INTRODUCTION
Recent declines in native and managed bee populations threaten the
stability of pollination services that are vital for maintaining natural
and agricultural ecosystems (Beismeijer et al. 2006, Potts et al. 2010).
Several factors contribute to these declines, including the spread of
multi-host pathogens, habitat loss, and climate change (Ricketts et al.
2008, Burkle et al. 2013, Furst et al. 2014). Losses in pollinator
community biodiversity and abundance lead to changes in flower
visitation patterns (Beismeijer et al. 2006, Albrecht et al. 2012,
Burkle et al. 2013), as well as changes in the risk of infectious
disease within reduced pollinator communities (Figueroa et al. 2020,
Graystock et al. 2020, Fearon and Tibbetts 2021). Yet, it remains
unclear how differences in floral visitation behaviors within pollinator
communities affected by these declines may in turn affect the spread of
pathogens.
Many pollinator pathogens and parasites (hereafter, ‘parasites’) are
transmitted within and among species by visitation to flowers that were
previously visited by infected bees (Durrer and Schmid-Hempel 1994,
Graystock et al. 2015, Müller et al. 2019, Purkiss and Lach 2019). The
likelihood of parasite deposition and subsequent transmission on flowers
depends on multiple factors, including flower traits, flower morphology,
pollinator behavior, and the environment (Durrer and Schmid-Hempel 1994,
Alger et al. 2019, Figueroa et al. 2019, Russell et al. 2019). Depending
on the parasite, different plant components, including the floral
tissue, pollen, and nectar, are implicated in transmission among
pollinators (reviewed by McArt et al. 2014). In particular, differences
in the rates of parasite deposition and acquisition of microorganisms on
various flower parts may depend on how bees interact with the flowers
during foraging visits. For example, bees foraging for pollen had
greater rates of microbe deposition and acquisition on flowers than did
bees foraging for nectar (Russell et al. 2019). However, pollinator
visitation behaviors have been shown to have a complex relationship with
the prevalence of bee parasites on flowers. In a study on pollinator
viruses, flowers receiving longer visits were more likely to host
viruses, but those with high visitation rates were less likely to host
viruses (Alger et al. 2019). In a different study, Crithidia
bombii survived longer when deposited inside the corolla rather than on
the bract, but infection occurring from an encounter with the bract
resulted in more intense infection (Figueroa et al. 2019). Therefore,
the ways in which infected bees interact with specific flower features
and the duration and frequency of their visits will alter the likelihood
of parasite deposition on floral surfaces and influence the probability
of infection for later visitors. However, most studies on this topic
have been conducted in the laboratory and have not fully considered the
potential for parasite transmission via shared floral resources in
natural settings.
Agricultural fields and the surrounding hedgerows may represent
potential ‘hot spots’ for parasite transmission within and among bee
species on shared floral resources. Managed honeybees (Apis
mellifera) are frequently brought to agricultural fields to provide
pollination services, where they have ample opportunity to interact with
wild pollinators that are also attracted to plentiful crop flowers or
nearby hedgerows with wildflowers (Goulson and Hughes 2015). The
worldwide dispersal of A. mellifera (hereafter honeybees) and its
many parasites has consequently led to spillover (i.e., parasite
transmission from reservoir populations to sympatric wildlife) to many
naïve wild pollinators (Daszak et al. 2000, Keesing et al. 2006, Goulson
and Hughes 2015, Purkiss and Lach 2019). Since honeybee colonies tend to
send generalist foragers to a few flower patches at a time (Visscher and
Seeley 1982), it is possible that an infected colony may create
localized floral hot-spots where wild bees may acquire parasites.
Increasingly, parasites previously thought to only infect honeybees are
found in diverse populations of wild pollinators and seem to be
contributing to their decline (Furst et al. 2014, Arbulo et al. 2015,
Goulson and Hughes 2015, Porrini et al. 2017, Müller et al. 2019,
Purkiss and Lach 2019).
One parasite of particular concern is the widely-dispersed
microsporidian parasite Vairimorpha (= Nosema )ceranae (Tokarev et al. 2020), which has been rapidly
infecting honeybees and spilling over into wild bee populations over the
past three decades (Paxton et al. 2007, Chen et al. 2008, Fries
2010). Although V. ceranae is transmitted within honeybee
hives through contaminated feces and pollen stores, transmission may
also occur when bees encounter spores on contaminated flowers (Higes et
al. 2008b, 2010). Graystock et al. (2015) demonstrated that multiple
pollinator parasites, including V. ceranae , can be effectively
dispersed onto flowers by competent hosts and then vectored from flowers
back to colonies by other pollinator species. Additionally, V.
ceranae spores have been detected on the flowers of at least 14 plant
genera in the field (Graystock et al. 2020). Therefore, contamination of
shared flower resources is a likely mode of transmission for V.
ceranae between different pollinator species, with dispersal
potentially occurring through defecation on floral surfaces or through
the rubbing off of spores that were attached to the bee cuticle
(Graystock et al. 2015, Bodden et al. 2019, Piot et al. 2020).
Furthermore, Graystock et al. (2015) found that V. ceranaetransmission was very rapid in small experimental flight cages, but they
recognized that whether parasite dispersal is similar in nature will
depend on the characteristics of pollinator communities and
environmental conditions. Despite clear experimental evidence forV. ceranae transmission on flowers, the relationship between
specific pollinator visitation patterns and V. ceranae prevalence
across managed and wild pollinator species in the field has remained
understudied.
Here, we examine whether the prevalence of V. ceranae in managed
and wild bee populations is influenced by the floral visitation
behaviors of bees in the natural environment. We conducted an
observational study of V. ceranae in honeybee (A.
mellifera ) and bumblebee (Bombus spp.) populations among
different pollinator communities to understand how floral visitation
patterns differ among pollinator species and whether the visitation
patterns are linked with V. ceranae prevalence in both host
species. Specifically, we investigated how V. ceranae prevalence
is linked with the number of honeybee, bumblebee, and other pollinator
visits to flowers and the time each bee species spent interacting with
different parts of the flowers during each visit. We hypothesized that
higher numbers of visits and longer visits by potentially infected bees
would increase the likelihood of V. ceranae transmission and
correlate with higher V. ceranae prevalence. These findings will
be important for determining the pollinator visitation behaviors that
contribute the most to V. ceranae exposure and subsequent
infection in honeybees and bumblebees as well as helping to establish
whether V. ceranae transmission on flowers occurs under field
conditions.