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Effects of habitat loss on the plant-flower visitor network structure of a dune community

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Pollination is a valuable ecosystem service, and plant–pollinator interactions in particular are known to play a crucial role in conservation and ecosystem functioning. These mutualisms, like other ecological interactions, are currently threatened by different drivers of global change, mainly habitat loss, fragmentation, or modification of its quality. Most studies so far have focused on the impact of such disturbances on particular species interactions and we thus need more empirical evidence on the responses at a community-level. Here we evaluated how habitat loss influenced the pattern of interactions between plants and their flower visitors in a coastal dune marshland community. Using data from four years (2008–2011), we assessed the effect of a large disturbance in the area (occurring in 2010) that represented the loss of more than 50% of the vegetation cover. We found a considerable decrease in species richness and abundance of flower visitors, which resulted in a lower number of interactions after the disturbance. Not all functional groups, however, responded similarly. Contrary to the expected from previous findings, bees and wasps were less negatively influenced than beetles, flies and ants, possibly due to their higher movement capacity. Species interactions in the community were more specialized after habitat loss, resulting in a lower level of network nestedness and a higher modularity. At a species level, the number of flower visitors per plant decreased after the disturbance, and plants were visited by less abundant flower visitors. Our findings lead us to predict that the overall plant–flower visitor network became less robust and resilient to future perturbations. However, the fact that each functional group responds distinctly to disturbances makes it more difficult to foresee the final consequences on community composition and ecosystem functioning.
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Effects of habitat loss on the plant ower visitor network structure
of a dune community
Anna Traveset , Roc í o Castro-Urgal , Xavier Rotll à n-Puig and Amparo L á zaro
A. Traveset ( (, R. Castro-Urgal, X. Rotll à n-Puig (
0621) and A. L á zaro, Mediterranean Inst. for Advanced Studies - Biodiversity and Conservation, c/Miquel Marqu é s 21, ES-07190 Esporles,
Mallorca, Balearic Islands, Spain.
Pollination is a valuable ecosystem service, and plant pollinator interactions in particular are known to play a crucial role
in conservation and ecosystem functioning.  ese mutualisms, like other ecological interactions, are currently threatened
by diff erent drivers of global change, mainly habitat loss, fragmentation, or modifi cation of its quality. Most studies so
far have focused on the impact of such disturbances on particular species interactions and we thus need more empirical
evidence on the responses at a community-level. Here we evaluated how habitat loss infl uenced the pattern of interactions
between plants and their fl ower visitors in a coastal dune marshland community. Using data from four years (2008 2011),
we assessed the eff ect of a large disturbance in the area (occurring in 2010) that represented the loss of more than 50% of
the vegetation cover. We found a considerable decrease in species richness and abundance of fl ower visitors, which resulted
in a lower number of interactions after the disturbance. Not all functional groups, however, responded similarly. Contrary
to the expected from previous fi ndings, bees and wasps were less negatively infl uenced than beetles, fl ies and ants, possibly
due to their higher movement capacity. Species interactions in the community were more specialized after habitat loss,
resulting in a lower level of network nestedness and a higher modularity. At a species level, the number of fl ower visitors
per plant decreased after the disturbance, and plants were visited by less abundant fl ower visitors. Our fi ndings lead us to
predict that the overall plant ower visitor network became less robust and resilient to future perturbations. However, the
fact that each functional group responds distinctly to disturbances makes it more diffi cult to foresee the fi nal consequences
on community composition and ecosystem functioning.
e interactions between plants and their pollinators play a
crucial role in biodiversity, conservation and ecosystem func-
tioning. Habitat loss, fragmentation and changes in habi-
tat quality, and in landscape structure in general, represent
major threats to such interactions and thus to both plant
and pollinator species persistence in the communities. Stud-
ies examining such threats at a community level, however,
are still few and we thus have rather little empirical evidence
on the fi nal consequences of such habitat and landscape
changes for the functioning of this important ecosystem
service (Klein et al. 2007, Hagen et al. 2012, Ferreira et al.
2013, Nielsen and Totland 2014). Previous work has shown
that a reduction in habitat quality and landscape heterogene-
ity cause species losses and leads to changes in the pattern of
interactions among species, i.e. in the interaction network
structure (Tylianakis et al. 2007, Gonz á lez et al. 2011). By
reducing pollinator availability and diversity due to decreased
oral resource supplies as well as nesting sites, habitat
modifi cations can infl uence the levels of cross-pollination
and, ultimately, fruit and seed production (Aguilar et al.
2006, Winfree et al. 2011, Hagen et al. 2012, Viana et al.
2012, Ferreira et al. 2013, Vanbergen et al. 2014). Likewise,
variation in conspecifi c plant densities may aff ect plant
reproductive success by changing the pollinator-mediated
connectivity between individuals in a plant population at
diff erent spatial scales (Hegland et al. 2014, Vanbergen et al.
2014).  is indicates that, by altering interspecifi c interac-
tions at a plant community-level, habitat disturbance can cas-
cade down aff ecting the patterns of gene fl ow across levels of
biological organization and potentially driving evolutionary
changes (Eckert et al. 2010, Ferreira et al. 2013).
Rare and specialized interactions have shown to be
the fi rst to disappear after habitat reduction, and thus an
increase in the frequency of generalist plants and/or pollina-
tor species is usually observed (Ashworth et al. 2004, Aizen
et al. 2012, Vanbergen et al. 2014). A decrease in network
nestedness in disturbed habitats has been reported in several
systems (Vanbergen et al. 2014, Moreira et al. 2015, Revilla
et al. 2015), which has led authors to predict reductions
in the number of coexisting species (Bastolla et al. 2009),
and in the robustness and resilience of plant pollinator net-
works to further perturbations (Bascompte 2009, Fortuna
et al. 2013).  e loss of species and their interactions in a
disturbed network can also lead to the formation of isolated
compartments within the network (Spiesman and Inouye
2013) which run a higher risk of disappearing after future
disturbances than if species are connected in a cohesive
network. Diff erent models have shown that the distribution
© 2017  e Authors. Oikos © 2017 Nordic Society Oikos
Subject Editor: Paulo Guimar ã es Jr. Editor-in-Chief: Dries Bonte. Accepted 29 May 2017
Oikos 000: 001–010, 2017
doi: 10.1111/oik.04154
of number of interactions becomes more skewed when mov-
ing from pristine to disturbed systems, and that mutualis-
tic networks might collapse at critical habitat destruction
thresholds (Keitt 2009, Kaiser-Bunbury et al. 2010, Viana
et al. 2012, Fortuna et al. 2013).
Habitat degradation may also cause homogenization of
the plant pollinator networks by promoting higher link-
diversity but lower link-turnover in disturbed sites compared
to undisturbed ones (Nielsen and Totland 2014). Moreover,
the particular species network functional role can change
notably along a disturbance gradient.  us, a plant species
can act as a hub (being at the network core) in one site but as
a specialist (being at the network periphery) in another site
(Campos-Navarrete et al. 2013, Nielsen and Totland 2014).
Module and network hubs (i.e. species highly connected
within their modules and with other species in other mod-
ules, respectively), together with connectors (species that
link diff erent modules), are considered keystone species for
sustaining network structure and thus their removal due to a
disturbance would have the strongest eff ects and might even
collapse the network (Olesen et al. 2007, Kaiser-Bunbury
et al. 2010, Fortuna et al. 2013).
