Yu-Long Feng

Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant

Many studies have shown that individuals from invasive populations of many different plant species grow larger than individuals from native populations and that this difference has a genetic basis. This increased vigor in invasive populations is thought to be due to life history tradeoffs, in which selection favors the loss of costly defense traits, thereby freeing resources that can be devoted to increased growth or fecundity. Despite the theoretical importance of such allocation shifts for invasions, there have been no efforts to understand apparent evolutionary shifts in defense-growth allocation mechanistically. Reallocation of nitrogen (N) to photosynthesis is likely to play a crucial role in any growth increase; however, no study has been conducted to explore potential evolutionary changes in N allocation of introduced plants. Here, we show that introduced Ageratina adenophora, a noxious invasive plant throughout the subtropics, appears to have evolved increased N allocation to photosynthesis (growth) and reduced allocation to cell walls, resulting in poorer structural defenses. Our results provide a potential mechanism behind the commonly observed and genetically based increase in plant growth and vigor when they are introduced to new ranges.

NO EVIDENCE FOR TRADE-OFFS: CENTAUREA PLANTS FROM AMERICA ARE BETTER COMPETITORS AND DEFENDERS

The natural enemies hypothesis has led to a number of ideas by which invaders might evolve superior competitive ability. In this context, we compared growth, reproduction, competitive effect, competitive response, and defense capabilities between invasive North American populations of Centaurea maculosa and populations in Europe, where the species is native. We found that Centaurea from North America were larger than plants from European populations. North American Centaurea also demonstrated stronger competitive effects and responses than European Centaurea. However, competitive superiority did not come at a cost to herbivore defense. North American plants were much better defended against generalist insect herbivores and slightly better defended against specialists. North Americans showed a stronger inhibitory effect on the consumers (resistance) and a better ability to regrow after attack by herbivores (tolerance). Better defense by North Americans corresponded with higher constitutive levels of a biochemical defense compound precursor, tougher leaves, and more leaf trichomes than Europeans. North American F1 progeny of field collected lines retained the traits of larger size and greater leaf toughness suggesting that genetic differences, rather than maternal effects, may be the cause of intercontinental differences, but these sample sizes were small. Our results suggest that the evolution of increased competitive ability may not always be driven by physiological trade-offs between the allocation of energy or resources to growth or to defense. Instead, we hypothesize that Centaurea maculosa experiences strong directional selection on novel competitive and defense traits in its new range.

Novel weapons and invasion: biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate (±)-catechin

Recent studies suggest that the invasive success of Centaurea maculosa may be related to its stronger allelopathic effects on native North American species than on related European species, one component of the “novel weapons” hypothesis. Other research indicates that C. maculosa plants from the invasive range in North America have evolved to be larger and better competitors than conspecifics from the native range in Europe, a component of the “evolution of increased competitive ability” hypothesis. These hypotheses are not mutually exclusive, but this evidence sets the stage for comparing the relative importance of evolved competitive ability to inherent competitive traits. In a competition experiment with a large number of C. maculosa populations, we found no difference in the competitive effects of C. maculosa plants from North America and Europe on other species. However, both North American and European C. maculosa were much better competitors against plants native to North America than congeners native to Romania, collected in areas where C. maculosa is also native. These results are consistent with the novel weapons hypothesis. But, in a second experiment using just one population from North America and Europe, and where North American and European species were collected from a broader range of sites, competitive interactions were weaker overall, and the competitive effects of C. maculosa were slightly stronger against European species than against North American species. Also consistent with the novel weapons hypothesis, (±)-catechin had stronger effects on native North American species than on native European species in two experiments. Our results suggest that the regional composition of the plant communities being invaded by C. maculosa may be more important for invasive success than the evolution of increased size and competitive ability.

Specific leaf area relates to the differences in leaf construction cost, photosynthesis, nitrogen allocation, and use efficiencies between invasive and noninvasive alien congeners

Comparisons between invasive and native species may not characterize the traits of invasive species, as native species might be invasive elsewhere if they were introduced. In this study, invasive Oxalis corymbosa and Peperomia pellucida were compared with their respective noninvasive alien congeners. We hypothesized that the invasive species have higher specific leaf (SLA) than their respective noninvasive alien congeners, and analyzed the physiological and ecological consequences of the higher SLA. Higher SLA was indeed the most important trait for the two invaders, which was associated with their lower leaf construction cost, higher nitrogen (N) allocation to photosynthesis and photosynthetic N use efficiency (PNUE). The higher N allocation to photosynthesis of the invaders in turn increased their PNUE, N content in photosynthesis, biochemical capacity for photosynthesis, and therefore light-saturated photosynthetic rate. The above resource capture-, use- and growth-related traits may facilitate the two invaders’ invasion, while further comparative studies on a wider range of invasive and noninvasive congeners are needed to understand the generality of this pattern and to fully assess the competitive advantages afforded by these traits.

Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species.

The general-purpose genotype hypothesis and the hypothesis of the evolution of invasiveness predict that invasive species are characterized by particular traits that confer invasiveness. However, these traits are still not well-defined. In this study, ecophysiological traits of eight populations of the invasive shrub Buddleja davidii from a wide range of European locations and five co-occurring native woody species in Germany were compared in a common garden experiment. We hypothesized that the invader has higher resource capture ability and utilization efficiency than the natives. No differences were detected among the eight populations of B. davidii in any of the traits evaluated, indicating that the invader did not evolve during range expansion, thus providing support to the general-purpose genotype hypothesis. The invader showed significantly higher maximum electron transport rate, maximum carboxylation rate, carboxylation efficiency, light-saturated photosynthetic rate (Pmax) and photosynthetic nitrogen utilization efficiency (PNUE) than the five natives. Leaf nitrogen content was not significantly different between the invader and the natives, but the invader allocated more nitrogen to the photosynthetic machinery than the natives. The increased nitrogen content in the photosynthetic machinery resulted in a higher resource capture ability and utilization efficiency in the invader. At the same intercellular CO2 concentration, Pmax was significantly higher in the invader than in the natives, again confirming the importance of the higher nitrogen allocation to photosynthesis. The invader reduced metabolic cost by increasing the ratio of Pmax to dark respiration rate (Rd), but it did not reduce carbon cost by increasing the specific leaf area and decreasing leaf construction cost. The higher nitrogen allocation to the photosynthetic machinery, Pmax, PNUE and Pmax/Rd may facilitate B. davidii invasion, although studies involving a wide range of invasive species are needed to understand the generality of this pattern and to fully assess the ecological advantages afforded by these features.

Volatile chemicals from leaf litter are associated with invasiveness of a Neotropical weed in Asia

Some invasive plant species appear to strongly suppress neighbors in their nonnative ranges but much less so in their native range. We found that in the field in its native range in Mexico, the presence of Ageratina adenophora, an aggressive Neotropical invader, was correlated with higher plant species richness than found in surrounding plant communities where this species was absent, suggesting facilitation. However, in two nonnative ranges, China and India, A. adenophora canopies were correlated with much lower species richness than the surrounding communities, suggesting inhibition. Volatile organic compound (VOC) signals may contribute to this striking biogeographical difference and the invasive success of A. adenophora. In controlled experiments volatiles from A. adenophora litter caused higher mortality of species native to India and China, but not of species native to Mexico. The effects of A. adenophora VOCs on seedling germination and growth did not differ between species from the native range and species from the nonnative ranges of the invader. Litter from A. adenophora plants from nonnative populations also produced VOCs that differed quantitatively in the concentrations of some chemicals than litter from native populations, but there were no chemicals unique to one region. Biogeographic differences in the concentrations of some volatile compounds between ranges suggest that A. adenophora may be experiencing selection on biochemical composition in its nonnative ranges.

Growth, biomass allocation, morphology, and photosynthesis of invasive Eupatorium adenophorum and its native congeners grown at four irradiances

Eupatorium adenophorum is one of the more noxious invasive plants worldwide. However, the mechanisms underlying its invasiveness are still not well elucidated. In this study, we compared the invader with its two native congeners (E. heterophyllum and E. japonicum) at four irradiances in terms of growth, biomass allocation, morphology, and photosynthesis. The higher light-saturated photosynthetic rate (Pmax) and total leaf area of the invader may contribute to its higher relative growth rate (RGR) and total biomass compared with its native congeners. Total biomass and RGR increased significantly with the increase of Pmax and total leaf area. The higher support organ mass fraction and the lower root mass fraction of the invader may also contribute to its higher RGR and biomass through increasing carbon assimilation and reducing respiratory carbon loss, respectively. The higher growth rate of the invader increased its total leaf area, ramet number, and crown area. These traits may help the invader to form dense monoculture, outshading native plant species. However, consistently higher leaf area ratio, specific leaf area, and leaf mass fraction were not found across irradiances for the invader compared with its native congeners. Higher plasticity in response to irradiance was also not found for the invader. The invader retained advantages over the natives across irradiances, while its performance decreased with lower irradiance. The results indicate that the invader may be one of the few super invaders. Reducing irradiance may inhibit its invasions.

