The Worldwide Importance of Honey Bees as Pollinators in Natural Habitats (PDF)

The worldwide importance of honey bees rspb.royalsocietypublishing.org as pollinators in natural habitats...

The worldwide importance of honey bees rspb.royalsocietypublishing.org as pollinators in natural habitats Keng-Lou James Hung1,†, Jennifer M. Kingston1, Matthias Albrecht2, David A. Holway1 and Joshua R. Kohn1 Research 1 Section of Ecology, Behavior and Evolution, Division of Biological Sciences, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0116, USA 2 Cite this article: Hung K-LJ, Kingston JM, Agroecology and Environment, Agroscope, Reckenholzstrasse 191, CH-8046, Zürich, Switzerland Albrecht M, Holway DA, Kohn JR. 2018 K-LJH, 0000-0002-1557-3958 The worldwide importance of honey bees as pollinators in natural habitats. Proc. R. Soc. B The western honey bee (Apis mellifera) is the most frequent floral visitor of 285: 20172140. crops worldwide, but quantitative knowledge of its role as a pollinator out- Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 side of managed habitats is largely lacking. Here we use a global dataset of http://dx.doi.org/10.1098/rspb.2017.2140 80 published plant – pollinator interaction networks as well as pollinator effectiveness measures from 34 plant species to assess the importance of A. mellifera in natural habitats. Apis mellifera is the most frequent floral visitor in natural habitats worldwide, averaging 13% of floral visits across all Received: 25 September 2017 networks (range 0–85%), with 5% of plant species recorded as being exclu- Accepted: 4 December 2017 sively visited by A. mellifera. For 33% of the networks and 49% of plant species, however, A. mellifera visitation was never observed, illustrating that many flowering plant taxa and assemblages remain dependent on non-A. mellifera visitors for pollination. Apis mellifera visitation was higher in warmer, less variable climates and on mainland rather than island sites, Subject Category: but did not differ between its native and introduced ranges. With respect Ecology to single-visit pollination effectiveness, A. mellifera did not differ from the average non-A. mellifera floral visitor, though it was generally less effective Subject Areas: than the most effective non-A. mellifera visitor. Our results argue for a ecology deeper understanding of how A. mellifera, and potential future changes in its range and abundance, shape the ecology, evolution, and conservation Keywords: of plants, pollinators, and their interactions in natural habitats. Apis mellifera, floral visitation, meta-analysis, plant – pollinator network, pollination, pollination effectiveness 1. Introduction The western honey bee (Apis mellifera L.) provides highly valued pollination ser- vices for a wide variety of agricultural crops , and ranks as the most frequent Author for correspondence: single species of pollinator for crops worldwide. A long history of domesti- Keng-Lou James Hung cation and intentional transport of A. mellifera by humans has resulted in its e-mail: [email protected] current cosmopolitan distribution that includes all continents except Antarctica and many oceanic islands. Given the advanced state of knowledge concerning this species and its role in agriculture, it seems surprising that the importance of A. mellifera as a pollinator in natural habitats remains poorly understood [3–5]. Clarifying the role of A. mellifera as a pollinator in natural habitats is important for several reasons. First, animal-mediated pollination represents a vital ecosys- tem service [6,7]; an estimated 87.5% of flowering plant species are pollinated by animals. Quantification of the pollination services provided by the cosmo- † politan, super-generalist A. mellifera will thus provide insight into the Present address: Department of Evolution, functioning of many terrestrial ecosystems. Second, non-A. mellifera pollinators Ecology and Organismal Biology, The Ohio are declining as a result of habitat loss, habitat degradation and other factors State University, 318 West 12th Avenue, including pesticides, pathogens, parasites and climate change [10–12]. In cases Columbus, OH 43210, USA. where A. mellifera populations can withstand these perturbations, the degree to which they replace pollination services formerly performed by extirpated pollina- Electronic supplementary material is available tors [13–17] deserves scrutiny. Third, recent increases in the mortality of managed A. mellifera colonies in some regions of the world [11,18] may extend to popu- online at https://dx.doi.org/10.6084/m9. lations of free-living A. mellifera [19–21]. Threats to A. mellifera populations figshare.c.3956575. could thus affect the reproduction and population dynamics of plants in natural & 2018 The Author(s) Published by the Royal Society. All rights reserved.  