3. RESULTS
The three parasite groups were detected in both the bumblebee species
with evident differences in terms of infection rate. Infection ofMicrosporidia occurred in similar rates in B. pascuorumand B. terrestris (42.71 % in B. pascuorum and 46.88% inB. terrestris ), while different patterns of infections were
detected in the case of trypanosomatid (8.33 % in B. pascuorumand 46.88% in B. terrestris ) and neogregarines (1.04 % inB. pascuorum and 15.63% in B. terrestris ).
The combination of coinfection rates highlighted different coinfection
patterns in the two bumblebee species (Table 2), with B.
terrestris hosting a higher parasite richness compared to B.
pascuorum . In particular, B, pascuorum showed a 51.04% rate of
carrying 0 infections, while B. terrestris demonstrated a much
lower probability (21.88%). Furthermore, 78.13% of B.
terrestris carried at least one parasite, while in B. pascuorumit was 48.96%.
[ TABLE 2]
The two bumblebee species responded differently to the factors
describing the urbanization phenomenon. The probability of infection
significantly increased in response to floral abundance (Figure 2a,
Table 3) and decreased in response to ENN (Figure 2b, Table 3) inB. pascuorum. All the other predictor variables (i.e. ,
percentage of green habitat, distance from hives, floral diversity and
the number of hives in the surrounding of sites) did not show
significant effects on parasite richness (Table 3). However, none
influenced B.terrestris’ probability of infection, as it was not
influenced by the evaluated predictor variables.
[ FIGURE 2]
Parasite richness was lower in B. pascuorum, with a maximum of 2
target parasites per sample, compared to B. terrestris whose
maximum 3 target parasites. Nevertheless, local variables such as the
floral abundance and the distance from honeybee hives significantly
shaped parasite richness. Specifically, the parasite richness increased
in response to floral abundance in B. pascuorum (Figure 3a, Table
3) and distance from honeybee hives in B. terrestris (Figure 3b,
Table3). All the other predictor variables (i.e percentage of
green habitat, ENN, floral diversity and the number of hives in the
surrounding of sites) did not show significant effects on parasite
richness (Table 3).
[ FIGURE 3]
[ TABLE 3]
4. DISCUSSION
In this study we explored urban pollinator-parasite interactions
focusing on the relationships between parasites’ incidence and
coinfection rate with the green habitat availability and fragmentation,
floral resources availability, and the proximity to beehives.
Our results showed cleardifferences in the infection and co-infection
rate in the two bumblebee species, with B. pascuorum emerging as
less prone to host parasites compared to B. terrestris. These
differences are largely due to trypanosomatids (Crithidia spp.)
and neogregarines (Apicystis spp.) that were detected with higher
rates in B.terrestris. Moreover, coinfections due to two or more
target parasites were extremely rare in B. pascuorum but
relatively common in B. terrestris. A higher parasite prevalence
in B. terrestris compared to B. pascuorum and other
congenerics has been previously reported (Cameron et al., 2011; Goulson
et al., 2012; Jabal-Uriel et al., 2017) but a reliable explanation of
these interspecific differences has not been provided yet. In this
context, a number of factors could be involved and constitute valid
research questions to be further addressed. The first factor could be
that the lower occurrence of infected individuals in B. pascuorummay suggest a lack of tolerance of this species towards infections that
could significantly reduce the survival of infected individuals and thus
the possibility to collect and analyze infected specimens (as we
collected only living individuals in this study). On the other hand,B. pascuorum may be particularly resistant towards parasite
contamination due to morphological, physiological or ecological aspects
(e.g., its nesting and foraging habits). Large body size and foraging
breath are bee traits supposed to increase exposure to parasites (Cohen
et al., 2021), and this could explain the observed idiosyncratic pattern
of infection between the two investigated bumblebee species, withB. pascuorum being smaller and with a slightly narrower foraging
breath (Harder 1985). Furthermore, the two bumblebees also differ in
colony size, where B. terrestris and B. pascuorum could
reach 1000 and 150 individuals per colony, respectively (Von Hagen &
Aichhorn, 2014) and this might mediate their epidemiology via
intra-colony transmission.
Based on our results, the landscape green habitat fragmentation
significantly shapes parasite occurrence, and in particular it seems to
reduce the probability of infection in B. pascuorum. This finding
disproves our expectation of having higher parasite occurrence in the
more fragmented habitats due to aggregation of bumblebee hosts in the
few green remnants available (amplification effect, Becker et al.,
2015). In an urban context, the dispersion of green areas and the
presence of inhospitable surfaces (concrete) affects the incidence of
bumblebees as they could hardly arrive and forage in progressively
isolated green areas. In this case, a lower hosts availability could
explain the observed reduction in parasite occurrence. Therefore, future
investigation will benefit from a clear determination of the community
of flower visitors in terms of species richness and abundance. This will
allow a deeper comprehension of the indirect effects of land-use
features mediated by dilution, thus lower parasite prevalence due to
higher species richness and diversity (Civitello et al., 2015) , or
amplification effects.
