Specialist Foragers in Forest Bee Communities Are Small, Social Or Emerge Early

Home , Andrena alleghaniensis, Andrena banksi, Andrena carlini, Andrena cressonii, Andrena erigeniae, Andrena erythronii

Received: 5 November 2018 | Accepted: 2 April 2019 DOI: 10.1111/1365-2656.13003

RESEARCH ARTICLE

Specialist foragers in forest bee communities are small, social or emerge early

Colleen Smith1,2 | Lucia Weinman1,2 | Jason Gibbs3 | Rachael Winfree2

1Graduate Program in Ecology & Evolution, Rutgers University, New Abstract Brunswick, New Jersey 1. Individual pollinators that specialize on one plant species within a foraging bout 2 Department of Ecology, Evolution, and transfer more conspecific and less heterospecific pollen, positively affecting plant Natural Resources, Rutgers University, New Brunswick, New Jersey reproduction. However, we know much less about pollinator specialization at the 3Department of Entomology, University of scale of a foraging bout compared to specialization by pollinator species. Manitoba, Winnipeg, Manitoba, Canada 2. In this study, we measured the diversity of pollen carried by individual bees forag- Correspondence ing in forest plant communities in the mid-Atlantic United States. Colleen Smith Email: [email protected] 3. We found that individuals frequently carried low-diversity pollen loads, suggesting that specialization at the scale of the foraging bout is common. Individuals of Funding information Xerces Society for Invertebrate solitary bee species carried higher diversity pollen loads than did individuals of Conservation; Natural Resources social bee species; the latter have been better studied with respect to foraging Conservation Service; Garden Club of America bout specialization, but account for a small minority of the world’s bee species. Bee body size was positively correlated with pollen load diversity, and individuals Handling Editor: Julian Resasco of polylectic (but not oligolectic) species carried increasingly diverse pollen loads as the season progressed, likely reflecting an increase in the diversity of flowers in bloom. Furthermore, the seasonal increase in pollen load diversity was stronger for bees visiting trees and shrubs than for bees visiting herbaceous plants. 4. Overall, our results showed that both plant and pollinator species’ traits as well as community-level patterns of flowering phenology are likely to be important determinants of individual-level interactions in plant–pollinator communities.

KEYWORDS floral constancy, foraging behaviour, individuals, phenology, pollinator

1 | INTRODUCTION between plants (Brosi, 2016). Foraging bout specialization, or the specialization of an individual pollinator within a foraging bout (i.e. Pollinators’ interactions with plants tend to be generalized when a single foraging trip), affects plant reproductive success because viewed at the species level, with most pollinator species collect- individuals that move sequentially between plants of the same spe- ing floral resources from multiple plant families (Waser, Chittka, cies transfer more conspecific pollen and less heterospecific pollen Price, Williams, & Ollerton, 1996). Although such a species-level between flowers (Campbell & Motten, 1985; Morales & Traveset, understanding of plant–pollinator interactions yields important 2008). Here, we use the term foraging bout specialization to refer to insights about communities, for example with respect to their sta- patterns of both random foraging (e.g. when an individual happens bility (Bascompte, Jordano, & Olesen, 2006) and restoration (Kaiser- to specialize, because there is only one rewarding plant species in its Bunbury et al., 2017), it also obscures the biology of individual-level foraging path) and non-random foraging (i.e. floral constancy, when interactions, which can strongly affect patterns of pollen transfer an individual specializes despite there being multiple rewarding

