Conservation measures or hotspots of disease transmission? Agri-environment schemes can reduce disease prevalence in pollinator communities

Abstract

Insects are under pressure from agricultural intensification. To protect pollinators, conservation measures such as the EU agri-environment schemes (AES) promote planting wildflowers along fields. However, this can potentially alter disease ecology by serving as transmission hubs or by diluting infections. We tested this by measuring plant–pollinator interactions and virus infections (DWV-A, DWV-B and ABPV) across pollinator communities in agricultural landscapes over a year. AES had a direct effect on DWV-B, reducing prevalence and load in honeybees, with a tentative general dilution effect on load in early summer. DWV-A prevalence was reduced both under AES and with increasing niche overlap between competent hosts, likely via a dilution effect. By contrast, AES had no impact on ABPV, its prevalence driven by the proportion of bumblebees in the community. Epidemiological differences were also reflected in the virus phylogenies, with DWV-B showing recent rapid expansion, while DWV-A and ABPV showed slower growth rates and geographical population structure. Phylogenies indicate that all three viruses freely circulate across their host populations. Our study illustrates how complex interactions between environmental, ecological and evolutionary factors may influence wildlife disease dynamics. Supporting pollinator nutrition can mitigate the transmission of important bee diseases, providing an unexpected boost to pollinator conservation. This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’.

Shift in virus composition in honeybees ( Apis mellifera ) following worldwide invasion by the parasitic mite and virus vector Varroa destructor

“…This genotype is now much more prevalent worldwide (e.g. [30,75]) and is apparently currently replacing DWV-A in varroa-infested honeybee populations royalsocietypublishing.org/journal/rsos R. Soc. Open Sci.…”

“…This genotype is now much more prevalent worldwide (e.g. [ 30 , 75 ]) and is apparently currently replacing DWV-A in varroa-infested honeybee populations [ 44 – 46 ], underscoring the continuing influence of the mite on bee virus epidemiology and evolution. The ability of DWV-B to replicate in the mite [ 76 ], in contrast to DWV-A, which seems to be primarily mechanically transmitted by varroa ([ 77 ], but see [ 78 ]), along with the faster replication of DWV-B in honeybees [ 79 ], might have contributed to the progressive displacement of DWV-A by DWV-B.…”

“…More than 20 000 species of wild bees play critical roles in agriculture and native ecosystems [ 104 ]. Increased viral loads in honeybees in the presence of varroa may lead to undesired spillover to co-foraging insect pollinators or bee predators [ 51 , 68 , 75 , 105 , 106 ], the consequences of which for biodiversity and ecosystem functioning deserve more attention [ 37 ], as do the risks of developing new reservoirs or outbreaks of novel variants [ 107 ]. The development of a global beekeeping industry that includes current strategies of varroa mite control or the development of mite-tolerant honeybees [ 108 , 109 ] should include awareness of multi-host virus dynamics and strategies that mitigate the risk of viral spillover from honeybees to wild bee species and other flower visitors [ 37 , 110 ].…”

Infectious disease ecology and evolution in a changing world

“…This represents a serious threat to poplars and could affect both natural and planted forests. Finally, Manley et al [37] explore how conservation measures to protect pollinators-planting wildflowers along fields-affect disease prevalence in pollinator communities. They found wildflower patches did not act as transmission hubs, but reduced the prevalence of some viral infections, playing an unintended but additional role in pollinator conservation.…”