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Received: 11 September 2019    Accepted: 19 November 2019
DOI: 10.1111/1365-2745.13332
RESEARCH ARTICLE
Alien plants and flower visitors disrupt the seasonal dynamics
of mutualistic networks
Blanca Arroyo-Correa1,2  
1
Integrative Ecology Group, Estación
Biológica de Doñana, CSIC, Sevilla, Spain
2
School of Biosciences, Autonomous
University of Barcelona, Barcelona, Spain
3
Department of Ecology, Montana State
University, Bozeman, MT, USA
4
Conservation Biology Lab, Department
of Ecology, São Paulo State University, Rio
Claro, SP, Brazil
Correspondence
Blanca Arroyo-Correa
Email: blanca.arroyo.correa@gmail.com
Funding information
Coordination for the Improvement of Higher
Education Personnel (CAPES, Brazil)
Handling Editor: Jane Catford
Journal of Ecology. 2019;00:1–12. wileyonlinelibrary.com/journal/jec© 2019 British Ecological Society     1
| Laura A. Burkle3  | Carine Emer4
Abstract
1. Alien species can drastically disrupt ecological processes such as those involving
plant–pollinator interactions, performing central roles that may affect the struc-
ture of native pollination networks. However, most studies to date have focused
on a single trophic level of alien species, evaluating either the impacts of an alien
pollinator or an alien plant species, and have neglected their joint effects on the
seasonal dynamics of mutualistic networks.
2. Here, we aim to fill this gap by investigating how alien plant and flower visitor (here
used as a proxy for pollinator) species structure temporal networks, and how these
species affect the beta-diversity of interactions across a flowering season. Our study
system is located in the South Island of New Zealand, where 68% of the sampled
plant species and 14% of the flower visitor species that interact with them are alien.
3. Alien flower visitor species exhibited higher interaction degree, specialization and
strength than their native counterparts, while alien plant species showed the op-
posite pattern. We found that invader complexes (in which alien species inter-
act significantly more with each other than with native species) were established
across the season, and interactions involving alien plant species were the main
connectors of the temporal networks. Both alien plant and flower visitor species
increased total interaction turnover through the flowering season by promoting
interaction rewiring in the case of alien plants and by increasing species turnover
in the case of alien flower visitors.
4. Synthesis. This study provides one of the first empirical reports of alien species shap-
ing the seasonal dynamics of plant–flower visitor networks. We demonstrate that the
presence of alien species may simultaneously lead to a homogenization of plant spe-
cies composition and increase the diversity of plant–flower visitor interactions through
a flowering season. Additionally, we highlight the importance of considering the role
of different trophic levels when analysing the impact of alien species in plant–flower
visitor communities. Overall, our findings suggest that management strategies should
pay particular attention to the timescale at which interactions with alien species
dissolve or form, and to the consequences and drivers of such seasonal dynamics.
KEYWORDS
beta-diversity, ecological networks, interaction turnover, invader complex, invasion ecology,
mutualism, plant–pollinator interactions
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Journal of Ecology
1 |  I NTRO D U C TI O N
In a rapidly changing world, where many species have been intro-
duced outside of their native range due to human activities, under-
standing how alien species affect ecological processes is crucial if we
aim to reduce biodiversity loss (Gurevitch & Padilla, 2004; Traveset
& Richardson, 2014). The impacts of alien species have long been
studied in plant–pollinator interactions (e.g. Olesen, Eskildsen, &
Venkatasamy, 2002; Padrón et al., 2009). Yet, their effects on the pol-
lination of native species are not consistent across species or regions,
varying from negative (Bjerknes, Totland, Hegland, & Nielsen, 2007),
to neutral (Bartomeus, Vilà, & Santamaría, 2008) and even to posi-
tive effects (Moragues & Traveset, 2005). To date, most studies focus
on a single trophic level of the invasion, investigating either the ef-
fects of alien plants (e.g. Emer, Vaughan, Hiscock, & Memmott, 2015;
Kaiser-Bunbury, Valentin, Mougal, Matatiken, & Ghazoul, 2011) or
alien pollinator species (e.g. Goulson, 2003; Trøjelsgaard, Heleno, &
Traveset, 2019). In addition, fluctuations in resource availability over
a flowering season, due to, for example, phenological constraints,
may influence how alien species interact among themselves and
integrate into the native communities (Dupont, Padrón, Olesen, &
Petanidou, 2009). Yet, we lack a clear understanding of whether, how
and when the presence of both alien plant and alien animal species
alter community-level patterns of mutualistic interactions.
A network approach to animal–plant mutualisms has proven to
be an efficient tool to evaluate the integration of alien species into
plant–pollinator communities (Memmott, 2009; Tylianakis & Morris,
2017). Alien species often exhibit high degree (i.e. number of inter-
actions performed) and high generalism (i.e. the capacity to interact
with a high diversity of partner species) in the networks in which
they occur (Aizen, Morales, & Morales, 2008; Memmott & Waser,
2002). Such characteristics can facilitate the establishment of alien
species in communities because they can promptly interact with the
local assemblage of partner species (Traveset & Richardson, 2014).
Hence, they can function as central nodes in the networks they
have invaded, performing many interactions with both native and
alien partners and increasing the dependence of other species on
them, that is, increasing their species strength (Stouffer, Cirtwill, &
Bascompte, 2014). Such concentration of interactions by a few alien
species can potentially decrease mutualism strength among native
co-occurring species (Aizen et al., 2008). Additionally, preferential
interactions among alien species might create ‘invader complexes’,
defined as ‘groups of alien species interacting more with each other
than expected by chance’ (D’Antonio & Dudley, 1993). Invader com-
plexes can promote ‘invasional meltdowns’, in which alien species
facilitate one another, thereby improving the conditions for their
survival and spread (Simberloff & Von Holle, 1999). These alien–alien
interactions can disrupt native plant–pollinator mutualisms by mod-
ifying the structure of the native community (Padrón et al., 2009).