1158 | © 2019 The Authors. Journal of Animal Ecology wileyonlinelibrary.com/journal/jane J Anim Ecol. 2019;88:1158–1167. © 2019 British Ecological Society SMITH eT al. Journal of Animal Ecolog y | 1159 plant species in its foraging path), both of which have similar con- alone. Large species require more overall pollen for their offspring sequences for plants in terms of their effects on pollen transfer. and can fit a larger volume of pollen in their pollen loads (Müller Despite the potential functional importance of pollinator foraging et al., 2006; Ramalho et al., 1994). They will thus likely visit more bout specialization, little is known about its prevalence across a wide individual flowers during a single foraging bout, which would cause diversity of pollinator species. them to also encounter more plant species. Second, individuals of Most of what we know about foraging bout specialization comes generalist bee species (hereafter “polylectic” bees) are able to use from studies of bees in only two of the roughly 440 bee genera: pollen from more plant species than individuals of specialist bee spe- Apis (honeybees) and Bombus (bumblebees). Studies of bees in these cies (hereafter “oligolectic” bees), which are physiologically and be- genera suggest that foraging bout specialization is quite common. haviourally limited to only a few plant taxa for pollen (Praz, Müller, & Foraging honeybees have been found to carry pure pollen loads an Dorn, 2008; Williams, 2003). Thus, we expect individuals of polylec- overwhelming majority (i.e. >90%) of the time, and bumblebees also tic species to carry more diverse pollen loads than individuals of tend to carry pure pollen loads more often than not, though less fre- oligolectic species (Cripps & Rust, 1989; Müller, 1996). Finally, we quently than honeybees (range 49% to 76% of the time; Free, 1963; expect bees that visit herbs to carry more diverse pollen loads than Grant, 1950; Leonhardt & Blüthgen, 2012). However, studies of hon- bees that visit trees or shrubs, because the large floral displays pro- eybees and bumblebees might tell us little about the prevalence of duced by trees and shrubs could induce a foraging bee to stay on one foraging bout specialization in other bee taxa, for two reasons. First, plant longer and save the search costs of foraging elsewhere. This both Apis and Bombus are eusocial, while 90% of bee species are should lead to fewer encounters with other plant species (and also not (Danforth, Cardinal, Praz, Almeida, & Michez, 2013). Second, and an increase in the rate of selfing, a mating cost from the plant's per- more generally, if bee species vary in their foraging behaviour, then spective; Kunin, 1993, Barrett & Harder, 1996, Castilla et al., 2017). studies of just a few bee species might not be very informative for Alternatively, each of these traits may matter very little if most bees understanding foraging bout specialization across many bee species. exhibit floral constancy, a behaviour that increases foraging effi- In the few pollen load studies of bees from other genera, we see ciency by removing the cognitive demands associated with switching that, in some species, as many as 97% of individuals carry pure pollen between plant species (Chittka et al., 1999; Gegear & Laverty, 2005). loads while foraging (in stingless bees; Ramalho, Giannini, Malagodi- Because all bees benefit from increased foraging efficiency, floral Braga, & Imperatriz-Fonseca, 1994), but in other species, only 34% of constancy might be very common, and there might be little variation individuals carry pure pollen loads (in mason bees; Eckhardt, Haider, between individuals for these traits to explain. Dorn, & Müller, 2014). However, because research has focused on Finally, foraging bout specialization by pollinators could vary Apis and Bombus, we know very little about how common foraging over time with seasonal changes in the diversity of plant species in bout specialization is in bees across a wider diversity of genera and bloom. All regions exhibit seasonal changes in the diversity of floral life histories (but see Grant, 1950; Motten, 1986; Pornon, Andalo, resources available to pollinators (Ogilvie & Forrest, 2017). In regions Burrus, & Escaravage, 2017). with shortened growing seasons, floral diversity tends to exhibit uni- The life-history traits of pollinators, and also of the plant spe- modal or bimodal patterns, with diversity increasing as environmen- cies in their environment, could affect how commonly individuals tal conditions become more favourable (e.g. Anderson & Hubricht, exhibit foraging bout specialization. First, generalist solitary bee 1940, Heinrich, 1976, Kochmer & Handel, 1986, Morales, Dodge, & species might be less specialized in their foraging behaviour than Inouye, 2005, Makrodimos, Blionis, Krigas, & Vokou, 2008, Craine, social bee species. Social species may have a tendency to specialize Wolkovich, Towne, & Kembel, 2012). Studies show that individuals while foraging for a number of reasons related to cognitive ability respond to increases in floral diversity by visiting more plant species and resource partitioning (Chittka, Thomson, & Waser, 1999; Jones within a foraging bout (Flanagan, Mitchell, & Karron, 2011; Kunin, & Agrawal, 2017), and two experiments have shown that individuals 1993; Lucas et al., 2018). However, if some bees (e.g. social bees, of social bees species exhibited foraging bout specialization more small bees, oligolectic bees) have a strong tendency to exhibit for- often than individuals of solitary bee species; in both studies, the aging bout specialization, changes in floral diversity over time might social bees were faster to learn to associate floral rewards with a have little effect on foraging bout specialization in these species. plant species’ morphology (Amaya-Márgez & Wells, 2008; Dukas & In this study, we measure foraging bout specialization for for- Real, 1991). However, neither study included more than one social est bee communities native to eastern US temperate deciduous or solitary bee species, and there has yet to be a rigorous test of the forests. These forests, which once covered much of eastern North pattern that social bees are more specialized foragers than solitary America, support diverse native bee communities in which adult ones, where individuals are compared across multiple social and sol- bees of many species are active for two to three months, from the itary bee species foraging in the same environment. start of spring in March through the closing of the forest canopy Next, bee body size, bee dietary breadth and the growth form in May (Harrison, Gibbs, & Winfree, 2018). Forest bees are under- of the available plants could each affect how specialized a forager studied with respect to floral resource use and are largely neglected will be, because they affect the number of rewarding plant species by common pollinator conservation efforts, such as pollinator floral a foraging bee encounters. First, we expect individuals of large bee restorations, which tend to only include summer-blooming plants species to carry more diverse pollen loads, even if this is by chance (Hicks et al., 2016; Wood et al., 2018); thus, there is a great research 1160 | Journal of Animal Ecology SMITH eT al. need for understanding the foraging needs of these species. We also and along forest edges, searching for plants with flowers in bloom. chose this system because it provides a natural gradient in flower- We sampled bees from as many plant species as we could find, 48 ing diversity; only a few species flower in the earliest weeks, but plant species in total (mean = 15.0 ± 5.2 SE plant species per site; diversity steadily increases over the course of the spring (Anderson Table S2). We used an insect net to collect any bee we observed & Hubricht, 1940; Heinrich, 1976; Kochmer & Handel, 1986). We visiting a flower, placing each individual bee into a separate clean measured pollinator foraging patterns in plant–pollinator communi- vial. Because our primary interest was in the polylectic bee spe- ties throughout this period by removing and identifying the pollen cies whose foraging at the individual level has greater potential collected into individual bees’ scopae and corbiculae (pollen-car- to vary, we minimized collecting a highly abundant bee species, rying structures). These pollen loads provide a history of the plant Andrena erigeniae Robertson 1891, which is narrowly oligolectic species a female bee has visited for pollen during a single foraging on a single plant species, Claytonia virginica L. We froze all bees bout, because the bee removes the pollen from her pollen-carrying in coolers in the field and stored them at −30°C in a laboratory structures when she returns to her nest after each foraging bout. freezer until processing. Bees were identified using published revi- Pollen loads thus enable the measurement of pollen foraging bout sions (see Gibbs, Ascher, Rightmyer, & Isaacs, 2017 for references; specialization across many individuals and species. LaBerge, 1986). To better understand the dynamics of pollen foraging across We checked whether floral diversity increased during the course many bee species, we ask the following: (a) What is the distribution of spring at our study sites by examining how the diversity of plant of pollen load diversities across individual bees collected while for- species we collected bees from changed over time. We found a pos- aging? (b) Do species-level traits (bee sociality, bee body size, bee itive relationship, as expected based on other studies in our region dietary breadth or plant growth form) affect the diversity of pollen (Figure S1). carried by individuals? and (c) Is there a seasonal gradient in the diversity of individual pollen loads, and is this mediated by plant or 2.2 | Pollen analysis pollinator species-level traits? In the laboratory, we removed and stained pollen from the pollen- collecting structures (scopae or corbiculae) of all female non-para- 2 | MATERIALS AND METHODS sitic forest bees. Because a female bee removes her pollen load after each foraging trip, pollen loads represent a history of the plant spe- 2.1 | Study design and data collection cies a bee has visited up to the point it was collected during the cur- Temperate deciduous forests support many native bee species, rent foraging bout. Additionally, because female bees actively pack most of which are active as adults only in the spring when the forest pollen into scopae and corbiculae, the pollen load also represents canopy has not closed due to leaf-out, and spring ephemeral herbs the pollen actually chosen by the foraging female for her offspring's and animal-pollinated trees are in bloom (March–May in our study consumption. system). Our study focused on native bees in the genera Andrena, We removed pollen from each bee's scopal structures used two Augochlora, Augochloropsis, Bombus, Colletes, Lasioglossum and Osmia 1-mm3 cubes of fuchsin (Kearns & Inouye, 1993). We dabbed each (hereafter “forest bees”), because these genera are known to include cube over the scopal hairs or corbiculae of a specimen, including species associated with forest habitat (Harrison et al., 2018), and we both legs (for bees with scopae or corbiculae on their legs), covering wished to better understand floral resource use by this understud- as much surface area as possible. We stopped either when the cube ied group. We excluded all male bees and parasitic species because was covered in pollen or there was no pollen left on the specimen. these bees do not collect pollen (Michener, 2000). Fuchsin cubes were then melted onto glass slides using a hot plate. We collected bees at four forested study sites in New Jersey and We identified pollen to the finest taxonomic level possible under Pennsylvania (Table S1). All sites were deciduous forests, located in a light microscope. Pollen identifications were conducted using a the Piedmont ecoregion, with oak–hickory or maple–beech–birch pollen reference library we curated from our study sites. The library overstories and a mix of native and non-native plants in the herba- contained a total of 127 plant species, including both forest and for- ceous and shrub layers. Average land cover at a 1 km radius around est-edge plant species. Pollen reference libraries were compiled by each site was 55.9% (±12.5% SE) forest, 16.0% suburban (±5.0% collecting freshly dehiscent anthers from plants in bloom at a site SE), 14.9% (± 6.7% SE) agricultural, 1.1% (± 0.9% SE) water and 12.2 and staining pollen from these anthers using fuchsin gel. We were (±4.9% SE) wetland matrix habitat. not able to distinguish some closely related plant species by their We visited sites between 23 March 2016 and 20 May 2016. pollen and thus in some cases use genus-, family- or higher-level Sites were visited on separate days by two to three data collectors groupings (Table S3). Lastly, not all pollen in bee pollen loads was at a time. All sampling was conducted between 10:00 and 19:00 in our pollen reference libraries. We used morphospecies classifica- on sunny days when the temperature was high enough for bees to tions for these pollens, but these morphospecies-level pollens con- be active (>14°C), but we otherwise did not standardize sampling stituted only 6.5% of all pollen in pollen loads. Hereafter, we refer between sites. At each site, we walked over an area of approxi- to all pollen groups (of family, genera, species and morphospecies) mately 26,390 m2 (±8,875 m2 SE), both through the understorey as “morphotypes”. SMITH eT al. Journal of Animal Ecolog y | 1161

