INTRODUCTION

Interspecies disease transmission can have profound impacts on human and animal health , as strikingly evidenced by the recent Covid-19 pandemic. Emerging infectious diseases have been linked with rapid declines of global entomofauna , where disease transmissions between domesticated animals and wildlife populations are of particular concern . Globally traded managed western honey bees (Apis mellifera ) suffer from a range of emerging pathogens . Thereby, they may act as an important source of pathogens for wild arthropods with whom they share the environment . Overlapping ranges, niches and behaviors promote cross-species disease transmission . Thus, commercial pollinators have been mentioned as key drivers of disease emergence in other beneficial insects and pathogen spillover from honey bees is a possible cause for the decline of wild pollinators, including bumble bees (Bombusspp., .
RNA viruses have a high potential to cross species barriers due to their large population sizes and error prone replication that enable rapid adaptive change . Many (RNA) viruses that were first described in honey bees have been subsequently detected across the wider arthropod community . Based on the co-occurrence of viruses and shared viral strands within a site, frequent interspecific virus transmission is suspected, especially between honey bees and bumble bees . In contrast to burgeoning evidence for the occurrence of honey bee associated viruses in other arthropods, knowledge on their impacts in alternative hosts is limited .
The few studies that investigated pathogenicity outside of honey bees report potential clinical symptoms in Bombus spp. (Vespa crabro , , ants (Lasius niger , , and spiders (Agelena labyrinthica , . However, except for wing deformities in field-observations – a clinical symptom associated with Deformed wing virus (DWV) – reports on pathogenicity are based on laboratory worst case scenarios with exposure (injection, feeding) to copious amounts of viral copies (e.g., . Thus, it remains unclear if pollinator populations in the field are affected by frequent exposure to viruses from managed honey bees, as claimed in the literature .
When investigating potential impacts of viruses on wild bee populations, it is important to consider additional stressors affecting their fitness and resilience. Among the most important drivers of current insect declines are habitat loss and fragmentation . Habitat loss and fragmentation often lead to homogenized landscapes poor in floral resources and, in consequence, lowered pollinator abundance and species diversity . Fragmented agroecological systems pose a particular challenge to biodiversity, not only in regards of their landscape composition and configuration, but also in terms of pollution through agrochemicals . Consequently, pollinators inhabiting such landscapes are inevitably faced with multiple intertwined stressors, which may reinforce each other’s adverse effects . In fact, both nutritional stress and exposure to pesticides have been shown to impact honey bee immune pathways , potentially leading to synergistic stressor effects, as suppression of insect immune systems can increase pathogen susceptibility . Furthermore, habitat composition and configuration in fragmented landscapes influence transmission dynamics of infectious diseases via shared floral resources, which act as viral hotspots and are the most likely route for cross-species virus transmission among pollinators
The probability of susceptible hosts being exposed is likely increased in fragmented landscapes with limited and spatially clumped floral resources . Second, essential floral resources can increase the tolerance of the hosts to withstand pathogens , since the availability of high quality and diversity pollen and nectar resources positively influences bee health and reduces pathogen susceptibility . Hence, host responses to landscape structure or increased floral numbers, e.g., through altered foraging patterns or diet breadth (Gómez-Martínez et al. 2022), may shape pathogen prevalence and disease outbreaks in bee communities . While modelling suggests that benefits from floral resources, corridors and other connections may outweigh the possible risks of increased pathogen transmission , empirical studies linking landscape structure and disease transmission, and their impact on pollinator fitness, are lacking because controlled experimental manipulations of landscapes, target hosts and pathogens, are often infeasible .
Here, we take advantage of the intensive viticulture to study how landscape structure affects viral load dynamics in bumble bee field colonies, and how this is linked to colony development. More specifically, we asked i) how the composition of viruses in bumble bee colonies changes following exposure to the environment; ii) if and how the most dominant viruses are correlated with colony development; and iii) whether the landscape structure affects the viral load, richness, and turnover in bumble bee colonies.