Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses

Abstract

In California valley grasslands, Avena fatua L. and other exotic annual grasses have largely displaced native perennial bunchgrasses such as Elymus glaucus Buckley and Nassella pulchra (A. Hitchc.) Barkworth. The invasion success and continued dominance of the exotics has been generally attributed to changes in disturbance regimes and the outcome of direct competition between species. Here, we report that exotic grasses can also indirectly increase disease incidence in nearby native grasses. We found that the presence of A. fatua more than doubled incidence of infection by barley and cereal yellow dwarf viruses (B/CYDVs) in E. glaucus. Because B/CYDV infection can stunt E. glaucus and other native bunchgrasses, the indirect effects of A. fatua on virus incidence in natives suggests that apparent competition may be an additional mechanism influencing interactions among exotic and native grasses in California. A. fatua's influence on virus incidence is likely mediated by its effects on populations of aphids that vector B/CYDVs. In our study, aphids consistently preferred exotic annuals as hosts and experienced higher fecundity on them, suggesting that the exotics can attract and amplify vector populations. To the best of our knowledge, these findings are the first demonstration that exotic plants can indirectly influence virus incidence in natives. We suggest that invasion success may be influenced by the capacity of exotic plant species to increase the pathogen loads of native species with which they compete.

Landscape epidemiology of plant diseases

“…More generally, the indirect effects on the abundance of one species caused by the presence of a second one mediated by shared pathogens or predators (apparent competition) is recognized as an important factor influencing community dynamics and vegetation patterns (Morris et al 2004). It may account for the invasion success of exotic annual grasses in California Valley grasslands (Malmstrom et al 2005). Conversely, an alternative host could act as a sink, contributing to the decrease in the prevalence in the focal species.…”

Pathogen-induced reversal of native dominance in a grassland community

“…Although several mechanisms have been suggested to explain the apparent enigma in which an inferior competitor has invaded and remained numerically dominant across much of California for more than a century (e.g., grazing, rainfall changes, and perennial seed limitation; see refs. 10 and 13), disease has only recently been suggested as a potential factor in this invasion (14). Although it has been shown that invasion by annual grasses can increase the prevalence of a viral pathogen (14), there have been no quantitative tests to determine whether these effects could alter the long-term competitive dominance hierarchy of native and exotic grasses in California.…”

“…10 and 13), disease has only recently been suggested as a potential factor in this invasion (14). Although it has been shown that invasion by annual grasses can increase the prevalence of a viral pathogen (14), there have been no quantitative tests to determine whether these effects could alter the long-term competitive dominance hierarchy of native and exotic grasses in California. Here, we develop a dynamical model that uses field-based parameter estimates to examine whether the invasion by nonnative annual grasses may have altered the long-term community-wide dynamics of a globally distributed generalist virus of grasses, resulting in widespread invasion and persistent domination of the California grassland flora by a suite of otherwise competitively inferior introduced grasses from southern Europe.…”

“…Based on experimental and observational data, it has been suggested that pathogens may allow invasion by a species previously excluded by direct competition in communities as wideranging as monkeys, mussels, and grasslands (14,23,24); however, short-term studies tell us little about the ultimate outcome of interactions among potentially long-lived species (25). To our knowledge, there have been no studies that use models fitted with field-estimated parameters to examine the long-term demographic implications of this potentially widespread phenomenon (17).…”

Disease in Natural Plant Populations, Communities, and Ecosystems: Insights into Ecological and Evolutionary Processes

“…7A). The presence of the annual exotic Avena fatua increases spring populations of aphid vectors and leads to the doubling of BYDV incidence in native grasses (79) (Fig. 7B).…”