For each bee, we systematically surveyed about half of all pol- pollen load richness. We also plotted separate histograms for each len grains that had adhered to the surface of the two fuchsin cubes of the nine most common bee species (N ≥ 20) in our data, to exam- (thus, we use a standard amount of sampling effort for each bee). We ine how these distributions vary between bee species (Appendix S1: vertically scanned half of each fuchsin stain at 200x magnification Figure S3). and recorded all pollen morphotypes we observed in each scan. We We used linear mixed-effects models to examine the importance counted the number of scans in which each morphotype occurred to of traits and seasonality to foraging bout specialization, modelling quantify each pollen morphotype's relative incidence in the pollen individual pollen load diversity as a function of species’ traits, day- load. To avoid analysing pollen that might be contamination, we only of-year, and the interactions between traits and day-of-year. We recorded pollen morphotypes that had at least five pollen grains in started with a global model in which the response variable was the a slide. We excluded individual bees from analyses if they carried no richness of pollen carried by an individual bee. The explanatory vari- detectable pollen (n = 25). ables included four species-level traits: sociality (social or solitary), lecty (oligolectic or polylectic), bee body size, and the growth form of the plant the individual was foraging from when collected (woody 2.3 | Classifying species’ traits or herbaceous), as well as the day-of-year of collection and all two- We classified bees and plants by the following species-level traits: way interactions between species’ traits and day-of-year. Though bee sociality, bee species-level dietary specialization (hereafter, three-way interactions might be important for explaining pollen lecty), bee body size and plant growth form (Table S4). To categorize load diversity, we did not include these in our model to avoid model bees by their sociality and lecty, we used a previously compiled traits over-fitting. database of bees in the northeastern United States (Bartomeus et We included site and its interaction with day-of-year as addi- al., 2013). We categorized bees as either solitary or social, and as tional explanatory variables to account for non-independence of either oligolectic (pollen specialists) or polylectic (pollen generalists). individuals from the same site. To account for non-independence We consider oligolectic species to be those that only collect pol- between individuals of the same species, we included species as a len from a single plant family, genus or species. We used the USDA random intercept and slope effect in the model, allowing the rela- Plants database (USDA & NRCS, 2018) to classify each plant species tionship between day-of-year and pollen load diversity to vary by that we collected a bee from by its growth form as either herbaceous species (Gelman & Hill, 2007). or woody. To make model intercepts and interactions interpretable, we We measured bee body size for the majority of species using a standardized and centred continuous explanatory variables (i.e. published independent dataset (Cariveau et al., 2016), though for day-of-year and body size). To account for heteroscedasticity, we seven species not in the independent dataset and for all species loge-transformed pollen load diversity and log10-transformed bee from the genus Bombus, we measured bee body size using specimens body size. We used the r package “lme4” to fit mixed models to data from our own data, using the same methods as Cariveau et al. (2016). (Bates, Mächler, Bolker, & Walker, 2015; R Core Team, 2018).

Queens and workers in the genus Bombus differed markedly in body We used an exploratory method, AICc, to determine the optimal size, so for this genus we measured the body sizes of queens and fixed structure of model. We compared the AICc value of the global workers separately. For between 1 and 10 specimens of each bee model with all possible submodels containing the variable day-of- species, we measured intertegular distance, the distance between year (using the “dredge” function in the r package “MuMIn”; Bartón, the bee's wing bases. Intertegular distance is strongly correlated 2017). We picked the model with the lowest AICc value. with dry body mass, and we used a published equation to convert We checked assumptions of normality and homogeneity of vari- intertegular distance to body mass (Cane, 1987). ance for the global and best-fitting models using diagnostic plots of model residuals. We checked that explanatory variables did not covary by calculating the variance inflation factor for each fixed 2.4 | Calculating pollen load diversity effect in the final model. None exceeded three, suggesting there We measured the diversity of pollen in individual pollen loads using is minimal colinearity between explanatory variables (Zuur, Ieno, richness. Walker, Saveliev, & Smith, 2009). We estimated the best-fitting We also compared different choices of diversity metrics by re- model's goodness-of-fit by calculating the marginal R2, the variance running our analyses using Hill-Shannon diversity (which provides explained by the fixed effects alone, and the conditional R2, the vari- a balanced measure of rare and common species) and Hill-Simpson ance explained by both the fixed and random effects (Bartón, 2017; diversity (which emphasizes common species) in place of richness Johnson, 2014; Nakagawa & Schielzeth, 2013). (Jost, 2006, Appendix S1: Figure S2). To assess the significance of variables in the final model, we used parametric bootstrapping to obtain 95% confidence intervals around model parameter estimates. Using the R command “boot- 2.5 | Analysis methods Mer,” we generated 1,000 bootstrapped samples from the model We examined the distribution of pollen load diversities across all and refit the model to these samples to obtain bootstrapped pa- individual bees in our study (question i) by plotting histograms of rameter estimates (Bates et al., 2015). We then calculated the 1162 | Journal of Animal Ecology SMITH eT al.

2.5 and 97.5 percentile values of the bootstrapped parameter diversity distributions (Figure S3). However, the percentage of individ- estimates. uals carrying pure pollen loads varied between bee species, as did the We concluded that a trait affects individual pollen load diversity average richness of pollen individuals carried (Appendix S1: Table S6). (question ii) if the trait was included in the best-fitting model, and the bootstrapped confidence intervals around its parameter estimate 2. Do species-level traits affect the diversity of pollen carried by in that model did not overlap with zero. Because we centred the individuals? variable day-of-year around its mean, the main effects of all traits that interact with day-of-year are interpretable as the effect of the The best-fitting model of individual pollen load diversity included trait on pollen load diversity on the mean day of sampling, April 25 the main effects of day-of-year, sociality, lecty, body size, plant (Schielzeth, 2010). growth form and site, and the interactions between day-of-year and We concluded that a trait mediated the effect of day-of-year lecty, between day-of-year and plant growth form, and between on pollen load diversity (question iii) if the interaction between a day-of-year and body size (Table S7). It explained 38% of variation trait and day-of-year was included in the best-fitting model and if its in individual pollen load diversity (conditional R2 = 0.383), with bootstrapped confidence intervals around the parameter estimate 24% of the variation explained by the fixed effects alone (marginal 2 in that model did not overlap with zero. If there was a significant R = 0.243). There were three other models within three AICc values interaction between day-of-year and a categorical trait, then we ex- of the best-fitting model (Table S7; Figure S4). amined the confidence intervals around the day-of-year coefficient Individuals of solitary bee species carried significantly higher- for each trait value. diversity pollen loads than individuals of social species (Table 1; To hedge against the possibility that our results could be due to Figure 2). Being solitary instead of social was associated with a 28.7% an arbitrary choice among equally credible models, we also ran the increase in pollen load diversity (when reporting effect sizes, all parametric bootstrapping analysis on all models within three AICc other variables are held at their reference levels or means). Social values of the best-fitting model (Figure S4). bees in the genus Bombus carry very large pollen loads, which might be relatively undersampled. To approximately control for differences between social and solitary bees in pollen load size, we com- 3 | RESULTS pared the pollen load diversities of social and solitary bees within the genus Lasioglossum (N = 90) and found that, directionally, the In total, we removed pollen from 441 individuals of 56 forest bee effect of sociality was the same (Figure S5). species (Table S5). TABLE 1 Parameter estimates of the best-fitting model of pollen load richness (log transformed) and bootstrapped 95% 1. What is the distribution of pollen load diversities across indi- e confidence intervals. Significant parameters are highlighted in vidual bees collected while foraging? bold. The model intercept represents the model prediction when categorical variables are held at the reference level and continuous Across the entire season, 33.4% of individual bees carried pure (i.e. variables are held at their means (reference level = solitary, single morphotype) pollen loads (Figure 1). The average richness of a polylectic bees visiting herbaceous plants at site1). Parameter pollen load was 2.28 (±0.07 SE; median = 2). The distribution of pollen estimates of categorical variables represent the difference in the model prediction between the non-reference and reference levels. load diversities was right-skewed; most individuals carried pollen loads Parameter estimates of continuous variables are interpretable as with one or a few pollen morphotypes (Figure 1). Each of the common the change in log(richness) with each standard deviation of the bee species (N ≥ 20) we examined also had right‐skewed pollen load variable. The variable size is log10-transformed

