Agriculture changes plant disease dynamics in nearby wild plants

The term “biological diversity” was first used in 1916 by J. Arthur Harris in AAAS’s The Scientific Monthly journal but the word “biodiversity” has only been used in publications since 1988. Today, everyone is familiar with it. Over the last year, scientists and policymakers have highlighted that protecting biodiversity is vital for human health and avoiding the future global pandemics. Agriculture is one of the main drivers of destroying or reducing biodiversity around the world and leads to simplified landscapes. Across these landscapes, crop diseases can quickly establish and spread. Biodiversity can either increase (e.g., more specialised diseases, alternative plant hosts for generalists) or decrease (e.g., less spread, more resilient hosts) infection risk. The role of biodiversity on plant diseases for wild plants has not often been investigated.

Drs Hanna Susi and Anna-Liisa Laine from the Universities of Helsinki and Zurich investigated the relationship between biodiversity and viral infection in 27 ribwort plantain (Plantago lanceolata) populations close to, and far away from agricultural fields in Finland. The researchers found relatively more diverse viral communities at the edges of fields and fewer infections at sites with higher plant diversity. This study suggests that infection dynamics (virus species diversity and infection rate) in wild plant populations are altered by crop cultivation. The researchers previously developed metagenomic tools to identify five ribwort plantain viruses,  and recently found that plantain genotype is the key determinant of virus community structure.

In the latest study, Susi and Laine sampled 15 ribwort plantain populations (agricultural edge) within a distance of 20 m of agricultural fields and 12 populations (natural ) that were 200 m away from any crop or pasture, across a highly fragmented landscape in Finland. The scientists collected 267 plant samples and were screened for two DNA viruses (Plantago lanceolata latent virus, Plantago latent caulimovirus) and three RNA viruses (Plantago betapartitivirus, Plantago enamovirus and Plantago closterovirus).  Around each sampled plant, the plant diversity and richness were recorded within 0.5 m² plots. Spatial connectivity between ribwort plantain populations was calculated, and soil N and P were measured.

Almost 60% of  the 267 samples plants were infected by one or more viruses, the most common virus being Plantago latent caulimovirus. Overall, 151 plant species were identified in the plots and infection prevalence negatively correlated with plant diversity, suggesting the biodiversity decreases disease risk in wild ribwort plantain populations. Whilst plant diversity and richness did not differ between the agricultural edge and natural populations, more virus species were found at the edges. 

“Consistent with our predictions, we find more diverse virus communities in host populations close to cultivated fields”, Susi and Laine wrote.

“Moreover, we find that agricultural land use can alter the mechanisms by which host species richness regulates disease pressure and richness in wild plant populations.”

Soil N and P levels were much higher around the fields compared to the natural sites.
This nutrient spillover could have made the ribwort plantains “more attractive and tasty” to insects that could have carried viruses. Three of the viruses found in this study belong to families (Caulimoviridae, Luteoviridae and Closteroviridae) that are generalists and can infect crops. 

“[W]e propose that the lack of dilution effect [biodiversity decreasing disease risk] in lands adjacent to agricultural fields may be due to a combination of infection spillover – of potentially different virus isolates – from crops to the natural environments, and altered vulnerability in plant populations subjected to leached agrochemicals”.

Population connectivity was suggested to be the driver of virus infections. Well-connected populations had lower infection rates, probably due to higher genetic diversity as ribwort plantains are wind pollinated and populations near each other could cross-pollinate. 

This study showed that agricultural land use changed the viral disease dynamics in a widespread plant and biodiversity reduced infection rates. Landscape management can be optimised by understanding how biodiversity and population connectivity can reduce plant disease epidemics.