Yet, much of our understanding of the effects of alien species on
the structure of flower-visiting networks is derived from data aggre-
gated across the entire flowering season (but see e.g. Dupont et al.,
2009; Kaiser-Bunbury et al., 2011). Network studies pooling data
ARROYO-CORREA et al.
over extensive temporal spans can provide important information
about overall community patterns and the complexity of biological
systems (Bascompte, Jordano, Melian, & Olesen, 2003; Tylianakis &
Morris, 2017). However, their long-time frames fail to capture the
dynamics of interaction build-up, and their structure can be signifi-
cantly different from temporally resolved networks (Rasmussen,
Dupont, Mosbacher, Trøjelsgaard, & Olesen, 2013). By decompos-
ing networks into more refined temporal frames, one can make
inferences about how communities assemble over time (Olesen,
Bascompte, Elberling, & Jordano, 2008) and how non-native, alien
species influence the establishment of interactions.
In this context, temporal variation in network structure over
the course of a flowering season may be caused by phenological
constraints, translating into changes in the identity of the inter-
acting partners (Petanidou, Kallimanis, Tzanopoulos, Sgardelis,
& Pantis, 2008). Thus, the number of interactions a given species
establishes within a community can vary within (Basilio, Medan,
Torretta, & Bartolini, 2006) and among years (Alarcón, Waser, &
Ollerton, 2008), which in turn can influence their role as connec-
tors of temporal networks (Olesen, Stefanescu, & Traveset, 2011).
Hence, the temporal effects of alien species on flower-visiting net-
works could be assessed by considering the extent to which each
species is participating in interactions through a flowering season.
That said, beta-diversity indexes, which are usually applied to inves-
tigate patterns of species composition and turnover across space,
can be useful to detect patterns of temporal changes in mutualistic
interactions (e.g. CaraDonna et al., 2017; Poisot, Canard, Mouillot,
Mouquet, & Gravel, 2012; Simanonok & Burkle, 2014) in the pres-
ence of alien species as well. The effects of alien species on the
temporal beta-diversity of interactions (i.e. interaction turnover)
may be caused by (a) species turnover and/or (b) interaction rewir-
ing. Interaction turnover caused by species turnover is defined as
changes in pairwise animal–plant interactions as animal or plant
species become present or absent over time. Meanwhile, interac-
tion turnover caused by interaction rewiring is defined as the reas-
sembling of pairwise interactions when both partners occur but do
not interact (Burkle, Myers, & Belote, 2016). Thus, a combination
of network tools and beta-diversity indexes (Trøjelsgaard, Jordano,
Carstensen, & Olesen, 2015) is promising to investigate the role
of alien species in driving the temporal assembly of flower-visiting
networks.
Here, we aimed to understand the role of alien plant and alien
flower visitor species on the structure of invaded flower-visiting
networks throughout a flowering season. We collected data over
2.5 months during a flowering season in the subalpine vegetation of
the South Island of New Zealand, where native and alien plant and
insect flower visitor species co-occur. Specifically, we investigated (a)
the extent to which the network roles of alien plant and flower visi-
tor species (i.e. degree, specialization and species strength) differed
from the roles performed by native species, and whether the pat-
terns depended on the trophic level analysed; (b) the extent to which
interactions involving alien species represented temporal connec-
tions between sequential time frames of the invaded flower-visiting
ARROYO-CORREA et al.
networks; (c) how alien plant and flower visitor species shaped the
temporal beta-diversity of interactions; and (d) whether alien species
formed temporal invader complexes. Due to their typically generalist
behaviour (Traveset & Richardson, 2014), we expected alien species
to be involved in a higher number and more diverse interactions, ex-
hibiting higher degree, lower specialization and higher strength than
their native counterparts. Therefore, we predicted that alien species
would be active for longer periods during the season (Memmott &
Waser, 2002), playing important roles in connecting sequential time
frames of the flower-visiting networks.
Further, the diversity of interactions performed by alien species
and their longer phenologies may shuffle interactions among native
species, potentially affecting seasonal beta-diversity patterns by
promoting interaction rewiring while homogenizing the community
composition. Finally, because alien species in our study system were
from the same geographic origin (Allen, Duncan, & Lee, 2006), they
potentially shared close evolutionary trajectories favouring morpho-
logical trait matching between them (Anderson, Terblanche, & Ellis,
2010). Thus, we expected alien plant and alien flower visitor species
to interact more frequently with each other in comparison with the
number of interactions established between alien and native spe-
cies, thereby forming temporal invader complexes throughout the
flowering season.
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Study site
The study was carried out at Cass Mountain Research Field Station,
located in the Cass River basin near the Craigieburn Range, in
the middle of the South Island of New Zealand (43°02′09.2″S,
171°45′22.0″E, 580 m a.s.l.). The field station is located in a moist
and temperate climate zone with subalpine vegetation that includes
open fields composed of grasses and shrubs (Wardle, 1991). The
current biota of New Zealand has been influenced by human-driven
introductions of plant and animal species since European settle-
ment in 1,840 (Allen et al., 2006). It has been suggested that plant
introductions in New Zealand have averaged 11 species per year
since European settlement (Atkinson & Cameron, 1993), represent-
ing around 40% of the total plant community richness (Vitousek,
D'Antonio, Loope, Rejmanek, & Westbrooks, 1997). Likewise, na-
tive European bumblebees (Bombus spp.), the cosmopolitan hoverfly
Eristalix tenax, the invasive cabbage butterfly Pieris rapae, and several
other bee species including Apis mellifera became established on the
South Island of New Zealand following a series of introductions in
the late nineteenth and early twentieth century (Donovan, 1980;
Goulson & Hanley, 2004).