Changes in pollinators diversity are frequently reported
mostly due to increased isolation of habitat patches and
reduced landscape complexity caused by environmental
simplifi cation (Ferreira et al. 2013). However, not all pol-
linator species respond similarly to habitat changes. Social
bees, for instance, are known to be sensitive to changes in the
distribution of nesting and foraging habitats in the landscape
(Williams et al. 2010, Carvell et al. 2012, Kennedy et al.
2013, Garibaldi et al. 2014); thus, land cover changes
can directly aff ect individual survival probability, locally
reducing species abundance (Ferreira et al. 2015). Solitary
bees, however, may be more aff ected by habitat destruction
as they are more specialized in food resources or nesting
sites than social bees (Williams et al. 2010, Ferreira et al.
2015). By contrast, non-social insects with free-living prog-
eny (e.g. dipterans, coleopterans) may be less aff ected by
distance between resource patches, as they do not need to
return to their brood cells repeatedly after foraging (Jauker
et al. 2009, Parsche et al. 2011). Moreover, fl ower visitor
abundance and species richness have been shown to increase
with fl oral abundance (Hegland and Boeke 2006, Hagen
and Kraemer 2010) and plant diversity (Potts et al. 2003,
Ghazoul 2006, Bl ü thgen et al. 2007, Ebeling et al. 2008).
In general, there is still scarce information on how diff er-
ent pollinator functional groups can respond to habitat dis-
turbance (Burkle et al. 2013, Aguirre-Guti é rrez et al. 2015,
L á zaro et al. 2016) and how they change their interaction
patterns with plants in the community (e.g. their rewiring
capacity within the network).
In this study, we aimed at evaluating the impact of habitat
disturbance (habitat loss, in particular) on the patterns of
plant – fl ower visitor interactions in a coastal dune marshland
community at the north of Mallorca (Balearic Islands, western
Mediterranean Sea).  e plant – fl ower visitor network of this
community was monitored for four consecutive years, from
2008 to 2011. After the fl owering season of 2010, the study
area was greatly disturbed due to the construction of a golf
course that caused the loss of ca 50% of the vegetation cover,
leaving the bare soil (Fig. 1).  is provided an opportunity
to assess the extent to which substantial habitat loss altered
the interactions between plants and their fl ower visitors.
Our specifi c questions were the following: 1) did network
structural properties change after habitat disturbance more
than the expected from temporal changes in the previous
years? 2) To what extent were fl oral resources and species
richness and abundance of fl ower visitors aff ected by the dis-
turbance? 3) At the species level, how consistent across years
were degree (linkage level), contribution to nestedness, level
of selectiveness, strength, and weighted closeness centrality,
and did these parameters change notably after the distur-
bance? 4) Which fl ower visitors functional groups and which
plant species (regarding traits such as fl ower abundance and
oral symmetry) experienced the greatest changes in species
level parameters after the disturbance? 5) If networks had a
modular structure, how consistent in time were species roles
regarding modularity, and did they change more after the
disturbance relative to previous years?
Study site
e study was carried out in Son Bosc (39 ° 46 28.11 N ,
3 ° 07 45.34 E), a diverse dune marshland in northern
Mallorca, adjacent to S Albufera Natural Park.  e
predominant vegetation consists of Daucus carota (Apiaceae),
Helichrysum stoecha s (Asteraceae), Lotus corniculatus
Figure 1. Aerial photograph showing the study area before (A) and
after (B) the disturbance (soil removal for a golf course construction).
e green line marks the study area, the red line the disturbed area
and the vertical black and white pattern the study area damaged.
(Fabaceae), Lotus cytisoides (Fabaceae), Scabiosa atropurpurea
(Dipsacaceae) and Teucrium dunense (Lamiaceae) and over
80 fl owering species have been recorded in the area, mostly
annual plants although also some shrubs like Cistus salviifolius
(Cistaceae) and Myoporum tenuifolium (Myoporaceae). Such
a high diversity of fl owers allows maintaining an also high
diversity of fl ower-visitors (ca 125 spp.), a good fraction of
which nest in the sandy soils of this area. Specifi cally, this
area bears the highest bee species richness of Mallorca Island
(D. Baldock pers. comm.).
We performed censuses in Son Bosc during four consecu-
tive years, from 2008 to 2011. During the summer of 2010,
an area of ca 2.3 ha was disturbed due to the construction
of a golf course, representing 52.3% of the total area covered
in our study (ca 4.5 ha; delimited in green in Fig. 1). Given
that the largest disturbance occurred when most plants had
already fl owered in 2010, we expected the highest impact on
the plant – fl ower visitor network the following year.  us,
during 2011, we kept censusing all fl owering plants in the
remaining unaltered area including as well other plant
species that were still present in the surroundings of the
disturbed area (bare soil).
Sampling methods
All plants in bloom were monitored throughout the fl owering
season, from early April to the end of July. Once or twice
per week, we made insect censuses on fl owers from
haphazardly selected individuals from all fl owering plant
species. Censuses were done from 10:00 a.m. to 17:00 p.m.
on sunny and non-windy days. Insect visits to fl owers were
recorded from a distance of approximately 1 m to minimize
interference with insect behavior. We recorded contacts of
insect visitors to fl owers during 3 5 min periods. Due to
the small fl ower size of most species, insects nearly always
touched the reproductive parts of the fl ower, although we
did not record this or their behaviour. Hence, we use the
term fl ower - visitation networks, regardless of the effi ciency
of each insect visitor in the pollination process. We must
note, however, that considering such effi ciency and distin-
guishing between true pollinators from those that act as
cheaters might lead to a diff erent network structure, e.g. the
network might be more specialized (Alarc ó n 2010, Genini
et al. 2010). During each census we recorded: 1) identity of
owering plant species; 2) number of open fl owers of each
individual plant observed; 3) identity of each fl ower visitor;
4) number of individuals of each species visiting fl owers; and
5) number of fl owers visited by each fl ower visitor. When
ower visitors could not be identifi ed in the fi eld, these were
collected (usually after fi nishing the census) for identifi ca-
tion by taxonomists. We categorized fl ower visitor species
into the following functional groups (as done in previous
studies; Fenster et al. 2004): ants, bees, beetles, hoverfl ies,
ies (mainly muscoid fl ies), butterfl ies, wasps and others
(mostly hemiptera).
Time spent censusing fl ower visitors along the entire
season was on average 36.3 h. Most intensive sampling
was from 2009 to 2011, when we also estimated fl ower
abundance fortnightly at each site. In each fl ower census,
we recorded the number of all open fl owers of each fl ower-
ing plant encountered within permanent belt transects; we
surveyed 13 transects (50 2 m) in 2009 and 10 transects
in 2010 and 2011, covering a total area of 1300 m
2 and
1000 m
2 , respectively. Further details on sampling can be
found in Castro-Urgal et al. (2012).
Network parameters
We built four quantitative interactions matrices (one for
each year) using the number of visits per unit time as link
weight. For each network, we calculated the most widely
used quantitative descriptors of the structure of weighted
ecological interaction networks (Tylianakis et al. 2010).
At network level, these were: connectance (C), weighted
nestedness (WNODF), complementary specialization H 2 ,
interaction evenness (IE) and quantitative modularity (Q).