areas, with potential shifts in the composition of plant encountered networks from different studies that were less than 2 assemblages [22,23], and in turn, the ecosystem services 50 km apart, we excluded those that sampled a smaller number of plant or pollinator taxa, or documented fewer interactions. We rspb.royalsocietypublishing.org (e.g. carbon sequestration, soil retention) that these plants pro- vide. Lastly, where introduced populations of A. mellifera attain chose 50 km as a threshold to avoid over-representing studies that include many networks within a locality (e.g. [32,37]), while high densities [24–26], they may compete with other pollina- keeping separate those networks originating from distinct tors [27–29] or compromise plant reproductive success. localities within the same geographical region, such as networks These phenomena are of broad ecological, evolutionary and documented on different islands from the same archipelago (e.g. conservation importance, but to our knowledge, there cur- ). When studies included multiple years of data collection at rently exists no global quantitative synthesis of the numerical the same sites using the same protocols, we pooled data from all importance of A. mellifera as a pollinator in natural ecosystems study years into a single network. in their native or introduced ranges. All networks retained for analyses met the following criteria. Here, we address questions concerning the importance of The data were collected in natural habitats, here defined as Proc. R. Soc. B 285: 20172140 A. mellifera by exploiting a recent trend in pollination largely unmanaged assemblages of plant species where the research—the documentation of community-level, plant –pol- identities and relative abundances of plant species are not purpo- linator interaction networks (hereafter ‘pollination networks’). sefully manipulated (thus excluding, for example, agricultural, urban and experimental habitats; see the electronic supple- Quantitative pollination network studies document the iden- mentary material, table S1-1). Each network consisted of tity and frequency of each type of pollinator visiting each Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 observations on five or more plant species when pooled across plant species within a locality. Network data are used to the sites making up an individual study. All networks documen- address a variety of questions (e.g. [32–34]), but key for our ted a broad range of pollinators; studies with a narrow goals here, they provide an underused opportunity to gauge taxonomic scope (e.g. social bees, bird pollinators with incidental the importance of A. mellifera in natural habitats, particularly observations of A. mellifera) or those that a priori excluded because the role of A. mellifera has rarely been the focus of A. mellifera were not included. We also excluded networks from these studies [25,26,35]. We compiled a database of 80 quanti- sites that were known to be heavily influenced by A. mellifera tative pollination networks from natural habitats worldwide. colonies stocked for adjacent agricultural pollination. Thus, our To further assess the importance of A. mellifera as a pollinator, estimates of the numerical importance of A. mellifera may be con- we also compiled data on per-visit pollination effectiveness of servative with respect to mosaic landscapes where natural habitats are intermixed with agricultural fields with managed A. mellifera relative to other floral visitors from studies of 34 A. mellifera colonies. We did not a priori exclude networks plant species. from localities outside of the presumed climatic niche of Our meta-analyses address three interrelated lines of A. mellifera , or where A. mellifera was never introduced. In inquiry concerning the ecological importance of A. mellifera all, we obtained 80 networks (see the electronic supplementary in natural habitats: (i) what proportions of floral visits are con- material, table S1-1) from 60 peer-reviewed studies and three tributed by A. mellifera foragers to individual networks graduate theses [37,41,42]. While lacking coverage in some worldwide, and to individual plant species within networks? regions (figure 1), our dataset attains geographical coverage com- (ii) what environmental factors govern the relative contribution parable to other recent studies that examine the importance and of A. mellifera to community-level floral visitation, and do levels conservation of pollinators at a global scale [2,12,43]. of visitation differ between its native and introduced ranges? For each network, we obtained the following data from their and (iii) given that pollination network studies often use visita- associated publications or from study authors when data were not available from publications: latitude, longitude and final tion frequency as a proxy for pollinator importance (e.g. ), year of data collection. When these data were not available and how does the per-visit pollination effectiveness of A. mellifera authors could not be reached, we used the approximate geo- compare to the effectiveness of other floral visitors? graphical centre of the study locality listed in the publication, and the year of publication as the last year of data collection. We defined the native status of A. mellifera based on and 2. Material and methods ; although we caution that the native status of A. mellifera in the British Isles and northern Europe remains unresolved. (a) Database for network synthesis We also extracted the following information from each study, We used two approaches to compile our dataset of pollination when available: the proportion of all floral visits contributed networks. First, we performed a literature search using the ISI by A. mellifera (in two networks this metric was estimated by cal- Web of Science database with the search terms [ pollinat* net- culating the proportion of the total visitation rate, summed work], [ pollinat* web] and [ pollinat* visit* community], across plant species, contributed by A. mellifera; see the electronic examining all studies available as of August 2016. Second, we supplementary material, table S1-1), the proportion of plant downloaded all pollination network data from the Interaction species receiving at least one visit by A. mellifera, and the rank Web Database of the National Center for Ecological Analysis of A. mellifera with respect to both the proportion of all floral and Synthesis website (http://data.nceas.ucsb.edu/) and the visits contributed