Historical changes in northeastern US pollinators related to shared ecological traits Ignasi Bartomeusa,b,1, John S. Ascherc,d, Jason Gibbse, Bryan N. Danforthe, David L. Wagnerf, Shannon M. Hedtkee, and Rachael Winfreea,g aDepartment of Entomology, Rutgers University, New Brunswick, NJ 08901; bDepartment of Ecology, Swedish University of Agricultural Sciences, Uppsala SE-75007, Sweden; cDivision of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024-5192; dDepartment of Biological Sciences, Raffles Museum of Biodiversity Research, National University of Singapore, Singapore 117546; eDepartment of Entomology, Cornell University, Ithaca, NY 14853; fDepartment of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269-3043; and gDepartment of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08901

Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved February 1, 2013 (received for review October 24, 2012) Pollinators such as are essential to the functioning of ter- characterized by particularly intensive land use and may not be restrial ecosystems. However, despite concerns about a global representative of changes in the status of bees in other parts of pollinator crisis, long-term data on the status of bee are the world. Thus, the existence of a widespread crisis in pollinator limited. We present a long-term study of relative rates of change declines, as often portrayed in the media and elsewhere (4), rests for an entire regional bee fauna in the northeastern United States, on data of limited taxonomic or geographic scope. based on >30,000 museum records representing 438 species. Over Environmental change affects species differentially, creating a 140-y period, aggregate native species richness weakly de- “losers” that decline with increased human activity, but also creased, but richness declines were significant only for the genus “winners” that thrive in human-altered environments (14). Al- Bombus. Of 187 native species analyzed individually, only three though there are likely winners and losers among bees, the declined steeply, all of these in the genus Bombus. However, there identity of these species is largely unknown (6). In general, certain were large shifts in community composition, as indicated by 56% life-history traits are predicted to make species more vulnerable of species showing significant changes in relative abundance over (15), such as having a small niche breadth (e.g., a specialized diet; time. Traits associated with a declining relative abundance include 16). However, predictions for some other traits such as body size small dietary and phenological breadth and large body size. In have resulted in contrasting predictions (17, 18). In bees, addi- addition, species with lower latitudinal range boundaries are in- tional traits such as nest site location and brood parasitism or creasing in relative abundance, a finding that may represent a re- sociality also determine a species’ response to environmental sponse to climate change. We show that despite marked increases change (19–21). in human population density and large changes in anthropogenic Here we present a long-term study of relative rates of change land use, aggregate native species richness declines were modest for all 47 northeastern North American bee genera, comprising fi outside of the genus Bombus. At the same time, we nd that 438 species. To achieve a long-term (140-y) dataset, we data- certain ecological traits are associated with declines in relative based, identified, and filtered >30,000 bee specimens from major abundance. These results should help target conservation efforts collections of leading northeastern North American museums. focused on maintaining native bee abundance and diversity and therefore the important ecosystems services that they provide. Results and Discussion Changes in Species Richness. We first binned the 30,138 specimens bee declines | global change | pollination into 10 time periods, each containing a similar number of in- dependent records. For the non-Bombus species, we found that ollination is an essential ecosystem function because 87% of the number of rarefied bee species per time period has declined Pthe world’sangiospermspeciesarepollinatedbyanimals by 15%, but the trend is not significant (permutation test P = (1), including most of the leading global food crops (2). Bees 0.07; Fig. 1A and Fig. S1A). Modest richness declines are in (: Apoidea: Anthophila) are regarded as the most accordance with the few field data available (22, 23). For important pollinators, both for their efficiency and their ubiquity Bombus, species richness declined by 30% over the 140-y period (3). However, despite concerns about pollinator declines and (permutation test P = 0.01; Fig. 1B and Fig. S1B). Our result a global pollinator crisis (4), long-term data on the status of bee confirms previous studies documenting North American declines populations are scarce (5). Thus, a recent US National Academy in Bombus species richness (7–9). Last, we identified 20 exotic of Sciences report concluded that “for most pollinator species, species (i.e., not native to the United States) in our study area the paucity of long-term data and the incomplete knowledge of (Table S1) and found that the number of exotic species collected fi even basic and ecology make de nitive assessment of increased by a factor of 9 over time (permutation test P = 0.01; fi status exceedingly dif cult” (6). Fig. 1C). Heretofore, most studies reporting bee population declines A limitation of our study, and of previous published studies of have been focused on the bumble bee genus, Bombus. Some long-term trends in pollinators (13), is that sampling effort is Bombus species are declining sharply in North America (7–9) and elsewhere (10, 11), although others remain numerous (7) or are expanding their ranges (10). Furthermore, Bombus may not Author contributions: I.B., J.S.A., and R.W. designed research; I.B., J.S.A., J.G., and D.L.W. be representative of the world’s 442 other bee genera because performed research; B.N.D. and S.M.H. contributed new reagents/analytic tools; I.B. ana- they may have been impacted by recent pathogen introductions lyzed data; and I.B. and R.W. wrote the paper. from managed Bombus colonies (7). Much less is known about The authors declare no conflict of interest. the status of other genera, which account for >95% of the This article is a PNAS Direct Submission. ∼20,000 described species of bees worldwide (12). The only long- Data deposition: The data reported in this paper have been deposited in the DRYAD term analysis to date that included species other than Bombus repository, http://dx.doi.org/10.5061/dryad.0nj49. showed significant declines in estimated species richness in the 1To whom correspondence should be addressed. E-mail: [email protected]. United Kingdom and the Netherlands when comparing pre- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. versus post-1980 records (13). However, both study areas are 1073/pnas.1218503110/-/DCSupplemental.