At species level, we obtained the following metrics both for
each plant and fl ower visitor species in the networks: degree,
strength, species selectiveness (d ) (termed index of special-
ization in other studies; Bl ü thgen et al. 2006), weighted
closeness centrality (wCC), contribution to nestedness ni (see
Supplementary material Appendix 1 for defi nitions of each
parameter), standardized connection c and participation
values z ’ . We used the bipartite package ver. 1.18 (Dormann
et al. 2009) run in R to obtain all these network metrics,
except WNODF and contribution to nestedness which were
obtained with the software NODF ver. 2.0 ( < www.keib. > )(nestedness based on overlap and decreas-
ing fi ll; Almeida-Neto and Ulrich 2011).  e signifi cance
of WNODF values was assessed against 100 randomizations
using the ‘ rc ’ and ‘ p null models; the ‘ rc ’ model resamples
with row/column weights fi xed, while the p model ran-
domizes proportional to the respective marginal distribution
(Almeida-Neto and Ulrich 2011).
Quantitative modularity ( Q ) was estimated using the
QuanBIMo algorithm (Dormann and Strauss 2014), which
is implemented in R . It consists of a recurrent Markov chain
Monte Carlo (MCMC) algorithm to fi nd the best division
of nodes (species) into modules. A total of 10
steps were used with a tolerance level of 10
10 . As Q values
can vary among diff erent runs, we repeated the calculations
100 times for each network using the computeModules
function and selected the iteration with maximum likeli-
hood as the best estimation of Q. To account for Q s depen-
dence on network size and test the signifi cance of modularity
values, we calculated a z-score for each network by running
the same algorithm in 100 random networks with identi-
cal marginal totals as the empirical network (using the null
model r2d ; Guimer à and Amaral 2005) and comparing the
modularity values between random and empirical networks.
Such tests were done in the bipartite package (Dormann and
Strauss 2014).
Following Guimer à and Amaral (2005), we identifi ed
species with important roles in the network by computing
standardized connection and participation values ( c and z ,
respectively). While c refers to the even distribution of links
across modules, z refers to within-module degrees.
Statistical analysis
All analyses were conducted in R ver. 3.1.2 ( < www.r-project.
org > ). To compare species richness of fl ower visitors among
habitat disturbance (2011) than the three previous years
(Table 1).  e number of plant species was also reduced
after the disturbance but to a lower extent than the number
of fl ower visitors (Table 1). All networks showed a highly
consistent connectance around 5%.  e networks were sig-
nifi cantly nested (p 0.001), meaning that the partners of
the most specialized species are a subset of those that interact
with the most generalist species (Table 1).  e lower nested-
ness in 2011 might thus result from the loss of some generalist
species after the disturbance and/or from an increase in
specialized interactions; the latter is actually supported by
the higher H 2 value in 2011 (Table 1). Interaction evenness
was moderate (ca 0.50) across the four years of the study
(Table 1). Finally, the networks were signifi cantly modu-
lar each year; however, while both modularity (Q) and the
number of modules were higher in 2011 than the other
years, this was not the case for z-scores (Table 1).
Overall, species richness of fl ower visitors was lower in
2011 (mean SE: 10.75 3.65) compared to the previous
years (14.71 2.23) ( χ 2 8.25, df 3, p 0.046). How-
ever, this diff erence was mostly due to a decrease in beetle
and fl ie species richness (Table 2).  e other groups barely
changed across the four years of the study. Regarding fl ower
visitor abundance, the best model showed that it varied sig-
nifi cantly among all the study years, consistently among
functional groups (year: χ 2 72.45, df 3, p 0.0001).
It was lowest in 2011 (visits min
– 1 : 0.09 0.02), highest
in 2010 and 2009 (1.10 0.11 and 1.12 0.004,
respectively), and intermediate in 2008 (0.18 0.02).
years, we performed a generalized linear model (GLM) using a
Poisson distribution and log as link function. In this analysis,
year was included as a fi xed categorical factor whereas the
number of species in each fl ower visitor functional group as
sampling units.  e interannual variations in species level
network parameters and abundances were analysed by means
of generalized linear mixed models (GLMM, package lme4 )
that included species as a random factor to avoid pseudorep-
lication. We used separate models for plants and fl ower visi-
tors, and for each network parameter.  e models for plants
only included year as fi xed categorical predictor variable,
whereas those for fl ower visitors also included functional
group and its interaction with year. If the interaction was
non-signifi cant, we run the models with the fi xed variables
separately and chose the best model based on AIC. All func-
tional groups were included in the models, except for the
others group owing to its low species number. Due to the
nature of the data, we used: 1) Poisson distribution and log
link functions for the degree analyses, after checking for the
absence of overdispersed data (Zuur et al. 2009); 2) Gaussian
distribution and log link function for the models of selec-
tiveness; and 3) gamma distribution and log link function
for the rest of the variables.  e consistency among years in
species roles within the network was also analysed by means
of GLMMs, including c and z as response variables, year as
xed factor, and species as random factor. Plant species were
the sampling units, and data were adjusted to a gamma dis-
tribution in each model.
As we found signifi cant diff erences in both plant degree
and selectiveness between 2011 and the average of the three
previous years, we further assessed whether such diff erences
were associated to changes in the prevalence of plant spe-
cies with diff erent fl ower symmetry and diff erent ower
abundances. For this, we performed two separate GLMs
to analyse the after-disturbance change in degree and selec-
tiveness (calculated as the diff erence between the degree/
selectiveness in 2011 and the average degree/selectiveness
in the previous years) as response variables, and fl ower
symmetry (zygomorphic versus actinomorphic) and fl ower
abundance (average from 2009 2011) as independent pre-
dictor variables. In both models, sampling units were the
study plant species, and a Gaussian distribution was used
given that the response variables fullfi lled the assumptions
of normalilty.
Post hoc analyses to test for diff erences among levels of
a signifi cant factor were conducted using Tukey a posteriori
tests (package multicomp in R).
Data deposition
Data available from the Fileshare Repository: < https:// > .
(Traveset et al. 2017).
Overall community structure
e number of fl ower visitor species, number of links and
weighted nestedness were much lower the year following
Table 1. Network parameters for each study year. WNODF: weighted
nestedness, H
2 : index of specialization (selectiveness), IE: interac-
tion evenness. For modularity, the z-score is given, as the Q observed
is compared to that expected with a null model based on marginal
totals (representing abundance distributions of plants and fl ower
visitors; see Dormann and Strauss 2014 for further details).
2008 2009 2010 2011
No. plants 56 68 67 52
No. fl ower visitors 120 110 123 86
No. links 347 390 494 248
Connectance 0.052 0.052 0.060 0.055
WNODF 7.698 8.67 9.412 5.456
2 0.589 0.618 0.547 0.685
IE 0.532 0.529 0.514 0.497
Modularity (Q) 0.307 0.370 0.368 0.568
Number of modules 8 8 6 13
Modularity z-score 316.60 760.34 722.79 303.58
Table 2. Species richness in each fl ower visitor group across the four
study years. The groups in which species richness was considerably
reduced after habitat disturbance are marked with an asterisk.
Flower visitor group 2008 2009 2010 2011
Ants 6 3 4 2
Bees 29 35 38 31
Beetles 25 24 29 18
Butterfl ies 7 5 3 3
Flies 25 18 23 11
Hoverfl ies 5 6 6 5
Wasps 13 13 14 15
Others 11 6 6 1
observed in weighted closeness centrality and contribution
to nestedness, but these did not seem to be related to the
disturbance, as both parameters were signifi cantly diff erent
between 2008 and the other years (Fig. 2C D), whereas the
values in 2011 did not diff er signifi cantly from those in other
years (Fig. 2C D).