and the proportion of plant species visited. Web of Life Ecological Networks Database (http://www.web- Additionally, we used geographical information system (GIS) of-life.es/) available as of December 2014. We collected all analysis to obtain elevation data and bioclimatic variables (, studies and plant– pollinator interaction network datasets that http://www.worldclim.org) for each network based on its documented visitation frequency (i.e. number of individuals global positioning system (GPS) coordinates. We also categorized observed contacting flowers or number of floral contacts per each network as being on an island or a mainland; the latter unit time) between each pair of plant and pollinator taxa. We category includes all continents as well as islands greater than defined a network as the sum of recorded plant– pollinator inter- 200 000 km2, namely Great Britain (United Kingdom), Honshu actions in all sites from a single study that fell within a 50 km (Japan) and Greenland. For studies for which raw data were diameter circle, regardless of the number of sites that constitute not available, we contacted the corresponding authors to request the network. Sites within the same study that are separated by data, or, in cases where data could not be shared, requested sum- more than 50 km were treated as separate networks. When we mary statistics on plant– pollinator interactions. When raw  3 rspb.royalsocietypublishing.org Proc. R. Soc. B 285: 20172140 Apis mellifera all other floral visitors Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 Figure 1. Proportion of all floral visits contributed by the western honey bee (Apis mellifera) in 80 plant – pollinator interaction networks in natural habitats worldwide. Apis mellifera is generally considered a native species in Europe, the Middle East, and Africa; and introduced elsewhere. (Online version in colour.) numeric data were unavailable from the publication or from regression using package gamlss in R (v. 3.3.1 ). One net- authors, we used IMAGEJ to extract data from figures, where pos- work located above the Arctic Circle was excluded from this sible (see the electronic supplementary material, table S1-1). analysis because bioclimatic data were unavailable (hence, n ¼ Owing to the different methodologies and data reported by 79). We note that the exclusion of networks with no A. mellifera each study, not all of the above-mentioned variables were visits did not qualitatively alter our results (see the electronic extracted from all networks. supplementary material, table S2-1). To incorporate bioclimatic variables , we first performed principal components analysis (PCA) to avoid constructing (b) Frequency and patterns of Apis mellifera visitation models with highly collinear terms. We performed one PCA We calculated the global mean and median proportion of all floral for the 11 variables measuring temperature, and a separate visits contributed by A. mellifera, using each network as a data PCA for the eight bioclimatic variables measuring precipitation point (n ¼ 80 networks). Calculations were repeated after exclud- (see the electronic supplementary material, table S3). We then ing networks that documented no A. mellifera visits, in order to reduced bioclimatic variables to the first two principal com- examine the role of A. mellifera specifically in localities where it ponents of the temperature and precipitation variables, which occurs. Additionally, we examined plant species in 41 networks accounted for 86% and 89% of the variance, respectively. We con- in which (i) A. mellifera was present, and (ii) data on the number structed a full model containing the following explanatory of visits contributed by A. mellifera and non-A. mellifera visitors variables, without interactions: latitude, longitude, altitude, were available for each plant species. Across these networks, we land category (mainland versus island) and the first two princi- calculated the mean and median proportion of plant species that pal components of temperature and precipitation variables. We were (i) not visited by A. mellifera, (ii) numerically dominated by used R package glmulti to generate all possible permutations A. mellifera (i.e. A. mellifera contributing 50% of all floral visits), of the full model on which to perform zero-inflated, multiple b and (iii) visited exclusively by A. mellifera. Because plant species regression; and then selected the best-fit model using corrected receiving few visits overall may tend to have extreme values of Akaike’s information criterion (AICc) scores. We also used the proportion of visits by A. mellifera, we restricted the analysis best-fit environmental model to address whether the proportion to 834 plant taxa with 10 visits recorded. Additionally, to aid of visits contributed by A. mellifera, after accounting for environ- in visualizing the distribution of the numerical importance of mental factors, was affected by (i) A. mellifera native status (native A. mellifera across plant species, we also calculated for each net- versus introduced), and (ii) year of data collection. work the proportion of plant species that fell into each of 10 bins with respect to the proportion of visits contributed by A. mellifera (range ¼ 0–1; bin width ¼ 0.1). We then constructed a histogram by calculating the mean and 95% confidence intervals of each (d) Pollination effectiveness We used two approaches to compile data on pollination effective- bin across all 41 networks. ness. First, we performed a literature search using the ISI Web of Science database with the search term [ pollinat*] in combination (c) Environmental correlates of Apis mellifera visitation with one