Species roles in -pollinator communities are conserved across native and alien ranges Carine Emer, Jane Memmott, Ian P. Vaughan, Daniel Montoya, Jason M. Tylianakis

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Carine Emer, Jane Memmott, Ian P. Vaughan, Daniel Montoya, Jason M. Tylianakis. Species roles in plant-pollinator communities are conserved across native and alien ranges. Diversity and Distributions, Wiley, 2016, 22 (8), pp.841-852. ￿10.1111/ddi.12458￿. ￿hal-02640827￿

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Distributed under a Creative Commons Attribution - NonCommercial - NoDerivatives| 4.0 International License Diversity and Distributions, (Diversity Distrib.) (2016) 22, 841–852

BIODIVERSITY Species roles in plant–pollinator RESEARCH communities are conserved across native and alien ranges Carine Emer1,2*, Jane Memmott1, Ian P. Vaughan3, Daniel Montoya1,4,5 and Jason M. Tylianakis6,7

1Life Sciences Building, University of Bristol, ABSTRACT 24 Tyndall Avenue, Bristol BS81TQ, UK, Aim Alien species alter interaction networks by disrupting existing interactions, 2Departamento de Ecologia, Universidade for example between and pollinators, and by engaging in new interac- Estadual Paulista (UNESP), 13506-900 Rio Claro, S~ao Paulo, Brazil, 3Cardiff School of tions. Predicting the effects of an incoming invader can be difficult, although Biosciences, Cardiff University, Museum recent work suggests species roles in interaction networks may be conserved – Avenue, Cardiff CF103AX, UK, 4Center for across locations. We test whether species roles in plant pollinator networks dif- Biodiversity Theory and Modeling, Station fer between their native and alien ranges and whether the former can be used d’Ecologie Theorique et Experimentale, to predict the latter. Centre National de la Reserche Cientifique, 5 Location World-wide.

A Journal of Conservation Biogeography 09200 Moulis, France, INRA, UMR 1347 Agroecologie, Dijon Cedex 21065, France, Methods We used 64 plant–pollinator networks to search for species occurring 6Centre for Integrative , School of in at least one network in its native range and one network in its alien range. Biological Sciences, University of Canterbury, We found 17 species meeting these criteria, distributed in 48 plant–pollinator Private bag 4800, Christchurch 8140, New networks. We characterized each species’ role by estimating species-level net- Zealand, 7Department of Life Sciences, work indices: normalized degree, closeness centrality, betweenness centrality Imperial College London, Silwood Park and two measures of contribution to modularity (c- and z-scores). Linear Campus, Buckhurst Road, Ascot, Berkshire mixed models and linear regression models were used to test for differences in SL5 7PY, UK species role between native and alien ranges and to predict those roles from the native to the alien range, respectively.

Results Species roles varied considerably across species. Nevertheless, although species lost their native mutualists and gained novel interactions in the alien , their role did not differ significantly between ranges. Consequently, closeness centrality and normalized degree in the alien range were highly pre- dictable from the native range networks.

Main conclusions Species with high degree and centrality define the core of nested networks. Our results suggest that core species are likely to establish interactions and be core species in the alien range, whilst species with few interactions in their native range will behave similarly in their alien range. Our results provide new insights into species role conservatism and could help ecol- ogists to predict alien species impact at the community level. *Correspondence: Carine Emer, Life Sciences Keywords Building, University of Bristol, 24 Tyndall and Distributions Avenue, Bristol BS81TQ, UK. biological invasions, centrality, conservatism, ecological networks, pollination, E-mail: [email protected] predicting invasion.

Schurkens, 2001; Madjidian et al., 2008; Roy et al., 2012), INTRODUCTION change the community structure (Albrecht & Gotelli, 2001; Predicting novel species interactions is a crucial challenge in Memmott & Waser, 2002; Carpintero et al., 2005) and dis- today’s rapidly changing world. Alien species are an impor- rupt species interactions (Traveset & Richardson, 2006; Aizen

Diversity tant driver of novel ecosystems (Hobbs et al., 2006) due to et al., 2008; Tylianakis et al., 2008). Studies on alien species their ability to out-compete native species (Chittka & mostly focus on species considered to be invasive, which