Flower abundance positively infl uenced the after-
disturbance change in plant species degree ( χ 2 4.57,
df 1, p 0.03) but not in selectiveness ( χ 2 0.60, df 1 ,
Species-level network properties
Plant species
At the species level, network parameters diff ered signifi cantly
among years, except plants strength (Table 3). In 2011, plants
degree was signifi cantly lower (Fig. 2A) and selectiveness was
signifi cantly higher (Fig. 2B) than the previous years; that
is, the number of fl ower visitors per plant decreased after
the disturbance, and plants were visited by less abundant
ower visitors. Signifi cant diff erences among years were also
Table 3. Results of the generalized linear models comparing species level network parameters among the study years for plants and fl ower
visitors. When the interaction between year and functional group was signifi cant, the LRT for the interaction is given, but both factors were
also included in the models.
Species-level network index
Flower visitors
Year Flower visitor group
2 55.14, p 0.0001 χ
2 36.34, p 0.006
Strength χ
2 5.14, p 0.162
χ 18
2 36.40, p 0.006
Selectiveness (d )
χ 3
2 27.59, p 0.0001 χ
2 64.09, p 0.0001
Weighted closeness centrality χ
2 139.78, p 0.0001 χ
2 51.78, p 0.0001
Contribution to nestedness χ
2 15.4, p 0.001
χ 18
2 51.79, p 0.0001
Standardized connection ( c )
χ 3
2 10.55, p 0.014
2 34.99, p 0.009
Participation values ( z ) χ
2 4.07, p 0.25
χ 18
2 20.37, p 0.31
Figure 2. Mean ( SE) values of (A) degree; (B) selectiveness (d ); (C) weighted closeness centrality; and (D) contribution to nestedness for
plants across the study years. Diff erent letters indicate signifi cant diff erences among years. Note that the higher the negative value, the more
the species contributes to nestedness (following defi nition by Almeida-Neto and Ulrich 2011).
on the after-disturbance change in either degree ( χ 2 0.82,
df 1, p 0.37) or selectiveness ( χ 2 0.81, df 1 ,
p 0.37), i.e. both actinomorphic and zygomorphic species
responded similarly to the disturbance regarding these two
p 0.44). In other words, those species producing more
owers were those most aff ected by the decrease in number
of fl ower visitors after the disturbance, although they were
not necessarily those showing a higher selectiveness. On the
other hand, fl ower symmetry did not have a signifi cant eff ect
Figure 3. Mean ( SE) values of (A) degree, (B) strength, and (C) selectiveness (d ) across years for each fl ower visitor group. In all cases,
the interaction between year and fl ower visitor group was signifi cant at p 0.05. Diff erent letters indicate signifi cant diff erences among
years within each functional group.
Lastly, ies and hoverfl ies tended to contribute more,
but ants less, to nestedness in 2011 than the other years,
though diff erences were not signifi cant.  e rest of groups
showed interannual variations that were not related to the
disturbance (Fig. 4B).
Species roles in the networks
Standardized connection, c , varied among years for plant
species (Table 3), although such variation was unrelated to
the disturbance (Fig. 5A). By contrast, the loss of habitat did
infl uence c for fl ower visitors, although this was contingent
upon the functional group (Table 3, Fig. 5B). Both ants and
butterfl ies showed lower c in 2011 compared to the previ-
ous years whereas the other fl ower visitors showed either no
signifi cant variation across years or variation was not related
to the disturbance (Fig. 5B).
On the contrary, participation values, z , showed low
temporal variation for both plants (Table 3) and fl ower
visitors (year: χ 2 2.92, df 3, p 0.40; functional group:
χ 2 5.11, df 6, p 0.53), and there was not signifi cant
interaction year functional group; Table 3).
Flower visitor species
For all species level network parameters, a signifi cant inter-
action was found between year and fl ower visitor functional
group (Table 3), indicating that such groups do not vary
consistently along time. Ants, beetles, and butterfl ies showed
lower degrees in 2011 compared to the other years, whereas
the rest of functional groups either showed no annual
diff erences in their degree, or these were not due to the
disturbance (Fig. 3A). Ants also showed a reduced strength
in 2011 compared to the previous years (Fig. 3B), whereas
the other groups showed either no variation among years or
the variation was not related to the disturbance (Fig. 3B).
e loss of habitat led to a higher insect selectiveness,
d , in all functional groups, although only ants and beetles
were signifi canty more selective after the disturbance than
the previous years (Fig. 3C).
Regarding weighted closeness centrality, ants and
butterfl ies showed lower values in 2011 than the previous
years, although diff erences were signifi cantly only for ants
(Fig. 4A).  e other fl ower visitor groups showed either an
increase (bees, beetles and fl ies) or no interannual variations
in this metric (Fig. 4A).
Figure 4. Mean ( SE) values of (A) weighted closeness centrality, and (B) contribution to nestedness across years for each fl ower visitor
group. Note that, according to the defi nititon of contribution to nestedness (Almeida-Neto and Ulrich 2011), a species with negative values
contributes more than one with positive values. In all cases, the interaction between year and fl ower visitor group was signifi cant at
p 0.05. Diff erent letters indicate signifi cant diff erences among years within each functional group.
in 2011 was in fact higher when compared to the previous
years, what would support the lower nestedness values of that
year. Other studies have also documented decreases in net-
work nestedness in disturbed habitats (Vanbergen et al. 2014,
Moreira et al. 2015, Revilla et al. 2015) though not always
(Spiesman and Inouye 2013). A reduced nestedness is often
associated with lower stability and resilience of plant pollina-
tor networks to perturbations (Bastolla et al. 2009, Fortuna
et al. 2013), although there is controversy on this (James et al.
2012, Saavedra and Stouff er 2013, Rohr et al. 2014).
Greater modularity in disturbed habitats compared to
undisturbed ones has also been reported (Spiesman and
Inouye 2013). A more modular network is thought to
reduce the opportunity for species to facilitate one another
by sharing mutualistic partners and thus to have a destabi-
lizing eff ect ( é bault and Fontaine 2010). Dormann and
Strauss (2014) showed that quantitative modularity (Q) was
positively related to complementary specialization H 2 , using
22 quantitative pollination networks. We thus expected that
an increase in H 2 after habitat disturbance might result in a
higher modularity. Both Q and the number of modules were
actually higher in 2011 than the previous years, supporting
the expectation. Nevertheless, when comparing the z-scores,
the temporal diff erences disappeared.
e habitat loss in our study area showed to notably impact
some of the structural properties of the plant ower visitor
network. Although most metrics varied across years, the
number of fl ower visitors and the number of links in the
network decreased much more after the disturbance than
the three previous years.  is is concordant with results from
other studies showing a reduction in pollinator availability
and diversity attributed to a decrease in fl oral resource sup-
plies as well as nesting sites after disturbance (Winfree et al.