of the following terms: [efficiency], [effectiveness], [‘pollen deposition’], [‘seed set’], [‘fruit set’], or [‘pollination frequency biology of’], examining all studies available as of August 2016. We constructed multiple regression models to identify environ- Second, we examined the literature cited sections of each of the mental factors that best explain variation in the visitation studies found through the first approach for additional studies frequency of A. mellifera among networks. The response variable not captured in the initial literature search. Data points in this in these regression models was the proportion of all floral visits analysis consist of studies of focal plant species that compared in each network contributed by A. mellifera. Owing to the A. mellifera and at least one other pollinator taxon with respect strongly non-normal distribution of the data as well as the pres- to pollen deposition, seed set, or fruit set resulting from single ence of numerous zeroes, we performed zero-inflated, multiple b floral visits. We used seed set data whenever available  (a) (b) 4 60 0.8 proportion of plant species 0.7 rspb.royalsocietypublishing.org 50 0.6 no. networks 40 0.5 30 0.4 0.3 20 0.2 10 0.1 0 0 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Proc. R. Soc. B 285: 20172140 proportion of visits by A. mellifera proportion of visits by A. mellifera Figure 2. The distribution of the proportion of floral visits contributed by the western honey bee (Apis mellifera) (a) across 80 plant – pollinator interaction networks in natural habitats worldwide, and (b) across plant species in 41 networks where A. mellifera was documented and where the numbers of visits to each plant species by A. mellifera and other floral visitors were available. Bars show the mean value of each bin across networks; whiskers show 95% confidence intervals. Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 because it is most directly related to plant reproductive fitness (b) Environmental correlates of Apis mellifera visitation , fruit set when seed counts were unavailable and pollen deposition when measures of seed and fruit set were unavailable. frequency When raw data were unavailable, we used IMAGEJ to extract data The best-fit zero-inflated, multiple beta regression model from figures. In all, we obtained 32 studies reporting single-visit of environmental variables revealed that the proportion of visi- pollination effectiveness data for 34 plant species, spanning 22 tation by A. mellifera in networks increases with the first plant families (see the electronic supplementary material, table principal component of temperature variables, with higher S1-2). Of these, 18 plant species in 15 families were undom- values corresponding to higher overall temperature, higher iso- esticated, and 16 plant species in seven families were grown in thermality, lower annual temperature range and less seasonality agricultural settings. For each plant species considered, we divided the pollination effectiveness of A. mellifera by the mean (table 1; further statistics are reported in the electronic sup- effectiveness of all other visitors studied to obtain the relative plementary material, table S2-2). Apis mellifera visitation was effectiveness of A. mellifera. We also divided A. mellifera effective- also higher in mainland than island networks (table 1), but we ness by that of the most effective non-A. mellifera visitor. We then found no effect of native status on the proportion of visits used one-sample t-tests to examine whether the pollination effec- contributed by A. mellifera (table 1). Nevertheless, it is note- tiveness of A. mellifera differed significantly from that of the worthy that eight of the 10 networks with the highest average, or the most effective, non-A. mellifera floral visitor. A. mellifera visitation came from introduced range localities. In five of these networks [25,26,35,37,52], A. mellifera accounted for more than half of the total visits recorded. Lastly, we found that study year was unrelated to the proportion of A. mellifera 3. Results visits in natural habitats worldwide (table 1). (a) Frequency and patterns of Apis mellifera visitation Apis mellifera was recorded in 88.89% (16 out of 18) of the pol- (c) Pollination effectiveness lination networks from its native range and in 61.29% (38 out A literature survey of single-visit pollinator effectiveness data of 62) of the networks from its introduced range (figure 1; see revealed that A. mellifera does not differ from the average also the electronic supplementary material, table S1-1). non-A. mellifera floral visitor, with the effectiveness of Across all networks, the mean proportion of visits contribu- A. mellifera averaging 90.1% that of other visitors (one- ted by A. mellifera was 12.64% (figure 2a; median ¼ 1.56%); sample t-test, t33 ¼ 1.25, p ¼ 0.22; figure 3a). On the other among the 54 networks in which A. mellifera was recorded, hand, A. mellifera was generally less effective than the most this proportion increased to 18.72% (median ¼ 8.13%). Apis effective non-A. mellifera visitor, with A. mellifera effectiveness mellifera was the most frequent floral visitor in 17 networks averaging 75.6% that of the top non-A. mellifera visitor (one and visited the most plant species in 14 networks. sample t-test, t33 ¼ 3.28, p ¼ 0.0024; figure 3b). The relative Across 41 networks in which A. mellifera was present and effectiveness of A. mellifera did not differ between non- the proportion of visits to each plant species by A. mellifera agricultural (n ¼ 18) and agricultural (n ¼ 16) plant species, was recorded, we found a positively skewed distribution of either