Journal of Environmental Management 318 (2022) 115450

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Journal of Environmental Management

journal homepage: www.elsevier.com/locate/jenvman

Insect pollination services in actively and spontaneously restored quarries

converge differently to natural reference ecosystem
Carolina Carvalho a, *, Amália Oliveira a, b, c, Elsa Caeiro b, d, Otília Miralto a, b, c, Marta Parrinha a,
Ana Sampaio a, b, c, Carmo Silva a, b, c, António Mira a, b, c, Pedro A. Salgueiro a, b, c
a
UBC – Conservation Biology Lab, Portugal
b
MED – Mediterranean Institute for Agriculture, Environment and Development, Institute for Advanced Studies and Research, University of Évora, Mitra, 7002-554,
Évora, Portugal
c
Department of Biology, University of Évora, Mitra, 7002-554, Évora, Portugal
d
SPAIC - Portuguese Society of Allergology and Clinical Immunology, Lisbon, Portugal

A R T I C L E I N F O A B S T R A C T

Keywords: Ecological restoration has the potential to accelerate the recovery of biodiversity and ecosystem services in
Ecological networks degraded ecosystems. However, current research queries whether active restoration is necessary. We evaluated
Ecological restoration plant-pollinator networks during spring at replicated sites within an actively restored quarry, at abandoned
Ecosystem services
quarries undergoing spontaneous restoration, and within a natural reference area, to compare pollinator com­
Insect pollinators
Spontaneous succession
munity composition and function. Overall, we aimed to assess which approach is more effective in rehabilitating
Vegetation structure pollination networks. We found that while both approaches allowed for the restoration of pollination function,
active restoration provided faster recovery: pollination network structure was more similar to the reference
ecosystem after 20–30 years of active restoration, than 40 years of natural succession in spontaneously restored
areas. Different restoration approaches sustained distinct pollinator communities providing a similar service in
different areas: honey bees played an important role in the natural area, bumblebees in the abandoned quarries
and wild bees in the restored sites, suggesting a possible conflict between diverse wild bee communities and
honey bee homogenized pollinator communities. In quarries, flower resource availability and diversity influ­
enced networks’ structural properties by constraining species interactions and composition. In spontaneously
restored areas a rich herbaceous layer of ruderal species from early successional stages buffered against the
shortage of flower resources at critical periods. Active restoration, though effective, should include practices that
consider wild bee communities and mitigate flower resource scarcity. The use of “bridging” plants that flower in
different periods, should be considered in active restoration programs to enhance the pollinator community.

1. Introduction damaged, transformed or entirely destroyed as a direct or indirect

Extractive industry is amongst the most harmful human activities,
with long-lasting impacts on local ecosystems (Palmer et al., 2010). Yet,
the growth of the industry steadily increases (IRP, 2019) and damaged
ecosystems are left abandoned and devoid of vegetation. Restoring these
highly degraded areas is essential to reverse biodiversity loss and the
depletion of ecosystem services (Benayas et al., 2009). However, this
task is challenged by demanding conditions imposed by landform con­
straints and environmental degradation (Salgueiro et al., 2020).
Active (‘assisted’) ecological restoration provides an opportunity to
accelerate the recovery of an ecosystem that has been degraded,
consequence of human activities (SER, 2004). However, the issue of
whether assisting restoration is always necessary is still a subject of
considerable debate (Holl and Aide, 2011; Prach and Tolvanen, 2016).
Active restoration often involves the application of costly reclamation
techniques, while spontaneous succession (‘passive restoration’) relies
on ecological succession (Prach and Hobbs, 2008). Although the latter
approach takes longer to resemble natural reference systems, especially
in highly damaged sites (e.g., quarries), it often provides early succes­
sional heterogeneous surfaces with extreme abiotic conditions (dry,
acidic and nutrient poor soils; Tropek et al., 2010). As a consequence,
spontaneous succession can create refugia for distinct species of

* Corresponding author.
E-mail address: carolina_maria_carvalho@protonmail.com (C. Carvalho).

