Dual drivers of plant invasions: Enemy release and enhanced mutualisms

Invasive plants often express aboveground traits, such as higher growth than native plants, which promote their success. This may reflect low levels of invertebrate herbivory and/or high rates of arbuscular mycorrhizal fungi (AMF) association. However, the root traits that contribute to invasive success are less well known. Moreover, the combined roles of aboveground herbivory, AMF and root traits in the invasion process are poorly understood.We conducted field surveys at 17 sites along a latitudinal gradient in China (22.77 °N to 42.48 °N) to investigate the relationships among aboveground herbivory, AMF colonization and root traits for five pairs of closely related invasive and native Asteraceae plant species. We experimentally manipulated aboveground insect feeding for two of these pairs of plant species in a middle latitude (34.79 °N) common garden. We measured aboveground invertebrate abundance, leaf damage, AMF colonization, root morphological traits associated with nutrient uptake, and root soluble sugar concentrations.In the field survey, invasive plants had lower leaf damage and Hemiptera abundances plus higher AMF colonization, thinner roots with more surface area and higher concentrations of root soluble sugars than native plants. Leaf damage decreased with increasing latitude for native plants. In the common garden, invasive plants had lower leaf damage and Hemiptera abundances plus higher AMF and greater surface area of fine roots than native plants. Leaf damage and Hemiptera reduced AMF colonization via a phenotypic effect of reduced fine root soluble sugars.Our results indicate that low aboveground invertebrate herbivory on invasive plants contributes to their success directly by increasing their growth and indirectly via root soluble sugars that increase their AMF colonization. Invasive plants appear to benefit from greater root volume and surface area but this did not vary with latitude or aboveground invertebrate herbivory. These results highlight the importance of considering above- and belowground processes simultaneously to understand how they interact to determine plant invasion success.

Methods
SAS9.4 analyzes the field survey and Common garden data:

We used SAS 9.4 for all analyses. For the field survey, we conducted a series of mixed model ANOVAs to test the dependence of invertebrate chewing damage, AMF colonization, root length density (overall, fine roots, coarse roots), root surface area density (overall, fine, coarse), root tissue density, root average diameter, aboveground mass, belowground mass density, root soluble sugar concentrations (fine, coarse) and invertebrate abundance (Hemiptera or others; Poisson distribution) on the fixed effects latitude (3-level), origin (native or invasive), and their interaction. We analyzed Hemiptera abundance separately because they were mainly sucking herbivores (especially aphids) that do not cause visual damage to leaves. We included the random effects species pair nested in latitude (nested because one pair only occurred at low latitude), location nested in latitude, and plot nested in latitude × location × pair × origin. We used adjusted means post hoc tests to determine differences among means for significant effects with more than two levels. We used Spearman correlations to examine the correlations among variables. We repeated the ANOVAs using only the four Bidens species in the common garden experiment to more closely compare the results of the field survey and common garden experiment.

For the common garden experiment, we tested the dependence of the same set of variables on the fixed effects origin (native and invasive), treatment (open and closed cage), time (July and August), and their interactions in ANOVAs. We included species nested in origin as a random term. We used Spearman correlations to examine the correlations among variables. We conducted another set of analyses to examine the relationships of AMF colonization rate with leaf damage (visual damage to plants which was mostly from chewing), Hemiptera abundance (almost all were sucking herbivores that do not cause visual leaf damage), soluble sugar concentration in fine roots, and fine root surface area. We chose fine root surface area because root morphological traits were strongly correlated and it has a clear mechanistic link to AMF colonization. First, we calculated the average values for each species for each of these four variables to control for differences among species unrelated to our herbivory treatments. Then we used the differences between these average values and measured values to examine the phenotypic relationships among the five variables (i.e., phylogenetically controlled analyses) using regressions for the effects of herbivores on root variables (because we experimentally manipulated aboveground herbivores) and Spearman correlations for the relationships among root variables.