2011, Hagen et al. 2012, Ferreira et al. 2013, Vanbergen
et al. 2014). Despite this, network connectance was highly
consistent in time, suggesting that the number of links
changes with a similar proportion as the number of species
does; this has also been reported in other studies that have
examined temporal variation in the structure of pollination
networks (Petanidou et al. 2008). Moreover, the nested pat-
tern of interactions was weaker the year following the dis-
turbance, which suggests that some generalist species (either
plants or fl ower visitors) disappeared or were less abundant
and thus likely had fewer interactions and/or that more
specialized interactions appeared among the prevalent species
in the community.  e level of network specialization ( H 2 )
Figure 5. Mean ( SE) s tandardized connection, c, across years in (A) plant species, and (B) fl ower visitor functional groups.  e interaction
between year and functional group was signifi cant at p 0.05. Diff erent letters indicate signifi cant diff erences among years (A), or among
years within each functional group (B).
resources availability, together with a likely reduction in avail-
able nesting sites for some insect species, led to a reduction
in species richness and abundance of fl oral visitors, which
translated in turn to a less nested and more modular network
composed of more specialized interactions. Not all fl ower-
visitor functional groups were similarly aff ected; beetles, fl ies
and ants were more negatively infl uenced by the disturbance
than other groups such as bees and wasps, what we attribute
to their overall lower mobility.  ese ndings do not sup-
port, thus, the idea that non-social insects with free-living
progeny are less infl uenced by habitat destruction than
social bees (Jauker et al. 2009, Parsche et al. 2011). Future
empirical studies from other systems are necessary to under-
stand the mechanisms by which diff erent functional groups
of fl ower visitors respond to disturbances and to assess the
consequences of such diff erent responses on ecosystem
Acknowledgements We thank Jaume Reus, Pep Mora, Joan
Torrandell and Zeeba Khan for assistance in the fi eld, and David
Gibbs, David Baldock, Jordi Ribes, Marcos B á ez, M. Carles-Tolr á ,
Paco Laroche, Pedro Orom í , Xavier Canyelles and Xavier Espadaler
for insect identifi cations.
Funding is study is framed within projects CGL2010-18759/
BOS and CGL2013- 44386-P fi nanced by the Spanish Ministry of
Economy and Competitiveness. RCU was supported by a predoc-
toral grant from the Spanish Government (Ministry of Economy
and Competitiveness and Ministry of Education, Culture and
Sport), whereas AL was supported by a postdoctoral contract
co-funded by the Regional Government of the Balearic Islands and
the European Social Fund 2014 2020.
Permissions e Servei de Protecci ó d Esp è cies, Espais de Natura
Balear (Conselleria de Agricultura, Medi Ambient and Territori)
provided permissions to work at the study site.
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Supplementary material (available online as Appendix oik-
04154 at < > ).
Appendix 1.
... The SEM partitions the direct and cascading indirect effects of forest fragmentation on floral resource availability, plant and pollinator community structure and the architecture of species interaction networks, using ~20,000 flower visitation records from 68 flowering plant species on 41 islands and 16 mainland sites in the Thousand Island Lake (TIL; Fig. 1) region of eastern China. The TIL system offers a unique opportunity to overcome potential confounding influences of heterogeneous initial At the whole network scale, habitat loss has well-recognized negative effects on plant-pollinator interactions and network architecture [8][9][10][24][25][26] , based predominantly on studies in non-forest systems. Habitat loss causes non-random loss of interactions 8,[27][28][29] , which disrupts plant-pollinator interactions, leading to higher network modularity and lower nestedness 9,26 , which will intensify competition among species at the same trophic level 30,31 and destabilize networks in the face of disturbance 24,32 . ...
... The TIL system offers a unique opportunity to overcome potential confounding influences of heterogeneous initial At the whole network scale, habitat loss has well-recognized negative effects on plant-pollinator interactions and network architecture [8][9][10][24][25][26] , based predominantly on studies in non-forest systems. Habitat loss causes non-random loss of interactions 8,[27][28][29] , which disrupts plant-pollinator interactions, leading to higher network modularity and lower nestedness 9,26 , which will intensify competition among species at the same trophic level 30,31 and destabilize networks in the face of disturbance 24,32 . Meanwhile, network connectance typically increases as habitat area declines 9 , suggesting that fewer potential resource linkages remain in the network 33,34 . ...
... Connectance, defined as the fraction of observed interactions relative to the total possible interactions within a network 54 , is considered as a primary attribute of the network. However, the definition of connectance always overestimates the potentially realizable interactions (that is, ignoring 'forbidden links' in an evolutionary or ecological context), especially for large networks that contain a large number of plants and pollinators that are never likely to interact with one another, and which can cause connectance to be insensitive to changes in realized interactions 26,56 . Here we propose a different measure of 'relative connectance' to more reasonably constrain the number of potential interactions. ...
Full-text available
Edge effects often exacerbate the negative effects of habitat loss on biodiversity. In forested ecosystems, however, many pollinators actually prefer open sunny conditions created by edge disturbances. We tested the hypothesis that forest edges have a positive buffering effect on plant-pollinator interaction networks in the face of declining forest area. In a fragmented land-bridge island system, we recorded ~20,000 plant-pollinator interactions on 41 islands over 3 yr. We show that plant richness and floral resources decline with decreasing forest area at both interior and edge sites, but edges maintain 10-fold higher pollinator abundance and richness regardless of area loss. Edge networks contain highly specialized species, with higher nestedness and lower modularity than interior networks, maintaining high robustness to extinction following area loss while forest interior networks collapse. Anthropogenic forest edges benefit community diversity and network robustness to extinction in the absence of natural gap-phase dynamics in small degraded forest remnants.
... In particular, for the Mediterranean countries, about 50% of the Coleoptera and Lepidoptera show significant downward trends, and some regional bee extinctions are being detected (Sánchez-Bayo & Wyckhuys 2019). Compared to central and northern European countries, the Mediterranean basin has received less attention in pollination diversity studies (but see, for instance, Petanidou & Vokou 1990;1993;Petanidou et al. 2008;Tur et al. 2013;Castro-Urgal & Traveset 2016;Beltran & Traveset 2018;Traveset et al. 2018;Azpiazu et al. 2020;Lázaro et al. 2020). Furthermore, the negative impacts of pollinators' decline in the Mediterranean region at a community level have still been poorly described (Fontaine et al. 2006;Herrera 2020). ...
... Community-level studies, such as those encompassing plant-pollinator interaction networks, provide precious and updated information on the species composition and abundance of pollinators in specific areas. In the Balearic Islands, and specifically in Mallorca, studies with this network approach have been carried out at different locations, from sea level (Castro-Urgal et al. 2012;Castro-Urgal & Traveset 2014Traveset et al. 2018;Lázaro et al. 2020) to the highest altitude of the island (Tur et al. 2013(Tur et al. , 2016. However, no assessment of pollination diversity at the island level and the conservation status of the different taxa have been performed so far. ...
... The dataset used in our study was obtained by compiling previous data from other studies (Castro-Urgal et al. 2012;Tur et al. 2013;Castro-Urgal & Traveset 2014Traveset et al. 2018). Direct censuses of pollinator visits to flowers were performed in 10-13 (50 x 2 m) belt transects in the coastal dune, in 30 random plots of 0.5 m2 in the rocky coastal, and nine belt transects (three 20 m x 2 m, four 25 m x 2 m, one 30 m x 2 m and one 40 m x 2 m) in the mountain community. ...
Full-text available
Although the Mediterranean basin is a hotspot of pollinator diversity, little is still known about how such diversity is distributed in the region and about its conservation status. This study contributes to filling this information gap by studying pollinator diversity parameters in one of the main Mediterranean islands, Mallorca, and further evaluating their conservation category according to the IUCN criteria. We focus on three communities, two coastal and one mountain shrubland, which we have studied for several years. For each community, we obtained the following variables: (1) Shannon diversity (H'), (2) Pielou's index (J'), (3) Number of pollinators per plant (Lp), (4) Flower visitation rate (FVR), (5) Specialisation index (d') and (6) Normalised degree of pollinators, i.e. the number of plants visited per pollinator species relative to the total number of plant species in the community (ND). All pollinators were categorised into functional groups to test for differences in such variables among them. Differences across communities, years and functional groups were tested through GLMMs. The three communities showed differences in pollinator species composition, species richness and diversity. Pollinator diversity also varied with time, especially in the coastal community, which suffered a major disturbance during one of the study years. Regardless of the functional group, the pollinator specialisation degree seems context-dependent. Native and endemic species might disappear in the short term if appropriate management measures are not taken to narrow down the threats to pollinator populations. Further research is urgently needed to assess most insect pollinators' conservation status in the Mediterranean before such rich diversity is lost forever.