https://doi.org/10.1016/j.jenvman.2022.115450
Received 6 September 2021; Received in revised form 26 May 2022; Accepted 28 May 2022
Available online 20 June 2022
0301-4797/© 2022 Elsevier Ltd. All rights reserved.
C. Carvalho et al.
conservation concern that may thrive in these conditions (Tropek et al.,
2010; Williams, 2011), while enhancing α (local species diversity) and β
diversities (species turnover between sites) over large areas (Holl and
Aide, 2011).
The effectiveness of these approaches and how they converge to
attain restoration goals has usually been evaluated using the composi­
tion of communities (Ruiz-Jaen and Aide, 2005). Compositional ap­
proaches traditionally focus on measuring the presence and/or
abundance of species (Cadotte et al., 2011). However, these approaches
have been known to provide limited insight into ecosystem attributes
and restoration success. For instance, there is evidence that although
post-restoration species assemblages can be quite distinct from natural
undisturbed communities in similar conditions, they can still provide
ecosystem services with as much efficiency (Denning and Foster, 2018;
Forup and Memmott, 2005; Williams, 2011).
Considering functional goals instead of compositional ones may be a
more appropriate approach in some contexts, such as restoration after
mineral exploration and mining (Shackelford et al., 2013). In fact,
ecological interactions might be lost at a higher rate than species
become extinct, as species’ functional role may lose its expression before
the disappearance of the species itself (Valiente-Banuet et al., 2015).
However, most restoration projects fail to take species interactions into
consideration in planning, implementation and evaluation of restoration
actions (Kaiser-Bunbury et al., 2010; Montoya et al., 2012), often
explicitly assuming that if vegetation is re-established animal commu­
nities and the processes they mediate will naturally appear (Cross et al.,
2019).
Mutualistic interactions, in particular, have been pointed out as good
candidates for evaluation of restoration success (Kaiser-Bunbury et al.,
Fig. 1. Map of the study area, representing sampling area types and location of surveyed sites and surrounding land uses.
2
Journal of Environmental Management 318 (2022) 115450
2010). Pollination is among the most well-studied mutualistic in­
teractions (Goldstein and Zych, 2016), since it is vital for the mainte­
nance of both wild plant communities and agricultural productivity
(Potts et al., 2010). It is estimated that close to 90% of flowering plant
species benefit from pollinators, and it has been demonstrated that
pollination influences seed viability, fruit production and genetic vari­
ability of plant populations through cross-fertilization (Cusser and
Goodell, 2013; Forup et al., 2008; Menz et al., 2011). As pollinator
communities decline (Christmann, 2019), failure to promote and
manage this service could lead to the collapse of plant communities in
restored areas (Menz et al., 2011). Therefore, in order to improve the
long-term success of restoration it is pivotal to effectively reinstate
pollination services by ensuring these areas have the necessary resources
for pollinators to thrive (Cusser and Goodell, 2013).
In this study, we compared plant-pollinator networks in actively
restored quarries and quarries subjected to spontaneous ecological
succession to evaluate which approach is more effective in rehabilitating
this ecological process. We assessed both community composition and
functioning in actively and passively restored quarries and compared
them with a natural area representing the reference ecosystem. Since
active restoration aims at accelerating the process of recovery, we ex­
pected to find higher similarity between pollinator community compo­
sition and network structure of actively restored quarries and natural
areas throughout the flowering period. However, in a highly seasonal
environment such as Mediterranean landscapes, we envision that flower
resource availability will mediate the composition of pollinator com­
munities, thus producing changes in network structure through time and
between areas.
C. Carvalho et al.
2. Methods
2.1. Study area
Our study was carried out in Arrábida Natural Park (PNA), Setúbal,
Portugal (centroid: 38◦ 29′ N 8◦ 57′ W; Fig. 1), where the Mediterranean
maquis – a dense sclerophyllous shrubland – dominates the landscape
along with very sparse herbaceous vegetation and rocky limestone
outcrops. Perennial hard-leaved shrub species, such as Cistus albidus,
C. ladanifer, Rosmarinus offinallis and Erica arborea are among the most
dominant species (Freire et al., 1996).
Due to its limestone rich substrate, extractive industry has a strong
presence in the area, and 300 ha are authorized for exploitation (Freire
et al., 1996). Since the 1980’s, legislation requires restoration of
quarries no longer under exploitation. Several quarries deactivated prior
to this legislation remained abandoned and exposed to spontaneous
ecological succession.
We defined three areas that comprised: (1) a natural reference
ecosystem (natural area), (2) an actively restored quarry (restored area)
and (3) quarries where spontaneous revegetation processes were
allowed (abandoned area). The natural reference ecosystem comprised
the typical Mediterranean dense shrub maquis (2817 ha, 24.6% of the
area of the PNA). The restored area was located within an active quarry
(SECIL, Companhia Geral de Cal e Cimento, S.A.) encompassing 44 ha of
a 99 ha area licensed for quarrying. Limestone extraction was performed
from top to bottom leaving a series of 10 m large terraces separated
about 20 m apart in height. Restoration practices in the sampled areas
have been under way since early 1990, involving the reintroduction of
substrate and planting of native shrub species and the naturalized
Aleppo pine (Pinus halepensis). This fast growing species has resulted in a
dense 6–8 m arboreal layer absent from natural and abandoned areas,
and constrains the growth of shrub and herbaceous layer (Nunes et al.,
2014). The abandoned area consisted of three closely located, smaller
quarries (about 2.8 ha each) which were deactivated in 1982 (Esteves,
2015). No subsequent actions were undertaken except for the removal of
the extractive activity and infrastructure. Consequently, soil formation
and vegetation establishment has occurred gradually without human
intervention, following ecological succession. Vegetation structure was
in general sparse, representing an early successional stage after distur­
bance. Both the abandoned and restored areas are surrounded by the
same type of Mediterranean maquis found in the natural area.
2.2. Field sampling
We established three sampling sites (spatial replicates) in each area
(Fig. 1). Adjacent sites were separated by a minimum of 250 m to assure