DOI: 10.1111/ddi.12458 ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/ddi 841 C Emer et al. means that rather little is known about those alien species locations, this indicates that species roles in networks should that remain at low population size or have fewer interactions also be conserved. For example, species roles in predator– with (and hence, impact on) the recipient community. prey networks can be conserved from an evolutionary Whilst many studies have tried to identify key features perspective, such that dynamically important species in one that predict which species will become invasive and which network will be important in the other networks in which it communities are more likely to be invaded (Thuiller et al., occurs (Stouffer et al., 2012). Similarly, species roles in host- 2005; Richardson & Pysek, 2006; Pysek & Richardson, 2007), parasitoid networks were found to be intrinsic characteristics these remain of limited practical value. For example, it conserved over different temporal and spatial scales (Baker remains difficult to predict whether a mutualistic interaction et al., 2015). will facilitate the establishment and dispersal of an alien spe- Despite evidence of an intrinsic component of species net- cies (Hulme, 2012). The limited practical value of current work roles, species interactions and network roles may also work is partially due to the need for detailed information on be affected by local environmental and biotic conditions each species involved in the potential novel interactions, (Tylianakis et al., 2008; Trøjelsgaard et al., 2015). Moreover, which is usually very time-consuming to gather. Therefore, the number and type of interactions a species has increase new methods to simplify predictions are required. An alter- with that species’ abundance (e.g. Trøjelsgaard et al., 2015), native could be to assess the role a given species plays in the and species abundance and interactions may change during topology of interaction networks (e.g. Martın Gonzalez et al., different stages of invasion (Aizen et al., 2008). Finally, pat- 2010; Stouffer et al., 2012; Albrecht et al., 2014). Species terns of non-random association among species based on roles summarize their ability to interact with, and potentially their phylogenetic relatedness (Rezende et al., 2007) suggest affect, other species in the community in a way that is rela- that co-evolved interactions may be important for structur- tively easy to sample compared with measures of multiple ing mutualistic networks. Therefore, it is currently not clear species and community traits. The application of species whether species roles can be extrapolated from one location roles in ecological networks to predict invasion currently to another that differs in its evolutionary history and local remains untested. community traits. Ecological networks have been of considerable use when Here, we aim to understand whether species roles differ trying to understand how alien species integrate into local and can be predicted from the native to the alien range of communities (Memmott & Waser, 2002; Garcia et al., 2014; their distribution. Specifically, we use measures of plant and Maruyama et al., 2016) and how they affect the overall species roles in plant–pollinator networks (normalized mutualistic network structure (Olesen et al., 2002; Santos degree, closeness and betweenness centrality, and c- and et al., 2012; Albrecht et al., 2014). In general, alien species z-scores) recorded in both their native and alien ranges to are generalists, that is they interact with many species in the test whether they differ consistently or can be predicted community in which they occur (Aizen et al., 2008; Santos between ranges. Based on the findings that species roles and et al., 2012). Generalist species tend to occupy central posi- ecological interactions can be temporally, spatially and phy- tions in ecological networks, and by interacting with other logenetically conserved (Rezende et al., 2007; Gomez et al., generalists and specialists (Memmott & Waser, 2002; Aizen 2010; Stouffer et al., 2012; Baker et al., 2015), we predict that et al., 2008) they contribute to the pattern of nestedness that a species’ network role will be similar in its native and alien characterizes many mutualistic networks (Bascompte et al., ranges, such that the former can be used to predict the latter. 2003; Bascompte & Jordano, 2007). In addition to its num- By including both specialist and generalist species, we can ber of direct interaction partners (termed ‘degree’), a species’ draw conclusions about both rare and common alien species. position allows it to connect different parts of the network and maintain network cohesiveness. This helps to define its METHODS role in structuring the overall network topology (Martın Gonzalez et al., 2010), including elements of network struc- We searched for plant–pollinator networks where we could ture such as clustering or modularity (Olesen et al., 2007). potentially find species recorded in both their native and Thus, the species’ position in the network, that is its network alien range. We found 48 plant–pollinator networks of which role, captures key information on its interactions with, and 42 were downloaded from the ‘Web of Life’ database potential effects on, other species in the community. (Ortega, 2014), three are our own data sampled in New Zeal- Recent work suggests that species roles are conserved and and three are unpublished data from Lopezaraiza-Mikel across different locations. Species interactions, either general- and Memmott in Hawaii; Table S1. Our criteria of species/ ist or specialist, have been shown to be phylogenetically con- network inclusion in the dataset were to have a target species served across space and time (Jordano et al., 2003; Rezende occurring in at least one network as native and one network et al., 2007; Gomez et al., 2010), because intrinsic (inherited) as alien. Thus, each network can contain more than one tar- characteristics of species can constrain who can interact with get species, each of which may be either in its native or its whom (Eklof€ et al., 2013) and can be related to native and alien range. As some of these networks contain only the alien species roles in network topology (Maruyama et al., presence/absence of interactions and the sampling effort of 2016). If these traits show low intraspecific variability across these networks is mostly unknown, we analysed all networks