4656–4660 | PNAS | March 19, 2013 | vol. 110 | no. 12 www.pnas.org/cgi/doi/10.1073/pnas.1218503110 A 240 species 220

Bombus 200 180 Bee photo sayi Number of non- 1981-2002 1913-1931 1872-1913 1931-1960 1965-1972 1972-1981 2002-2006 2006-2008 2008-2011 1960-1965 B 18 species

16

Bombus 14 12 Bee photo

Number of Bombus citrinus 1906-1919 1919-1937 1899-1906 1963-1975 1986-2005 2005-2008 2008-2011 1877-1899 1937-1963 1975-1986

C 12 10 8 6 4 ECOLOGY 2 0 Bee photo Number of exotic species exotic of Number Anthidium manicatum 1872-1914 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 1914-1932 2008-2011 1932-1960 1960-1965

Fig. 1. Trends in species richness over time. Number of bee species (± SE) in a standard number of independent specimen records per time period. Dashed line indicates a nonsignificant trend and solid line a significant trend. (A) All native bee species excluding Bombus (rarefied to 1,000 specimens). (B)Genus Bombus (rarefied to 400 specimens). (C) Exotic bee species (rarefied to 1,000 specimens). unknown, particularly in the earlier time periods. Although the data show steep declines for this species in the southern part of rarefaction techniques we use partially correct for this, rarefied its range, recent records demonstrate persistence, especially in richness may reflect changes in species composition and domi- northern areas within the core of the species’ historic range. nance as well as changes in species richness; thus, our results Many other species with significant declining trends are common should be interpreted as combining these two metrics. For ex- and are still collected regularly, but nevertheless should be ample, one possible interpretation is that some species are be- monitored because such slow declines could be taken as an early coming more common over time whereas other species are warning signal of imperilment. Last, nine of the 87 rare species becoming less so. (defined as having 10 < n < 30 specimens; all of these species were excluded in our species-level analysis because of inadequate Changes in Composition. In a second, species-level analysis, only sample size) have not been recorded from the past 10 years three of 187 species, all in the genus Bombus, exhibited a rapid (these are listed in Table S1) (24). Furthermore, our failure to and recent population collapse [generalized linear model (GLM) detect particular species in the most recent period is conservative using presence-absence as response variable; P < 0.05]. Two of because the greatest collection effort took place during this pe- these species, Bombus affinis and Bombus pensylvanicus, have riod (Fig. 1). recently been identified as being of conservation concern based There are several important caveats to our species- and genus- on data independent of ours (7), whereas Bombus ashtoni, a so- level results, which stem from limitations of our dataset. First, cial parasite of B. affinis and the related B. terricola, was also small sample sizes prevented us from statistically analyzing trends identified as declining in our study. One additional species, for the rarest species, which are potentially of the greatest con- patellata, stood out as being of conservation concern, servation concern. Second, our analyses measure relative changes having shown a gradual, historical (pre-1950) decline, and has in abundance with respect to other species in the collections, not not been collected in the region since 1991 (Table S1). In con- absolute changes. Third, some groups (e.g., ) are par- trast to the paucity of steep declines, there have been large shifts ticularly difficult to identify; the most taxonomically problematic in relative abundance over time, as indicated by the fact that species are noted in Table S1. 29% of the species decreased significantly, whereas 27% had significant increases (GLM using year as the predictor and the Ecological Traits Associated with Species Responses. Investigation of proportion of records per year as the response variable, with the ecological traits that differ between increasing and decreasing response weighted by the total number of specimens collected in species can provide a more mechanistic understanding of how that year; P < 0.05; Table S1). For example, although we did not biodiversity is affected by environmental changes. In our study detect a rapid and drastic decline for Bombus terricola, which has system, during the past 140 y, human population density more been previously identified as of conservation concern (7), we do than doubled, from 140 people/km2 in 1900 to 325 people/km2 in find a significant decline in its relative abundance. Although our 2000, with associated increases in human land use (25). We first