Parameter Estimate Lower C.I. Upper C.I. 0.5 Intercept 0.765 0.623 0.907 s

0.4 Day‐of‐year 0.121 0.034 0.201 Site2 0.207 0.058 0.368 0.3 Site3 0.033 −0.184 0.272 0.2

tion of individual Site4 −0.041 −0.189 0.104 Growth −0.060 −0.175 0.056 0.1 Propor Lecty −0.157 −0.446 0.123

0.0 Size 0.169 0.096 0.247 0246810 Sociality −0.252 −0.419 −0.066 Pollen load diversity (Richness) Day‐of‐year:Growth 0.150 0.026 0.276 Day‐of‐year:Lecty −0.336 −0.572 −0.096 FIGURE 1 Distribution of individual pollen load diversities, with Day-of-year:Size 0.059 −0.004 0.128 diversity measured using richness SMITH eT al. Journal of Animal Ecolog y | 1163

There was no significant difference in the diversity of pollen col- Sociality Solitary lected by individuals belonging to oligolectic and polylectic species Social (Table 1). The non-significant difference was driven by seven individuals of one oligolectic bee species, Andrena erythronii (results when these seven individuals were removed from the analysis: lecty main 7.5 effect [C.I.] = −0.35 [−0.67, −0.03]). Individuals from this species carried surprisingly diverse pollen loads and only a small percentage of host pollen (Figure 3b; Table S8). The determinations for this bee

ersity species were verified using a published key and reference specimens (LaBerge, 1987). Plant growth form was included in the best-fitting model, but 5.0 was not significantly associated with pollen load diversity (Table 1). The variable site was also included in the best-fitting model as a main effect. Individuals from different sites varied in the diversity of pollen they carried, from an average of 2.1 to 2.6 pollen morpho- Individual pollen load div types (Table 1). These results were robust to the use of different diversity met- 2.5 rics (Appendix S1; Figure S2) and to the choice of model (Figure S4).

3. Is there a seasonal gradient in the diversity of individual pollen loads, and is this mediated by plant or pollinator species-level traits? 0.00.5 1.01.5 2.0 Body mass (mg) (logged) The final model included significant interactions between day-

FIGURE 2 The effects of body size and sociality on the richness of-year and lecty and between day-of-year and plant growth form of pollen collected by individual bees. The solid lines show the (Table 1). An interaction between day-of-year and body size was model predictions, back-transformed from the log scale. For the included in the final model, but it was not significant. The inter- model prediction, all other variables are held at their reference action between day-of-year and sociality was not included in the levels or means final model (Table 1). Day-of-year had a greater effect on the diversity of pollen carried Bee body size was significantly positively associated with pollen by polylectic bees than on the diversity of pollen carried by oligolec- load diversity (Figure 2; Table 1), with the largest bees carrying an tic bees (Table 1; Figure 3). For polylectic bees, the estimated num- estimated 130.6% additional morphotypes of pollen in their pollen ber of pollen morphotypes a bee carried increased by 0.9 from the loads compared to the smallest bees. first day-of-sampling to the last, an increase of 54.2%; for oligolectic