independence, well above the mean distance (130 m) for successful
pollen transfer in urban habitats (Martins et al., 2017; Van Geert et al.,
2010).
At each site, a 150 m transect was walked by two researchers during
30 min to sample the insect pollinator community. Each transect was
visited twice a day (once in the morning and once in the afternoon) in
order to avoid bias from pollinators’ daily activity patterns. Each survey
took place once per month from February to May 2019, with an interval
of at least three weeks between sampling sessions, in a total of 36 sur­
veys across all sites. Each transect was thus sampled for a total of 4 h
during the whole study. This period covered the majority of the flow­
ering season for most dominant species present in the region (Sup.
Materials A). Surveys only took place on days with favorable conditions
for pollinator activity, such as dry weather, low cloud cover and low to
moderate wind speed (Cusser and Goodell, 2013; Forup and Memmott,
2005). Diurnal insects were collected using entomological nets and
collection jars while visiting or hovering over flowers. We tried to cap­
ture all insect diversity in each area, only avoiding the capture of all
individuals of very abundant species (e.g., honey bees). All captured
insects were stored in individual tubes to avoid pollen contamination,
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Journal of Environmental Management 318 (2022) 115450
and frozen until handling at the laboratory.
We sampled floral availability and vegetation cover in a total of 10
quadrats (50 × 50 cm) along each transect, on alternate sides, 15 m
apart from each other. Floral availability was assessed in each survey by
counting floral units within each quadrat. Floral units were either
flowers or compact inflorescences defined as being different entities by
forcing a pollinator to fly in order to move from one unit to the next
(Timóteo et al., 2018). Flower samples (2 or 3 per species) were also
collected in each survey and kept in individual paper bags for pollen
harvesting. Percentage cover of bare soil and of all layers of vegetation
was estimated visually in a single survey, using a sampling area of 100 ×
100 cm centered in each quadrat point.
2.3. Laboratory methods
Pollen from each plant species was collected from mature anthers,
stained with a solution of glycerin gelatin with basic fuchsine gel, and
mounted on a microscope slide (Forup and Memmott, 2005). Micro­
scope slides were sealed and all the samples compiled into a reference
collection.
Pollen was extracted from individual insects into a coverslip-sized
area of a microscope slide lightly covered in vaseline. The insect body
was then rubbed on this surface, avoiding specialized pollen transport
structures since this pollen is unlikely to be available for pollination
(Alarcón, 2010; Forup and Memmott, 2005). Tweezers used to handle
the insects were sterilized with alcohol in between handling each indi­
vidual to avoid pollen contamination. Microscope slides were stained
with a drop of a solution of glycerin gelatin with basic fuchsine gel for
24 h, and examined under light microscopy (40x or 100x magnification).
Grains were identified through comparison to the reference collection
and counted in each slide. Only species containing five or more occur­
rences per slide were considered for network analyses, in order to pre­
vent possible contamination bias (Forup et al., 2008; Forup and
Memmott, 2005). Insects and pollen grains were identified to the lowest
possible taxonomic level. Most pollen grains were identified to species
level, with exception of genera Allium and Carduus, as well as some
grains belonging to unidentified species of Asteraceae and Poaceae. Of
all Cistus species found on site, only Cistus crispus was readily distin­
guishable and considered separately, while grains belonging to other
Cistus species (C. albidus, C. monspeliensis, C. salviifolius, and C. ladanifer)
were pooled together into a species complex. Insects were grouped ac­
cording to the lowest taxonomic level to which they were identified
(discriminated in Sup. Materials B).
2.4. Data analysis
2.4.1. Community composition
We compared the composition of pollinator communities by calcu­
lating Bray-Curtis dissimilarity between sites. We performed a con­
strained correspondence analysis (CCA) in order to assess compositional
differences between space (sites) and time (months). The CCA was
performed using a species matrix representing the pollinator commu­
nities for each site and month, constrained by a matrix of vegetation
structure variables. The model variables were chosen considering the
structural characteristics that most differentiated the distinct areas (bare
soil, herbaceous, shrub and tree cover, and number of floral units). Since
communities are expected to vary between months, the effect of time
was partialled out before ordination.
2.4.2. Community function
We used the pollen transport data to build quantitative pollination
networks. Pollen-based networks provide a more extended record of
visitation history than the generalized visitation networks, which are
restricted to a snapshot of a single interaction (Alarcón, 2010; Ballan­
tyne et al., 2015; Bosch et al., 2009). Using this type of pollination
network, while still not a measure of effective pollination, is a proxy as it
C. Carvalho et al.
ratifies that a pollinator is able to collect and transport pollen from a
given flower. The measure used to quantify each interaction between a
plant and a pollinator was the total number of pollen grains of that given
plant carried by all individuals of a pollinator taxon. A network was
constructed for each site at each sampling session, totaling 36 networks.
Ecological networks allow the calculation of several metrics, which
characterize different aspects of network structure and species behavior
(Kaiser-Bunbury and Blüthgen, 2015). These metrics were used to
compare the structure of network interactions at sites with different
restoration approach, and identify critical species providing pollination
services as well (see also Cagua et al., 2019; Kaiser-Bunbury et al., 2017;
Olesen et al., 2007). We computed the following network-level metrics:
interaction strength asymmetry (ISA), linkage density (LD), interaction
evenness (IE), specialization asymmetry (SA), Shannon diversity of
interaction (ID), H2 (a measure of specialization for the whole network),
number of pollinator taxa, number of plant taxa, robustness of the
pollinator community to plant extinction, robustness of the plant com­
munity to pollinator extinction, and modularity (metric descriptions are
provided in Sup. Material C). These metrics were calculated for each of
the 36 networks and then compared using linear mixed models with two