... Alternatively, one could ask to what degree a driver of global environmental change, such as habitat loss, affects the architecture of plant-pollinator networks and therefore their resilience (35,39,45,54,94,102). For example, a study in sandhill habitats in Florida has shown that the direct effects of habitat loss on species richness and abundance lead indirectly to more modular and connected networks (94). ...
... Similarly, in a coastal dune marshland, habitat loss resulted in a reduction in species richness and abundance of pollinators. This translated into an increase in modularity, as in the previous study in Florida, and a reduction in nestedness, which was interpreted by the authors as potentially reducing the robustness of these pollination networks (102). Habitat loss has also been found to reduce the specialization of interactions, which has led toward the functional homogenization of the resulting impoverished communities. ...
Full-text available
There is growing awareness of pollinator declines worldwide. Conservation efforts have mainly focused on finding the direct causes, while paying less attention to building a systemic understanding of the fragility of these communities of pollinators. To fill this gap, we need operational measures of network resilience that integrate two different approaches in theoretical ecology. First, we should consider the range of conditions compatible with the stable coexistence of all of the species in a community. Second, we should address the rate and shape of network collapse once this safe operational space is exited. In this review, we describe this integrative approach and consider several mechanisms that may enhance the resilience of pollinator communities, chiefly rewiring the network of interactions, increasing heterogeneity, allowing variance, and enhancing coevolution. The most pressing need is to develop ways to reduce the gap between these theoretical recommendations and practical applications. This perspective shifts the emphasis from traditional approaches focusing on the equilibrium states to strategies that allow pollination networks to cope with global environmental change. Expected final online publication date for the Annual Review of Entomology, Volume 68 is January 2023. Please see for revised estimates.
... These interactions even disappear at faster rates compared to species loss (Valiente-Banuet et al., 2015) and therefore contribute substantially to the degradation of ecosystem functions and services (Griffiths et al., 2016;Keyes et al., 2021). Not only mutualistic interactions, such as pollination and facilitation (Montoya et al., 2012;Traveset et al., 2018), but also trophic interactions, such as herbivory and predation, can have important effects on ecosystem functioning (Lavorel et al., 2013;Schmitz, 2008). To realistically gauge the effect of disappearing trophic interactions, a precise quantification and understanding of food web structure is necessary (Novak et al., 2011). ...
Full-text available
Trophic interactions are often deduced from body size differences, assuming that predators prefer prey smaller than themselves because larger prey are more difficult to subdue. This has mainly been confirmed in aquatic ecosystems, but rarely in terrestrial ecosystems, especially in arthropods. Our goal was to validate whether body size ratios can predict trophic interactions in a terrestrial, plant‐associated arthropod community and whether predator hunting strategy and prey taxonomy could explain additional variation. We conducted feeding trials with arthropods from marram grass in coastal dunes to test whether two individuals, of the same or different species, would predate each other. From the trial results, we constructed one of the most complete, empirically derived food webs for terrestrial arthropods associated with a single plant species. We contrasted this empirical food web with a theoretical web based on body size ratios, activity period, microhabitat, and expert knowledge. In our feeding trials, predator‐prey interactions were indeed largely size‐based. Moreover, the theoretical and empirically based food webs converged well for both predator and prey species. However, predator hunting strategy, and especially prey taxonomy improved predictions of predation. Well‐defended taxa, such as hard‐bodied beetles, were less frequently consumed than expected based on their body size. For instance, a beetle of average size (measuring 4 mm) is 38% less vulnerable than another average arthropod with the same length. Body size ratios predict trophic interactions among plant‐associated arthropods fairly well. However, traits such as hunting strategy and anti‐predator defences can explain why certain trophic interactions do not adhere to size‐based rules. Feeding trials can generate insights into multiple traits underlying real‐life trophic interactions among arthropods.
... However, this mutualism is being severely affected by diverse anthropogenic factors, mainly the loss and fragmentation of natural habitats (Hagen & Kraemer, 2010;Potts et al., 2010;Watanabe, 2013). Habitat loss and degradation dramatically change the composition and structure of biological communities, negatively impacting the availability of floral resources, and the abundance and behaviour of animals that visit flowers (Aguilar et al., 2006(Aguilar et al., , 2019Potts et al., 2005;Quesada et al., 2011;Traveset et al., 2018;Wilcock & Neiland, 2002). ...
Full-text available
1. Plant‐pollinator interactions are fundamental to ecosystem functioning; however, the role that succession and phenology have on these interactions is poorly understood, particularly in endangered tropical ecosystems. In highly diverse ecosystems such as tropical dry forests (TDF), variation in water and food availability determines the life cycles of animal pollinators. Therefore, understanding patterns of flowering phenology and plant‐pollinator interactions across seasons in successional environments is key to maintaining and restoring TDF. 2. We analysed the functional dynamics of plant‐floral visitor interactions at the community level across a successional gradient in a Mexican TDF. We evaluated changes in the diversity of blooming plant species and floral visitors, phenological patterns, interaction network metrics, and beta diversity among early, intermediate, and late successional stages, between dry and rainy seasons. 3. We found a higher diversity of blooming plant species and a higher richness of animal species in the intermediate and late successional stages. Peak abundance of floral visitors overlapped with flowering peaks in the late successional stages, but this was not consistently the case in the early and intermediate stages. Plant‐floral visitors networks differed in structure according to successional stage and season, but specialisation metrics were higher in late successional stages. Interaction networks were more dissimilar between dry and rainy seasons within successional stages than within seasons between successional stages, suggesting connectivity across successional sites during each season. In addition, closely related plant species do not share the same pollination systems in any successional stage. 4. Synthesis. Our results showed that plant‐floral visitor interactions are dynamic and vary with flowering phenology and with successional changes in plant and animal diversity. Plant‐floral visitor interactions were more diverse and specialised in the late successional stages. In the rainy season, differences in network structure among successional stages are due to interaction rewiring, while in the dry season it is caused by species turnover. Our results demonstrate that seasonality plays a key role in community diversity and network structure and highlight the importance of conserving mature forests to ensure the maintenance of critical pollination interactions across all successional stages.
... These shifts fragmented the network by reducing the "bridges" among modules [13]. Previous studies also demonstrated the structural role of species change in response to disturbances, such as fire and habitat loss [32,46]. ...
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Species interactions are the backbone of the structure and dynamics of communities. The extensive research into the link between structure and stability has been primarily theoretical and focused on monotrophic networks. Therefore, how the disruption of multitrophic interactions alters communities' response to perturbations in nature remains an open question. Here, we explored how non-native ungulates affect pollination-seed dispersal multilayer networks in Patagonia, Argentina. Ungulates disrupt a hummingbird-mistletoe-marsupial keystone interaction, which alters community composition. We calculated interlayer connectivity, modularity, and species' roles in connecting modules for intact vs. invaded networks. To link structural changes to stability, we quantified network tolerance to a single random species removal (disturbance propagation) and sequential species removal (robustness) using a stochastic coextinction model. Non-native ungulates reduced the connectivity between pollination and seed dispersal and produced fewer modules with a skewed size distribution. Moreover, species shifted their structural role, primarily from connectors to peripherals, thereby fragmenting the network by reducing the "bridges" among modules. These structural changes altered the dynamics of cascading effects in the community, increasing disturbance propagation and reducing network robustness. Our results highlight the importance of understanding the mechanisms that alter the structure and subsequent stability of multitrophic communities in nature.