(a) Polylectic (b) Oligolectic Growth Herbaceous plant Woody plant

7.5 Bee Polylectic

ersity Oligolectic FIGURE 3 The effect of day-of-year Andrena erythronii on the richness of pollen collected by individuals of (a) polylectic and (b) oligolectic species. Individuals in 5.0 the species Andrena erythronii, which carried unusually diverse pollen loads for an oligolectic bee, are highlighted in pink. Lines show model predictions, back-transformed from the log scale. Individual pollen load div 2.5 The dashed line is the model prediction for bees visiting herbaceous plants, and the solid line is the model prediction for bees visiting woody plants. For model predictions, all other variables are held at Apr 01 Apr 15 May 01 May 15 Apr 01 Apr 15 May 01 May 15 their reference levels or means Day of year 1164 | Journal of Animal Ecology SMITH eT al. bees, the estimated number of pollen morphotypes decreased by (Byrne & Bates, 2007), and in bees, this explanation is supported 1.5, or 53.6%. by two previous studies, both of which found that a social bee spe- The final model also included a significant interaction between cies was faster to learn to associate a plant species’ reward with its day-of-year and plant growth form (Table 1). Day-of-year had a morphology and as a result was more likely to exhibit foraging bout greater effect on the pollen load diversities of bees visiting trees specialization (Amaya-Márgez & Wells, 2008; Dukas & Real, 1991). and shrubs than on the pollen load diversities of bees visiting her- In our study, we also show that social bees are more likely to exhibit baceous plants (Table 1; Figure 3). For example, bees visiting woody foraging bout specialization than solitary ones, but unlike previous plants carried an estimated 1.9 additional pollen morphotypes from research, we show that this pattern exists across individuals from the first day of sampling to the last, an increase of 163.8%, whereas many social and solitary bee species, 21 social bee species in three the diversity of pollen carried by bees visiting herbaceous plants in- genera and 35 solitary bee species in five genera. creased by only 54.2%. Bee body size also affects foraging bout specialization, with We also examined the bootstrapped confidence intervals around small bees being more specialized foragers than large bees. Across the day-of-year coefficient at each trait level and found that the the tree of life, body size is one of the major explanatory variables slope of the relationship between day-of-year and pollen load di- in ecology (Brown, Gillooly, Allen, Savage, & West, 2004). It affects versity was significantly positive for polylectic bees visiting herba- most aspects of an individual's life history and ecology, including ceous plants (slope [C.I.] = 0.12 [0.03, 0.20]) and woody plants (slope metabolism, home range and resource requirements (Brown et al., [C.I.] = 0.27 [0.17, 0.37]). It was not significantly different from zero 2004; Reiss, 1988), all of which are likely to affect foraging bout spe- for oligolectic bees visiting herbaceous plants (slope [C.I. = −0.21, cialization. A bee that collects more pollen and flies farther distances [−0.45, 0.02]) or woody plants (slope [C.I.] = −0.06 [−0.31, 0.18]). while foraging (Greenleaf, Williams, Winfree, & Kremen, 2007; We got qualitatively similar results when analysing other diversity Ramalho et al., 1994) will probably encounter more plant species, metrics, and when analysing other top-ranked models (ΔAICc < 3), just by chance. Thus, larger bees would be expected to visit more with one exception (Figures S2 and S4). The fourth ranked model plant species during a foraging bout, even without presuming they did not include an interaction between day-of-year and plant growth seek out greater pollen diversity. Studies of monospecific crop fields form, which was significant in the main analysis (Figure S4). It instead have found that large bees are more effective pollinators than small included a significant interaction between day-of-year and body size, bees because they deposit more pollen grains onto plant stigmas with day-of-year having a greater effect on the diversity of pollen car- (Bartomeus, Cariveau, Harrison, & Winfree, 2018; Larsen, Williams, ried by large bees than on the diversity of pollen carried by small bees & Kremen, 2005). However, our result suggests that, in diverse wild (Figure S4). plant communities, large bees could also transfer a greater proportion of heterospecific pollen between flowers, reducing some of their effectiveness as pollinators. 4 | DISCUSSION Foraging bout specialization in polylectic bee species becomes less frequent as spring progresses, most likely due to the wider va- Pollinator foraging bout specialization affects patterns of pollen riety of plants blooming later in the season (Anderson & Hubricht, transfer among plants and thus could affect plant reproduction. 1940; Heinrich, 1976; Kochmer & Handel, 1986). Floral diversity sets However, most of what we know about it comes from studies of bees an upper limit on pollen load diversity, so that, as long as generalized in only two genera, Apis and Bombus. Here, we show that, across 56 foraging is energetically profitable for at least some individuals, it bee species in seven genera, most individuals carry low-diversity probably tends to increase the average diversity of individual pol- pollen loads, but the percentage of individuals carrying completely len loads within a community. Many regions with shortened grow- pure (i.e. single morphotype) pollen loads is much lower than has ing seasons exhibit seasonal patterns in floral diversity similar to the been found in studies of Apis and Bombus. In our study, only 34% of one in our study region, with floral diversity increasing to one or all individuals carried pure pollen loads, compared to >90% in studies two peaks as abiotic conditions become favourable (e.g. Anderson & of Apis and between 49% and 75% in studies of Bombus (Free, 1963; Hubricht, 1940, Heinrich, 1976, Kochmer & Handel, 1986, Morales Grant, 1950; Leonhardt & Blüthgen, 2012). Furthermore, we show et al., 2005, Makrodimos et al., 2008, Craine et al., 2012). As a result, that foraging bout specialization is affected by plant and pollinator seasonal declines in pollinator foraging bout specialization among life-history traits, as well as seasonality. polylectic bees, which in many communities comprise the majority In our data, social bee species, which have been the focus of of bee species (Minckley & Roulston, 2006), are likely to be common. most previous studies, carry less diverse pollen loads than solitary In contrast to polylectic bees, oligolectic bees did not become bee species, which represent the great majority of bee species on more generalized in their foraging behaviour over time. With the ex- Earth (Figure 2; Table 1). A potential explanation is that social bees ception of individuals from one species, they carried mostly or only have a greater capacity for learning than solitary ones and thus learn pollen from their host plants, even in late spring when floral diversity more quickly which plant species in their environment is a profitable was high (Figure 3b). Surprisingly, oligolectic bees were not different one to specialize on (Jones & Agrawal, 2017). There is evidence in from polylectic bees in the average diversity of pollen they carried other animal taxa that sociality and learning capacity are correlated (Table 1), but this was primarily due to seven individuals from one SMITH eT al. Journal of Animal Ecolog y | 1165 ostensibly oligolectic species, Andrena erythronii, which carried un- Second, the bees we collected were at all stages of their foraging usually diverse pollen loads. This species has previously been found bouts, and bees at the start of their bout would have visited a smaller to collect non-host pollen when its host plant is not in bloom, so it number of plants. Though it is possible to obtain pollen loads from is likely this species is more flexible in its pollen use than suggested bees that have completed entire foraging trips, by removing pollen as by a typical definition of oligolecty (Michener & Rettenmeyer, 1956). bees return to their nests, it is not feasible to do this for a wide array It is also possible we would have observed a stronger effect of lecty of bee species. These sampling limitations, despite potentially biasing had we collected a common oligolectic bee in our system, A. erige- our absolute estimates of foraging bout specialization, apply similarly niae, in proportion to its abundance. across bees and therefore should not strongly bias our conclusions Plant growth form also affected seasonal changes in pollinator regarding the effects of species’ traits and community-level patterns foraging bout specialization, with visitors to woody plants being of flowering phenology on foraging bout specialization. more strongly affected by day-of-year than visitors to herbaceous In conclusion, we show that specialization at the scale of a plants. We expected the opposite, that the large floral displays pro- foraging bout is common across a wide diversity of bee species, duced by trees and shrubs would cause pollinators to specialize, even but not all bee species are equally likely to exhibit foraging bout in late spring when floral diversity is high. Though polylectic bees specialization at all times. Bee species that are solitary, large or were more specialized foragers on woody plants than on herbaceous polylectic are less likely to exhibit foraging bout specialization ones in early spring, as the spring progressed bee foraging behaviour than species that are social, small or oligolectic, either throughout on woody and herbaceous plants became similar (Figure 3a). A possi- an entire growing season, or when floral diversity peaks. A next ble explanation is that in early spring, bees are more likely to special- step for future research is to investigate how changes in pollinator ize on trees, because large floral displays are particularly attractive foraging bout specialization over time and among species affect when flowers in the landscape are otherwise sparse. In late spring, plant fitness. when flowers are more abundant, herbs and trees may be more similarly attractive, and foragers may be less likely to specialize on trees. ACKNOWLEDGEMENTS Our result has implications for plant fitness and timing of reproduction because plants blooming later in spring were more likely to be We thank two anonymous reviewers for providing detailed visited by bees that also visited other plant species during the same comments that improved the manuscript. We also thank mem- foraging bout. This could indicate a potential reproductive cost to bers of the Winfree laboratory for helpful comments; Cameron delaying bloom, via reduced pollination quality (Morales & Traveset, Kanterman and Michael Botros for field and laboratory assistance; 2008). Other studies have shown that the presence of co-flowering and the Xerces Society for Invertebrate Conservation, the Natural plant species can reduce plant fitness by decreasing pollinator for- Resources Conservation Service, and the Garden Club of America aging bout specialization (Campbell & Motten, 1985; Flanagan et al., for providing funding. 2011; Flanagan, Mitchell, Knutowski, & Karron, 2009), and studies show that plants in more diverse regions experience more pollen AUTHORS’ CONTRIBUTIONS limitation than plants in less diverse regions (Alonso, Vamosi, Knight, Steets, & Ashman, 2010; Vamosi et al., 2006). Our result emphasizes C.S. and R.W. conceived the idea for the study. C.S. and L.W. col- that temporal differences in floral diversity could also be important. lected data. J.G. identified bee specimens. All authors contributed to Furthermore, temporal changes in floral diversity have the poten- the writing of the manuscript. tial to act as agents of selection on flowering time, because plants can avoid periods of high floral diversity by blooming earlier or later. DATA ACCESSIBILITY Future research should investigate to what extent seasonal changes in pollinator foraging bout specialization affect plant fitness and tim- Data are available from the Dryad Digital Repository: https ://doi. ing of reproduction. org/10.5061/dryad.2bm34c2 (Smith, Weinman, Gibbs, & Winfree, Our methods of estimating foraging bout specialization imposed 2019). two limitations on our study. First, we were not able to identify all pollen to species, and it is possible, for example, that some mono- ORCID typic pollen loads actually contained multiple pollen species within the same family or genus. Low taxonomic resolution is a well-known Colleen Smith https://orcid.org/0000-0003-0702-6927 limitation of pollen load data, and most pollen studies combine at least some pollen species by genus or family (e.g. Lopezaraiza-Mikel, Hayes, Whalley, & Memmott, 2007, Tur, Vigalondo, Trøjelsgaard, REFERENCES Olesen, & Traveset, 2014, Keller et al., 2015, Wood et al., 2018). In our Alonso, C., Vamosi, J. C., Knight, T. M., Steets, J. A., & Ashman, T. L. data, 67% of all pollen in pollen loads was only resolved to the mor- (2010). Is reproduction of endemic plant species particularly pollen pho-group (not the species) level (Table S3), though our pollen mor- limited in biodiversity hotspots? Oikos, 119(7), 1192–1200. https :// pho-groups contained few species (mean = 3.8 ± 0.58 SE, median = 3). doi.org/10.1111/j.1600-0706.2009.18026.x 1166 | Journal of Animal Ecology SMITH eT al.