We surveyed plant–flower visitor interactions at three sites at
the base of Cass Mountain range, c. 1.5 km apart. Due to the lim-
ited average flying capacity of the flower visitor species present at
the study sites and the montane characteristics of the local terrain,
the likelihood of movement of flower visitor individuals among the
Journal of Ecology |
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study sites was considered low. Therefore, each site was treated as
an independent assemblage of species. Four consecutive surveys
per site were conducted from late December 2012 to early March
2013, therefore including the flowering season in our study area
(Figure S1b). With each of these surveys, we built the correspond-
ing temporal network, totalling 12 temporal networks (four per site).
Hence, the four temporal networks constructed per site represent
four subsections of a full-season network. This methodological ap-
proach that accounts for the temporal component of mutualistic
networks has been widely used in pollination network studies (e.g.
Kaiser-Bunbury, Muff, Memmott, Müller, & Caflisch, 2010; Souza et
al., 2018).
The adequacy of splitting interaction data across the flowering
season into four time slices according to flowering phenology was
confirmed with linear discriminant analyses (LDA) using the ‘mass’ r
package (Venables & Ripley, 2002). We constructed a date-by-plant
species data matrix, in which the matrix entries indicated the abun-
dance of flowering species on a particular date of the flowering sea-
son. In this matrix, each date was associated with one of the four
time slices previously established across the season. For each site,
we performed a LDA with time slice as the dependent variable and
abundance of each flowering plant species as independent variables.
To analyse differences among the four time slices in composition
and abundance of flowering species, we used pairwise t test com-
parisons with the first and second discriminant functions’ scores as
dependent variables and the time slices as independent variables.
LDA results confirmed that flowering phenology was effective in
distributing our data into four distinct groups (i.e. time slices; Figure
S2; Table S1).
Within each site, we established a 500 × 5 m plot, subdivided
into 20 subplots (25 × 5 m each; Figure S1a). To avoid temporal and
spatial pseudoreplication within and among sites, we sampled five
subplots per site per day in the field, randomizing the order of the
sites and subplots to be sampled in the morning and afternoon each
day. We also avoided bad weather conditions that could influence
flower visitor behaviour, such as rain and strong winds. Interaction
data were collected by the same person slowly walking an estab-
lished transect in each subplot. All insects observed visiting flowers
and touching their reproductive structures were collected, and the
interaction was recorded. The amount of time spent in each sub-
plot varied depending on insect and floral abundance (and the time
needed to process the collected insects). With this methodological
approach, we standardized the sampling effort per flower over a con-
sistent area. These individual-level observations were then pooled
at the species-level to build flower-visiting networks. Therefore, the
number of hours and days spent to complete a survey (i.e. to sample
all 20 subplots per site) varied according to flowering phenology, the
local assemblage of flower visitors and weather conditions (number
of days in each survey: min nine days; max 18 days; Figure S1b).
Specimens of plants were collected for species confirmation
or further identification by local taxonomists when needed. All in-
sects were collected with an entomological net, transferred to killing
tubes containing acetyl acetate, frozen and pinned for identification.
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Journal of Ecology
Insects were identified by taxonomists at the National Museum of
Cardiff, UK. Our sampling removed relatively few of the insects vi-
sually seen in the overall communities. Furthermore, lethal sampling
of bee specimens in a similar temperate meadow system did not af-
fect abundance, richness, evenness or functional group composition
even after sampling the same site every 2 weeks for 5 years (Gezon,
Wyman, Ascher, Inouye, & Irwin, 2015). Therefore, we assumed that
the removal of insect individuals in our study sites did not affect the
temporal variation in interaction composition. However, because all
sites and subplots were treated equally, even if insect removal had
slight temporary effects on the behaviour of remaining insects, it
would be similar across sites and subplots.
2.2 | Flower-visiting networks
We built each network as an Amn adjacency matrix in which m repre-
sents the plant species (rows), and n the flower visitor insect species
(columns), while the mn elements represent the visitation frequency
of insect i1…n in plant j1…m. We constructed temporal networks rep-
resenting the data recorded in each of the four surveys, therefore
creating four matrices per site (N = 12 temporal networks) that rep-
resented the dynamics of plant–flower visitor interactions during the
flowering season.
2.3 | Species role
To determine whether alien and native species played different roles
in structuring flower-visiting networks over the flowering season,
we calculated the following metrics for each species in each tem-
poral network: (a) normalized degree—the number of observed links
per species weighted by the total number of links in the network, a
proxy for the diversity of interactions a given species can perform;
(b) specialization level (d′)—which measures how strongly a species
deviates from an expected random choice of available interaction
partners; a species that exclusively interacts with an abundant spe-
cies has a lower d′ value (i.e. less specialized) than a species that ex-
clusively interacts with a rare species (Blüthgen, Menzel, & Blüthgen,
2006); and (c) species strength—the sum of the dependencies of all
interaction partners on that species, quantifying the importance
of a species for the community with which it interacts (Barrat,
Barthelemy, Pastor-Satorras, & Vespignani, 2004). Across species,
there were no significant relationships between the metrics, except
for a positive correlation between species strength and normalized
degree (r = .68; Table S2). We retained all metrics in our analyses, and
we interpreted the results accordingly, given this positive correla-
tion. In doing so, we aimed to assess whether higher degree species
also showed higher strength, probably as a result of being connected
to low degree species. Then, we investigated whether the role of
each trophic level (i.e. plant or flower visitor species) was related to
their status as alien or native species by fitting generalized linear
mixed models (GLMMs) with Gaussian errors and using the ‘lmertest’
ARROYO-CORREA et al.
package (Kuznetsova, Brockhoff, & Christensen, 2016). Prior to
model fitting, we log-transformed normalized degree and species
strength to meet model assumptions. Individual models were fit-
ted for each trophic level separately, with each of the three metrics
as the dependent variable tested against species ‘status’ (native vs.
alien). Time was nested within site as a random factor to account for
differences in species composition among sites and over time.