Bartomeus et al. PNAS | March 19, 2013 | vol. 110 | no. 12 | 4657 assessed the phylogenetic signal (λ) of species relative rates of New York State Museum, and the Bohart Museum of Entomology (University change itself, but found that although they do differ across bee of California, Davis). To focus the geographic extent of our study area, we genera, the strength of this signal at the genus level is not strong used records ranging from 38° to 45° N latitude and −85° to −70° W lon- (26; = 0.24, P < 0.001; Fig. 2). The best-fit phylogenetic gen- gitude (Fig. S3). This region has the most extensive historical collections of λ bees in the New World because of its early settlement and large number of eralized least squares model (PGLS) based on the Akaike In- universities. For each specimen, species identifications were made or verified formation Criterion shows that species with a small dietary by an expert taxonomist associated with our project (J.S.A. or J.G.), and full breadth, narrow phenological breadth, and large body size are label data were captured into the Planetary Biodiversity Inventory database more likely to be in decline (dietary breadth estimate = 0.008 ± (33). Once databased, records were filtered, cleaned, and standardized in 0.002, P = 0.001; phenological breadth estimate = 0.00009 ± the following ways. We retained only specimens for which we had data on 0.00004, P = 0.01; body size estimate = −0.003 ± 0.001, P = 0.01; the locality and the year. Because the method used to collect bees in the Fig. 3 A–C). The body size result holds when Bombus, which are field can affect the taxa collected (34), we excluded specimens known to be unusually large and also may be declining for particular reasons collected by methods other than hand netting. To ensure independence of (7), are excluded from the analysis (body size estimate = 0.003 samples, we used only one specimen of a given species from a given col- − fi ± 0.001, P = 0.06). In addition, species with lower northern lection event, de ned by unique combinations of collector, date, and loca- latitude range boundaries are increasing in relative abundance tion. Although this required removing ∼40% of the records from our analysis, it was an important step to minimize bias in our analyses. We re- within our study area (northern latitude estimate = −0.002 ± fi moved taxa for which the species-level taxonomy is still unresolved (e.g., in 0.0004, P < 0.001; Fig. 3D), a nding that may represent a posi- the genus Nomada). We also excluded the honey bee Apis mellifera,because tive response to climate change on the part of these species (27). it is a managed species. For museum collections where complete databasing Mean April temperature has increased by more than 1° during of all species was not possible, we avoided temporal bias in our dataset by the past 40 y in our study region and climate-associated pheno- deciding a priori which genera were most important to include (e.g., which logical advances for bees have been already demonstrated (28); had the smallest sample sizes in our existing dataset), and then fully data- climate change may also be affecting bee population abundances basing these genera across all time periods. We also excluded Bombus and distribution. Brood parasitic species are predicted to be specimens held by Cornell University to ensure that our data were inde- pendent from those used in a previous study of Bombus declines (7). The more vulnerable to decline because they are dependent on par- fi ticular host bees (19, 29; but see ref. 30). However, we found no data used in our nal analysis consisted of 30,138 specimens, collected by at least 1,550 different known collector teams (with 3,708 specimens being differences between parasitic and nonparasitic species in terms of fl collected by unknown collectors), in 11,295 different collection events. their rates of decline. We likewise did not detect any in uence Our final dataset included 438 species from 47 genera (Table S1). The of sociality (31; Fig. S2A) or nest site location (Fig. S2B) on rate of frequency distribution of these is predictably