when compared with the average non-A. mellifera visi- the proportion of visits contributed by A. mellifera to individ- tor (figure 3a; Welch’s two-sample t-test, t30.75 ¼ 0.44, p ¼ ual plant species (figure 2b). Apis mellifera was the only 0.67) or when compared with the top non-A. mellifera visitor documented visitor to 4.48% of plant taxa (median ¼ 0%, (figure 3b; Welch’s two-sample t-test, t24.46 ¼ 0.96, p ¼ 0.34). range ¼ 0% –66.67%) and contributed the majority (50%) of visits to 17.28% of plant taxa (median ¼ 0%, range ¼ 0%– 100%). However, A. mellifera went unrecorded as a visi- tor to nearly half (49.38%) of plant taxa (median ¼ 47.22%, 4. Discussion range ¼ 0% –100%). The overall patterns we report remain While A. mellifera is acknowledged to be a widely introduced similar when we expand the analysis to include plant species [53,54], super-generalist [55,56] species that occupies a central where fewer than 10 visits were recorded (i.e. those species role in many pollination networks [9,24,57], our study presents, that might be expected to produce extreme values; see the to our knowledge, the first quantitative synthesis demonstrat- electronic supplementary material, figure, S4-1). ing the importance of A. mellifera as a floral visitor in natural  (a) (b) 5 3 p = 0.22 3 p = 0.0024 efficiency (Apis/other pollinators) efficiency (Apis/top non-Apis) rspb.royalsocietypublishing.org 2 2 1 1 0 0 p == 0.67 P 0.67 Pp = 0.34 0.34 Proc. R. Soc. B 285: 20172140 non-crop crop non-crop crop Figure 3. Average single-visit pollination effectiveness of the western honey bee (Apis mellifera) relative to (a) the mean effectiveness of all other floral visitor taxa, and (b) the effectiveness of the most effective non-A. mellifera taxon. p-values at the bottom-centre of each panel reflect two-sample t-test comparisons of A. mellifera relative effectiveness in non-crop (n ¼ 18) versus crop (n ¼ 16) plant species; p-values at the top-left reflect one-sample t-test comparisons of A. mellifera to the mean Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 or most effective non-A. mellifera pollinator after combining data from non-crop and crop plant species. Boxes show central 50% of data and median; whiskers show quartiles + 1.5 interquartile range, or most extreme values of data, whichever is closest to median. Points indicate extreme values. Table 1. The best-fit, zero-inflated, multiple beta regression models relating environmental variables to the proportion of visits contributed by the western honey bee (Apis mellifera) in plant – pollinator interaction networks worldwide (n ¼ 79 networks where bioclimatic variables were available). (Temperature PC1 increases with overall temperature and isothermality, and decreases with temperature seasonality and annual range. Models examining the influence of A. mellifera native status and last year of study on proportion of visits by A. mellifera were constructed by adding these two variables to the best-fit model of environmental variables.) model (DAICc)/variable estimate t value p value best-fit environmental model (BFEM) (DAICc ¼ 0) Cox – Snell R 2 ¼ 0.19 temperature PC1 m ¼ 0.39 4.24 ,0.001 land category (mainland ¼ 1, island ¼ 0) m ¼ 0.81 2.27 0.026 BFEM þ Apis native status (DAICc ¼ 1.39) Cox – Snell R 2 ¼ 0.20 temperature PC1 m ¼ 0.41 4.31 ,0.001 land category (mainland ¼ 1, island ¼ 0) m ¼ 0.74 2.04 0.045 Apis native status (native ¼ 1, introduced ¼ 0) m ¼ 0.31 0.99 0.33 BFEM þ last study year (DAICc ¼ 2.25) Cox – Snell R 2 ¼ 0.19 temperature PC1 m ¼ 0.39 4.75 ,0.001 land category (mainland ¼ 1, island ¼ 0) m ¼ 0.81 2.26 0.026 last study year (years CE) m ¼ 0.0056 0.31 0.76 BFEM þ Apis native status þ last study year (DAICc ¼ 3.75) Cox – Snell R 2 ¼ 0.20 temperature PC1 m ¼ 0.41 4.95 ,0.001 Land category (mainland ¼ 1, island ¼ 0) m ¼ 0.74 2.03 0.046 Apis native status (native ¼ 1, introduced ¼ 0) m ¼ 0.30 0.96 0.34 last study year (years CE) m ¼ 0.0041 0.23 0.82 habitats at a global scale. Despite considerable variance in its see the electronic supplementary material, S5). Given that local abundance (figures 1 and 2a), A. mellifera appears to be Bombus is the only other pollinator genus comparable to A. mel- the most important, single species of pollinator across the natu- lifera with respect to both local importance and global ral systems studied, owing to its wide distribution, generalist distribution [7,9,54], it seems unlikely that any other single pol- foraging behaviour and competence as a pollinator. The linator species contends with A. mellifera with respect to numerical dominance of A. mellifera is further underscored worldwide numerical importance in natural habitats. That by our finding that, in a subset of 68 networks with sufficient said, with appropriate data, it would be instructive to compare taxonomic resolution, the average proportion of floral visits the worldwide importance of A. mellifera with that of other cos- contributed by A. mellifera was more than double that contrib- mopolitan and widely introduced pollinator taxa, such as the uted by all bumblebee species (Apidae: Bombus) combined hover fly (Syrphidae) species Syrphus ribesii (L.) and Eristalis (A. mellifera mean ¼ 13.79%, Bombus mean ¼ 6.26%, p ¼ 0.055; tenax (L.) , or with that of pollinator taxa that numerically  dominate pollination networks in key biomes, such as stingless [19–21], but ongoing research suggests that unmanaged 6 bees (Apidae: Meliponini) in tropical ecosystems [24,59]. A. mellifera populations may be better able to cope with para- rspb.royalsocietypublishing.org We quantify for the first time, to our knowledge, that sites and pathogens compared to managed populations. despite