fixed factors – area type (natural, restored and abandoned) and month –,
and their interaction. The natural area values were set as reference for
comparison. Since the structure of our data consisted of a repeated
measures approach, site was considered a random factor in the models,
thus controlling for possible site-related effects. In addition, due to a
high spatial clustering of sites that could cause issues of
pseudo-replication, we validated the mixed model results through ran­
domizations. Samples were randomized 1000 times, and mixed models
were run each time with randomized samples. Statistical t-values were
retrieved from each randomization model for each variable and 95%
confidence intervals (CI95%) were calculated, and afterwards compared
with true model t-values. If true model t-values fell over the CI95% of the
randomized samples, we sustained evidence for statistical inference.
We also assessed the importance of specific pollinators in the net­
works. The most important pollinators were determined based on
abundance and amount of pollen transported, by measuring them in
each of the 36 networks. Species level metrics for each relevant polli­
nator taxon identified were calculated from overall area networks
combining data of the four months for each site, totaling nine global
networks. This approach intended to account for all interactions of the
same pollinator with different plants, thus weighting pollinator impor­
tance for the entire array of pollinated plants. We calculated the
following species-level metrics for each pollinator taxon: species
strength (SS), pollination service index (PSI), partner diversity and the
specialization metric Blüthgen’s D (Sup. Material C). The values were
then compared using a generalized linear model (Gaussian family, link:
identity) including only area type as a fixed factor.
Finally, we investigated possible relationships between the abun­
dances of the most important pollinator taxa by calculating Pianka’s
measure of niche overlap (Krebs, 2014). A linear regression was applied
relating the abundance of each pair of pollinator taxa to determine
possible relations between them.
All the analyses were performed in R 4.0.2. (R Core Team, 2018).
Package bipartite (Dormann et al., 2008) was used to build networks and
compute network and species level metrics; package nlme (Pinheiro
et al., 2019) was used to analyze linear mixed-effects models; CCA and
Bray-Curtis dissimilarity were performed with vegan package (Oksanen
et al., 2018); spaa package (Zhang, 2016) was used to calculate niche
overlap.
3. Results
3.1. General results
A total of 1513 insects were captured, of which 679 (44.35%) carried
pollen from 35 plant taxa (Sup. Materials D). The insects belonged to
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Journal of Environmental Management 318 (2022) 115450
167 taxonomic groups (Sup. Materials B), of which 93 were found car­
rying pollen on at least one occasion. Number of pollinator taxa and
interactions were evenly balanced between restored (Npollinators = 51;
Ninteractions = 126) and abandoned areas (Npollinators = 54; Ninteractions =
133), but slightly lower in natural areas (Npollinators = 32; Ninteractions =
81 (Table 1). Overall, we obtained 269 distinct interactions between
pairs of plant and pollinator taxa.
The pollinators with the largest number of pollen grains belonged to
Hymenoptera, Diptera and Coleoptera. Among hymenopterans, Apoidea
(bees) carried 86% of all pollen grains transported. In addition, the
proportion of individuals found carrying pollen in Apoidea was gener­
ally higher than in the other groups (Sup. Materials B). Diptera (Empis
tessellata) and Coleoptera pollinators (Oedemeridae and Melyridae)
carried less than 5% of all pollen grains altogether (Sup. Materials B).
The remaining pollinators were even less relevant, each of them carrying
less than 1% of all pollen grains (e.g. species of Lepidoptera).
Since Apoidea was responsible for the majority of pollen transport
we considered three groups within this superfamily: (1) honey bees (Apis
mellifera, responsible for 40% of pollen transport), (2) bumblebees
(Bombus terrestris and B. ruderatus, 26% of pollen transport), (3) and wild
bees (23 taxa, 20% of pollen transport). Since single species of wild bees
were found in much lower abundance when compared to honey bees
and bumblebees, the last group included all solitary bee taxa captured
(Sup. Materials B). Bumblebees were significantly more abundant in the
abandoned area. Number of honey bees was significantly higher in the
natural area especially earlier in the season (February) when they were
most abundant, while wild bee abundance was higher in restored areas
only in a specific month (March) (Fig. 2, Sup. Material E).
The plant taxa benefitting from largest pollen transport were Ros­
marinus officinalis, the Cistus species complex and Rubus ulmifolius
(Fig. 2). While Rosmarinus officinalis and Cistus spp. were common in all
areas, Rubus ulmifolius appeared mostly in the abandoned area.
3.2. Community composition
Despite explaining only 23% of variance, CCA managed to clearly
separate the different areas according to vegetation structure (Fig. 3).
The first axis was mostly explained by tree cover, which correlates with
the restored area where the non-native Aleppo pine was planted. The
second axis generally describes a gradient from open areas (dominated
by either bare soil or herbaceous cover) to dense shrub cover. While the
abandoned area was strongly associated with bare soil and herbaceous
cover lacking shrub cover, the natural area was mostly associated with
high shrub cover and reduced herbaceous cover. Neither of these areas
show any correlation with tree cover, since trees are mostly absent in
them.
Regarding pollinator species, neither bumblebees nor honey bees
were related to any particular area, but wild bees overlapped with the
restored area polygon (Fig. 3). Bray-Curtis dissimilarity index showed
that the composition of pollinator communities appeared to be most
distinct between restored sites and the other areas (average dissimilarity
values = 0.60 ± 0.12), while both natural and abandoned locations
showed higher similarity (average dissimilarity values = 0.47 ± 0.04)
(Sup. Material F). Pollinator communities of the restored area also
Table 1
Summary table of number of insect taxa captured, number of insect taxa that
carried pollen (pollinator) and plant taxa for which pollen was found in polli­
nators, and the number of individual interactions between a pollinator and a
plant observed in each area.
Number of Number of Number of Number of
insect taxa pollinator taxa plant taxa Interactions
Natural 85 32 19 81
Restored 96 51 25 126
Abandoned 94 54 27 133
Total 167 93 35 269
C. Carvalho et al. Journal of Environmental Management 318 (2022) 115450