2.4 | Temporal network connectors
We aimed to identify which type of species interaction (i.e. native
plant species–native flower visitor species, native plant–alien flower
visitor, alien plant–alien flower visitor and alien plant–native flower
visitor) was predominant through the flowering season and therefore
was most important in connecting the temporal networks. To do so,
we built a binary Amn matrix for each site in which m corresponds to
each of the temporal networks (1 to 4) and n to the plant–flower visi-
tor interactions recorded through the flowering season in that site;
cells received the value of 1 when an interaction n was recorded in
a given time m, and 0 otherwise. Then, we calculated betweenness
centrality (BC) for each plant–flower visitor interaction (Freeman,
1978; González, Dalsgaard, & Olesen, 2010) as a proxy for the im-
portance of alien species associations in connecting the temporal
networks. Interactions with BC > 0 play a significant role as temporal
network connectors, therefore contributing to the cohesiveness of
the plant–flower visitor community through the flowering season.
The significance of differences in BC among interaction types was
tested with nonparametric pairwise comparisons using Dunn's tests
(Dinno, 2017) following a Kruskal–Wallis test.
2.5 | Contribution of alien species to temporal beta-
diversity
To investigate the contribution of alien species to interaction beta-
diversity (i.e. turnover of interactions) over time, we estimated the
turnover of plant–flower visitor interactions (βCC) across the flower-
ing season using binary temporal networks to calculate the Jaccard
similarity index among them. Because overall interaction turnover
(βCC) is driven by several ecological processes, we first partitioned it
as: βCC = βST + β0, where βST denotes interaction turnover due to spe-
cies turnover, that is changes in interactions as plant and/or flower
visitor species become present or absent over time, and β0 denotes
interaction turnover due to interaction rewiring, that is changes in
interactions due to changes in interacting partners (e.g. Dupont et
al., 2009). Then, we divided the total contribution of species turno-
ver to interaction turnover (βST ) into three components, following
the approach developed by Novotny (2009): βST = βP + βA + βPA . That
is, the contribution of species turnover to interaction turnover (βST )
can be driven by plant species turnover (βP), flower visitor species
turnover (βA), and simultaneous turnover of both plant a flower visi-
tor species (βPA). We calculated overall interaction turnover (βCC) and
ARROYO-CORREA et al.
its components for sequential pairwise combinations of interac-
tion networks using modified ‘betalink’ R Script (Poisot et al., 2012;
Simanonok & Burkle, 2014).
To further analyse the effects of alien species on the temporal
dynamics of mutualistic networks, we assessed how alien plant and
flower visitor species contributed to the interaction beta-diversity
over time. To do so, we built two simulated networks for each of
the 12 temporal networks, identical to the observed data except for
the removal of (a) alien plant species or (b) alien flower visitor spe-
cies and the interactions they performed. Hence, we obtained 12
‘alien plant removal’ networks and 12 ‘alien flower visitor removal’
networks. Given that species turnover and interaction rewiring are
expected to depend on species richness and/or network size (e.g.
Burkle et al., 2016; Kraft et al., 2011) independently of their status
as alien or native, we compared the results from our alien-removal
simulations against the removal of random species using null models.
Because our aim was to quantify whether the contribution of alien
species was different than expected by chance and not to predict
how the community would change after the removal of alien spe-
cies, in this analysis we did not considered the potential interaction
rewiring among the remaining species in the networks (e.g. Kaiser-
Bunbury et al., 2010).
Our null models involved the creation of new simulated net-
works in which we randomly removed the same number of species
as the number of species removed in the ‘alien removal’ networks,
considering each trophic level separately. The random removal of
species was iterated 1,000 times across each of the 12 observed
temporal networks. Therefore, we obtained 12,000 ‘random plant
removal’ networks and 12,000 ‘random flower visitor removal’ net-
works. Finally, we obtained the beta-diversity indices described
above for the alien-removal and the random-removal simulated
networks. To test the significance of the differences between ‘alien
plant removal’ and ‘random plant removal’, and between ‘alien flower
visitor removal’ and ‘random flower visitor removal’ networks, we
used generalized linear mixed models (GLMMs) with a gamma distri-
bution. Each beta-diversity index was tested as a dependent variable
against the type of network (alien-removal or random-removal), and
pairwise temporal comparisons (i.e. temporal network 1 vs. temporal
network 2, etc.) were nested within site as a random factor to control
for potential spatial and temporal pseudoreplication.
2.6 | Invader complexes
To test for the existence of invader complexes, we first estimated
the modularity of each temporal network to further determine
whether species interacted significantly more in the same module
depending on their native or alien status. Modularity was estimated
by the ‘computeModules’ function, using the Beckett algorithm
(Beckett, 2016). Module composition stabilized after 50 iterations,
and therefore, this was the final network configuration used to as-
sign species to modules. We used the species composition in each
module to construct a two-way contingency table for each of the 12
Journal of Ecology |
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temporal networks (i.e. 12 contingency tables). Each contingency
table contained two descriptors (flower visitor and plant species)
with two levels (native and alien species). Therefore, each of the
four cells of the tables described one type of interaction: alien
plant–alien flower visitor, alien plant–native flower visitor, native
plant–native flower visitor or native plant–alien flower visitor. For
each temporal network from each site, cells were filled with the fre-
quency with which the corresponding interaction type was repre-
sented in the modules. The significance of the associations between
plant and flower visitor descriptors was tested with Fisher's exact
tests of independence.