skewed (35), such that only 80 decline. Overall, ecological traits explained a small proportion of species have more than 100 independent records, and 187 species more than 2 the variation (F = 13.61 on 180 DF, P < 0.0001; λ = 0, r = 0.22), 30 independent records. Fifty-four species are represented by a single indicating that a diversity of responses exists among species with specimen; however, because the number of singletons present show no those traits. Last, species that have increased significantly in rela- trend by time period, they should not have a strong influence on measured tive abundance over the 140-y period include some known to tol- changes in species richness over time (Fig. S4A). Species accumulation curves erate human disturbance (32) as well as exotic species (Table S1). indicate that our databasing efforts captured nearly all of the species di- versity present in the study area (36; Fig. S4B; see SI Text, Investigation of Methods Potential Bias for investigation of potential bias in our data). Bee Specimen Data. We obtained our dataset by entering information from We compiled information on six ecological traits for the complete set of pinned bee specimens from the American Museum of Natural History and 187 species for which we ran individual species-level analyses (SI Text, Eco- from collections maintained by the University of Connecticut, Cornell Uni- logical Traits). versity, Rutgers University, Connecticut Agricultural Station, University of New Hampshire, University of Massachusetts, Vermont State Bee Database, Changes in Aggregate Species Richness over Time. To investigate changes in bee communities over time, we first binned the data such that they had a similar number of independent specimen records per bin. We created the bins using quantiles from the overall cumulative distribution function such that each bin represented an equal number of quantiles. Hence, each bin comprises a similar number of records, but different numbers of years (36). This approach allowed us to maximize the sample size of each bin; it also minimized the influence of periods with low collection effort. To assure that the number of bins chosen did not affect our conclusions, we performed a sensitivity analysis on the number of bins used. Results were similar across the range of 3–10 bins (Fig. S1). To estimate species richness changes over time, we first rarefied all bins to a common number of specimens (1,000 independently collected individuals for all non-Bombus species and 400 for Bombus, representing 82% and 79% of the specimens in the smallest bin, respectively), and then calculated the mean ± SE number of species per time period (36). The resampling method allowed us to standardize sampling effort across time periods and gave us SE estimates, thus correcting for the fact that true sampling efforts in museum collections are unknown. This method provided a relative rather than an absolute measure of species’ abundances, because an apparent decline in some species could in fact be due to an increase in abundance of another species. As such, although it is standard in the ecological literature to refer to this measure as “species richness,” it actually measures both evenness and richness. To estimate sta- tistical significance, we used a permutation test to randomly reorder the time periods and then calculated the correlation between time period and species richness across 1,000 such permutations. Bin size was not equal and hence we were unable to evaluate whether the rates of change reported are Fig. 2. Estimates of relative rate of change over the 140-y interval for dif- linear or take some other form. The reported P value is equal to the fraction ferent bee genera. Estimates are derived from logistic regression models. of these permutations that had higher or lower correlations compared with Negative values indicate declining trends. Boxplot width is proportional to the correlation we observed using the chronological time period sequence. the number of species sampled for each genus. Rarefaction analysis was done with the package vegan in R (37).

