Enemy release in salt marshes: How herbivorous crabs help an invasive grass to outcompete the native reed

Biological resistance plays a key role in minimizing plant invasions, even when abiotic conditions are favorable for invasion. Through competition with native plants and herbivory by native herbivores, invasive plants can impact ecosystem functions profoundly. While the effect of invasive plants on native plants& performance via competition has been well documented across ecosystems, less is known about the role of facilitation versus inhibition by herbivores in plant invasions, especially in stressful environments. Our main aims were to investigate the role of herbivores (crabs) in plant invasions in coastal wetlands and understand the underlying mechanisms of competition and herbivory on invader performance (i.e., growth and reproduction). We investigated the crabs' effects on the growth (plant mean height, relative growth rate (RGR), and aboveground biomass) and reproduction (sprout density) of the invasive species Spartina alterniflora and the native grass Phragmites australis in East China. Thereto, we conducted a 2-year crab exclusion experiment across three different habitats (low S. alterniflora zone, middle S. alterniflora and P. australis zone, and high P. australis zone) in a salt marsh wetland and a feeding preference trial of crabs in terms of plant traits in the lab. Our results showed that crabs had a strong negative effect on the plant mean height, aboveground biomass, RGR, and sprout regeneration of P. australis in both the high P. australis zone and the middle zone where the two plant species co-occurred. In contrast, the absence of crabs significantly decreased the density of new sprouts of S. alterniflora in both the low S. alterniflora zone and the middle zone. Our lab feeding experiments showed that crabs had a feeding preference for P. australis, as related to its lower total organic carbon content and smaller C/N ratio, and higher N content and N/P ratio compared to S. alterniflora. These findings are consistent with the enemy release hypothesis as opposed to the biological resistance hypothesis. That is to say, S. alterniflora appeared to benefit from not having co-evolved with native herbivorous crabs, hence the preferential feeding by native crabs on P. australis facilitated the success of S. alterniflora introduced to a novel wetland area. Thus, our study provides a new perspective for understanding how native herbivores contribute to the competitive advantage of an invasive plant species to outcompete the native reed through enemy release.