Photosynthesis, nitrogen allocation and specific leaf area in invasive Eupatorium adenophorum and native Eupatorium japonicum grown at different irradiances

The mechanisms underlying biological invasions are still not well elucidated. In this study, ecophysiological traits of invasive Eupatorium adenophorum and native E. japonicum were compared at 10 irradiances in field. I hypothesized that the invader may allocate a higher fraction of leaf nitrogen (N) to photosynthesis and have higher light-saturated photosynthetic rate (P(max)) and specific leaf area (SLA) than E. japonicum. The invader had a significantly higher ability to acclimate to high irradiance than E. japonicum, while it showed a similar shade-tolerant ability. The invader indeed allocated a higher fraction of leaf N to photosynthesis than E. japonicum, which, with its high leaf N content (N(A)), resulted in a higher N content in photosynthesis (N(P)), contributing to its higher biochemical capacity for photosynthesis and P(max). However, the invader had a significantly lower SLA than E. japonicum, contributing to its higher P(max) but increasing its area-based leaf construction cost. The abilities to acclimate to a wider range of irradiance and to allocate a higher fraction of leaf N to photosynthesis, and the higher P(max), N(A), N(P) and leaf area ratio may contribute to the invasion of the invader. High SLA is not always necessary for invasive species.

Photosynthetic characteristics, dark respiration, and leaf mass per unit area in seedlings of four tropical tree species grown under three irradiances

We investigated the effect of growth irradiance (I) on photon-saturated photosynthetic rate (Pmax), dark respiration rate (RD), carboxylation efficiency (CE), and leaf mass per unit area (LMA) in seedlings of the following four tropical tree species with contrasting shade-tolerance. Anthocephalus chinensis (Rubiaceae) and Linociera insignis (Oleaceae) are light-demanding, Barringtonia macrostachya (Lecythidaceae) and Calophyllum polyanthum (Clusiaceae) are shade-tolerant. Their seedlings were pot-planted under shading nets with 8, 25, and 50 % daylight for five months. With increase of I, all species displayed the trends of increases of LMA, photosynthetic saturation irradiance, and chlorophyll-based Pmax, and decreases of chlorophyll (Chl) content on both area and mass bases, and mass-based Pmax, RD, and CE. The area-based Pmax and CE increased with I for the light-demanders only. Three of the four species significantly increased Chl-based CE with I. This indicated the increase of nitrogen (N) allocation to carboxylation enzyme relative to Chl with I. Compared to the two shade-tolerants, under the same I, the two light-demanders had greater area- and Chl-based Pmax, photosynthetic saturation irradiance, lower Chl content per unit area, and greater plasticity in LMA and area- or Chl-based Pmax. Our results support the hypothesis that light-demanding species is more plastic in leaf morphology and physiology than shade-tolerant species, and acclimation to I of tropical seedlings is more associated with leaf morphological adjustment relative to physiology. Leaf nitrogen partitioning between photosynthetic enzymes and Chl also play a role in the acclimation to I.

Nitrogen allocation, partitioning and use efficiency in three invasive plant species in comparison with their native congeners.

In this study, we hypothesized that invasive species may allocate a higher fraction of leaf nitrogen (N) to photosynthesis than phylogenetically related native species. To test this hypothesis, we determined N allocation and other ecophysiological traits of three invasive species in comparison with their respective native congeners by measuring response curves of photosynthesis to intercellular CO2 concentration. The invasive species of Peperomia and Piper indeed allocated a higher fraction of leaf N to photosynthesis and were more efficient in photosynthetic N (NP) partitioning than their native congeners. The two invasive species partitioned a higher fraction of NP to carboxylation and showed a higher use efficiency of NP, while their native congeners partitioned a higher fraction of NP to light-harvesting components. The higher N allocation to photosynthesis and the higher NP partitioning to carboxylation in the two invaders were associated with their higher specific leaf area. Nitrogen allocation and partitioning were the most important factors in explaining the differences in light-saturated photosynthetic rate and photosynthetic N use efficiency (PNUE) between the two invasive species and their native congeners. The differences in N allocation-related variables between the invasive and native species of Amaranthus could not be evaluated in this study due to the method. Except PNUE, resource capture- and use-related traits were not always higher in all three invasive species compared to their native congeners, indicating that different invasive species may have different syndrome of traits associated with its invasiveness.