842 Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd Native–alien species roles in pollination networks as binary matrices. In addition, here, a flower visitor was species importance for network cohesiveness (Freeman, 1979; considered to be a pollinator, irrespective of whether effec- Martın Gonzalez et al., 2010). Species with high betweenness tive pollination was demonstrated. To define species range as can potentially connect different parts of the network that native or alien, we used the following online information: could be otherwise sparsely linked or even isolated; thus, Global Database (http://www.issg.org/data alien species that tend to be highly generalist may be linking base/welcome/), Global Invasive Species Information Net- previously isolated species in plant–pollinator networks and work (http://www.gisin.org), Delivering Alien Invasive Spe- affect the overall network structure. cies Inventories for Europe (http://www.europe-aliens.org/), 4. and 5. c- and z-scores: the combination of these two met- GB Non-Native Species Secretariat Website (http://www.non rics describes a species’ role in the topology of the network nativespecies.org), Plant Pest Information Network of New as a hub, peripheral or connector within and among mod- Zealand (http://archive.mpi.govt.nz/applications/ppin), Cen- ules (Olesen et al., 2007) based on the modularity of the net- tre for Invasive Species and Ecosystem Health (http:// work (Guimera & Amaral, 2005). The z-score calculates the www.bugwood.org/), Weeds in Australia (http://www.envi- standardized number of links a species has within a module, ronment.gov.au/biodiversity/invasive/weeds/) and Invasive and the c-score calculates the among module connectivity, Species of Japan (https://www.nies.go.jp). which is the number of links a given species establishes among different modules. Therefore, high values of c and z are related to generalist species that have many interactions Species roles throughout the whole network, either as hubs connecting Species roles in networks can be described by a variety of species within modules or as connectors linking different different, yet often correlated metrics. Our intent here was modules. On the other hand, low values of c and z describe not to provide an exhaustive comparison of different peripheral species that tend to be specialists. Alien plant spe- potential measures of species roles or to determine which cies that invade a new range may act as network hubs by metrics were best conserved and why. Rather, we focused attracting many different pollinator species through provid- on testing a ‘proof of concept’ that roles could be con- ing high amounts of nectar; for example, Himalayan balsam served, so we focused on five complementary metrics that (Impatiens glandulifera Royle) acts as a ‘magnet species’ in could potentially capture different aspects of species its alien range (Chittka & Schurkens, 2001; Lopezaraiza- ecology: Mikel et al., 2007), whilst alien pollinator species may act as 1. Normalized degree – the number of interactions per spe- network connectors whilst searching for floral resources in cies (i.e. degree) divided by the number of possible interact- different modules. ing partners, which controls for differences in network size. To allow comparisons across networks with different size, Normalized degree is the most local centrality index that closeness and betweenness were each scaled to sum to 1. Spe- characterizes a species’ network position, such that species cies role metrics were calculated using bipartite (Dormann with high degree are core in the network structure and et al., 2009) and rnetcarto packages (Doulcier & Stouffer, enhance robustness (Sole & Montoya, 2001; Dunne et al., 2015) for R; correlations among these metrics are shown in 2002). Additionally, normalized degree estimates how gener- Table S5. alist/specialist a species is relative to other species in the same trophic level of the community in which it occurs. Statistical analysis 2. Closeness centrality (hereafter, closeness) – the average distance (path length) to all other species in the network. Are there differences in species roles in their native versus alien Closeness incorporates the number of immediate connections range? to adjacent nodes and the connections of those nodes, so is a more global measure of location than degree. In bipartite To answer whether species roles differed from native to networks, closeness and betweenness are measured for the alien ranges, we used linear mixed-effects models (LMMs) unipartite projection of each trophic level based on shared in the LME4 package (Bates et al., 2014). Individual models interaction partners, such that higher closeness indicates a were fitted for normalized degree, closeness, betweenness, greater number of interaction partners shared with other and c- and z-scores. The first four metrics were logit-trans- species in the same trophic level that also share partners with formed to solve the issue of being bounded from zero to many other species (Freeman, 1979; Martın Gonzalez et al., one (Warton & Hui, 2011). Range (native versus alien) was 2010). Thus, closeness is a measure of niche overlap with modelled as a fixed factor, whilst network and species were other species at the same trophic level via shared pollinators fitted as random effects to account for multiple observa- and the potential for either positive or negative indirect tions from the same network and to group native and alien effects via short path lengths (Morales & Traveset, 2008; Car- measures from the same species. Residual plots were used valheiro et al., 2014). to check model adherence to assumptions. The overall vari- 3. Betweenness centrality (hereafter, betweenness) – the pro- ance explained by the model, and the proportion that could portion of the shortest paths linking any pair of species in be attributed to the fixed factor (range) and the random the network that cross through a given species. It estimates factors were estimated by calculating: (1) conditional

Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd 843 C Emer et al.