Fig. 2. Overall pollination networks pooling all pollen transport data collected for each area (all months and sites). Line width represents the strength of interactions,
and bar width represents total amount of pollen grains carried by each pollinator taxa (upper level) and total amount of pollen transported for each plant taxa (lower
level). Only the most representative groups of pollinators and plants are identified.

seemed to hold higher within-dissimilarity, consistent with the higher
variability found in the CCA for that area (Fig. 3).
3.3. Community function
In general, we found no significant differences on network-level
metrics attributable to independent effects of the area (Sup. Materials
G Table G.1). In fact, the temporal trends of restored and natural areas
were similar throughout the months, with maximum and minimum
values agreeing concurrently (ISA, ID, SA, and modularity, Fig. 4). The
abandoned area metrics differed from this pattern, showing different
trends (ISA, modularity) or peaking values opposite to those observed in
the other two areas (ID, SA). Significant differences detected in this
study were therefore attributable to either month or interaction effects
between area and month.
Independent monthly effects were observed in Interaction Evenness
(IE significantly lower in February), Linkage Density (LD, significantly
higher in March), and plant community robustness (significantly lower
in April and May).
In many cases, the interaction between area and month was signifi­
cant (ISA, SA, ID, number of pollinator taxa, number of plant taxa and
modularity), showing that metrics varied inconsistently between areas