4658 | www.pnas.org/cgi/doi/10.1073/pnas.1218503110 Bartomeus et al. A B 0.04 0.04

0.02 0.02

0.00 0.00

-0.02 -0.02 Rate of change (estimate) change of Rate Rate of change (estimate) change of Rate

-0.04 -0.04

Oligolectic Polylectic 123456

CDBody size (mm)

0.04 0.04

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-0.02 -0.02 Rate of change (estimate) change of Rate (estimate) change of Rate

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40 60 80 100 120 140 42 44 46 48 50

Phenological breadth (days) Northernmost latitude recorded

Fig. 3. Relationships among species traits, phylogeny, and rates of change in relative abundance over time. The three most speciose genera are colored to demonstrate how traits are often shared among species within a genus: Bombus (blue), (red), and Lasioglossum (green). (A) Dietary breadth (floral specialization); boxplot width is proportional to number of species and individual species values are indicated along each side. (B)Bodysizemeasuredasthe intertegular distance (mm). (C) Phenological breadth (days of adult activity per year). (D) Northern distributional limit (degrees latitude).

Given the different collection, identification, and databasing efforts that relative abundance over time as estimated by the slope of the individual have been focused on Bombus (as indicated by the nonparametric multidi- species models. Both the outcome variable and all traits included in mensional scaling plot; Fig. S5), we analyzed this genus separately. All other the models show a significant phylogenetic signal (λ) when tested alone. genera were analyzed altogether. Exotic species were excluded from anal- Phylogenetic signal was calculated using packages Phytools (40) and Geiger yses, except when explicitly noted. (41) in R (Table S2). The variance-covariance between rate of change in abundance and each trait was then estimated simultaneously with λ and Changes in Relative Abundance. To analyze relative trends in individual species fitted to the generalized least squares models (42). The best model based on over time, we selected all native bee species with more than 30 records (mean AIC is presented. Note that when the full model λ is estimated to be 0 (as the number of specimens per species = 143.2 ±11.7 SE) and investigated how the one we report), the estimate from the PGLS model is not identical to that of probability of finding a given species in the collection changes over time. For astandardlinearmodel. this analysis, we used a general linear model with a binomial distribution and a logit link. This analysis did not use resampling methods. Instead, each Potential Bias Due to Unknown Sampling Effort over Time. All museum data— year was weighted by the total number of specimens collected that year to including ours—are subject to potential biases if collectors change their account for differential sampling effort among years. The logit link trans- methodology over time. We discussed this issue with data providers and the forms the response to probabilities constrained between 0 and 1, and the main contemporary collectors to ensure a proper interpretation of the data. directionality and magnitude of change is given by the model estimate. For For example, our dataset includes records from a diverse array of land use species showing overdispersion, a quasibinomial distribution was used. types across all time periods, but early collectors (19th and early 20th cen- The analysis described is designed to find gradual, long-term declines. tury) may have been more prone to creating synoptic collections in which However, it has low power for detecting recent, steep declines. Thus, we used each species is represented by only one specimen, whereas contemporary a second model for the latter purpose. The second model uses species collectors are more likely to be conducting ecological studies in which their presence/absence information for each year. This model is uninformative for goal is to collect each species in proportion to its abundance. Although there species collected in most years, but can detect abrupt disappearances/extir- is no definitive way to resolve this issue, we were able to explore and pations. Again, Bombus was analyzed separately, using as the outcome minimize potential collecting bias. First, we filtered the data to use only one variable the proportion of each Bombus species with respect to all Bombus specimen of each species per collection event, thus largely removing the collected in a given year. Likewise, exotic bee species were analyzed sepa- “redundant” specimens of common species. Second, the fact that we had rately, using as the outcome the proportion of each exotic species with re- 1,550 collectors and that 88% of these each contributed fewer than 20 spect to all non-Bombus species collected in a given year. All other taxa were specimens makes systematic bias in collector behavior over time less likely. analyzed together. Third, if the bias hypothesized existed, it would bias the results toward finding steeper declines in species richness than in fact occur. This is a bias Ecological Traits Associated with Species Responses. To correct for phyloge- against our main finding of relatively weak and nonsignificant richness netic nonindependence among traits, we inferred a phylogenetic tree declines, at least for taxa other than Bombus. (SI Text, Phylogenetic Tree; Fig. S6). We used this tree to determine whether ecological traits were correlated with relative change of abun- ACKNOWLEDGMENTS. We thank all those who collected the bees used in dance over time using a PGLS approach (38) as implemented in the our analyses and the museums for access to their collections, J. Pickering for R package Caper (39). Our outcome variable was the rate of change in maintaining www.discoverlife.org, R. T. Schuh for access to the Planetary

Bartomeus et al. PNAS | March 19, 2013 | vol. 110 | no. 12 | 4659 Biodiversity Inventory database, and D. Sol and D. Cariveau for comments [09DEP10012AA (to D.L.W.)]. This work was also supported by a Postdoctoral on the manuscript. Data capture was supported by National Science Foun- Fellowship from the Spanish Education Ministry Grant EX2009-1017 (to I.B.) dation Division of Biological Infrastructure Grant 0956388 (to J.S.A.), with and a Rutgers University Pre-Tenure Career Enhancement Award (to R.W., additional support from Robert G. Goelet and a state wildlife grant I.B., and J.S.A.).