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Scientific Reports, 7(1), 1–11. https ://doi.org/10.1038/s41598-017-16785-5 1 Appendix S1: Supplementary methods, results, tables and figures

3 Supplementary methods and results

4 Pollen load diversity measurements using Hill numbers

5 We used a Hill numbers approach to measuring diversity because this is theoretically

6 preferable to other diversity metrics and provides a way to explicitly indicate the emphasis given

7 to rare versus common species (Jost, 2006). Hill diversities are based on one general equation, of

8 which species richness and forms of the traditional Shannon and Simpson indices are special

9 cases (Jost, 2006). Specifically, Hill-Shannon is the traditional Shannon index exponentiated,

10 and Hill-Simpson is the inverse of the traditional Simpson index. All Hill diversities are in the

11 same units, called the effective number of species, which is the number of species that would be

12 present in a perfectly even community (i.e., one in which each species was represented by the

13 same number of individuals) with the same diversity metric value as the one being studied.

14 We calculated pollen load diversity with Hill numbers using incidence data (that is, the

15 frequencies with which pollen morphotypes occur across multiple microscope scans of a slide).

16 For the ith pollen morphotype in a pollen load, !! is the proportion of scans containing that

!! 17 morphotype, and !! = ! , the relative incidence of the pollen morphotype in the pollen load. ! !!

18 Hill numbers based off incidence data are described by the following equation (Chao et al.,

19 2014):

! ! !!! ! p! for q ≥ 0 q ≠ 1 ! !!! ! = !

exp − p! ln p! for q = 1 !!!

1 20 where S = the number of pollen morphotypes in the individual pollen load and q = the diversity

21 order, which is used to indicate the Hill number’s sensitivity to rare or common species. When q

! ! 22 = 0, ! is species richness, which is sensitive to rare species; when q =1, ! is Hill-Shannon

! 23 diversity, which provides a balanced measure of rare and common species; and when q=2, ! is

24 Hill-Simpson diversity, which is more sensitive to common species.

25 We use a diversity order of q = 0 (i.e., species richness) for our main analysis. To ensure

26 our results were robust to our choice of diversity metric, we also reran our analyses using

27 diversity orders of q = 1 (i.e., Hill-Shannon diversity) and q = 2 (i.e., Hill-Simpson diversity).

28 Our results were qualitatively the same between the three different diversity orders (Fig.

29 S2). In the analyses of all three diversity orders, there were significant main effects of site, day-

30 of-year, sociality and body size, and significant interactions between day-of-year and lecty and

31 between day-of-year and plant growth form (Fig. S2).

33 Comparing the distributions of individual pollen load diversities across bee species

34 We examined the distributions of individual pollen load diversities for nine common bee

35 species in our data (N ≥ 20). All species we examined had right skewed pollen load diversity

36 distributions, with most individuals carrying low diversity pollen loads (Fig. S3). However, the

37 percentage of individuals carrying pure pollen loads varied widely among species, ranging from

38 85.2% of Andrena zizeae to only 4.0% of A. nasonii (Table S6). The median richness of

39 individual pollen loads ranged from one (in A. zizeae, C. inaequalis, and L. subvirdatum) to three

40 (in B. bimaculatus; Table S6).

2 43 References

44 Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K., & Ellison, A. M.

45 (2014). Rarefaction and extrapolation with Hill numbers: a framework for sampling and

46 estimation in species diversity studies. Ecological Monographs, 84(1), 45–67.

47 doi:10.1890/13-0133.1

48 Jost, L. (2006). Entropy and diversity. Oikos, 113, 363–375. doi:10.1111/j.2006.0030-

49 1299.14714.x

3 51 Supplementary tables 52 53 Table S1. Locations of study sites. 54 Site Name Location Latitude Longitude Hutcheson Memorial Forest USA, NJ, Somerset County 40.5006 -74.5639 Institute Woods USA, NJ, Mercer County 40.3240 -74.6631 Sourland Mountain Preserve USA, NJ, Somerset County 40.4731 -74.6956 Bowman's Hill USA, PA, Bucks County 40.3285 -74.9432 55 56

4 57 Table S2. Plant species and the number of bees collected off of each.

Plant species Bees collected Acer negundo 12 Acer platanoides 1 Acer rubrum 38 Anemone canadensis 3 Aquilegia canadensis 5 Aronia arbutifolia 2 Barbarea vulgaris 54 Cardamine impatiens 3 Cerastium nutans 1 Cerastium spp. 1 Cercis canadensis 4 Chrysogonum virginianum 2 Cornus alternifolia 8 Cornus florida 3 Dicentra cucullaria 8 Dodecatheon meadia 2 Eleagnus umbellata 6 Erythronium americanum 5 Euphorbia esula 9 Geranium maculatum 11 Glechoma hederacea 10 Hepatica nobilis_var._obtusa 1 Hydrophyllum virginianum 11 Lamium purpureum 2 Lonicera morrowii 4 Malus pumila 7 Malus spp. 19 Mertensia virginica 38 Packera aurea 8 Physocarpus opulifolius 3 Polemonium reptans 2 Prunus americana 7 Prunus avium 45 Pyrus calleryana 9 Ranunculus bulbosus 11 Ranunculus ficaria 8 Rhododendron calendulaceum 1 Rhododendron periclymenoides 2 Rhododendron prinophyllum 2 Rubus pensilvanicus 2

5 Stylophorum diphyllum 6 Taraxacum officinale 29 Tradescantia virginiana 2 Trifolium repens 2 Viburnum opulus 1 Viola spp. 2 Zizia aurea 30 58

6 60 Table S3. Pollen morphotypes (n=46) found on the bees in our study. Thirty pollen morphotypes

61 were resolved to the species level. The rest are grouped by clade, family or genus. For each

62 pollen morphotype, we list the taxonomic level of the grouping and the mean relative incidence

63 of the morphotype across all pollen loads. The five most common pollen morphotypes were Acer

64 (17.9%), Rosaceae (16.4%), Brassicaceae (12.0%), Mertensia virginica (10.5%) and Zizea aurea

65 (6.7%).