Pseudo R-squared (R2GLMM ), to estimate total (fix+rand) RESULTS variance explained by the fixed and random effects com- 2 bined, (2) marginal Pseudo R-squared (R GLMM(fix)), to We compiled information on 12 plant species and five polli- estimate the variance explained by range and (3) the differ- nator species that occurred in at least one network in a 2 2 ence between the two (R GLMM(fix+rand) R GLMM(fix)) native range and one network in an alien range (Table 1). to estimate the contribution of the random effects only These 17 species, from 19 different countries, were dis- 2 (R GLMM(rand)) (Nakagawa & Schielzeth, 2013), using the tributed in all continents except Antarctica (Fig. 1, MUMIM package (Barton, 2013). Then, to determine Table S1); this translates into a large range of different habi- whether any difference in species roles between native and tats, climatic conditions and species richness. In total, we exotic range could have occurred due to biogeographical worked with 167 occurrences of the 17 target species (i.e. patterns from tropical to temperate zones (Olesen & Jor- one occurrence corresponds to the occurrence of a species in dano, 2002; Schleuning et al., 2012), we reran the above either its native or alien range; note that multiple target spe- models including the absolute latitude as a fixed effect cies can occur in the same network; Table S2). interacting with range. Likewise, we reran the models with trophic level (plant or pollinator) and its interaction with Are there differences in species roles between their range to determine whether any differences between native native and alien range? and alien range only applied to one trophic level. There was no significant difference between native and alien ranges in any of the measures of species’ role (Table 2). In Does a species’ role in the native range predict its role in the other words, we found no evidence that, for example, species alien range? consistently interact in a more generalist way in their exotic To test whether a species’ role in the native range can pre- versus native range. Rather, the variance explained by the dict its role in the alien range, we fitted five linear regres- sions relating species’ mean normalized degree, closeness, betweenness, and the c- and z-scores in the alien range to Table 1 The 17 plant and pollinator species analysed in this the mean values in their native range. Normalized degree study (see Table S1 for further information about each was strongly influenced by an outlier, which was removed network). and consequently improved model fit (Appendix S1). Model validation to check for homoscedasticity and nor- Number of networks present mality of the residuals was performed following Zuur et al. (2009) and Crawley (2013). As previously, we reran these Native Alien regressions including, separately, absolute latitude and Plant species Family networks networks trophic level and their interactions with species’ role in the Achillea millefolium L. Asteraceae 4 5 native range to determine whether the predictive power Cirsium arvense (L.) Scop Asteraceae 3 6 depended on these variables. Latitude was determined for Cytisus scoparius (L.) Link Fabaceae 1 1 each species as the absolute difference between latitudinal Eupatorium cannabinum L. Asteraceae 1 2 mean in the native range and the latitudinal mean in the Hieracium pillosela L. Asteraceae 2 4 alien range. The latitudinal mean was obtained by averaging Hypochaeris radicata L. Asteraceae 5 6 the absolute latitude of all occurrences each species has in Leucanthemum vulgare Lam. Asteraceae 2 4 its native and alien ranges. Lotus corniculatus L. Fabaceae 3 1 Subsequently, we jackknifed the linear regression models Taraxacum officinale Asteraceae 4 1 to provide an unbiased assessment of how accurately spe- F.H. Wigg cies roles could be predicted in alien networks based on Trifolium pratense L. Fabaceae 2 4 their mean role in the native networks (Efron, 1983). Each Trifolium repens L. Fabaceae 3 10 Verbascum thapsus L. Scrophulariaceae 2 3 species was removed from the linear regression in turn, the Total plant occurrences 32 47 regression refitted, and predictions of the role metrics were generated for that species in the alien networks based on Insect species Order its mean value across its native networks. The observed mean values in the alien range were then compared against Apis mellifera L. Hymenoptera 9 28 the predicted values using Pearson’s correlations. Individual Bombus hortorum L. Hymenoptera 7 4 species roles and mean species roles were tested for correla- Bombus terrestris L. Hymenoptera 9 6 tion (presented as the Spearman coefficient in Table S5), Eristalis tenax L. Diptera 5 11 and a Bonferroni correction was used in both LMMs and Pieris rapae L. Lepidoptera 3 6 linear regression models (LMs). All statistical and network Total insect 33 55 occurrences analyses were run in R v. 2.15.3 and v. 3.1.1 (R Core Team, Total 65 102 2014).