the global distribution and often high local abundance In our pollination networks, the degree to which A. mellifera of A. mellifera, it is a frequent visitor to only a minority of insect- foragers originated from managed versus unmanaged colonies pollinated plant species (figure 2b). Even in networks where probably varies. However, in one network numerically more than half of all visits are contributed by A. mellifera, dominated by A. mellifera , genetic testing indicated that approximately 16% of the plant species, on average, receive the majority of A. mellifera foragers were derived from feral, fewer than 10% of their visits from A. mellifera (see the elec- Africanized colonies. tronic supplementary material, figure S4-2). Although Most network studies equate visitation frequency with individual A. mellifera colonies are known to forage extensively the importance of a particular pollinator, but pollination on only a fraction of the plant species available at any given biologists usually define pollinator importance as the per- Proc. R. Soc. B 285: 20172140 time , the skewed pattern of floral visitation documented visit effectiveness multiplied by visitation frequency. here (figure 2b) is nonetheless surprising given that A. mellifera Our survey of pollinator effectiveness estimates involving has the greatest diet breadth of any pollinator species studied A. mellifera (figure 3) suggests that the average importance [55,56]. This result underscores the importance of maintaining of A. mellifera as a pollinator is satisfactorily estimated by robust, diverse assemblages of non-A. mellifera pollinators to its visitation frequency. However, given that A. mellifera exhi- Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 provide pollination services for the majority of flowering bits poor effectiveness at pollinating certain plant taxa [57,72], plant species in natural habitats. additional studies are needed to demonstrate the importance From a different perspective, A. mellifera often numerically of A. mellifera as a pollinator of any particular plant species. dominated a portion of the plant species in a given network. Repeated visits by abundant pollinators, for example, can While non-A. mellifera pollinators may find such plant taxa damage flowers and reduce reproductive success. On inherently unprofitable in some cases, they may be displaced plant species where A. mellifera attains high visitation rates, by A. mellifera via interference or exploitative competition negative relationships between visitation frequency and in other cases (e.g. ). In instances where A. mellifera numeri- plant reproductive fitness may occur and are worthy of cally dominates plant species belonging to the ‘core’ of a investigation. pollination network (i.e. the subset of locally abundant plant As a numerically abundant, super-generalist pollinator, species that are visited by a variety of pollinator taxa [31,62]), A. mellifera may influence the fitness and behaviour they may exert a strong influence on co-occurring pollinators of competing pollinators, enhance or reduce plant. While this phenomenon has been documented in the reproduction, and facilitate the spread of non-native weeds native range of A. mellifera , it may be especially consequen- and pathogens. Given the ecological importance of tial in its introduced range, where plant species numerically A. mellifera, changes in its distribution and abundance may dominated by A. mellifera presumably coevolved with, and impact the evolutionary trajectory of co-occurring animal-pol- supply food for, native pollinators. Our results thus linated plants and pollinators. Our study quantifies the suggest that A. mellifera may disrupt interactions between current importance of A. mellifera in natural communities, plants and other pollinators in many areas, including localities and also highlights the vital importance of non-A. mellifera pol- where A. mellifera attains only modest abundance (see the linators, whose key role in maintaining ecosystem function electronic supplementary material, S4-3). cannot be replaced by A. mellifera. Our study underscores the Our analyses of how A. mellifera visitation correlates with need for more data on how A. mellifera, and potential changes environmental variables revealed significant associations in its range and population size, shape the ecology, evolution with climatic and geographical predictors, but no effect of and conservation of plants, pollinators and their interactions native status (table 1). Release from pathogens and parasites in natural habitats on local and global scales. can contribute to the success of introduced species , but this mechanism may be less important for A. mellifera given Data accessibility. Project data are made available in the electronic that major pathogens and parasites have spread worldwide supplementary material. with the trafficking of managed colonies [17,18]. Nevertheless, Authors’ contributions. The study was conceived by K.-L.J.H., D.A.H. and the majority of networks with the highest proportion of J.R.K. Data were collected by K.-L.J.H., J.M.K., M.A and J.R.K. Data analysis was conducted by K.-L.J.H. All authors contributed to the A. mellifera visits come from introduced range localities. writing of the manuscript and gave final approval for publication. Researchers have long recognized the potential for introduced Competing interests. We have no competing interests. A. mellifera to impact co-occurring pollinators (e.g. [29,65]) and Funding. Funding to K.