Virus infection and grazing exert counteracting influences on survivorship of native bunchgrass seedlings competing with invasive exotics.

Invasive annual grasses introduced by European settlers have largely displaced native grassland vegetation in California and now form dense stands that constrain the establishment of native perennial bunchgrass seedlings. Bunchgrass seedlings face additional pressures from both livestock grazing and barley and cereal yellow dwarf viruses (B/CYDVs), which infect both young and established grasses throughout the state. Previous work suggested that B/CYDVs could mediate apparent competition between invasive exotic grasses and native bunchgrasses in California. To investigate the potential significance of virus-mediated mortality for early survivorship of bunchgrass seedlings, we compared the separate and combined effects of virus infection, competition and simulated grazing in a field experiment. We infected two species of young bunchgrasses that show different sensitivity to B/CYDV infection, subjected them to competition with three different densities of exotic annuals crossed with two clipping treatments, and monitored their growth and first-year survivorship. Although virus infection alone did not reduce first-year survivorship, it halved the survivorship of bunchgrasses competing with exotics. Within an environment in which competition strongly reduces seedling survivorship (as in natural grasslands), virus infection therefore has the power to cause additional seedling mortality and alter patterns of establishment. Surprisingly, clipping did not reduce bunchgrass survivorship further, but rather doubled it and disproportionately increased survivorship of infected bunchgrasses. Together with previous work, these findings show that B/CYDVs can be potentially powerful elements influencing species interactions in natural grasslands. More generally, our findings demonstrate the potential significance of multitrophic interactions in virus ecology. Although sometimes treated collectively as plant ‘predators’, viruses and herbivores may exert influences that are distinctly different, even counteracting. Keywords: apparent competition, barley yellow dwarf virus, grazing, invasive species, pathogen Introduction European settlers introduced Avena spp. (wild and slender oats), Bromus spp. (bromes) and other annual grasses into California several hundred years ago. In a dramatic example of invasion success, these exotic grasses have almost completely displaced native grassland vegetation, including native perennial bunchgrasses (Clements 1934; Heady 1977; Bartolome et al. 1986; Hamilton 1997). Currently, bunchgrass communities comprise less than 0.1% of valley grassland area (Davis et al. 1998) [estimates for Great Central Valley Region], and most bunchgrass individuals must both compete with dense stands of exotic annuals and contend with grazing by cattle and sheep. Competition for water and light can be intense, with smaller bunchgrasses succumbing to pressure from the quicker growing annuals (Dyer & Rice 1997; Dyer & Rice 1999; Hamilton et al. 1999), and bunchgrass populations are often recruitment limited (Dyer & Rice 1997; Hamilton et al. 1999; Seabloom et al. 2003). However, the capacity of the exotics to intensify resource competition does not fully explain their success and current dominance (Seabloom et al. 2003; Corbin & D’Antonio 2004) and factors such as changes in disturbance patterns may have played influential roles in directing the trajectories of native and exotic species. Viruses may be one such factor shaping grassland dynamics (Malmstrom 1998; Malmstrom et al. 2005a, b). Although a group of generalist aphid-vectored viruses called the barley and cereal yellow dwarf viruses (B/CYDVs; Luteoviridae) have been widespread in California grasses and cereals (Griesbach et al. 1990a; Griesbach et al. 1990b) since 1951 or earlier (Oswald & Houston 1951), they have been largely overlooked in previous studies of grassland ecology. We have established experimentally that BYDV collected from California grasslands can cause notable stunting and loss of fecundity over the short term, and mortality over the long term (several years), in a broad range of native bunchgrasses, in the absence of other environmental constraints (Malmstrom et al. 2005a). We observed similar fecundity loss in established bunchgrass populations with naturally acquired B/CYDV infection (Malmstrom et al. 2005a) and substantial infection-associated mortality in commercial bunchgrass seed production fields (C.M.M., pers. observ.). In addition, we found that exotic annuals such as Avena and Bromus can attract and enhance the fecundity of the aphid vectors for B/CYDVs and substantially increase virus incidence in young bunchgrasses nearby (Malmstrom et al. 2005b). Together, these findings suggest that B/CYDVs could influence grassland dynamics by mediating apparent competition between native and exotic species. In apparent competition, the presence of one host species alters the influence of a shared pathogen (or predator) on a second species and thus indirectly leads to the second species’ decline (Holt 1977). In general, B/CYDV pressure in California appears to be strong and widespread, with some spatial and temporal variation (Oswald & Houston 1951; Griesbach et al. 1990a; Griesbach et al. 1990b), as is typical with B/CYDVs world-wide (Irwin & Thresh 1990). Large aphid flights (Pike et al. 1989) exert broad synoptic virus pressure, while local movement of aphids and virus among neighbouring plants contributes additional variability. B/CYDV incidence can be high: infection rates among young bunchgrasses were found to exceed 70% after only 2 years of exposure to natural virus pressure (Malmstrom et al. 2005b). In established natural populations, rings of infected seedlings can sometimes be found around older, infected bunchgrasses (C.M.M., unpubl. data), suggesting that established plants might serve as reservoirs that increase virus pressure on nearby seedlings. Given the widespread virus pressure in California, and the likelihood that seedlings experience significant exposure in some situations, the goal of this study was to compare the effects of virus infection on bunchgrass seedling with those of two other factors (interspecific competition and grazing) that are recognized as influential in grasslands. To capture the range in variability of bunchgrass response, we infected young individuals of two bunchgrasses species that show different sensitivity to B/CYDV infection (Malmstrom et al. 2005a), subjected them to competition with three different densities (0, low, high) of exotic annuals (Bromus) and to two clipping treatments (+, –) at each density, and monitored their first-year growth and survivorship in a large field experiment. In addition, because the survivorship of bunchgrass seedlings competing with exotics can be strongly influenced by water and light availability (Dyer & Rice 1999; Hamilton et al. 1999), we quantified Bromus’ influence on environmental resources by measuring soil moisture and canopy properties in subplots. We focused on first-year responses to treatments, because bunchgrass populations are often recruitment limited and bunchgrass individuals are particularly vulnerable to competition when they are small (Dyer & Rice 1997; Hamilton et al. 1999; Seabloom et al. 2003). We predicted that infected individuals would survive less well in competitive situations and regrow more poorly after grazing, because B/CYDV infection causes phloem limitations that impair carbohydrate transport (Esau 1957; Irwin & Thresh 1990) and stunt bunchgrasses (Malmstrom et al. 2005a). We thus expected that survivorship would be lowest when bunchgrasses had to contend simultaneously with infection, competition and grazing.