Do virus‐resistant plants pose a threat to non‐target ecosystems? II. Risk assessment of an Australian pathosystem using multi‐scale field experiments

Abstract

It has been widely argued that the acquisition of novel disease resistance genes by wild host populations following the release of novel pathogen-resistant plants into agricultural systems could pose a significant threat to non-target plant communities. However, predicting the magnitude of ecological release in wild plant populations following the removal of disease remains a major challenge. In this paper we report on the second phase of a tiered risk assessment designed to investigate the role of disease on host growth, survival, fecundity and fitness in a model pathosystem (the pasture species Trifolium repens infected with Clover yellow vein virus, ClYVV) and to assess the level of risk posed to at-risk native plant communities in southeast Australia by newly developed genetically modified and conventionally bred virus-resistant T. repens genotypes. Multi-year field experiments conducted in woodland and grassland environments using host-pathogen arrays derived from 14 ClYVV isolates and 21 T. repens genotypes indicate that viral infection reduces fecundity, growth and survival of wild T. repens plants but that the severity of these effects depends on host tolerance to infection, isolate aggressiveness and specific spatial and temporal environmental conditions. Demographic modelling showed that by reducing host survival and growth, ClYVV also limits the intrinsic population growth rate and niche size of wild T. repens populations. Given the significant fitness cost associated with viral infection we conclude that virus-resistant T. repens genotypes may pose a threat to some high conservation-value non-target ecosystems in SE Australia. We also argue that long-term, multi-tiered experiments conducted in a range of controlled and non-controlled environments are necessary to detect and accurately quantify risks associated with the release of disease-resistant plants in general.

New pasture plants intensify invasive species risk

“…Widespread establishment of enhanced pasture taxa is likely to exacerbate the current environmental weed problem (17,34,35,37). New taxa may interbreed with existing weed populations, with potential to worsen environmental impacts (37)(38)(39).…”

“…New taxa may interbreed with existing weed populations, with potential to worsen environmental impacts (37)(38)(39). Increased genetic diversity in pasture plants and other weeds enhances their capacity to invade natural areas across a broad range of conditions (40)(41)(42).…”

“…For example, in a CO 2 enrichment experiment, Bromus madritensis (introduced for pasture in parts of the United States) (43) rapidly adapted to drier conditions, increasing its potential to spread in arid ecosystems as CO 2 increases (44). Introducing new taxa of existing environmental weeds is therefore likely to increase impacts (35,37) and facilitate spread into areas previously unsuitable due to environmental limitations such as those found in mountains (45) or regions with high salinity (46,47), soil deficiencies (42), low rainfall (44), or low temperature (48).…”

“…Accurate assessment also depends on accurate information. Therefore, a second priority is to develop and routinely apply improved methods for assessing environmental weed risks, such as tiered approaches that use field and glasshouse trials, species distribution modeling, and weed risk assessment questionnaires (37,65).…”

“…natural areas, risks associated with particular plant characteristics (updated regularly as new research is completed), and evidence from experimental trials (37,69,70); (iii) a strong postrelease monitoring program for early detection and rapid control (necessary because it remains difficult to accurately predict which species will become environmental weeds despite research gains in this area; 23,71,72); and (iv) if a taxon becomes an environmental weed, industry pays for its management, with costs allocated to industry organizations, government and private plant breeders, seed companies, and farmers relative to their culpability and ability to pay (Fig. 3).…”