-L.J.H. include NSF Doctoral Dissertation plants (e.g. ) at the local scale. Numerical dominance of Improvement grant DEB-1501566; the Mildred E. Mathias Graduate introduced A. mellifera may also lead to homogenization Student Research grant and the Institute for the Study of Ecological of pollinator faunas, and of pollination networks, across large and Evolutionary Climate Impacts Graduate Fellowship from the spatial scales. Accordingly, further studies are needed to clarify University of California Natural Reserve System; the Frontiers of Innovation Scholar Fellowship, an Academic Senate grant, and the why A. mellifera reaches high levels of abundance in some parts McElroy Fellowship from the University of California, San Diego; of its introduced range (e.g. [25,26]) and how its local the Sea and Sage Audubon Society Bloom-Hays Ecological Research abundance modifies its impacts on native plants and pollinators. grant; and the California Native Plants Society Educational grant. Despite recent increases in the mortality of managed Acknowledgements. The authors gratefully acknowledge the following A. mellifera colonies in Europe and North America [68,69], individuals who provided raw data, summaries of data, and helpful our analyses found that study year was unrelated to the discussions on the use of their data: T. Abe, R. Alarcón, J. Albrecht, I. Bartomeus, J. Bascompte, N. Blüthgen, L. Burkle, M. Campos- proportion of A. mellifera visits in natural habitats world- Navarrete, L. Carvalheiro, A. Gotlieb, M. Hagen, S. Hegland, wide (table 1). Agents responsible for increased mortality in C. Kaiser-Bunbury, M. Koski, X. Loy, H. Marrero, C. Morales, managed colonies can affect wild or feral A. mellifera colonies A. Nielsen, O. Norfolk, N. Rafferty, R. Ramos-Jiliberto, D. Robson,  H. Taki, K. Trøjelsgaard, C. Tur, D. Vázquez, M. Vilà and summarized data publicly available. J. Ollerton and R. Junker 7 Y. Yoshihara. We thank all authors who have made their raw or provided insightful comments in peer review. rspb.royalsocietypublishing.org References 1. Calderone NW. 2012 Insect pollinated crops, insect 15. Dick CW. 2001 Genetic rescue of remnant tropical 28. Thomson D. 2004 Competitive interactions between pollinators and US agriculture: trend analysis of trees by an alien pollinator. Proc. R. Soc. Lond. B the invasive European honey bee and native aggregate data for the period 1992 –2009. PLoS 268, 2391–2396. (doi:10.1098/rspb.2001.1781) bumble bees. Ecology 85, 458–470. (doi:10.1890/ ONE 7, e37235. (doi:10.1371/journal.pone.0037235) 16. Hanna C, Foote D, Kremen C. 2013 Invasive species 02-0626) 2. Garibaldi LA et al. 2013 Wild pollinators enhance management restores a plant-pollinator mutualism 29. Roubik DW, Moreno JE, Vergara C, Wittmann D. fruit set of crops regardless of honey bee in Hawaii. J. Appl. Ecol. 50, 147–155. (doi:10.1111/ 1986 Sporadic food competition with the African Proc. R. Soc. B 285: 20172140 abundance. Science 339, 1608 –1611. (doi:10.1126/ 1365-2664.12027) honey bee: projected impact on neotropical social science.1230200) 17. Hermansen TD, Britton DR, Ayre DJ, Minchinton TE. bees. J. Trop. Ecol. 2, 97– 111. (doi:10.1017/ 3. Aebi A, Vaissière BE, vanEngelsdorp D, Delaplane 2014 Identifying the real pollinators? Exotic honey S0266467400000699) KS, Roubik DW, Neumann P. 2012 Back to the bees are the dominant flower visitors and only 30. Gross CL, Mackay D. 1998 Honeybees reduce fitness Downloaded from https://royalsocietypublishing.org/ on 01 December 2024 future: Apis versus non-Apis pollination: a response effective pollinators of Avicennia marina in in the pioneer shrub Melastoma affine to Ollerton et al. Trends Ecol. Evol. 27, 142–143. Australian temperate mangroves. Estuaries Coasts (Melastomataceae). Biol. Conserv. 86, 169 –178. (doi:10.1016/j.tree.2011.11.017) 37, 621– 635. (doi:10.1007/s12237-013-9711-3) (doi:10.1016/S0006-3207(98)00010-X) 4. Ollerton J et al. 2012 Overplaying the role of honey 18. Wilfert L, Long G, Leggett HC, Schmid-Hempel P, 31. Memmott J. 1999 The structure of a plant-pollinator bees as pollinators: a comment on Aebi and Butlin R, Martin SJM, Boots M. 2016 Deformed food web. Ecol. Lett. 2, 276– 280. (doi:10.1046/j. Neumann (2011). Trends Ecol. Evol. 27, 141–142. wing virus is a recent global epidemic in honey 1461-0248.1999.00087.x) (doi:10.1016/j.tree.2011.12.001) bees driven by Varroa mites. Science 351, 594– 32. Albrecht M, Riesen M, Schmid B. 2010 Plant-pollinator 5. Butz Huryn VM. 1997 Ecological impacts of 597. (doi:10.1126/science.aac9976) network assembly along the chronosequence of a introduced honey bees. Q. Rev. Biol. 72, 275–297. 19. Thompson CE, Biesmeijer JC, Allnutt TR, Pietravalle glacier foreland. Oikos 119, 1610–1624. (doi:10. (doi:10.1086/419860) S, Budge GE. 2014 Parasite pressures on feral honey 1111/j.1600-0706.2010.18376.x) 6. Ashman T-L et al. 2004 Pollen limitation of plant bees (Apis mellifera sp.). PLoS ONE 9, e105164. 33. Burkle LA, Knight TM. 2012 Shifts in pollinator reproduction: ecological and evolutionary causes (doi:10.1371/journal.pone.0105164) composition and behavior cause slow interaction and consequences. Ecology 85, 2408 –2421. 20. De la Rúa P, Jaffé R, Dall’Olio R, Muñoz I, Serrano J. accumulation with area in plant –pollinator (doi:10.1890/03-8024) 2009 Biodiversity, conservation and current threats networks. Ecology 93, 2329–2335. (doi:10.1890/ 7. Kearns CA, Inouye DW. 1997 Pollinators, flowering to European honey bees. Apidologie 40, 263–284. 12-0367.1) plants, and conservation biology. Bioscience 47, (doi:10.1051/apido/2009027) 34. Rafferty NE, Ives AR. 2011 Effects of experimental 297–307. (doi:10.2307/1313191) 21. Kraus B, Page REJ. 1995 Effect of Varroa jacobsoni shifts in flowering phenology on plant-pollinator 8. Ollerton J, Winfree R, Tarrant S. 2011 How many (Mesostigmata: Varroidae) on feral Apis mellifera interactions. Ecol. Lett. 14, 69 –74. (doi:10.1111/j. flowering plants are pollinated by animals? Oikos 120, (Hymenoptera: Apidae) in California. Environ. 