Summary
• This study examined the effects of infection with barley and cereal yellow dwarf viruses (BYDVs) on wild grass species in California, a region in which native perennial bunchgrasses have been largely replaced by exotic annual grasses. We sought to determine whether these widespread viruses compromise the fitness of wild hosts and thus have the potential to influence grassland dynamics. Plant viruses have been long overlooked in ecological studies, and their influence on wild hosts has often been assumed to be minimal.
•We examined the short-term and long-term consequences of infection on field-grown individuals from 18 different populations of wild California grasses (from seven native and one exotic species).
• Barley yellow dwarf virus infection was aggressive in most hosts and markedly impaired host fitness by reducing growth, survivorship, and fecundity.
• Previous work indicates that the presence of exotic grasses can more than double BYDV incidence in natives. Given the ubiquity of BYDVs, our results suggest that apparent competition and other virus-mediated processes may influence interactions among native and exotic grasses and potentially contribute to shifts in grassland community composition.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.2005.01479.x

Virus infection in remnant native bunchgrasses from invaded California grasslands.

The expanding field of plant virus ecology: historical foundations, knowledge gaps, and research directions.

Summary

1
In plant invasion ecology, viruses and other pathogens are often considered in terms of the enemy release hypothesis, which predicts that plants become invasive in new ranges if they escape pathogens from their home range. However, pathogens may sometimes facilitate host spread rather than hinder it.

2
Previously, we hypothesized that apparent competition mediated by barley and cereal yellow dwarf viruses (Luteoviridae: BYDVs, CYDVs) may have facilitated historical grassland invasion in California, USA, where Eurasian grasses displaced native grasses in the 18th and 19th centuries (the disease facilitation hypotheses). However, this could have happened only if the viruses were present during the invasion, which is unknown.

3
To investigate the historical ecology of BYDVs in California grasses, we analysed preserved virus infections in herbarium specimens and used the historical virus sequences to determine rough time estimates of relevant phylogenetic events.

4
The historical viral RNA sequences we identified in invasive and native grasses date from 1917 and are among the oldest recovered from plants thus far and the oldest from North America.

5
Herbarium evidence and phylogenetic analysis suggest that BYDVs were likely to have been present in wild grasses during the California grassland invasion and to have shared some functional characteristics with present-day isolates, supporting the disease facilitation hypothesis.

6
We found evidence of virus spread from California to Australia (or, less likely, from Australia to California) in the late 19th century, when much horticultural exchange occurred, as well as potential correspondence in the timing of virus diversification events and the beginning of extensive human exchange between the Old and New Worlds.

7
Synthesis. Increasing evidence indicates that viruses are important in the ecology of grasslands and may, in some cases, mediate apparent competition among species. Historical data provide essential insight into plant virus ecology and suggest the need to examine human influence on plant virus diversification and spread within natural ecosystems.

Barley yellow dwarf viruses (BYDVs) preserved in herbarium specimens illuminate historical disease ecology of invasive and native grasses

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.

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

We studied the effects of fungal endophyte infection of meadow ryegrass (Lolium pratense=Festuca pratensis) on the frequency of the barley yellow dwarf virus (BYDV). The virus is transferred by aphids, which may be deterred by endophyte-origin alkaloids within the plant. In our experiment, we released viruliferous aphid vectors on endophyte-infected and endophyte-free plants in a common garden. The number of aphids and the percentage of BYDV infections were lower in endophyte-infected plants compared to endophyte-free plants, indicating that endophyte infection may protect meadow ryegrass from BYDV infections.

/pdf/endophytic-fungus-decreases-plant-virus-infections-in-meadow-2fj26dpd8x.pdf

Endophytic fungus decreases plant virus infections in meadow ryegrass (Lolium pratense).

Samples of 2077 grasses and cereal plants representative of the Poaceae found in Tasmania were collected from a wide range of habitats throughout the State. Each sample was examined for infestation with aphids and then checked for infection with viruses causing barley yellow dwarf by both aphid transmission and serological tests. Aphid species found among the samples were Hyalopterus pruni, Rhopalosiphum maidis, R. padi and Sitobion fragariae. R. padi transmitted a vector non-specific type of barley yellow dwarf (PAV) and a vector specific type (RPV), either alone or together, while S. fragariae transmitted PAV alone and occasionally RPV when present in plants together with PAV. The other aphid species did not transmit. A total of 189 samples contained virus. Incidence was greatest in samples from the Bambusoideae subfamily (31%) and least in the Arundinoideae (4%). There was no difference in the level of infection between the native and introduced species that were represented. The Arundinoideae and Panicoideae were predominantly infected with RPV types, while the Pooideae, with the exception of Dactylis glomerata and Poa pratensis, were predominantly infected with PAV types. Many more infected plants contained both PAV and RPV (11.9%) than would have been expected had the two types of virus infected independently (2.5%). No infected plants were found among samples from 25 of the 56 species tested, and some of these may prove useful in breeding for resistance to barley yellow dwarf viruses.

GR Johnstone

Papers

Barley yellow dwarf viruses in, and aphids on, grasses (including cereals) in Tasmania