Network metrics (i.e. species-level metrics for species role,
betweenness centrality for temporal connectors and modularity
for invader complexes) were estimated using ‘bipartite’ r package
(Dormann, Gruber, & Fründ, 2008). All analyses were performed in R
version 3.4.1 (R Core Team, 2017).
3 | R E S U LT S
We recorded a total of 1,405 individuals of insect flower visitors
distributed among 100 species (Table S3) and participating in 412
plant–flower visitor interactions with 34 plant species (Table S4). Of
those, 334 interactions (81%) included at least one alien partner, ei-
ther an alien plant or an alien flower visitor species. Alien plant spe-
cies were the most represented group (23 spp, 68% of plant species).
Out of the nine alien plant families recorded, Asteraceae accounted
for almost 50% of the alien plant species. The set of native plants
comprised species from more families, and Asteraceae was again the
most represented group (36% of all native plant species). Regarding
flower visitors, alien species constituted a lower proportion of all
flower visitor species (14 spp, 14%). Approximately 30% of the alien
flower visitor species, including Apis mellifera and Bombus spp., were
found within the Apidae family. The native flower visitor families
with the greatest species richness were Syrphidae (21%), Tachinidae
(12%) and Colletidae (11%).
3.1 | The role of alien versus native species in
structuring flower-visiting networks
The role of alien and native species in the structure of the invaded
plant–flower visitor interaction networks depended on the trophic
level considered. Alien plant species had lower normalized degree
(estimate ± SE = 0.39 ± 0.16, t = 2.39, p = .020; Figure 1a), speciali-
zation (estimate ± SE = 0.12 ± 0.04, t = 2.64, p = .010, Figure 1b) and
species strength (estimate ± SE = −0.41 ± 0.09, t = −4.68, p < .010,
Figure 1c) when compared to native plant species. On the other
hand, alien flower visitor species had higher normalized degree (es-
timate ± SE = −0.16 ± 0.09, t = −1.92, p = .050; Figure 1a), speciali-
zation (estimate ± SE = −0.17 ± 0.03, t = −5.01, p < .010; Figure 1b)
and strength (estimate ± SE  =  −0.99  ±  0.22, t  =  −4.46, p < .010;
Figure 1c) than the native assemblage of flower visitor species.
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Journal of Ecology ARROYO-CORREA et al.

(a) (b) (c)

F I G U R E 1   The roles of native and alien plant and flower visitor species in structuring invaded flower-visiting networks (a, degree; b,
specialization and c, strength). Boxes indicate the 25th to 75th percentiles, the middle line is the median, and the maximum length of the
whiskers is 1.5 times the interquartile range. (*) Significant differences between alien and native species (p < .050)

TA B L E 1   Results from the betweenness centrality (BC) 3.3 | Contribution of alien species to temporal beta-
analyses for the different types of plant–flower visitor interactions diversity
composing the temporal networks

Number of We found significant differences in the interaction composition of

interactions
Interaction type with BC > 0 (%) BC (M ± SD)
Alien plant–alien flower visitor 26 0.029 ± 0.024
Alien plant–native flower visitor 34 0.036 ± 0.026
Native plant–alien flower visitor 3 0.024 ± 0.017
Native plant–native flower visitor 37 0.024 ± 0.024
Note: Interactions with BC > 0 are significant temporal network
connectors. The proportion of interactions of the different types is based
on the total number of interactions with BC > 0. Mean and standard
deviation (SD) correspond to the values among the three study sites.
3.2 | Temporal network connectors
Approximately one fourth of all plant–flower visitor interactions
played a role in connecting the networks through time in our commu-
nities (Table 1; Table S5). We found differences in betweenness cen-
trality (BC) between the pairwise combinations of alien and native
plant–flower visitor interactions (Kruskal–Wallis chi-squared = 7.98,
p < .050; Table S6). Interactions between native plants and native
flower visitors had lower BC compared with alien plant–alien flower
visitor interactions (Dunn z = 1.39, p < .050) and alien plant–native
flower visitor interactions (Dunn z = 2.63, p < .050). Overall, inter-
actions with native plant species had significantly lower potential
to connect the temporal networks (lower BC), while interactions
involving alien plant species, independently of the status of the
flower visitor species, contributed the most to temporal connectiv-
ity (Table 1).
flower-visiting networks across the season (Figure 2; Table S7). In
general, interaction turnover was high between each consecutive
temporal network (βCC = 0.82 ± 0.05 [M ± SD]). The largest contributor
to interaction turnover was the turnover of species (67.27% ± 0.06).
Total species turnover was slightly lower during the middle (between
time 2 and 3, βST  =  0.49  ±  0.07) than earlier (between time 1 and
2, βST = 0.59 ± 0.01) or later in the season (between time 3 and 4,
βST = 0.58 ± 0.06).
Both alien plant and flower visitor species had a significant effect
on the temporal beta-diversity of interactions (Figure 3; Table S8).
