Release of invasive plants from fungal and viral pathogens

Abstract

Invasive plant species both threaten native biodiversity and are economically costly, but only a few naturalized species become pests. Here we report broad, quantitative support for two long-standing hypotheses that explain why only some naturalized species have large impacts. The enemy release hypothesis argues that invaders' impacts result from reduced natural enemy attack. The biotic resistance hypothesis argues that interactions with native species, including natural enemies, limit invaders' impacts. We tested these hypotheses for viruses and for rust, smut and powdery mildew fungi that infect 473 plant species naturalized to the United States from Europe. On average, 84% fewer fungi and 24% fewer virus species infect each plant species in its naturalized range than in its native range. In addition, invasive plant species that are more completely released from pathogens are more widely reported as harmful invaders of both agricultural and natural ecosystems. Together, these results strongly support the enemy release hypothesis. Among noxious agricultural weeds, species accumulating more pathogens in their naturalized range are less widely noxious, supporting the biotic resistance hypothesis. Our results indicate that invasive plants' impacts may be a function of both release from and accumulation of natural enemies, including pathogens.

Conceptual Frameworks and Methods for Advancing Invasion Ecology

“…The latter sometimes even show the opposite pattern of what is predicted (Levine 2000;Stohlgren et al 2003Stohlgren et al , 2006. Second, the enemy release hypothesis (Keane and Crawley 2002), which states that the absence of enemies is one cause of invasion success, is supported by several studies (Wolfe 2002;Mitchell and Power 2003), but questioned by others (Frenzel and Brandl 2003;te Beest et al 2009). …”

“…Studies addressing enemy release can only focus on some of its aspects, and often do so without explicitly discussing this limitation. For example, some studies compare populations of invasive species in the new range to populations of the same species in the indigenous range and quantify infestation, i.e., abundance or diversity of predators or parasites that can be found on the species (Mitchell and Power 2003;Vignon et al 2009). Other studies use the same comparison but quantify damage typically caused by predators, e.g., leaf damage (Lewis et al 2006;Ebeling et al 2008).…”

Roles of parasites in animal invasions

“…The ENEMY RELEASE HYPOTHESIS proposes that invaders lose their (co-evolved) parasites in the process of invasion, leading to higher demographic success of invaders [24,25], which might give them a competitive advantage over natives [26]. Empirical support for this hypothesis comes from observations across a range of taxa, which confirm that invader populations harbour significantly fewer parasites than do native populations [12,24,25].…”

“…Empirical support for this hypothesis comes from observations across a range of taxa, which confirm that invader populations harbour significantly fewer parasites than do native populations [12,24,25]. Although potential mechanisms leading to such patterns are regularly proposed, such as the low probability of parasitized hosts being translocated and the potential for loss of parasites during such movements [24], there is still little empirical discrimination among mechanisms of parasite loss.…”

“…Each of these phases would require separate theoretical and empirical examination because, in one published model, parasite release appears unlikely to affect the chance of an invader becoming established but might affect the spread of an invader [27]. Also, accumulation of parasites over time in invader populations will influence invasion success [25]. Studies of invasive plants have demonstrated this effect [25], however, the impact of parasite accumulation on invasive animals requires further investigation.…”