The dependency between parasite abundance and host distribution in the
urban landscape may result from a major importance of floral resources
availability in increasing parasite occurrence, as resulted from our
analyses. When flowers are highly available and a rich pollinator
community is present there, it is expected to observe a dilution effect
of parasites in several hosts, especially over large surfaces (Piot et
al., 2019). However, our results may support the alternative hypothesis
that floral resources improve parasite transmission due to the higher
attractiveness of floral spots and the consequent higher bee
aggregation. In this context, both the probability of infection and the
parasite richness shown by B. pascuorum were higher where more
flowers were available for foraging. This result confirms the well-known
role of flowers as hubs for parasites spread among individuals
(Pinilla‐Gallego et al., 2022). Indeed, about 10% of flowers were found
to host one or more parasites of bees (Graystock et al., 2020) and
shorter and wider flowers promote higher transmillability
(Pinilla-Gallego et al., 2022). This could be a peculiarity of
“poor-quality”, fragmented landscapes and of disconnected urban green
areas, where flowers occur in aggregated ways or cover specific areas,
thus aggregating pollinators too and promoting infection, as higher bee
pathogens are found in flower strips near isolated semi-natural patches
(Piot et al., 2019). This highlights potential risks associated with
those interventions that aim at safeguarding pollinators through floral
strip planting since these could facilitate the spread of infections in
wild bee communities. While in B. pascuorum the probability of
infection and parasite richness were shaped by landscape and local
features a similar trend was not highlighted in B.terrestris that
resulted more susceptible to parasite infection independently from
landscape and local features.
Interestingly, B. terrestris parasite richness was affected by
the proximity to beekeeping sites. Other studies highlighted a major
role of apiculture for the spread of parasites (Nanetti et al., 2021;
Martínez-López et al., 2021) but without focusing on beekeeping
activities within the urban environment. This will require further
insights since the worry of pollinator decline is pushing many citizens
and cooperative companies to adopt honeybee hives in cities (Sponsler &
Bratman, 2021). In this study, parasite richness decreased in proximity
to honeybee hives, likely because apiculture disproportionally increases
the abundance of Apis mellifera in the city and thus favoring the
spread of parasites on the most abundant host rather than on alternative
bumblebee hosts. However, here we evaluated the impact of apiculture
using proxy variables of honeybee presence, that do not exhaustively
describe the local abundance of Apis mellifera and do not
consider beekeeping practices that are known to shape parasite
transmission to wild species (Piot et al., 2022). A detailed estimation
of these variables would improve the comprehension of the impact of
apiculture on the spread of parasites to urban and non urban wild bees.
5. CONCLUSIONS
Landscape and local features of urban green habitats shaped the
occurrence of parasites with marked differences among the two
investigated bumblebee species. This novel finding highlights the
importance of designing proper target conservation efforts based on
pollinator species-specific knowledge. The planting of flower strips is
gaining importance among the efforts to safeguard pollinators; however,
our findings also shed light on the potential detrimental effects of
these practices that must be considered by public administrators.
Further investigation related to the spatial arrangement of flower
patches, as well as an evaluation of the most suitable flower species in
terms of morphological traits and shapes with lower potential for
parasite transmission will be useful to refine these conservation
measures. Moreover, we recommend to consider the configuration of green
areas at the landscape scale, here confirmed as a driver able to shape
parasite dynamics, in implementing these conservation measures. The
results obtained here will contribute to the fine tuning of the
interventions aimed at improving pollinator health and wellbeing also in
urban areas, indirectly contributing to our well-being since as resumed
by the one-health concept human and ecosystem health are inextricably
linked.
ACKNOWLEDGEMENTS
Project funded under the National Recovery and Resilience Plan (NRRP),
Mission 4 Component 2 Investment 1.4 - Call for tender No. 3138 of 16
December 2021, rectified by Decree n.3175 of 18 December 2021 of Italian
Ministry of University and Research funded by the European Union –
NextGenerationEU,Project code CN_00000033, Concession Decree No. 1034
of 17 June 2022 adopted by the Italian Ministry of University and
Research, CUP, H43C22000530001 Project title “National Biodiversity
Future Center - NBFC” .
Also funded by PROGETTO LIFE20 PRE/BE/000008 - UrbanGreeningPlans - CUP
E42H21000060002 within the research agreement with Parco Nord Milano.
We are grateful to the staff of Parco Nord Milano for their support in
the field activities.
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DATA ACCESSIBILITY AND BENEFIT-SHARING
All relevant data are within the paper or stored in figshare at the
following linkhttps://figshare.com/s/c58df945039de5747072.
Benefits from this research arise from the sharing of our data and
results on public databases as described above.
AUTHOR CONTRIBUTIONS
Conceptualization, NT ; Investigation, NT, BC; Formal Analysis, NT, BC;
Writing - Original Draft, NT, BC; Writing - Review and Editing, NT, BC,
PB, EP, AG, MC ; Funding acquisition, PB, AG.
TABLES AND FIGURES