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4660 | www.pnas.org/cgi/doi/10.1073/pnas.1218503110 Bartomeus et al. Supporting Information

Bartomeus et al. 10.1073/pnas.1218503110 SI Text Third, we extracted the temporal extent of the flight period, or Investigation of Potential Bias. We investigated the following po- phenological breadth, of each bee species from our database tential sources of collecting bias in our data. First, we confirmed of 30,138 specimens in our study area (38° to 45° N and −85° that geographical coverage was consistent for all time periods (Fig. to −70° W). Despite the importance of phenological breadth for S3) and that there was no correlation between collection year, ecological questions and the large variation among pollinator latitude, or longitude (Pearson correlation year-latitude = −0.12, species in their phenological breadth, quantitative measures for year-longitude = 0.09). Second, we checked for bias in the identity this trait have rarely been reported. Preliminary analysis using of the bee species collected by different collectors. Such a bias species with large sample sizes showed that subsampling 30 in- could potentially result in trends in bee species over time, given dependently collected specimens is sufficient to characterize the that different collectors were active during different time peri- phenological period, with the range of start and end dates for the ods. The great majority of our collector teams, 1,365 of 1,550, estimates based on subsamples being <10 d. Thus, we conducted each contributed fewer than 20 specimens to our analysis; thus, the phenology analysis only for those species represented by at the potential for collector bias from any one collector is very least 30 independent collecting events. To estimate the length of small. Only 55 collector teams contributed more than 100 speci- the flight period, we used the mean 10th and 90th percentiles mens each. To explore the relationship between collector bias and across 100 subsamples of the data. This truncation helped to time, we ordinated bee community composition by collector and remove the influence of sample size and extreme records, thus looked for patterns over time. A nonparametric multidimensional making our measure more comparable across species. scaling plot (NMDS; stress = 0.11; variance explained = 0.97) of Fourth, geographical range limits were estimated using our full- the 55 top collectors as a function of similarity among their col- specimen database for North America (71,482 specimens) using lections showed that most collectors are generalists. Even though the maximum and minimum latitude recorded for each species. a minority of collectors was biased toward collecting particular Our database has poor coverage above 47° N latitude (roughly fi taxa, collector biases did not change signi cantly over time Québec City, Canada). Hence, the maximum latitude may be [Permutational ANOVA (PERMANOVA): F = 1.76; df = 2; P = underestimated for some species. However, if a bias against 0.14; Fig. S5). Despite this general lack of bias, the genus collecting bees at the northern latitudes exists, it does not affect fi Bombus appears to have been speci cally targeted by some the increasing trends reported for species with northern range collectors (Fig. S5; although excluding the three early collectors limits falling within our study area. who only collected Bombus did not qualitatively change our re- sults). For this reason, and also because Bombus has been better Phylogenetic Tree. Sequences for nuclear-coding genes for apoid studied than other genera, we performed all analyses separately and bees were downloaded from GenBank in September for taxa other than Bombus, and for Bombus alone. NMDS and 2011. The coding regions of 20 genes that were represented in PERMANOVA were done with the package vegan in R. three or more bee tribes were aligned using MUSCLE v. 3.8 (1). Minor adjustments were made by hand using MESQUITE Ecological Traits. We compiled information on six ecological traits v. 2.73 (2) to retain amino acid coding and to remove introns not for the complete set of 187 species for which we ran individual identified in some of the GenBank records. Most of the species species-level analyses. First, bee body size was measured as the in our database were not represented in the available GenBank intertegular distance, which is the distance between the two tegulae, small sclerites above the insertion points of the wings. All sequences. Therefore, we built a genus-level tree by selecting one specimens were measured either in the R.W. laboratory or in sequence per gene per genus (either the longest or, if more than the Cornell University Insect Collection. We measured female one species was equally long, at random) to form a concatenated specimens of all species because these are more abundant in matrix of 17,042 bp for genera. The maximum likelihood estimate collections and have the prominent role in maintaining pop- of the tree was generated using RAx-ML v. 7.2.8-alpha (3) under ulations. For Bombus, which varies widely in body size by caste, the GTRCAT model of sequence evolution. Overall, 349 of the intertegular distance of both queens and workers were recorded 443 world bee genera and 27 apoid genera were included in fi and analyzed separately. We only present the model with Bombus the nal tree (Fig. S6). Genera not represented in our database workers measurements because workers are far more abundant, were pruned from the tree using MESQUITE. When more than but using queens did not alter conclusions with regards to the body one species in a genus was represented in our database, the genus size analysis. was replaced with a polytomy with near-zero branch lengths. Second, data on nest substrate (hole, cavity, soil, stem, wood), Because phylogenetic trees for bees are controversial and not sociality (solitary, facultative social, eusocial), parasitism (yes, no) fully resolved, we did sensitivity analysis on the use of a phylo- and diet specialization (oligolectic, polylectic), were gathered genetic tree. Alternative simpler models that used taxonomy from the literature for all species analyzed. Voltinism (univoltine, (genus nested within family as random effects; dietary breadth multivoltine), or the number of generations per year, was recorded estimate = 0.008 ± 0.003, P = 0.006; phenological breadth esti- only when known (n = 62) because there is no information mate = 0.00009 ± 0.00005, P = 0.02; body size estimate = −0.003 ± available for many bee species. However, note that phenological 0.001, P = 0.01; northern latitude estimate = −0.002 ± 0.0004, P < breadth and the number of generations per year was correlated in 0.001) instead of a phylogenetic tree produced very similar results our dataset (r2 = 0.61). (reported in the main text).

1. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high 3. Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses throughput. Nucleic Acids Res 32(5):1792–1797. with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690. 2. Maddison W., Maddison D. (2010) Mesquite: A modular system for evolutionary analysis. Available at http://mesquiteproject.org/mesquite1.0/mesquite/download/MesquiteManual. pdf. Accessed February 20, 2013.

Bartomeus et al. www.pnas.org/cgi/content/short/1218503110 1of4 eod e i.Rcns acltdatrrrfigec iebnt h aenme fidvdas( individuals of number same the to bin time each rarefying after calculated Richness bin. per records S1. Fig. atmu tal. et Bartomeus elnn rn stse yapruaints.( test. permutation a by tested as trend declining (B) (A) Number of Bombus species Number of non-Bombus species estvt nlsso h ubro isue ocluaeseisrcns.Dt eebne oyedapoiaeyeulnmeso specimen of numbers equal approximately yield to binned were Data richness. species calculate to used bins of number the on analysis Sensitivity www.pnas.org/cgi/content/short/1218503110

2003-2007 2007-2011 A )Non- Bombus pce (rare species

fi 2001-2007 dt ,0 pcmn e i)ad( and bin) per specimens 1,000 to ed 2007-2011 2003-2007 2007-2011

1872-1930

1872-1965 ± E,fr3 for SE), B

) 1999-2005 Bombus 2003-2007 – 2005-2009 0bn.Sldln niae signi a indicates line Solid bins. 10 2007-2011 2009-2011 (rare fi dt 0 pcmn e bin). per specimens 400 to ed fi 2of4 2002-2006 cant 2005-2008 2006-2009 2008-2011 2009-2011 Fig. S2. Estimates of relative change over time, analyzed by life history trait. (A) Sociality. (B) Nest site location. Boxplot width is proportional to the number of bee species in each analysis category.

Fig. S3. Map of the study area with the collection events for three time periods of similar sample size (same time periods as used in the sensitivity analysis for n = 3).

Fig. S4. (A) Histogram of the number of singletons present in the entire dataset as a function of the collection year. (B) Species accumulation curve showing richness when randomly selecting number of sampling years (black bars = SE).

Bartomeus et al. www.pnas.org/cgi/content/short/1218503110 3of4 Fig. S5. Nonparametric multidimensional scaling plot (NMDS) of the 55 top collectors as a function of similarity among their collections shows that most collectors are generalists. Bee genera are represented by crosses and collectors by circles. Colors denote the activity period based on the three time periods (same time periods as used in the sensitivity analysis for n = 3 and in Fig. S3). Three of the more speciose genera (Bombus, Andrena,andLasioglossum) are labeled. Nonlabeled peripheral genera are in all cases rare. The ellipse shows the centroid and dispersion of the three time periods.