Total interaction turnover (βCC) was lower when alien plant species
and alien flower visitor species were removed in comparison with
the random removal of plant (alien removal = 0.84 ± 0.10; random
removal = 0.94 ± 0.06, p < .001) and the random removal of flower
visitor (alien removal = 0.84 ± 0.06; random removal = 0.91 ± 0.04,
p < .001) species. However, the difference in interaction turnover be-
tween alien plant and alien flower visitor species removal was driven
by different processes. The removal of alien plant species reduced
the contribution of interaction rewiring to interaction turnover
(β0  = 0.06 ± 0.07) compared to the removal of random plant species
(0.14 ± 0.12, p < .001). Meanwhile, the removal of alien flower visitor
species decreased the contribution of species turnover to interaction
turnover (βST = 0.60 ± 0.09) in comparison with the removal of ran-
dom flower visitor species (0.66 ± 0.10, p = .015). Additionally, flower
visitor species turnover (βA) was lower when alien flower visitor spe-
cies were removed (alien flower visitor species removal = 0.35 ± 0.11,
random flower visitor species removal = 0.44 ± 0.12, p < .001) and
higher when alien plant species were removed (alien plant species
ARROYO-CORREA et al. Journal of Ecology |
      7

(a) (b) (c)

1 1 1
2 4 2
4
2 4

3 3
3

F I G U R E 2   Temporal networks of plant–flower visitor interactions from the South Island of New Zealand. Graphs correspond to the
networks from (a) site 1, (b) site 2 and (c) site 3. Each node (circle) represents a unique pairwise interaction between a plant species and a
flower visitor species. Squares represent the four time slices in which interactions were sampled during the flowering season. Grey lines
connect the interactions to the time slice in which they were recorded. Therefore, nodes connected to the square number 1 correspond
to those plant–flower visitor interactions that occur earlier in the flowering season. In the other end of the gradient, nodes connected to
square number 4 are those interactions that appeared only at the end of the flowering season. Black nodes shared among squares mean that
the given interaction was present across time, that is, shared nodes are those interactions connecting the temporal networks, which were
persisting throughout the flowering season. Network graphs were built with ‘Network3D’ r package (Allaire et al., 2017)

F I G U R E 3   The distribution of values for species turnover (βST ), interaction rewiring (β0) and total interaction turnover (βCC) of alien-
removal and random-removal simulated plant–flower visitor networks. The results for the removal of plant species are shown in the top
panel and flower visitors in the bottom ones. Density was calculated using a kernel density estimate to visualize the continuous distribution
of the data
 |
8      
Journal of Ecology
F I G U R E 4   The presence of invader complexes and the
preferential interactions between alien species in an invaded plant–
flower visitor network from the South Island of New Zealand. Black
boxes represent modules and invader complexes are identified
when interactions within a given module are predominantly
performed by a pair of alien species. Darker colours correspond to
higher frequency of interactions. This graph is one of the temporal
networks sampled during a flowering season in our study sites in
the South Island of New Zealand (fourth temporal network in site 3,
see Section 2 for details)
removal = 0.48 ± 0.20, random plant species removal = 0.33 ± 0.21,
p  =  .028). In contrast, plant species turnover (βP)  did not change
when alien plant species were removed (alien plant species re-
moval = 0.09 ± 0.11, random plant species removal = 0.16 ± 0.12,
p  =  .062) or when alien flower visitor species were removed (alien
flower visitor species removal = 0.16 ± 0.10, random flower visitor
species removal = 0.11 ± 0.07, p = .063).
3.4 | Invader complexes
The evidence for the presence of invader complexes was strong in
eight temporal networks, weak in three networks, and we found no
evidence in one network (Table S9). The probability of an alien plant
species interacting in the same module with an alien flower visitor
species was, on average, 11.95 times greater than the probability of
interacting in the same module with a native flower visitor species,
supporting the invader complex hypothesis (Figure 4).
4 |  D I S CU S S I O N
Our results suggest that the effects of alien species in structuring the
seasonal dynamics of plant–flower visitor networks largely depend on
the trophic level being considered. While alien plant species were less
specialized and performed fewer interactions than native plant spe-
cies, alien flower visitors showed the opposite pattern. Interactions
ARROYO-CORREA et al.
between alien species were dominant, forming invader complexes
that might have facilitated the establishment of other alien species.
Furthermore, interactions involving alien plant species were the
main connectors of the temporal networks as they persisted longer
throughout the season. In addition, simulated alien species removal
significantly reduced the turnover of interactions, a pattern driven
by distinct underlying mechanisms for alien flower visitor and alien
plant species. First, simulated alien plant species removal reduced
interaction rewiring, suggesting that alien plants, despite homogeniz-
ing plant species composition, may increase interaction rewiring by
continuously attracting new flower visitor species over the season.
Second, alien flower visitor species removal reduced species turnover
even though they were participating in invader complexes through
the season, suggesting that the identity of those alien flower visitors
involved in invader complexes can change over time.