844 Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd Native–alien species roles in pollination networks

14

11 A B 27 46 8 26 30 22 C 15 G 12 E 33 34 29 25

47 48 13 D 19 F

(a) (b) (c)

46 1832 3135 37 39 38 40 109 17 16

(d) (e) (f) (g)

721

4345 44 1 23 20 42 2 41 3 28 46 24 5 36

Figure 1 The location of the 48 plant–pollinator networks. Panels a–g show the location of those networks that overlap in the full map. Numbers are the individual codes of each network identity (see Supplementary Material). models was primarily attributable to the random factors of the metrics tested (Table 2). Similarly, the random struc- 2 (R GLMM(rand) was 94%, 40% and 20% in the closeness, ture explained around one-third of the variance in the normalized degree and betweenness models, respectively), z-score (29%) and the c-score models (37%). The large vari- which were the network and the species identity, whilst ance retained by the random structure suggests that species range, the fixed term, was not statistically significant for any differ considerably in their network roles and that,

Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd 845 C Emer et al.

Table 2 Results of the linear mixed-effects models (LMMs) range 9 latitude interaction (Table S3). However, a signifi- testing whether species roles differ from the native to the alien cant range 9 trophic level interaction for closeness range. Pseudo R-squared values were calculated to estimate the (Table S3) revealed that the native range had lower closeness variance explained by the fixed and random structure of each for pollinators but not for plants. This indicates that pollina- model: R2 – estimates total variance explained by the fixed fixþrand tors may move into a more central role in their alien range and random effects combined; R2 – estimates the variance fix by pollinating generalist plants that are also pollinated by explained by range; R2 – estimates the contribution of the rand many other species and share those pollinators with many random effects only. other plants. Given that in our analyses there were more LMMs plant species than pollinator species, this interaction effect captured the difference between ranges for pollinators that 2 2 2 Estimates tPRfixþrand Rfix Rrand was otherwise masked by the lack of difference for plant spe- Normalized 0.305 1.227 0.226 0.408 0.011 0.397 cies. Moreover, pollinator species had higher c-scores than degree plant species independently of range, suggesting that the pol- Closeness 0.108 1.188 0.237 0.939 0.003 0.936 linators included in our analyses may be better network con- Betweenness 0.116 0.326 0.747 0.201 0.000 0.201 nectors (Table S3). In fact, most plant and pollinator species z-score 0.029 0.158 0.875 0.285 0.000 0.285 played peripheral roles in our networks (73%) but pollina- c-score 0.028 1.076 0.285 0.378 0.010 0.377 tors were the main connectors (88%), module hubs (75%) and the only network hubs (100%; Table S4). unsurprisingly, species roles depend on the local network (e.g. network size constrains the range of possible roles), and Does a species’ role in the native range predict its this large variance within native or exotic ranges of a species role in the alien range? blurred any significant differences between them. Even though network architecture can change across Two measures of species roles, closeness and normalized regions (Olesen & Jordano, 2002), we found no systematic degree, in the alien range could be predicted from the native 2 change in species roles with latitude, or any significant range data (F1,15 = 27.32, P = 0.0001, r = 0.65 and

(a) Normalized degree, P = 0.002, r 2 = 0.49 (b)Closeness, P = 0.0001, r 2 = 0.65 (c) Betweenness, P = 0.076, r 2 = 0.19 0.08 0.10 Alien range Alien range Alien range 0.04 0.06 0.02 0.04 0.06 0.08 0.00 0.02 0.00 0.10 0.20 0.30 0.05 0.10 0.15 0.20 0.25 0.30 0.01 0.03 0.05 0.07 0.00 0.05 0.10 0.15 0.20 0.25 Native range Native range Native range

(d)c−score, P = 0.644, r 2 = 0.01 (e) z−score, P = 0.062, r 2 = 0.21 Alien range Alien range −1.0 −0.5 0.0 0.5 1.0 0.2 0.3 0.4 0.5 0.6 0.2 0.3 0.4 0.5 0.6 −1.0 −0.5 0.0 0.5 1.0 1.5 Native range Native range

Figure 2 Results of the linear regression models testing whether a species’ role in the native range predicts its role in the alien range. (a) Normalized degree; (b) Closeness; (c) Betweenness; (d) c-score; and (e) z-score. Results of normalized degree are shown after the removal of an outlier.

846 Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd Native–alien species roles in pollination networks