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C. Carvalho et al. Journal of Environmental Management 318 (2022) 115450

Fig. 3. Results of CCA (first and second components) plotting the variables characterizing local vegetation structure: bare soil (bare_soil), herbaceous (herb_cov),
shrub (shrub_cov) and tree cover (tree_cov), and number of floral units (floral_units). Colored polygons enclose the sampled sites for each area constrained by
vegetation structure variables. Pollinator species are also plotted highlighting the three most relevant Apoidea groups: honeybees (triangle), bumblebees (squares)
and wild bee species (filled circles). The dotted ellipse represents 75% of wild bee groups, weighted by their abundance.

over time. The number of pollinator and plant taxa presented the larger
variation among all analyzed metrics, despite being very similar for all
areas in February. In the abandoned area, the number of pollinator and
plant taxa increased consistently over time. Between the restored and
natural areas, the restored sites had significantly higher values of
pollinator taxa in March, and of plant taxa in March and May.
Significant values were validated through the randomization pro­
cedure (see Supplementary Material H). No differences were detected
for specialization metric H2 and robustness of the pollinator community
to plant extinctions.
Species level metrics calculated for the overall area networks showed
significant differences for honey bees and bumblebees (Fig. 5, Sup.
Materials G Table G.2). For honey bees species strength was higher in
natural areas, indicating a higher importance for the plant community,
though the difference was most significant when compared to the
restored area. Pollination service (PSI) and specialization indices were
also significantly higher for honey bees in natural areas compared to the
other areas, indicating a better pollination service provision and a more
specialized behavior, respectively. Contrastingly, partner diversity was
significantly higher in abandoned locations, demonstrating more
generalized behavior in this area. For bumblebees, only species strength
(the dependence of the plant community on a given pollinator) was
significantly different, being much higher in the abandoned area. No
differences were detected for wild bees, though there was a tendency for
higher relevance for the plant communities in the restored area (SS,
Fig. 5).
Niche analysis showed high overlap (between 84.3% and 92.2%)
between all bee groups. Further exploring these relations, we found a
significantly inverse relationship between honey bee and wild bee
abundance (r2 = 0.453, p-value = 0.047), i.e., the combined abundance
of wild solitary bee species decreased with increasing abundance of
social honey bees. Relationships between bumblebees and honey bees
(r2 = 0.007, p-value = 0.831) as well as bumblebees and wild bees (r2 =
0.011, p-value = 0.788) were not significant.
4. Discussion
Our results show functionally similar network structures between
areas, but network metrics in the actively restored area more closely
followed the patterns found in the natural area, as expected. Differences
between the abandoned area and the other two areas occurred sporad­
ically within a few periods, which can be associated with intrinsic local
conditions, such as flower resource availability. Since independent ef­
fects of area type were not identified, our results also support that
pollination service is being provided similarly in all areas, though pro­
visioned by different species. Therefore, communities associated with
each area, though different, are not significantly less proficient
pollinators.

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C. Carvalho et al. Journal of Environmental Management 318 (2022) 115450

Fig. 4. Temporal trends of each network metric for the different area. Trend lines link mean values for each metric and error bars represent standard error. Asterisks
signal significant differences.