Alien plant species were visited by a lower number of flower vis-
itor species and were less specialized in comparison with the native
plant species which, in turn, showed higher degree and higher spe-
cialization. Hence, even though alien plants in our study sites were
visited by fewer flower visitor species (i.e. lower degree), the fre-
quency of visits by different flower visitor species was more evenly
distributed (i.e. lower d′ specialization). These findings partially
contradict our hypothesis that alien species would perform more
generalist interactions but expand our understanding of the poten-
tial mechanisms behind such generalization found in the literature
(e.g. Aizen et al., 2008; Bartomeus et al., 2008; Lopezaraiza-Mikel,
Hayes, Whalley, & Memmott, 2007). Furthermore, alien plants may
create ‘floral markets’ (sensu Chittka & Schürkens, 2001) by at-
tracting pollinators for the whole plant community, including native
and other alien species. In our study sites in the South Island of
New Zealand, species within the Asteraceae (e.g. Cirsium spp) and
Fabaceae (e.g. Lotus pedunculatus) families formed dense patches
of floral resources during the flowering season, likely functioning
as an attractor of flower visitors to the local assemblage of plants
(Lopezaraiza-Mikel et al., 2007). Interestingly though, as suggested
in a previous study (Chrobock, Winiger, Fischer, & Kleunen, 2013),
the lower strength of the alien plant species also revealed that the
overall flower visitor community depended more on the native flora
to obtain floral resources. These findings stand in contrast with
some studies (Bartomeus et al., 2008; Maruyama et al., 2016) sug-
gesting that flower visitors have a high dependency on alien plant
species. This discrepancy in outcomes among studies may be re-
lated to the use of a multispecies approach that considers all of the
alien species in the community (e.g. this study; Timóteo et al., 2018;
Vizentin-Bugoni et al., 2019), instead of focusing on a single or few
widespread and abundant alien species. The higher degree and
higher strength of the native plant species indicate that they are
providing food resources to a higher number of flower visitor spe-
cies, both alien and natives. Still, the combination of higher richness
of flower visitors and uneven frequency of visitations makes native
plant species more specialized than the alien ones, corroborating
the finding of previous studies as well (Norfolk, Gilbert, & Eichhorn,
2018; Waser, Chittka, Price, Williams, & Ollerton, 1996).
ARROYO-CORREA et al.
Alien flower visitor species participated in a higher number of
interactions (higher degree) than the native ones and still showed
higher specialization and higher strength. This result suggests that
the local flora may become more dependent on alien flower visitors
for pollination than on their sympatric native species. That is exactly
the opposite pattern we found for alien versus native plants; that is,
flower visitors may remain more dependent on native flora. In our
communities, the assemblage of alien flower visitors included diet
and habitat generalist species which formed distinct alien-based
functional groups such as the bees (Bombus spp. and Apis mellifera),
the hoverflies Eristalix tenax and the butterflies Pieris rapae (Goulson,
2003; Lewis, 1989). Additionally, alien pollinator species are often
highly abundant in the areas they invade (Valido, Rodríguez-
Rodríguez, & Jordano, 2019). In our study sites, we can infer the
abundance of alien flower visitor species from the frequency of in-
teractions they established with flowering plants. Therefore, they
potentially act as important pollinators for the local flora, visiting a
range of species with distinct flower morphologies, blooming strat-
egies and resource quality. A previous study (Trøjelsgaard et al.,
2019) showed a similar pattern in five Galápagos islands, where alien
flower visitors had more interaction partners and higher strength
(i.e. plant species were more dependent on those flower visitors)
in comparison with their native counterparts. However, when the
frequency of interactions was considered in our study, alien flower
visitors seem to prefer to visit a small subset of plant species (higher
specialization).
We found that alien plants and alien flower visitors interact more
with each other than expected by chance, supporting the presence
of invader complexes. Our findings are contrary to previous work
in two different oceanic islands whose data did not support the ex-
istence of invader complexes (Olesen et al., 2002), but our results
are consistent with the findings of Morales and Aizen (2006) and
Traveset et al. (2013), which report the occurrence of such com-
plexes. The combination of generalist characteristics and the pres-
ence of invader complexes may have facilitated the spread of alien
species in New Zealand (D’Antonio & Dudley, 1993). For example,
bumblebees and honeybees that were first introduced in New
Zealand to enhance crop pollination (Donovan, 1980) are now widely
established in both the South and North Island, possibly because of
the interactions they have been able to establish with both native
and introduced plant species (Olesen et al., 2002).
The temporal turnover of interactions across the season was
extremely high, confirming the importance of temporal scale in
the structure of mutualistic networks (see also Burkle & Alarcón,
2011; Olesen et al., 2008; Petanidou et al., 2008). Changes in
species composition over the season were the main drivers of
the seasonal turnover of plant–flower visitor interactions. Our
findings contradict a previous study also carried out in subalpine
plant–flower visitor communities in which the within-season in-
teraction turnover was primarily driven by interaction rewiring
(CaraDonna et al., 2017). This discrepancy between studies may
be due to differences in phenophases between the two systems
or to the coarser temporal resolution in our study in comparison
Journal of Ecology |
      9
with CaraDonna et al. (2017), which may strengthen the effects of
the turnover of species. Because it is more likely for two species
to continue to co-occur across shorter timespans compared to lon-
ger ones, if we had collected data at a finer temporal resolution,
we would expect interaction rewiring to contribute more strongly
to the total beta-diversity of interactions. Moreover, the constant
presence of alien species in our system likely changed the seasonal
dynamics of the local communities and may explain the different
outcomes between studies.
As expected with the directional turnover of species (Anderson
et al., 2011), and thus interactions, over a flowering season, the two
temporal networks in the middle of the season shared a higher num-
ber of interactions than those composing the networks at the start
and at the end of the season. Such a pattern is partially caused by
phenology given that the first and the last temporal networks lacked
many flowering plant species, which is not surprising since flow-
er-visiting networks are phenologically driven systems (Encinas-Viso,
Revilla, & Etienne, 2012; Rafferty & Ives, 2011). Temporal networks
were connected by a relatively low number of interactions, and
most plant–flower visitor associations occurred in a short window
of time. The betweenness centrality results revealed that alien spe-
cies, especially plants, played an important role in connecting the
temporal networks by performing interactions that persisted longer
in the flowering season. These findings are also supported by the
persistence of invader complexes across the season, which may facil-
itate the temporally prolonged presence of alien flower visitors in the
study area (Morales & Aizen, 2002; Olesen et al., 2002). As pheno-
logical overlap is one of the major factors influencing pollinator-me-
diated interactions between plant species (McKinney & Goodell,
2011), the longer persistence of alien–alien interactions may have
critical consequences on the direction of the impacts of alien spe-
cies on the pollination of native plant species. However, in order to
explore the overall ecological and evolutionary implications of such
pattern, it would be necessary to analyse the pollen transport fluxes
between native and alien plants (Alarcón, 2010), which can assist in
investigating the facilitative and competitive interactions between
those species (Emer et al., 2015; Lopezaraiza-Mikel et al., 2007).