2 F1,14 = 13.56, P = 0.0025, r = 0.49, respectively; Fig. 2). The roles, the roles of species generally did not differ consistently coefficients for closeness and normalized degree were 0.98 betweentheiralienandnativerangesand(2)twometricsof (SE 0.187) and 0.71 (SE 0.192), respectively, and both species roles, closeness and normalized degree, in the alien had intercepts that did not differ significantly from zero range could be predicted from the native range. Betweenness (closeness: t = 0.25, P = 0.809; normalized degree: t = 0.67, and z-score predictions from the native to the alien range were P = 0.512), suggesting that a species’ role in the native range marginally non-significant, but showed a trend towards positive is associated to that in the alien range. In contrast, the posi- correlation, which was unsurprising in the case of betweenness, tive trend in the relationship between native and alien range given its high correlation with normalized degree and closeness when estimating betweenness (slope = 0.208 SE 0.109) (Table S5b). Despite this overall predictive ability, we found and the z-score (slope = 0.412 0.204) was marginally non- that pollinators (but not plants) had a higher closeness in their 2 significant (F1,15 = 3.63, P = 0.076, r = 0.14 and alien range, probably due to their ability to exploit a wide 2 F1,15 = 4.07, P = 0.062, r = 0.21, respectively; Fig. 2) and range of resources and thus interact with generalist plants. Still, lacked any significance for the c-score model (F1,15 = 0.22, trophic level (pollinator versus plants) did not interact signifi- P = 0.644). Although the testing of correlated variables cantly with range, except for c-score, which showed higher val- (Table S5) increases the probability of type I error, the effects ues for pollinators, suggesting they may play a better role in for closeness and normalized degree remained significant connecting the whole networks than did plants. Our results when a Bonferroni correction was applied (corrected suggest that species role conservatism may occur, such that spe- alpha = 0.01). Moreover, of five variables tested, the proba- cies that are generalists or play a central role in their native bility of finding two significant at an alpha below 0.0025 is network are likely to play a similar role in their alien range. extremely low (6.2 9 10 5, calculated using the Bernoulli process described in Moran, 2003), indicating that overall Limitations the suite of species roles in the exotic range could be pre- dicted better from roles in the native range than would be In an ideal situation, the networks studied would have been expected by chance. collected using the same methods, aiming for quantitative data The predictive effects of closeness and normalized degree were collected over similar periods of time. The dataset used comes consistent when latitude and trophic level were included in the from different sources that used different sampling methodolo- models (Table S3). Neither latitude (normalized degree: gies, spatial and temporal scales. Moreover, it contains only

F3,13 = 0.355, P = 0.787; closeness: F3,13 = 1.61, P = 0.235; species that successfully established in the alien range; thus, it betweenness: F3,13 = 0.938, P = 0.450; c-score: F3,14 = 2.00, lacks information for those species that failed to establish in the

P = 0.173; z-score: F3,14 = 0.56, P = 0.652) or trophic level alien range. Moreover, our models do not consider species

(normalized degree: F3,13 = 0.262, P = 0.851; closeness: abundance, which is known to drive some network patterns

F3,13 = 1.708, P = 0.214; betweenness: F3,13 = 1.044, P = 0.406; (Bluthgen€ et al., 2007; Dorado et al., 2011; Staniczenko et al., c-score: F3,14 = 2.00, P = 0.173; z-score: F3,14 = 0.56, P = 0.652) 2013; Fort et al., 2016) as well as the effects of invasive species showed any significant interaction with range when tested for (Dostal et al., 2013; Carvalheiro et al., 2014; Traveset & predictive effects of species roles from the native to the alien Richardson,2014).Furthermore,theconservationstatusofthe range of a species distribution (Table S4). Congruent with areas from which the networks were sampled is mostly the LMM results, after model selection, we detected that the unknown. Thus, the native range should not be necessarily mean c-score was also higher for pollinators than for plants interpreted as a pristine environment given that we are likely independently of range (F2,14 = 12.02, P = 0.0009). working with altered environments in both ranges. This high In the jackknife validation of our predictions, predicted heterogeneity in the dataset generated high variance across dif- values of closeness in the alien range were highly correlated ferent networks (even within a species’ native or alien range), with the corresponding observed values (t = 15.339, which would have reduced the probability of detecting differ- P < 0.0001, r = 0.777), suggesting that the species closeness ences across ‘treatments’. In that sense, the absence of evidence in the native range is a good predictor of the species close- for differences in species roles in native versus alien range can- ness in the alien range. The predictive power of native range not be viewed as evidence of absence. That said, the positive was lower but still a good predictor for more than half of correlations we observed between native- and alien-range values the species when estimating normalized degree (t = 9.040, of closeness and normalized degree were robust enough to be P < 0.0001, r = 0.583), z-score (t = 8.045 P =<0.0001, seen despite the data being averaged across these heterogeneous r = 0.53) and c-score (t = 8.587, P < 0.001, r = 0.56), replicate networks and spanning species with a range of roles although not as good for betweenness (t = 5.621, from specialists to generalists. P < 0.0001, r = 0.401). The intrinsic roles of alien species in pollination DISCUSSION networks

Two consistent patterns emerged from our analyses of the 48 The correlation between species roles in their native and datasets: (1) although species differed considerably in their alien range in the five network statistics concurs with other

Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd 847 C Emer et al. authors who report that species have intrinsic properties in thereby obtaining different food resources (Traveset et al., ecological networks that persist over temporal and spatial 2013). Pollinators were the main connectors in our networks scales (Jordano et al., 2003; Gomez et al., 2010; Stouffer and that was more frequent in their alien range. Given that et al., 2012; Baker et al., 2015). From the roles estimated the main pollinator connectors in our network were social here, high degree and high closeness define the core of the (i.e. Apis mellifera and Bombus spp.), which are usu- nested network (i.e. those generalists that interact with both ally highly abundant in invaded areas (e.g. Aizen et al., 2008; specialists and generalists), and our results suggest that core Santos et al., 2012), and whose individuals reflect species will tend to maintain this role even when they enter the colony needs (Willmer & Finlayson, 2014 and references novel communities. Species with high degree, that is general- therein), it may be that these species’ roles vary according to ists, are expected to be good invaders because they can their population density and foraging behaviour. Yet, central increase their chance to establish and spread through the pollinator species may face high competition with the local population by interacting with many of the ‘available’ spe- pollinators with which they share interactions, a constraint cies. Conversely, specialist species with few interactions in that may make it difficult for pollinators to establish in a the native range will also have only few interactions in the novel community with low nectar/ resources, for alien range, and this may lower their chance of establishing example. into the novel community if, for example, the resource is Our findings also have implications for network persis- scarce and competition strong (Aizen et al., 2008, 2012), as tence. Rewiring, that is the reshuffling of interaction links shown in previous work that simulated invasion of food among species, can enhance network resilience and robust- webs (Romanuk et al., 2009). In turn, high closeness can be ness to disturbance (Staniczenko et al., 2010; Kaiser-Bunbury seen in species that interact with other central species in the et al., 2011; Olesen et al., 2011). Given that both plant and community, even if the focal species is not a generalist itself. pollinator links can be transferred from native generalist to In fact, in our dataset, the average normalized degree and alien generalist species (Aizen et al., 2008) and that the prob- average closeness were not significantly correlated (r = 0.24, ability of a native pollinator interacting with an alien plant Table S5b), such that a species could occupy a consistently increases with its degree and nestedness contribution (Stouf- central position in networks by interacting with central spe- fer et al., 2014), the introduction of a highly generalist alien cies, rather than by being a generalist itself. Therefore, the species may affect not only the local generalist species but combination of degree and closeness can potentially be good also the more specialized ones that connect to it via interac- indicators of species with high risk of introduction success in tion rewiring (Aizen et al., 2008). The consequences of this terms of invasion. On the other hand, the poor prediction of will depend on the centrality of the introduced species in betweenness and the c- and z-score, which indicate the role a combination with that of the native species. For example species plays as connecting different parts of the network, highly connected alien species will likely promote local spe- suggests that the role of species as connectors may depend cies rewiring, whilst the arrival of a poorly connected species on the local distribution of species into modules. (i.e. a specialist) may have a mild or even neutral effect on Most plant species depend on animal species for pollina- local species interactions. Moreover, a species that remains in tion (Waser & Ollerton, 2006; Ollerton et al., 2011), thereby its home range in which the community has changed due to any characteristic that enhances interactions with pollinators local extinctions and alien species invasion will find itself in would likely be favourable when colonizing a new area. Cen- a novel network of interactions. Given that species roles are tral alien plants may have an advantage in the new range in conserved, rewiring of interactions will be needed for the terms of gene flow if local pollinators show high fidelity. A local species to fit into the novel community (Gilljam et al., greater number of pollinator species constantly visiting dif- 2015). ferent conspecific flowers may promote greater deposition of conspecific pollen grains, therefore increasing pollination CONCLUSIONS (Brosi & Briggs, 2013; Huang et al., 2015). Nevertheless, the benefits of this increased visitation frequency may be partly In summary, there seems to be an intrinsic component of offset by an increase in heterospecific pollen transport (Fang species roles in plant–pollinator networks that is conserved & Huang, 2013) if, instead, the alien plant interacts with a across species native and alien ranges. Our results suggest generalist pollinator that visits different plant species there- that the core network position that a species occupies when fore increasing heterospecific pollen transfer and potentially introduced in a novel community will resemble how general- reducing seed set (Ashman & Arceo-Gomez, 2013). Still, ist or specialist it is in its native community. Our results heterospecific pollen transfer has been shown to be generally provide new insights into the recent literature about interac- low and has no low, or a species-specific effect on plant tions and species role conservatism and have implications reproduction (Bartomeus et al., 2008; Montgomery & regarding the potential links that alien species may be able to Rathcke, 2012; Fang & Huang, 2013; Emer et al., 2015). create or disrupt once introduced into novel communities. Moreover, central pollinator species may have an advantage Further studies incorporating community traits and the phy- over less connected species when arriving in an alien com- logenetic relationship between species with species network munity due to their ability to visit different flower species, roles will advance our understanding of how alien species

