Wendy M. Ridenour

Novel Weapons: Invasive Success and the Evolution of Increased Competitive Ability

When introduced to new habitats by humans, some plant species become much more dominant. This is primarily attributed to escape from specialist consumers. Release from these specialist enemies is also thought by some to lead to the evolution of increased competitive ability, driven by a decrease in the plants resource allocation to consumer defense and an increase in allocation to size or fecundity. Here, we discuss a new theory for invasive success – the “novel weapons hypothesis”. We propose that some invaders transform because they possess novel biochemical weapons that function as unusually powerful allelopathic agents, or as mediators of new plant–soil microbial interactions. Root exudates that are relatively ineffective against their natural neighbors because of adaptation, may be highly inhibitory to newly encountered plants in invaded communities. In other words, the novel weapons of some plant invaders provide them with an advantage that may arise from differences in the regional coevolutionary ...

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.

Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments

Biotic interactions can shape phylogenetic community structure (PCS). However, we do not know how the asymmetric effects of foundation species on communities extend to effects on PCS. We assessed PCS of alpine plant communities around the world, both within cushion plant foundation species and adjacent open ground, and compared the effects of foundation species and climate on alpha (within-microsite), beta (between open and cushion) and gamma (open and cushion combined) PCS. In the open, alpha PCS shifted from highly related to distantly related with increasing potential productivity. However, we found no relationship between gamma PCS and climate, due to divergence in phylogenetic composition between cushion and open sub-communities in severe environments, as demonstrated by increasing phylo-beta diversity. Thus, foundation species functioned as micro-refugia by facilitating less stress-tolerant lineages in severe environments, erasing a global productivity - phylogenetic diversity relationship that would go undetected without accounting for this important biotic interaction.

Plant invasions, generalist herbivores, and novel defense weapons

One commonly accepted mechanism for biological invasions is that species, after introduction to a new region, leave behind their natural enemies and therefore increase in distribution and abundance. However, which enemies are escaped remains unclear. Escape from specialist invertebrate herbivores has been examined in detail, but despite the profound effects of generalist herbivores in natural communities their potential to control invasive species is poorly understood. We carried out parallel laboratory feeding bioassays with generalist invertebrate herbivores from the native (Europe) and from the introduced (North America) range using native and nonnative tetraploid populations of the invasive spotted knapweed, Centaurea stoebe. We found that the growth of North American generalist herbivores was far lower when feeding on C. stoebe than the growth of European generalists. In contrast, North American and European generalists grew equally well on European and North American tetraploid C. stoebe plants, lending no support for an evolutionary change in resistance of North American tetraploid C. stoebe populations against generalist herbivores. These results suggest that biogeographical differences in the response of generalist herbivores to novel plant species have the potential to affect plant invasions.

Oxalate contributes to the resistance of Gaillardia grandiflora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa

Centaurea maculosa Lam. is a noxious weed in western North America that produces a phytotoxin, (±)-catechin, which is thought to contribute to its invasiveness. Areas invaded by C. maculosa often result in monocultures of the weed, however; in some areas, North American natives stand their ground against C. maculosa and show varying degrees of resistance to its phytotoxin. Two of these resistant native species, Lupinus sericeus Pursh and Gaillardiagrandiflora Van Houtte, were found to secrete increased amounts of oxalate in response to catechin exposure. Mechanistically, we found that oxalate works exogenously by blocking generation of reactive oxygen species in susceptible plants and reducing oxidative damage generated in response to catechin. Furthermore, field experiments show that L. sericeus indirectly facilitates native grasses in grasslands invaded by C. maculosa, and this facilitation can be correlated with the presence of oxalate in soil. Addition of exogenous oxalate to native grasses and Arabidopsis thaliana (L.) Heynh grown in vitro alleviated the phytotoxic effects of catechin, supporting the field experiments and suggesting that root-secreted oxalate may also act as a chemical facilitator for plant species that do not secrete the compound.

Is there a risk to living large? Large size correlates with reduced growth when stressed for knapweed populations

A central hypothesis in ecology is that plant life history evolution is constrained by fundamental “compromises between the conflicting selection pressures resulting from particular combinations of competition, stress, and disturbance”, with stress being defined as abiotic conditions that restrict production. Biogeographic differences among native and non-native ranges of invasive plants may provide unique opportunities for tests of this theory. We conducted a greenhouse experiment with Centaurea stoebe plants from North American and European populations. We compared the total biomass and phenotypic plasticity indices for plants from the native and non-native ranges under stressed and non-stressed conditions. The average size of Centaurea stoebe plants from 13 North American populations was greater than that of plants from 18 European populations regardless of stress treatment. However, when plants from the same populations were exposed to lower resources the differences in biomass between plants from North American and European populations were significantly less, suggesting that large plants were poorer stress tolerators. For all 31 populations the regression slope for the relationship between mean mass for populations in non-stressful conditions and mean mass in stressful conditions was less than 1.0, indicating that populations that produced large plants in good conditions also produced plants that grew disproportionately less in stressful conditions. These findings suggest that Centaurea stoebe may be evolving towards being a good “competitor” (sensu Grime, 1977) in its invasive range, but at the cost of being a good “stress tolerator”.