Pollen group Taxonomic level of grouping Mean (%) SE (%) Alliaria petiolata / Euphorbia esula Clade 0.99 0.27 Euonymus alata / Viburnum prunifolium Clade 0.59 0.19 Anemone / Aquilegia Family 1.64 0.54 Asteraceae Family 1.60 0.49 Betulaceae Family 0.32 0.24 Brassicaceae Family 12.04 1.25 Duchesnea indica/ Fragaria virginiana Family 0.46 0.19 Lauraceae Family 0.53 0.25 Ranunculaceae Family 3.02 0.68 Rosaceae Family 16.42 1.38 Acer Genus 17.92 1.52 Carex Genus 0.07 0.07 Cerastium Genus 0.26 0.22 Lonicera Genus 0.61 0.28 Magnolia Genus 0.07 0.05 Rhododendron Genus 1.20 0.48 Viola Genus 0.27 0.19 Ajuga reptans Species 0.17 0.12 Cercis canadensis Species 1.49 0.45 Claytonia virginica Species 0.72 0.29 Cornus alternifolia Species 1.60 0.54 Cornus florida Species 0.92 0.25 Dicentra cucullaria Species 0.55 0.22 Dodecatheon meadia Species 0.50 0.30 Duchesnea indica Species 0.08 0.09 Eleagnus umbellata Species 0.61 0.25 Erythronium americanum Species 0.50 0.25 Geranium maculatum Species 0.25 0.22 Glechoma hederacea Species 0.35 0.17

7 Hydrophyllum virginianum Species 1.33 0.44 Lamiaceae Species 0.01 0.01 Lamium purpureum Species 0.09 0.07 Liriodendron tulipifera Species 1.11 0.31 Mertensia virginica Species 10.49 1.33 Physocarpus opulifolius Species 0.08 0.08 Polemonium reptans Species 0.40 0.24 Rubus pensilvanicus Species 0.06 0.06 Sassafras albidum Species 0.04 0.03 Saxifraga pensylvanica Species 0.02 0.02 Saxifraga virginensis Species 0.11 0.11 Stylophorum diphyllum Species 0.78 0.28 Taraxacum officinale Species 5.41 0.89 Tradescantia virginiana Species 0.48 0.20 Trifolium repens Species 0.30 0.15 Viburnum opulus Species 0.06 0.07 Zizia aurea Species 6.74 1.16 Various morphospecies NA 6.72 0.75 67 68 69

8 70 Table S4. Species’ traits used in the analysis, the number of individual bees and bee species in

71 each trait category, as well as the number of plant species that individual bees in each trait

72 category were collected from. Two individuals from two facultatively social bee species were

73 categorized as social.

74 75 Individual Trait Values bees Bee species Plant species Sociality Social 104 21 33 Solitary 339 35 42 Lecty Oligolectic 47 7 14 Polylectic 396 49 47 Growth form Herbaceous 266 50 28 Woody 177 30 21 Body size Range: 1.2 to 121.5 mg 443 56 49 76

9 77 Table S5. List of bee species we removed pollen from and the number of individuals of each

78 species collected.

79 Species Authority n Andrena alleghaniensis Viereck, 1907 1 Andrena banksi Malloch, 1917 3 Andrena carlini Cockerell, 1901 26 Andrena cornelli Viereck, 1907 4 Andrena cressonii Robertson, 1891 12 Andrena distans Provancher, 1888 1 Andrena erigeniae Robertson, 1891 3 Andrena erythronii Robertson, 1891 7 Andrena fenningeri Viereck, 1922 6 Andrena forbesii Robertson, 1891 6 Andrena heraclei Robertson, 1897 2 Andrena hippotes Robertson, 1895 3 Andrena imitatrix Cresson, 1872 24 Andrena integra Smith, 1853 2 Andrena mandibularis Robertson, 1892 13 Andrena miserabilis Cresson, 1872 12 Andrena nasonii Robertson, 1895 24 Andrena perplexa Smith, 1853 1 Andrena pruni Robertson, 1891 5 Andrena robertsonii Dalla Torre, 1896 2 Andrena rugosa Cockerell, 1906 14 Andrena vicina Smith, 1853 4 Andrena ziziae Robertson, 1891 27 Augochlora pura (Say, 1837) 16 Augochloropsis metallica (Fabricius, 1793) 4 Bombus bimaculatus Cresson, 1863 24 Bombus griseocollis (De Geer, 1773) 6 Bombus impatiens Cresson, 1863 1 Bombus perplexus Cresson, 1863 5 Colletes inaequalis Say, 1837 24 Lasioglossum abanci (Crawford, 1932) 2 Lasioglossum birkmanni (Crawford, 1906) 2 Lasioglossum cattellae (Ellis, 1913) 1 Lasioglossum coeruleum (Robertson, 1893) 5 Lasioglossum coriaceum (Smith, 1853) 1 Lasioglossum cressonii (Robertson, 1890) 9 Lasioglossum foxii (Robertson, 1895) 19

10 Lasioglossum fuscipenne (Smith, 1853) 1 Lasioglossum gotham Gibbs, 2011 2 Lasioglossum illinoense (Robertson, 1892) 1 Lasioglossum imitatum (Smith, 1853) 6 Lasioglossum obscurum (Robertson, 1892) 1 Lasioglossum pilosum (Smith, 1853) 1 Lasioglossum quebecense (Crawford, 1907) 6 Lasioglossum subviridatum (Cockerell, 1938) 21 Lasioglossum truncatum (Robertson, 1901) 6 Lasioglossum versatum (Robertson, 1902) 5 Lasioglossum viridatum (Lovell, 1905) 1 Lasioglossum weemsi (Mitchell, 1960) 1 Osmia atriventris Cresson, 1864 15 Osmia bucephala Cresson, 1864 1 Osmia collinsiae Robertson, 1905 2 Osmia conjuncta Cresson, 1864 1 Osmia georgica Cresson, 1878 3 Osmia lignaria Say, 1837 1 Osmia pumila Cresson, 1864 47 80 81

11 82 Table S6. The nine most common bee species in our dataset (N ≥ 20), with the number of

83 individuals collected, the percentage of individuals carrying pure (i.e. single morphotype) pollen

84 loads, and the median richness of pollen loads.

Bee species N % pure pollen loads Median richness Osmia pumila 47 17.0 2.0 Andrena ziziae 27 85.2 1.0 Andrena carlini 26 7.7 2.5 Andrena imitatrix 24 45.8 2.0 Andrena nasonii 24 4.2 2.0 Bombus bimaculatus 24 25.0 3.0 Colletes inaequalis 24 58.3 1.0 Lasioglossum subviridatum 21 57.1 1.0 85

12 86 Table S7. Results of model selection: AICc values, ΔAICc values and weights of models within

87 ten AICc values of the best-fitting model. All models included day-of-year as a main fixed effect

88 and bee species as a random intercept and slope effect.

day site growth lecty size sociality day: site day: growth day: lecty day: size day: sociality AICc ΔAICc wi + + + + + + + + + 606.53 0.00 0.251 + + + + + + + + 607.78 1.25 0.134 + + + + + + + + + + 608.69 2.16 0.085 + + + + + + + 609.32 2.79 0.062 + + + + + + + + + 609.93 3.40 0.046 + + + + + + + + 610.44 3.90 0.036 + + + + + + + + 610.47 3.94 0.035 + + + + + + 611.22 4.69 0.024 + + + + + + + 611.43 4.90 0.022 + + + + + + + + + 611.93 5.40 0.017 + + + + + + + + 611.94 5.41 0.017 + + + + + + + 612.25 5.71 0.014 + + + + + + + + 612.28 5.75 0.014 + + + + + + 612.30 5.77 0.014 + + + + + + + 612.40 5.87 0.013 + + + + + + 612.46 5.93 0.013 + + + + + + + + 612.62 6.09 0.012 + + + + + + + + + + 612.63 6.10 0.012 + + + + + + + + 613.05 6.52 0.010 + + + + + + + + + 613.64 7.11 0.007 + + + + + + + + + 613.70 7.17 0.007 + + + + + + + 613.71 7.18 0.007 + + + + + + + + 613.72 7.19 0.007 + + + + + 613.86 7.32 0.006 + + + + + + + 613.91 7.38 0.006 + + + + + + + 613.99 7.45 0.006 + + + + + + 614.13 7.60 0.006 + + + + + + + + 614.20 7.67 0.005 + + + + + + + 614.23 7.70 0.005 + + + + + + + + + 614.38 7.85 0.005 + + + + + + + + + 614.38 7.85 0.005 + + + + + + + + + + + 614.81 8.27 0.004 + + + + + + + 614.83 8.30 0.004 + + + + + + + 614.84 8.31 0.004 + + + + + + + 614.89 8.36 0.004 + + + + + 615.00 8.47 0.004 + + + + + + 615.01 8.48 0.004 + + + + + + 615.31 8.78 0.003 + + + + + + 615.42 8.89 0.003 + + + + + + + + 615.50 8.96 0.003