848 Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd Native–alien species roles in pollination networks interact with, and potentially drive the formation of, novel Bates, D., Maechler, M., Bolker, B. & Walker, S. (2014) lme4: communities. Linear mixed-effects models using Eigen and S4. R package version 1.1-10. Available at: http://CRAN.R-project.org/ package=lme4 (accessed 19 February 2016). ACKNOWLEDGEMENTS Bluthgen,€ N., Menzel, F., Hovestadt, T., Fiala, B. & Bluthgen,€ We thank L. Young, J. Ladley, S. Kruis, M. Lambert for field- N. (2007) Specialization, constraints, and conflicting inter- work assistance and friendship, R.M. Machado for Fig. 1, S. ests in mutualistic networks. Current Biology, 17, 341–346. Timoteo, P. Maruyama and one anonymous referee for valu- Brosi, B.J. & Briggs, H.M. (2013) Single pollinator species able contributions on the reviewing process and the Univer- losses reduce floral fidelity and plant reproductive function. sity of Canterbury for logistical support on fieldwork. CE Proceedings of the National Academy of Sciences USA, 110, was funded by the Coordination for the Improvement of 13044–13048. Higher Education Personnel (CAPES, Brazil). JMT was Carpintero, S., Reyes-Lopez, J. & De Reyna, L.A. (2005) funded by a Rutherford Discovery Fellowship, administered Impact of Argentine ants (Linepithema humile) on an arbo- by the Royal Society of New Zealand. DM was funded by the real ant community in Donana~ National Park, Spain. Bio- EU in the framework of the Marie-Curie FP7 COFUND Peo- diversity and Conservation, 14, 151–163. ple Programme, through the award of an AgreenSkills/ Carvalheiro, L.G., Biesmeijer, J.C., Benadi, G. et al. (2014) AgreenSkills+ fellowship. 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Additional Supporting Information may be found in the Stouffer, D.B., Sales-Pardo, M., Sirer, M.I. & Bascompte, J. online version of this article: (2012) Evolutionary conservation of species’ roles in food Appendix S1 Outlier detection analyses. webs. Science, 335, 1489–1492. Stouffer, D.B., Cirtwill, A.R. & Bascompte, J. (2014) How Table S1 Description of the networks used for the analyses exotic plants integrate into pollination networks. Journal of of the species’ roles of plants and pollinators in the alien and Ecology, 102, 1442–1450. native range. The Global Invasive Species Database (GISD)Available at: Table S2 List of the target species and the networks in which http://www.issg.org/database/welcome/ (accessed 10 July they were recorded. Network ID follows Fig. 1 and Table S1 2014). in which details of each network are provided. The Non-native Species Secretariat (NNSS)Available at: http:// www.nonnativespecies.org (accessed 10 July 2014). Table S3 Results of the linear mixed-effect models (LMMs) The Plant Pest Information Network (PPIN)Available at: and the linear regression models (LMs) testing whether lati- http://archive.mpi.govt.nz/applications/ppin (accessed 10 tude and trophic level interact with species range to deter- July 2014). mine species’ roles. Thuiller, W., Richardson, D.M., Pysek, P., Midgley, G.F., Table S4 Species roles on pollination networks following Hughes, G.O. & Rouget, M. (2005) Niche-based model- Olesen et al. (2007): Peripheral z ≤ 2.5, c ≤ 0.62; Connector ing as a tool for predicting the risk of alien plant z ≤ 2.5, c > 0.62; Module hub z > 2.5, c ≤ 0.62; Network invasions at a global scale. Global Change Biology, 11, hub z > 2.5, c > 0.62. 2234–2250.

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Table S5 Correlation between normalized degree, closeness, Estadual Paulista (UNESP) in Brazil. The authors are part of betweenness, c- and z-scores. Values correspond to the a collaboration established during her doctorate at the Spearman correlation coefficient q. University of Bristol, UK.

Authors contributions: CE and JMT developed the study BIOSKETCH framework. CE gathered the data, ran the analyses, and wrote the manuscript. IPV provided statistical advice. DM con- Carine Emer is a community ecologist interested on under- tributed with the study design and discussion. JM advised on standing how anthropogenic disturbance affect animal-plant the collection of the field data, and JM and JMT commented interactions. Her research includes both mutualistic and and edited the versions of the manuscript. antagonistic processes in tropical and temperate habitats. Recently she has studied the effects of invasive species, habi- tat loss and fragmentation on ecological networks. She is Editor: Anna Traveset currently a postdoctoral researcher at the Universidade

852 Diversity and Distributions, 22, 841–852, ª 2016 John Wiley & Sons Ltd