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.