Finally, the simulated removal of alien species reduced in-
teraction turnover between temporal networks; yet, the drivers
of the temporal turnover of interactions were also trophic-level
dependent. This approach does not include the mechanisms by
which alien species integrate and affect native communities, such
as competitive exclusion and preferential attachment (Revilla &
Křivan, 2018), and does not consider the potential for interaction
rewiring to occur between the native species after aliens have
been removed. That said and considering a lack of pre-invasion
data for this system, these simulations (and comparisons to the
null models) can be seen as a first step towards understanding how
alien species influence the plant–flower visitor interaction com-
position through a flowering season. Alien plant species signifi-
cantly increased interaction turnover due to interaction rewiring,
suggesting that alien plants may be outcompeting native plants by
attracting pollinators that would otherwise interact with the local
 |
10      
Journal of Ecology
flora, as demonstrated in previous studies (Bjerknes et al., 2007;
Chittka & Schürkens, 2001).
Together with the betweenness analysis, our results demon-
strated that alien plant species have a long persistence through
the season – leading to a temporal homogenization of interacting
species composition – but they simultaneously have an important
role increasing the relative occurrence of interaction rewiring over
time. Towards the end of the season, many native species have
already passed their phenological optimum for reproduction (i.e.
blooming or flying activities), and the remaining species may start
to interact with each other even if they are not each other's pref-
erential partners (Olesen et al., 2008; CaraDonna et al., 2017). For
example, Bombus spp. started to interact with native plants at the
end of the season after the flowers of their alien plant partners had
stopped blooming. Likewise, late-season alien plant species might
offer additional resources for those native species of flower visi-
tors whose preferential partner is not flowering anymore (Shea &
Chesson, 2002). Moreover, the simulated removal of alien plants
also promoted an increase in the turnover of flower visitor species,
suggesting that alien plants may homogenize the temporal assem-
blage of flower visitors either by ‘rescuing’ native flower visitor
species that have lost their preferential flower resource (Chittka &
Schürkens, 2001) or by facilitating the persistence of alien flower
visitor species in the system through the maintenance of invader
complexes (D’Antonio & Dudley, 1993). Finally, total species turn-
over was lower in the networks in which alien flower visitor species
were removed, a pattern driven by the decrease in flower visitor
species turnover, compared to random species removal simula-
tions. That is, although alien flower visitor species participated in
invader complexes over the entire flowering season, the identity
of those flower visitor species can change over time and therefore
they may increase the interaction turnover due to species turnover.
5 |  CO N C LU S I O N S
This study provides one of the first empirical reports showing
that alien species have a crucial effect on the seasonal dynam-
ics of plant–flower visitor networks. We demonstrated that the
presence of alien species facilitates invader complexes and pro-
motes changes in the organization of plant–flower visitor inter-
actions over the flowering season. Additionally, we highlighted
the importance of considering the role of different trophic levels
when analysing the impact of alien species in plant–flower visi-
tor communities. Overall, our findings suggest that management
strategies should pay particular attention to the timescale at
which interactions with alien species dissolve or form, and to the
consequences and drivers of such seasonal dynamics. In the light
of our results, conservation plans should consider the potential
consequences of aggregating interaction data with an underly-
ing temporal structure when it comes to assessing the impacts of
alien species in the community structure. In our study system, the
transition to alien-dominated communities could simultaneously
ARROYO-CORREA et al.
lead to a homogenization of species composition and increase the
diversity of plant–flower visitor interactions through the flowering
season. Such changes may affect the persistence of interactions
performed exclusively by native species and may have conse-
quences for the maintenance of the ecosystem functioning.
AC K N OW L E D G E M E N T S
We thank Pedro Jordano, Ignasi Bartomeus and two anonymous
reviewers for their helpful comments on earlier drafts of the man-
uscript. We thank Jane Memmott, Jason Tylianakis, Laura Young,
Michele Lambert, Sarah Kruis, Jane Ladley and the University of
Canterbury for friendship, intellectual, logistical and field-assistance
support. C.E. was funded by the Coordination for the Improvement
of Higher Education Personnel (CAPES, Brazil).
AU T H O R S ’ C O N T R I B U T I O N S
C.E. conceived the idea and collected the data. B.A-.C. and C.E.
analysed the data and wrote the first draft of the manuscript.
B.A-.C., L.A.B. and C.E. contributed to subsequent drafts and gave
final approval for publication.
DATA AVA I L A B I L I T Y S TAT E M E N T
Plant–flower visitor interaction data used in this study are depos-
ited in the Zenodo Digital Repository: https​://doi.org/10.5281/
zenodo.3011651 (Arroyo-Correa, Burkle, & Emer, 2019).
ORCID
Blanca Arroyo-Correa  https://orcid.org/0000-0002-9402-3013
Laura A. Burkle  https://orcid.org/0000-0002-8413-1627
Carine Emer  https://orcid.org/0000-0002-1258-2816
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S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found online in the
Supporting Information section.
How to cite this article: Arroyo-Correa B, Burkle LA, Emer C.
Alien plants and flower visitors disrupt the seasonal
dynamics of mutualistic networks. J Ecol. 2019;00:1–12.
https​://doi.org/10.1111/1365-2745.13332​