1. INTRODUCTION
Land-use intensification, mainly induced by the expansion of
urbanization and agricultural activities, is often considered a major
threat to biodiversity and specifically to pollinator species
conservation (Dicks et al., 2020; Potts et al., 2010, Tommasi et al.,
2021 a). This is because landscape intensification leads to habitat loss
and green areas fragmentation, especially in urban environments
(Kovács‐Hostyánszki et al., 2017; Rathcke & Jules, 1993; Senapathi et
al., 2017). As a result, pollinator community composition is
impoverished by a decreased diversity of species in fragmented
landscapes, as specialist pollinators easily disappear (Xiao et al.,
2016). In turn, plant-pollinator interactions are expected to become
more generalised, possibly due to changes in floral composition and
distribution (Andrieu et al., 2009; Fortuna, and Bascompte 2006;
Matthews,Cottee‐Jones & Whittaker 2014). Local conditions related to
floral resources (e.g. , flower diversity and abundance) are
important drivers of pollinator community features, and have previously
been found to mitigate the negative impacts posed by land-use
intensification both on community composition and interactions (Tommasi
et al., 2021 a).
In landscapes intensively altered by human practices, green areas became
of high importance for biodiversity and the effects of this
fragmentation on pollinators could vary at different geographical and
taxonomic scales. This translates into changes in pollination efficiency
that have already been documented, albeit with idiosyncratic responses
depending on the investigated species (Xiao et al., 2016). At a small
scale (i.e., 20 m radius), the diversity of bees appears
negatively associated with the fragmentation of green areas (Hennig &
Ghazoul, 2012). Conversely, at higher scales (i.e., 200 or 1000 m
radius), the fragmentation of green patches corresponded to increased
pollinator species richness, flower visitation rates and pollination
(Hennig & Ghazoul, 2012; Theodorou et al., 2020). This variability in
responses to green habitat fragmentation highlights difficulties at
forecasting how land-use intensification affects pollinator communities
and the ecosystem service they provide. Furthermore, species can greatly
diverge in their foraging strategies and contribute differently to
pollination. Thus, the analysis of intraspecific variation in
plant-pollinator interaction in fragmented habitats is necessary to
comprehend the role of target species, and their changes in response to
anthropic disturbance (Biella et al., 2019 b; Fuster & Traveset, 2020).
Therefore, it is urgent to improve our comprehension of the effects of
green habitat fragmentation on pollinators to suggest ways for
mitigating the impact on green ecosystems.
In this framework, islands offer unique opportunities to investigate the
effects of pressures on biodiversity related to land-use (Castro-Urgal
& Traveset, 2014; Kaiser-Bunbury & Blüthgen, 2015; Picanço et al.,
2017; Steibl, Franke & Laforsch, 2021). Islands can be considered open
air laboratories for ecological studies for several reasons. First,
islands host simplified and isolated biotic communities, which allow to
easily evaluate species roles in ecosystem functioning (Kaiser-Bunbury,
Traveset & Hansen, 2010; Warren at al., 2015). Second, environmental
changes spread earlier and more rapidly on islands than in the
continent, also favored by small population sizes (Castro-Urgal &
Traveset, 2014). These aspects apply also to pollinator and plant
assemblages, which are usually simplified in insular ecosystems
(Kaiser-Bunbury, Traveset & Hansen 2010; Traveset at al., 2016). An
additional, relevant aspect is that dispersal events among islands are
occasional or rare, and this is a favourable property when studying the
effects that land-use changes as green areas fragmentation have on
plant-pollinator interactions (Kaiser-Bunbury & Blüthgen, 2015).
Therefore, islands are suitable scenarios for investigating the effects
of land-use intensification on pollinator foraging and thus on their
interactions with plants, which further supports the adoption of this
model system to solve ecological questions.
Many insular systems are peculiar and yet largely neglected, especially
in light of ecological research on terrestrial biodiversity and
interactions between taxa. This is the case of Maldives, in the Indian
Ocean, where studies on terrestrial biodiversity are extremely rare
(Steibl, Franke, & Laforsch, 2021). In addition, studies in insular
systems could be biased by poor taxonomy and species distribution
knowledge. In this framework, modern molecular approaches can
efficiently support investigation on species biodiversity and biological
interactions. In recent years, molecular tools such as DNA metabarcoding
have been increasingly applied in pollination ecology research to
achieve the goal of describing plant-pollinator interactions (Bell et
al., 2017; Pornon et al., 2016; Tommasi et al., 2021 a). By foraging on
flowers pollinators carry pollen grains that keep trace of their
foraging activity (Bosch, Martín González, Rodrigo, & Navarro 2009).
Standard DNA barcode loci can be used to characterize this pollen and
understand which plants were visited (Tommasi et al., 2021 b). In this
way, it is possible to reconstruct the interaction networks among plants
and their pollinators, as well as to better assess the resource use
preferences shown by flower visitors (Biella et al., 2019 a). This
approach ensures significant advantages, allowing to reduce the time
spent for field direct observation of interactions or to reduce the time
spent for pollen characterization in laboratories, while improving the
number of observed interactions (Bell et al., 2017). However, the
potential of DNA metabarcoding for identifying pollen can be amplified
when it is applied to contrasting scenarios in order to further
illuminate the effects of human disturbance (Soares, Ferreira, & Lopes,
2017). This molecular information can be easily translated into network
indices permitting reliable comparisons. Moreover, since flower
visitation does not necessarily lead to conspecific pollen deposition
(Ashman et al., 2020), the combination of DNA metabarcoding-based
network analysis with measurements of pollination efficiency
(e.g. , pollen deposition, pollen tube growth, fruit, and seed
set) (Stavert, Bailey, Kirkland, & Rader, 2020) could provide a
comprehensive overview of the effects of human disturbance on such
ecosystem interactions.
In this study, we combined the experimental advantage of an island model
with the application of DNA metabarcoding to increase our understanding
on how the fragmentation of green habitats (e.g. green patches or
parks in urbanized conditions) affects pollinator diversity, their
mutualistic interaction with plants, and the resulting efficiency of the
pollination service. To do so, we investigated pollinator communities in
the Maldives islands, an insular context largely neglected under a
pollination ecology perspective (but see Kevan, 1993). There, islands
are homogeneous in terms of composition of biotic communities and
geographical conditions, while varying in the degree of human
exploitation and impact (Fallati, Savini, Sterlacchini, & Galli, 2017).
This context results in a gradient of green area fragmentation and
provides a model condition that ensures better understanding and
interpretation of the impact of this fragmented landscape on
pollinators, allowing knowledge transfer to other geographical contexts
of landscape alteration.
Standing at the need to improve the comprehension of the effects of
green habitat fragmentation on pollinator communities, here we aimed at
evaluating how this phenomenon affect the ecosystem service of
pollination in tropical islands by investigating several aspects: i) the
pollinator species richness, ii) the plant-pollinator interactions,
considering both community and intraspecific variations, and iii) the
pollination efficiency.