... On the other hand, our results using empirical mutualistic networks show that increasing forest cover decreases nestedness. Indeed, some studies showed that disturbed areas are less nested (de Assis Bomfim et al. 2018, Traveset et al. 2018, Vidal et al. 2019, while the opposite pattern was observed by others, in which disturbed areas present higher nestedness (Menke et al. 2012, Vanbergen et al. 2017, Morrison et al. 2020). Our result is in line with those that point to a decrease in nestedness in forested landscapes. ...
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Habitat loss is a global threat to biodiversity with pervasive effects on species and populations. These impacts may generate cascading effects on ecological processes propagating across ecological networks. Thus, understanding how habitat loss affects ecological networks is fundamental for conservation. We used a database of 25 plant–frugivore networks distributed across the whole Brazilian Atlantic Forest to understand how landscape‐scale habitat loss shapes network structure, robustness, species role and traits related to seed dispersal. We compared whether these network properties have linear or non‐linear relationships and used centrality metrics and indirect effects to evaluate if habitat loss change the role of species in plant–frugivore networks. We found linear and non‐linear relationships with negative effects of habitat loss on the network structure. As a consequence of shifts in species richness and number of links, the number of interactions and the proportion of possible interactions observed (connectance) were negatively associated with habitat loss. In contrast, nestedness increased with habitat loss. Network robustness, mean bill width and mean seed size were not significantly related to habitat loss. In addition to changes in interaction patterns at network level, habitat loss also favors changes in interaction among species, shifting the species playing central roles in network organization or contributing to indirect effects in the networks. In forested landscapes, obligate frugivores are the main central species in the network, and the ones potentially contributing to indirect effects, while in deforested landscapes these roles are fulfilled by occasional frugivores. Thus, our results emphasize the widespread effect of habitat loss on plant–frugivore systems, adding evidence that its pervasive effects on biodiversity also proliferate on mutualistic interactions with negative consequences for seed dispersal that potentially go beyond the direct pairs of interacting species.
... These changes in network parameters overall describe stronger average interspecific associations and a more cohesive, less divided network at higher elevations. This result is important because cohesive networks can impart stability to the community, and has high resiliency to species loss and environmental change [72,73]. ...
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Understanding how non-trophic social systems respond to environmental gradients is still a challenge in animal ecology, particularly in comparing changes in species composition to changes in interspecific interactions. Here, we combined long-term monitoring of mixed-species bird flocks, data on participating species' evolutionary history and traits, to test how elevation affected community assemblages and interspecific interactions in flock social networks. Elevation primarily affected flocks through reassembling interspecific associations rather than modifying community assemblages. Specifically, flock networks at higher elevations (compared to low elevations) had stronger interspecific associations (larger average weighted degree), network connectivity (enhanced network density) and fewer subnetworks. A phylogenetic and functional perspective revealed that associations between similar species weakened, whereas connections between dissimilar and/or random species were unchanged or strengthened with elevation. Likewise, network assortativity for the traits of vertical stratum and breeding period declined with elevation. The overall pattern is a change from modular networks in the lowlands, where species join flocks with other species that have matching traits, to a more open, random system at high elevations. Collectively, this rewiring of interspecific networks across elevational gradients imparts network stability and resiliency and makes mixed-species flocks less sensitive to local extinctions caused by harsh environments.
... At the local scale, we observed that network specialization was positively affected by bare soil/dry crop cover, while flowering crops had a negative influence on network connectance. Traveset et al. (2020) found highly specialized plant-pollinator networks in areas with radical habitat loss (vegetation removal leading to bare soil). This network pattern was associated to low species abundance, which results in the disruption of the interactions after the disturbance. ...
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Land use change has been identified as a cause for biodiversity loss and has significant effects on pollinators and their interactions with plants. Interaction network analyses complement diversity estimators by providing information on the stability and functionality of the plant-pollinator community in an ecosystem. However, how land use changes affect insect diversity, and the structure of their plant-insect interaction networks, could depend on the intensity of the disturbance but also may be a matter of scale. Our study was carried out in a tropical highland landscape dominated by intense, yet diverse, small-scale agriculture. We studied the effects of land use, at a landscape scale, and local cover and plant ecological descriptors, at a local scale; on diversity descriptors of insect pollinator communities, the abundance of the most frequent flower visitors, and their interaction networks. Seminatural vegetation favored insect flower visitors at both scales. At the landscape scale, human settlements positively influenced bee diversity, and seminatural areas favored the abundance of frequent hoverfly and bumblebee species. At the local scale, bare soil cover negatively influenced honeybee abundance while flower-rich covers positively related to bumblebee abundance. Only local scale variables had influence on network metrics. Bare soil cover was related to higher network specialization, probably due to a low rate of honeybee interactions. Flower-rich covers negatively influenced network connectance but favored modularity. These results suggest that flower resources, provided by weed areas and flowering crops, promote a high rate of interactions between trophic levels and a non-random structure in the interaction networks that may be helping to sustain network stability. Our results highlight the role of seminatural vegetation, at both scales, in maintaining stable insect pollinator communities and interactions in heterogeneous agricultural landscapes of the tropics.
Major challenges for plant conservation are predicting the effect of habitat loss on pollination success and plant reproduction potential. Most studies report that pollinator movement is affected by quantitative and spatial characteristics of landscapes. However, little is known about the role of pollinator movement, impacted by floral volatiles and intraspecies interaction, on plant reproduction in fragmented landscapes. To clarify the effect of pollinator movement on plant reproduction relative to habitat loss, we developed an integrated model incorporating pollinator's foraging response with its dispersal process mediated by a density‐dependent dispersal (DDD) strategy. This model performed better in capturing behavior response of pollinators than do current methods. The integrated model was verified with field results of pollinator visitation and plant reproduction of saltcedar (Tamarix chinensis) inhabiting the Yellow River Delta, and then was compared against a dispersal strategy called density‐independent dispersal (DID). The model was applied to landscapes with various non‐habitat percentage (NHP) to explore the effect of habitat loss on plant reproduction. Results suggested that saltcedar populations differ in their responses to habitat loss, which depended on the spatial scales considered. At landscape scale, increasing NHP significantly inhibited dispersion extent of floral volatiles and therefore reduced pollinator visitation and subsequent seed production, especially when NHP exceeded the critical threshold of 0.6. However, at patch scale, comparing with DID strategy, the DDD strategy enabled pollinators to increase their utilization of flowers by 43.42% and 6.79% in low‐density and distant plant patches, whereas their utilization was reduced by 7.75% and 2.24% in high‐density and central patches, respectively. Plant reproduction was improved correspondingly in low‐density and distant patches under different NHPs. Consequently, habitat loss inhibits the volatiles dispersion and interferes the foraging success of pollinators, a major factor influencing plant reproduction at landscape scale. At patch scale, adaptive utilization of pollinators exhibiting DDD strategy alleviates the negative effect of habitat loss on plant production, and maintain plant population persistence. Since pollinator behavioral response is critical to plant reproduction, we recommend the use of the here presented integrated model to assess the impact of habitat loss on plant reproduction.
