4. DISCUSSION
In this study, a DNA metabarcoding approach to describe plant-pollinator
interactions has been coupled with pollinator traits and deposited
pollen data to disentangle the effects of habitat fragmentation in an
oceanic insular system. In this way, we described the direct effects of
green areas fragmentation at several levels, ranging from pollinator
species richness to their interactions with plants and the pollination
efficiency. Alongside, we provided a characterization of the
flower-visiting insects (i.e. , Hymenoptera and Diptera) of
Maldives islands and the associated flora, that to the best of our
knowledge were largely unexplored in this biodiversity hotspot.
Green areas fragmentation increased pollinator species richness. This
result is consistent with the observations from other studies at
comparable spatial scales. For instance, Theodorou et al. (2020), found
that bee richness increased with edge density of green spaces both in
urban and rural landscapes. A similar positive trend in species richness
was observed elsewhere at levels of disturbance comparable to those in
our study (Kremen, 2005; Rader, Bartomeus, Tylianakis & Laliberté,
2014). However, it seems that other guilds, such as soils
macroinvertebrates, have been found to decrease with fragmentation in
oceanic islands (Steibl, Franke & Laforsch, 2021). Nevertheless,
differences between pollinator and macroinvertebrate responses could be
searched in different natural histories of these groups. Given the
intermediate levels of Edge density on Maldives Islands (range 0.00 -
0.04) compared to continental levels, it seems appropriate to explain
our results to the Intermediate Disturbance Hypothesis according to
which species diversity is expected to increase when the disturbance is
of moderate entity (Huston, 2014; Rutgers-Kelly, 2005). This may occur
as a trade-off between the competitive exclusion that characterizes the
absence of disturbance and the abiotic limitation found in highly
disturbed conditions (Lazarina et al., 2019; Lazaro et al., 2016).
Moreover, an intermediate disturbance could potentially promote foraging
and nesting heterogeneity of pollinator insects, thus permitting to host
more species and guarantee their survival and reproduction (Wenzel,
Grass, Belavadi, & Tscharntke, 2020; Winfree et al., 2009). Our
interpretation is further supported because the maximum fragmentation in
our study system corresponded to a proportion of surfaces occupied by
infrastructures of about thirty percent (see Supporting Information, Fig
S2), that still represents an intermediate degree of disturbance
(Wenzel, Grass, Belavadi, & Tscharntke, 2020). At higher disturbances,
the pollinator richness is supposed to decrease, as observed by Rader et
al. (2014).
Our study found that green area fragmentation clearly shapes
plant-pollinator interactions both at the community and individual
levels. We observed a decrease in Connectance, indicating a lowered
proportion of realized interactions, that highlights a simplification of
plant-pollinator networks. As Connectance is often related to network
complexity and stability (May, 1972), it is likely to interpret that
increasing fragmentation will lead to impoverished, more simplified
networks. We understand this as an alarming aspect as a high complexity
could mean high functional redundancy and it is a desirable property of
functioning ecosystems (Kaiser-Bunbury et al., 2017). In spite of the
effects of fragmentation at the community level, idiosyncrasies emerged
when considering the interactions of pollinators of three different body
sizes. The largest among these bees, Xylocopa fenestrata, was the
only one that modified, and specifically increased, the number of
foraged plant species in response to increased fragmentation, as
indicated by DNA metabarcoding of pollen. Conversely, smaller species
did not show expansions or contractions of the number of foraged plant
species. Differential responses depending on body size offer the key to
interpret the effects of fragmentation, since size is a functional trait
related to flight range (Greenleaf, Williams, Winfree, & Kremen,
2007).In fact, small pollinators usually forage in smaller patches and
might even benefit from having small habitat fragments (Tscharntke,
Steffan-Dewenter, Kruess & Thies, 2002) and they likely did not suffer
from the level of fragmentation in oceanic islands. Differently, a
larger species flying across fragments could acquire more flower
resources and this is what we observed in X. fenestrata . Species
responding in different ways to land-use change were already observed,
according to their functional traits (Wenzel, Grass, Belavadi, &
Tscharntke, 2020). Therefore, it is a priority to couple community
trends and the responses of single species, as they are highly important
to preserve community structure and functionality for instance by
establishing new interactions after a disturbance event (e.g., Biella et
al., 2020).
The effects on the ecosystem service of pollination by green area
fragmentation were evaluated by quantifying pollination efficiency in a
panel of widely distributed plant species used here as sentinel cases.
Specifically, pollination efficiency associated with pollinator species
richness at the sites, also related to green area fragmentation. This
agrees with an increasing amount of evidence supporting a positive
relationship between pollinator richness and plant reproduction
(Fontaine, Dajoz, Meriguet. & Loreau, 2006; Garibaldi, Steffan-Dewenter
& Winfree, 2013; Mallinger & Gratton, 2015; but see Biella et al.,
2021). Furthermore, pollinator species richness in an area may increase
pollination efficiency through other mechanisms such as facilitation
(the interactions between different species affect their foraging
behaviours enhancing the pollen deposition), and temporal and/or spatial
complementarity (Mallinger & Gratton, 2015). However, in our dataset,
the positive trend of pollination efficiency with environmental
pollinator richness was independent to the amount of pollinator species
visiting a given plant, a measure of plant interaction generalism. This
suggests that not all plants respond in a similar way to pollinator
availability (see Biella et al., 2019 b). Overall, these results
highlight the importance of safeguarding pollinator biodiversity for
maintaining the equilibrium of pollination service.