13 + + + + + 615.55 9.02 0.003 + + + + + + + 615.65 9.12 0.003 + + + + + + + + + + 615.81 9.28 0.002 + + + + + + + + 615.85 9.31 0.002 + + + + + + + + 615.87 9.33 0.002 + + + + + + 615.94 9.41 0.002 + + + + + + 615.96 9.43 0.002 + + + + 616.19 9.65 0.002 + + + + + + + + + 616.32 9.79 0.002 + + + + + + 616.38 9.85 0.002 + + + + + + + + + + 616.42 9.89 0.002 89

14 91 Table S8. Oligolectic bee species collected, their host plants, and the pollen found in their pollen

92 loads. Pollen taxa from a bee species’ host plant is highlighted in gray.

Bee species N Host plant Pollen Mean (%) S.E. Andrena cornelli 4 Rhododendron spp. Rhododendron spp. 100.00 0.00 Andrena distans 1 Geranium maculatum Geranium maculatum 100.00 NA Andrena erigeniae 4 Claytonia virginica Claytonia virginica 75.76 15.30 Ranunculus spp. 24.24 15.30 Andrena erythronii 7 Erythronium spp. Acer spp. 31.19 9.16 Taraxacum officinale 25.78 7.54 Rosaceae 16.68 7.98 Stylophorum diphyllum 10.95 7.11 Erythronium americanum 8.57 7.05 Claytonia virginica 4.63 4.15 Betulaceae 1.05 1.05 Morphospecies1 0.71 0.71 Brassicaceae 0.43 0.43 Andrena integra 2 Cornus (Swida) spp. Cornus alternifolia 95.45 4.55 Zizia aurea 4.55 4.55 Andrena ziziae 27 Zizia spp. Zizia aurea 98.35 0.82 Morphospecies2 1.45 0.81 Rosaceae 0.21 0.21 Osmia georgica 3 Asteraceae Asteraceae 81.79 11.65 Ranunculus 16.76 12.31 Zizia aurea 1.45 1.45 93

15 96 Supplementary Figures

● ● 8 ●

6 ● ●

● ● ● ● ● 4

● ● ● ● Floral diversity (Rarefied richness) diversity Floral

2 ●

●

Apr 01 Apr 15 May 01 May 15 Date 98

99 Figure S1. Increase in floral diversity over time, with floral diversity measured as the rarefied

100 richness of plant species bees were collected from. To estimate floral diversity, we used all of

101 our data (N= 1301 bees) including males, parasitic species, and non-forest bees. We used

102 rarefaction to estimate plant species richness at an equal sample size (n = 26) for each site-date.

103 We excluded 10 site-dates which did not meet a minimum sample size of 25 bees.

16 Hill−Shannon Hill−Simpson Richness

Sociality ● ● ●

Size ● ● ●

Site4 ● ● ●

Site3 ● ● ●

Site2 ● ● ●

Lecty ● ● ● Significant ● No Intercept ● ● ● ● Yes Parameter

Growth ● ● ●

Day−of−year:Size ●

Day−of−year:Lecty ● ● ●

Day−of−year:Growth ● ● ●

Day−of−year ● ● ●

−0.5 0.0 0.5 −0.5 0.0 0.5 −0.5 0.0 0.5 104 Estimate

105 Figure S2. Results of parametric boostrapping analyses when Richness, Hill-Shannon diversity

106 and Hill-Simpson diversity (all loge-transformed) are used to measure pollen load diversity. The

107 points represent parameter estimates and lines represent bootstrapped 95% confidence intervals.

108 Points are in red if the bootstrapped confidence intervals do not overlap with zero.

109

17 Osmia pumila Andrena ziziae Andrena carlini N= 47 N= 27 N= 26 0.8 0.8 0.8 0.6 0.6 0.6 0.4 0.4 0.4 0.2 0.2 0.2 0.0 0.0 0.0 0 2 4 6 8 0 2 4 6 8 0 2 4 6 8 Andrena imitatrix Andrena nasonii Bombus bimaculatus N= 24 N= 24 N= 24 0.8 0.8 0.8 0.6 0.6 0.6 0.4 0.4 0.4 0.2 0.2 0.2 Frequency 0.0 0.0 0.0 0 2 4 6 8 0 2 4 6 8 0 2 4 6 8 Colletes inaequalis Lasioglossum subviridatum N= 24 N= 21 0.8 0.8 0.6 0.6 0.4 0.4 0.2 0.2 0.0 0.0 0 2 4 6 8 0 2 4 6 8 Pollen load diversity (Richness) 110

111 Figure S3. The distributions of individual pollen load diversities of common species (N ≥ 20),

112 with pollen load diversity measured using species richness.

113

114 115

18 Rank 1 Rank 2 Sociality ● ● Size ● ● Site4 ● ● Site3 ● ● Site2 ● ● Lecty ● ● Intercept ● ● Growth ● ● Day−of−year:Social Day−of−year:Size ● Day−of−year:Lecty ● ● Day−of−year:Growth ● ● Day−of−year ● ● Significant Rank 3 Rank 4 ● No ● Sociality ● ● Yes Parameter Size ● ● Site4 ● ● Site3 ● ● Site2 ● ● Lecty ● ● Intercept ● ● Growth ● Day−of−year:Social ● Day−of−year:Size ● ● Day−of−year:Lecty ● ● Day−of−year:Growth ● Day−of−year ● ● −0.5 0.0 0.5 −0.5 0.0 0.5 Estimate 116 117 Figure S4. Results of parametric boostrapping analyses of the top four ranked models (all ΔAICc

118 < 3) explaining pollen load richness (loge-transformed). The points represent parameter estimates

119 and lines represent bootstrapped 95% confidence intervals. Points are in red if the bootstrapped

120 confidence intervals do not overlap with zero. Results were qualitatively similar between the top

121 four ranked models, with one exception. The fourth-ranked model did not include the variable

122 plant growth form, or its interaction with day-of-year; this interaction was significant in the three

123 other top-ranked models. The fourth-ranked model instead included a significant interaction

19 124 between day-of-year and body size, with day-of-year having a greater effect on the diversity of

125 pollen carried by large bees than on the diversity of pollen carried by small bees.

126

127

20 Pollen load diversities of social and solitary Lasioglossum

7 ●

6 ●

5 ●

4 ● 3 Pollen load richness Pollen 2 1

Solitary Social Sociality 128

129 Figure S5. Box plots illustrating the difference in the richness of pollen carried by individuals of

130 solitary (N=27) and social bee (N=55) species in the genus Lasioglossum. To minimize co-

131 linearity between body size and sociality, we excluded the eight smallest individuals of social

132 Lasioglossum, which were outliers in terms of their body size [log10(body size) < 0.40]. The

133 boxes encompass the second and third quartiles of the data and the thick black line is the median.

134 The plot whiskers extend to 1.5 times the interquartile range and circles represent outliers.