trait value between N treatments, but a second index, the RTR, was used to determine the directionality of the response, which is indicated to the right of each PI_v column for individual traits. “Increase” means that all species in the group increased the trait value in response to increased N; “decrease” means that all species in the group decreased the trait value; and “mixed” means that at least one increase and one decrease were observed in the species group. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048821#pone.0048821.s002" target="_blank">Table S2</a> in the Supplementary Information shows RTR values for all traits and all species.</p

Differences in mean plasticity between invasive and non-invasive species by trait grouping.

<p>Values are means ± standard error for invasive and non-invasive species, where the plasticity indices of several traits in a grouping have been averaged together for each of the 5 invasive and 5 non-invasive species. For the biomass allocation grouping, each species' value is its mean plasticity index for the traits LMR, SMR, RMR and LAR; for the leaf-level grouping, each species' value is its mean plasticity index for the traits SLA, DMF, P_area, N_area, chl_area, protein_area, A_area, and g_s; and for the whole-plant grouping, each species' value is its mean plasticity index for the traits PNUE, WUEi, SAR_N, and SAR_P. After correction for multiple comparisons, no differences were statistically significant.</p

Descriptions of traits and performance measure (fitness proxy).

<p>Descriptions of traits and performance measure (fitness proxy).</p

ANOVA and ANCOVA statistics for trait values.

<p>Trait abbreviations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048821#pone-0048821-t001" target="_blank">Table 1</a>. Test statistics are for mixed-model, nested ANOVAs using “nitrogen level” and “invasive status” as fixed effects and “species” nested in “invasive status” as a random effect, except biomass allocation traits (top 4 rows), which were analyzed as mixed-model nested ANCOVAs with final harvest biomass as a covariate. Boldface denotes p-values less than.05; § denotes p-values significant at α = .05 when corrected for 17 comparisons by the Benjamini-Hochberg procedure.</p

Performance (RGR) of invasive and non-invasive species across nutrient treatments.

<p>Values are means ± standard error of invasive and non-invasive species groups in low-N and high-N treatment.</p

Trait reaction norms for invasive and non-invasive species across nutrient treatments.

<p>Dotted line  =  invasive species; solid line = non-invasive species. Trait abbreviations are as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048821#pone-0048821-t001" target="_blank">Table 1</a>. For each trait, the line links the mean in the low-N treatment to the mean in the high-N treatment, so steeper slopes indicate greater relative responses to the change in nutrient supply.</p

Stress Tolerance and Ecophysiological Ability of an Invader and a Native Species in a Seasonally Dry Tropical Forest

<div><p>Ecophysiological traits of <i>Prosopis juliflora</i> (Sw.) DC. and a phylogenetically and ecologically similar native species, <i>Anadenanthera colubrina</i> (Vell.) Brenan, were studied to understand the invasive species’ success in caatinga, a seasonally dry tropical forest ecosystem of the Brazilian Northeast. To determine if the invader exhibited a superior resource-capture or a resource-conservative strategy, we measured biophysical and biochemical parameters in both species during dry and wet months over the course of two years. The results show that <i>P. juliflora</i> benefits from a flexible strategy in which it frequently outperforms the native species in resource capture traits under favorable conditions (e.g., photosynthesis), while also showing better stress tolerance (e.g., antioxidant activity) and water-use efficiency in unfavorable conditions. In addition, across both seasons the invasive has the advantage over the native with higher chlorophyll/carotenoids and chlorophyll a/b ratios, percent N, and leaf protein. We conclude that <i>Prosopis juliflora</i> utilizes light, water and nutrients more efficiently than <i>Anadenanthera colubrina</i>, and suffers lower intensity oxidative stress in environments with reduced water availability and high light radiation.</p></div

Nutrient content in leaves of native (<i>Anadenanthera colubrina</i>) and invasive (<i>Prosopis juliflora</i>) species in a tropical dry forest in Brazil across seasons.

<p><i>Different letters on the same line denote statistical differences by Newman-Keul test with significance level of 5 percent between variables.</i></p><p>Values represent the average of replicates (n = 5±SE).</p