7
C. Carvalho et al.
4.1. Effects of quarry restoration on pollinator services
Monthly effects had, as expected, a significant impact on network
structure, with differences found mainly in February and April. These
differences may relate to uneven flower resource availability, both in
number and diversity (Sup. Materials H), as suggested in other studies
(e.g., for bacteria-bacteriophage: Poisot et al., 2011; plant-frugivore
networks: Carnicer et al., 2009; Ramos-Robles et al., 2016). Flower
resource availability and diversity mediate the structural properties of
networks by constraining species interactions. For instance, in February,
networks were dominated by the interactions between Apoidea (namely,
Apis mellifera and Bombus terrestris) and Rosmarinus officinalis. Since
February is the coldest of the analyzed months, with an average tem­
perature of 11.3 ◦ C (4.9 ◦ C lower than the annual average; information
retrieved from www.ipma.pt in February 2022), early blooming plants
and large-bodied social pollinators able to resist the lower temperatures
(McCabe et al., 2019) interact intensively. Consequently, as this rela­
tionship unbalances the network, interaction evenness and diversity are
lower.
Over the course of the season, as both pollinators and plants diver­
sified, differences in vegetation composition between areas become
more obvious. Between the sampling sessions of March and April, flower
availability sharply declined in all areas (Sup. Materials H Fig. H.2).
However, in abandoned sites, a richer herbaceous layer composed of
ruderal species from early successional stages likely maintained a high
floral diversity throughout the study period. While in natural and
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Journal of Environmental Management 318 (2022) 115450
Fig. 5. Summary of species level metrics
calculated for each bee group in each area
type (natural area in green, restored area in
blue, and abandoned area in orange). Bars
represent mean values and error bars repre­
sent standard error. For metrics and groups
where significant differences were found,
letters in bars are used to represent how the
different areas are grouped together. (For
interpretation of the references to colour in
this figure legend, the reader is referred to
the Web version of this article.)
restored sites pollinators become very dependent on the few plant spe­
cies available, the more diverse plant community in the abandoned area
buffered against the shortage of flower resources supporting an
increasingly diverse and specialized pollinator community (reflected by
a higher specialization asymmetry and modularity, characteristic of
larger networks (Olesen et al., 2007)).
Overall, metrics obtained in the restored area follow the same pat­
terns of the natural area, which indicates a similar state of the pollina­
tion service. Although metrics in the abandoned area tended to differ in
specific months, there was no evidence for area independent effects. The
abandoned area is still evolving from early successional stages and its
distinctive pattern can be explained by local conditions that operate in
specific periods of the flowering season, namely driven by the presence
of ruderal species which are absent in other areas. In this regard, our
results support that active restoration may speed-up the recovery of an
ecological process in quarried areas, while in ecological succession this
process takes longer to achieve similar functioning as in natural refer­
ence ecosystem.
4.2. Pollinator community: composition and function
Our results demonstrate that pollination, despite showing relatively
similar network structures between areas, is provisioned by different
species in the different areas. This result is also reported in other polli­
nation studies, where changes in species composition and interactions
can occur without major alterations of the overall network structure
C. Carvalho et al.
(Alarcón, 2010; Forup and Memmott, 2005; Forup et al., 2008; Nielsen
and Totland, 2014; Petanidou et al., 2008). In our study, compositional
analyses showed distinct communities occurring in each area, signaling
the restored area as the most dissimilar. These compositional differences
likely correspond to differences in vegetation structure, that can influ­
ence the availability and suitability of floral resources. For instance,
restoration practices have supplied the restored areas with non-native
conifer species, thus changing the structure of the habitat. Mexia et al.
(2020) has found for the same restored area that these practices have led
to further changes on native vegetation, with further effects on the
composition and structure of epigean beetle communities.
On the other hand, both natural and abandoned areas share higher
similarity of pollinator species, but agree less in their ecological func­
tion. This result implies that some pollinators may have different roles
within the networks depending on the area. Honey bees, for example,
acted differently across all areas, being more important pollinators in
the natural area where they were common and specialized (see also
Dormann, 2011). In contrast, bumblebees were more important for the
plant community of the abandoned quarries where they assumed a
generalist and opportunistic foraging behavior (see also Fontaine et al.,
2008). Wild bees showed a more consistent role across all areas, but
seemed to be more important in restored sites. These wild bee species
may benefit from bare soil cover and presence of stone piles, which are
appealing conditions for many ground-nesting and cavity-nesting spe­
cies, respectively (Tiedeken and FitzPatrick, 2016). In conclusion,
different pollinator communities show different importance in the pro­
vision of pollination services in each area: honey bees play the most