1461-0248.2010.01557.x) 321–326. (doi:10.1111/j.1600-0706.2010.18644.x) Entomol. 24, 1473–1480. (doi: 10.1093/ee/ 35. Olesen JM, Eskildsen LI, Venkatasamy S. 2002 9. Geslin B et al. 2017 Massively introduced managed 24.6.1473) Invasion of pollination networks on oceanic islands: species and their consequences for plant –pollinator 22. Potts SG et al. 2016 Safeguarding pollinators and importance of invader complexes and endemic interactions. Adv. Ecol. Res. 57, 147– 199. (doi:10. their values to human well-being. Nature 540, super generalists. Divers. Distrib. 8, 181–192. 1016/bs.aecr.2016.10.007) 220 –229. (doi:10.1038/nature20588) (doi:10.1046/j.1472-4642.2002.00148.x) 10. Potts SG, Biesmeijer JC, Kremen C, Neumann P, 23. Biesmeijer JC et al. 2006 Parallel declines in 36. Ballantyne G, Baldock KCR, Willmer PG. 2015 Schweiger O, Kunin WE. 2010 Global pollinator pollinators and insect-pollinated plants in Britain Constructing more informative plant –pollinator declines: trends, impacts and drivers. Trends Ecol. and the Netherlands. Science 313, 351–354. networks: visitation and pollen deposition networks Evol. 25, 345 –353. (doi:10.1016/j.tree.2010.01.007) (doi:10.1126/science.1127863) in a heathland plant community. Proc. R. Soc. B 11. Goulson D, Nicholls E, Botias C, Rotheray EL. 2015 24. Giannini TC, Garibaldi LA, Acosta AL, Silva JS, Maia 282, 20151130. (doi:10.1098/rspb.2015.1130) Bee declines driven by combined stress from KP, Saraiva AM, Guimarães PR, Kleinert AMP. 2015 37. Hung K-LJ. 2017 Effects of habitat fragmentation parasites, pesticides, and lack of flowers. Science Native and non-native supergeneralist bee species and introduced species on the structure and 347, 1255957. (doi:10.1126/science.1255957) have different effects on plant-bee networks. PLoS function of plant-pollinator interactions. PhD 12. Winfree R, Aguilar R, Vázquez DP, LeBuhn G, Aizen ONE 10, e0137198. (doi:10.1371/journal.pone. dissertation, University of California, San Diego, La MA. 2009 A meta-analysis of bees’ responses to 0137198) Jolla, CA, USA. anthropogenic disturbance. Ecology 90, 25. Abe T, Wada K, Kato Y, Makino S, Okochi I. 2011 38. Trøjelsgaard K, Jordano P, Carstensen DW, Olesen 2068–2076. (doi:10.1890/08-1245.1) Alien pollinator promotes invasive mutualism in JM. 2015 Geographical variation in mutualistic 13. Xia J, Sun SG, Guo YH. 2007 Honeybees enhance an insular pollination system. Biol. Invasions 13, networks: similarity, turnover and partner fidelity. reproduction without affecting the outcrossing rate 957 –967. (doi:10.1007/s10530-010-9882-9) Proc. R. Soc. B 282, 20142925. (doi:10.1098/rspb. in endemic Pedicularis densispica (Orobanchaceae). 26. Kato M, Kawakita A. 2004 Plant-pollinator 2014.2925) Plant Biol. (Stuttg) 9, 713 –719. (doi:10.1055/s- interactions in New Caledonia influenced by 39. Magrach A, González-Varo JP, Boiffier M, Vilà M, 2007-965259) introduced honey bees. Am. J. Bot. 91, 1814–1827. Bartomeus I. 2017 Honeybee spillover reshuffles 14. Junker RR, Bleil R, Daehler CC, Blüthgen N. 2010 (doi:10.3732/ajb.91.11.1814) pollinator diets and affects plant reproductive Intra-floral resource partitioning between endemic 27. Thomson DM. 2016 Local bumble bee decline linked success. Nat. Ecol. Evol. 1, 1299– 1307. (doi:10. and invasive flower visitors: consequences for to recovery of honey bees, drought effects on floral 1038/s41559-017-0249-9) pollinator effectiveness. Ecol. Entomol. 35, 760 – resources. Ecol. Lett. 19, 1247–1255. (doi:10.1111/ 40. Ruttner F. 1988 Biogeography and taxonomy of 767. (doi:10.1111/j.1365-2311.2010.01237.x) ele.12659) honey bees. Berlin, Germany: Springer.  41. Ingversen TT. 2006 Plant-pollinator interactions on 53. Ollerton J, Liede S. 1997 Pollination systems in the foraging Prosopis velutina in south-eastern 8 Jamaica and Dominica: the centrality, asymmetry Asclepiadaceae: a survey and preliminary analysis. Arizona. J. Appl. Ecol. 32, 519–527. (doi:10.2307/ rspb.royalsocietypublishing.org and modularity of networks. MSc thesis, University Biol. J. Linn. Soc. Lond. 62, 593–610. (doi:10.1111/ 2404649) of Aarhus, Aarhus, Denmark. j.1095-8312.1997.tb00324.x) 67. McKinney ML, La Sorte FA. 2007 Invasiveness and 42. Kevan PG. 1970 High arctic insect-flower visitor 54. Russo L. 2016 Positive and negative impacts of non- homogenization: synergism of wide dispersal and relations: the inter-relationships of arthropods and native bee species around the world. Insects 7, 69. high local abundance. Glob. Ecol. Biogeogr. 16, flowers at Lake Hazen, Ellesmere Island, Northwest (doi:10.3390/insects7040069) 394–400. (doi:10.1111/j.1466-8238.2007.000296.x) Territories, Canada. PhD dissertation, University of 55. Olesen JM et al. 2010 From Broadstone to 68. vanEngelsdorp D, Hayes J, Underwood RM, Pettis J. Alberta, Edmonton, Alberta, Canada. Zackenberg: space, time and hierarchies in 2008 A survey of honey bee colony losses in the 43. Rader R et al. 2016 Non-bee insects are important ecological networks. Adv. Ecol. Res. 42, 1–69. U.S., fall 2007 to spring 2008. PLoS ONE 3, e4071. contributors to global crop pollination. Proc. Natl (doi:10.1016/B978-0-12-381363-3.00001-0) (doi:10.1371/journal.pone.0004071) Acad. Sci. USA 113, 146–151. (doi:10.1073/pnas. 56. Willmer P. 2011 Pollination and floral ecology. 69. Moritz RFA, de Miranda J, Fries I, Le Conte Y, Proc. R. Soc. B 285: 20172140 1517092112) Princeton, NJ: Princeton University Press. Neumann P, Paxton RJ. 2010 Research strategies to