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The structure of pollination networks is an important indicator of ecosystem stability and functioning. Livestock grazing is a frequent land use practice that directly affects the abundance and diversity of flowers and pollinators and, therefore, may indirectly affect the structure of pollination networks. We studied how grazing intensity affected the structure of plant-flower visitor networks along a wide range of grazing intensities by sheep and goats, using data from 11 Mediterranean plant-flower visitor communities from Lesvos Island, Greece. We hypothesized that intermediate grazing might result in higher diversity as predicted by the Intermediate Disturbance Hypothesis, which could in turn confer more stability to the networks. Indeed, we found that networks at intermediate grazing intensities were larger, more generalized, more modular, and contained more diverse and even interactions. Despite general responses at the network level, the number of interactions and selectiveness of particular flower visitor and plant taxa in the networks responded differently to grazing intensity, presumably as a consequence of variation in the abundance of different taxa with grazing. Our results highlight the benefit of maintaining moderate levels of livestock grazing by sheep and goats to preserve the complexity and biodiversity of the rich Mediterranean communities, which have a long history of grazing by these domestic animals.
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Pollinators play an important role in ecosystem functioning, affecting also crop production. Their decline may hence lead to serious ecological and economic impacts, making it essential to understand the processes that drive pollinator shifts in space and time. Land-use changes are thought to be one of the most important drivers of pollinators’ loss, and there is increasing investment on pollinator-friendly landscape management. However, it is still unclear whether landscape history of a given region determines how pollinator communities respond to further landscape modification.
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Mutualistic plant-pollinator interactions play a key role in biodiversity conservation and ecosystem functioning. In a community, the combination of these interactions can generate emergent properties, e.g., robustness and resilience to disturbances such as fluctuations in populations and extinctions. Given that these systems are hierarchical and complex, environmental changes must have multiple levels of influence. In addition, changes in habitat quality and in the landscape structure are important threats to plants, pollinators and their interactions. However, despite the importance of these phenomena for the understanding of biological systems, as well as for conservation and management strategies, few studies have empirically evaluated these effects at the network level. Therefore, the objective of this study was to investigate the influence of local conditions and landscape structure at multiple scales on the characteristics of plant-pollinator networks. This study was conducted in agri-natural lands in Chapada Diamantina, Bahia, Brazil. Pollinators were collected in 27 sampling units distributed orthogonally along a gradient of proportion of agriculture and landscape diversity. The Akaike information criterion was used to select models that best fit the metrics for network characteristics, comparing four hypotheses represented by a set of a priori candidate models with specific combinations of the proportion of agriculture, the average shape of the landscape elements, the diversity of the landscape and the structure of local vegetation. The results indicate that a reduction of habitat quality and landscape het-erogeneity can cause species loss and decrease of networks nestedness. These structural changes can reduce robustness and resilience of plant-pollinator networks what compromises the reproductive success of plants, the maintenance of biodiversity and the pollination service stability. We also discuss the possible explanations for these relationships and the implications for landscape planning in agricultural areas.
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Climate change can alter species phenologies and therefore disrupt species interactions. Habitat destruction can damage biodiversity and population viability. However, we still know very little about the potential effects of these two factors on the diversity and structure of interaction networks when both act simultaneously. Here we developed a mutualistic metacommunity model to explore the effects of habitat destruction and phenological changes on the diversity and structure of plant–pollinator networks. Using an empirical data set of plant and pollinator interactions and their duration in days, we simulated increasing levels of habitat destruction, under projected scenarios of phenological shifts as well for histori- cally recorded changes in phenologies. On one hand, we found that habitat destruction causes catastrophic collapse in global diversity, as well as inducing alternative states. On the other hand, phenological shifts tend to make interactions weaker, increasing local extinction rates. Together, habitat destruction and phenological changes act synergistically, making metacommunities even more vulnerable to global collapse. Metacommunities are also more vulnerable to collapses under scenarios of historical change, in which phenologies are shortened, not just shifted. Furthermore, connectance and nestedness tends to decrease gradually with habitat destruction before the global collapse. Small phenological shifts can raise connectance slightly, due novel interactions appearing in a few generalist species, but larger shifts always reduce connectance. We conclude that the robustness of mutualistic metacommunities against habitat destruction can be greatly impaired by the weakening of positive interactions that results from the loss of phenological overlap.
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Recent evidence highlights the value of wild-insect species richness and abundance for crop pollination worldwide. Yet, deliberate physical importation of single species (eg European honey bees) into crop fields for pollination remains the mainstream management approach, and implementation of practices to enhance crop yield (production per area) through wild insects is only just beginning. With few exceptions, studies measuring the impacts of pollinator-supporting practices on wild-insect richness and pollination service success - particularly in relation to long-term crop yield and economic profit - Are rare. Here, we provide a general framework and examples of approaches for enhancing pollinator richness and abundance, quantity and quality of pollen on stigmas, crop yield, and farmers' profit, including some benefits detected only through long-term monitoring. We argue for integrating the promotion of wild-insect species richness with single-species management to benefit farmers and society.
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In theoretical ecology, traditional studies based on dynamical stability and numerical simulations have not found a unified answer to the effect of network architecture on community persistence. Here, we introduce a mathematical framework based on the concept of structural stability to explain such a disparity of results. We investigated the range of conditions necessary for the stable coexistence of all species in mutualistic systems. We show that the apparently contradictory conclusions reached by previous studies arise as a consequence of overseeing either the necessary conditions for persistence or its dependence on model parameterization. We show that observed network architectures maximize the range of conditions for species coexistence. We discuss the applicability of structural stability to study other types of interspecific interactions.
The structure of pollination networks is an important indicator of ecosystem stability and functioning. Livestock grazing is a frequent land use practice that directly affects the abundance and diversity of flowers and pollinators and, therefore, may indirectly affect the structure of pollination networks. Here we studied how grazing intensity affected the structure of plant-flower visitor networks along a wide range of grazing intensities by sheep and goats, using data from 11 Mediterranean plant-flower visitor communities from Lesvos Island, Greece. We hypothesized that intermediate grazing might result in higher diversity as predicted by the Intermediate Disturbance Hypothesis, which could in turn confer more stability to the networks. Indeed, we found that networks at intermediate grazing intensities were larger, more generalized, more modular, and contained more diverse and even interactions. Despite general responses at the network level, the number of interactions and selectiveness of particular flower visitor and plant taxa in the networks responded differently to grazing intensity, presumably as a consequence of variation in the abundance of different taxa with grazing. Our results highlight the benefit of maintaining moderate levels of livestock grazing by sheep and goats to preserve the complexity and biodiversity of the rich Mediterranean communities, which have a long history of grazing by these domestic animals.
Context Loss of natural habitat can isolate pollinator populations and negatively affect sexual reproduction of animal-pollinated plants. Objective We evaluated how the loss of natural forest affects pollinator diversity in the understory of the Atlantic Rainforest in Northeastern Brazil. Methods We focused on bees, the main group of pollinators for angiosperms. We assessed how changes in forest cover at regional (36 km2) and local (0.36 km2) scales affect bee richness and abundance. Results We sampled 492 bees from 59 species, of which 58 % were above ground nesting species and 73 % exhibited some level of sociality. Our results show that the loss of forest had negative effects on understory bee abundance, which was particularly accentuated for species that nest above ground. However, for social bees the effect of changes in forest cover at a local scale depended on regional forest cover, negative effects being only detected when landscapes had at least 35 % of forest. For bee richness, the null model was among the best models bringing considerable uncertainty about landscape effects on bee richness. Conclusions These findings suggest that management strategies and conservation practices must integrate proper actions that consider both local and regional scales. For existing fragmented landscapes, it is important to increase forest availability at the regional scale, while also maintaining high environmental heterogeneity at the local scale. We believe that with proper landscape planning this multiscalar approach can be not only more effective, but also easier to implement.