important role in the natural area, bumblebees in the abandoned
quarries and wild bees in the restored sites.
The inverse relationship between honey bee and wild bee abun­
dance, coupled with their high niche overlap, suggests a possible conflict
between both. There are growing concerns reported in the Mediterra­
nean basin signaling the replacement of wild bees by increasing honey
bee abundance, which may be leading the former to decline (Herrera,
2020). Consequently, high dominance of honey bees contributes to the
homogenization of pollinator communities. It is possible that the lower
abundance of honey bees in restored sites is favoring higher abundance
of wild bees.
4.3. Caveats and implications for restoration management and assessment
One of the main limitations of this study was the location of spatial
replicates which was constrained by the number of quarried sites with
particular restoration approaches. This resulted in a high spatial clus­
tering of sites of the different area types analyzed. We tried to overcome
this issue by selecting statistical methods that accounted for within site
random effects to control for possible bias, and by testing our results
through a randomization procedure. Our results suggest that active
restoration allowed for faster recovery of ecosystem function. After
20–30 years of active restoration, the pollination process in restored
areas was more similar to natural areas than 40 years of natural suc­
cession in spontaneously restored areas. Despite the slower rate, natural
succession also appeared to allow for function recovery, even showing
greater diversity and higher levels of specialization. However, aban­
doned areas were located at much smaller quarry sites, lessening the
effects of habitat degradation by being closer to remnant natural habi­
tats (Cusser and Goodell, 2013). Nevertheless, the ongoing natural
process of succession in the abandoned areas has allowed for the
establishment of ruderal opportunistic plants (e.g. Rubus ulmifolius,
Echium plantagineum) likely contributing to the maintenance of overall
complex networks. This outcome can support future restoration-assisted
approaches. For instance, the lower robustness of the plant community
in recently restored sites could be circumvented through the use of
native “bridging” plants that flower in different periods, such as her­
baceous plants (species of Allium, Carduus and Malva), providing nectar
and pollen resources when their availability from other plants is lower
9
Journal of Environmental Management 318 (2022) 115450
(Menz et al., 2011). This should promote floral heterogeneity,
strengthening the pollinator community and consequently increasing
the robustness of the plant community.
Our results also highlight the importance of considering ecosystem
function as well as compositional assessments in restoration planning
and evaluation as both are attributes of restored ecosystems (SER,
2004). In our study, though pollinator composition differed significantly
between areas, restored areas showed more similar functioning to the
natural reference ecosystem. Although ecosystem functioning has been
restored, the system has evolved into an alternative state of recovery
because plant and pollinator communities differ from the natural
reference areas. Nevertheless, our findings are in line with previous
research demonstrating that restoration can be achieved with distinct
biological communities providing function and ecosystem services as
effectively as the communities found in natural ecosystems (Denning
and Foster, 2018; Forup and Memmott, 2005; Williams, 2011). In this
regard, species composition assessments alone may fail to reflect
restoration success, diverting the allocation of limited resources into
unnecessary actions.
Finally, the relationship between wild and honey bee species needs
further clarification, especially considering the implications for resto­
ration. Although honey bees are widely acknowledged to promote
pollination, their effects on the local and diverse community of wild
bees, and on plant reproductive success, are of concern (Forup et al.,
2008; Herrera, 2020; Lomov et al., 2010). The provision of suitable
habitat conditions and varied flower resources as well as nesting sub­
strates (creation of sand pits, log piles, bee hotels) can be easily un­
dertaken in active restoration plans to promote wild bee occurrence and
abundance.
Data accessibility statement
Data available on Figshare 10.6084/m9.figshare.20072396.
Author contributions
Carolina Carvalho: Conceptualization, Methodology, Investigation,
Formal analysis, Writing – original draft Pedro A. Salgueiro: Concep­
tualization, Methodology, Investigation, Formal analysis, Writing –
original draft Amália Oliveira: Conceptualization, Methodology,
Investigation, Writing – review & editing Carmo Silva: Conceptualiza­
tion, Methodology, Resources, Writing – review & editing Ana Sam­
paio: Investigation, Writing – review & editing Marta Parrinha:
Investigation, Writing – review & editing Elsa Caeiro: Investigation,
Resources, Writing – review & editing Otília Miralto: Investigation,
Writing – review & editing António Mira: Resources, Writing – review
& editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
We are thankful to Alexandra Silva for her valuable assistance in the
experiment. Fieldwork and logistics were supported by SECIL — Com­
panhia Geral de Cal e Cimento, S.A., in the scope of the project “Estudo e
Valorização da Biodiversidade – Componente da Fauna – na Propriedade
SECIL-Outão, 5a Fase”. We are also grateful to Dr. Sean Tomlinson and
four other reviewers for their important contributes to improving the
manuscript.
C. Carvalho et al.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.jenvman.2022.115450.
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