Fig. S6. Maximum-likelihood estimate of phylogenetic relationships pruned to include only the subset of bee genera represented in our study. Outgroups not shown.

Other Supporting Information Files

Table S1 (DOCX) Table S2 (DOCX)

Bartomeus et al. www.pnas.org/cgi/content/short/1218503110 4of4 Table S1 List of all 438 species in our analysis showing the total number of unique collecting events represented in our database (sample size) and the last year the species was collected. We first show the GLM model output for the 187 native and 10 exotic species, each of which represented by 30 or more unique collection events, for which we modeled changes in relative abundance over time. The response variable was the proportion of specimens in a given year that belonged to the species, with collection year as the predictor. Negative estimates indicate declining trends. We considered centuncularis to be native but its status is unclear. For species for which we did not have sufficient data for modeling changes in relative abundance over time, we list the sample size and the last date of collection only. Plots of the GLM models are accessible in figshare http://dx.doi.org/10.6084/m9.figshare.153881.

Sample Last year Species Estimate SE p-value size collected Declining species Andrena barbilabris -0.0095 0.0024 0.0001 121 2010 Andrena bisalicis * -0.0075 0.0029 0.0108 82 2011 Andrena brevipalpis -0.0074 0.0027 0.0059 99 2011 Andrena canadensis -0.0067 0.0033 0.0441 65 2010 Andrena carlini -0.0047 0.0016 0.0038 620 2011 Andrena crataegi -0.0070 0.0018 0.0001 584 2011 Andrena distans -0.0116 0.0038 0.0025 47 2011 Andrena erigeniae -0.0100 0.0046 0.0287 33 2009 Andrena erythrogaster -0.0239 0.0038 0.0000 54 2004 Andrena geranii -0.0115 0.0044 0.0086 36 2002 Andrena integra -0.0079 0.0032 0.0136 68 2002 Andrena nubecula -0.0068 0.0029 0.0218 177 2010 Andrena placata -0.0088 0.0042 0.0373 88 2010 Andrena regularis -0.0089 0.0037 0.0179 50 2010 Andrena salictaria -0.0100 0.0036 0.0051 55 2005 Andrena sigmundi * -0.0119 0.0036 0.0008 55 2002 Andrena w-scripta * -0.0104 0.0046 0.0239 83 2006 Bombus affinis ** -0.0286 0.0146 0.0499 425 2001 Bombus ashtoni ** -0.0238 0.0126 0.0500 96 1997 Bombus auricomus -0.0087 0.0044 0.0494 31 2011 Bombus borealis -0.0394 0.0066 0.0000 47 2001 Bombus fervidus -0.0051 0.0016 0.0017 472 2011 Bombus pensylvanicus ** -0.0306 0.0144 0.0334 235 2006 Bombus ternarius -0.0142 0.0024 0.0000 255 2011 Bombus terricola -0.0071 0.0023 0.0025 513 2010 Bombus vagans -0.0081 0.0013 0.0000 733 2011 Coelioxys modesta -0.0096 0.0039 0.0147 45 2003 Coelioxys octodentata -0.0085 0.0036 0.0179 55 2011 -0.0127 0.0031 0.0000 73 2011 compactus -0.0068 0.0034 0.0458 137 2010 Colletes validus -0.0151 0.0037 0.0000 52 2009 Epeolus scutellaris -0.0087 0.0035 0.0134 57 2010 rubicundus -0.0076 0.0019 0.0001 199 2011 Lasioglossum cinctipes -0.0108 0.0029 0.0002 83 2011 Lasioglossum heterognathum -0.0061 0.0030 0.0448 77 2011 Lasioglossum imitatum -0.0095 0.0021 0.0000 326 2011 Lasioglossum leucocomum * -0.0091 0.0032 0.0045 68 2011 Lasioglossum perpunctatum -0.0112 0.0039 0.0044 45 2003 Lasioglossum pilosum * -0.0064 0.0024 0.0079 221 2011 Lasioglossum truncatum -0.0228 0.0035 0.0000 64 2002 Macropis ciliata -0.0188 0.0048 0.0001 32 2008 Macropis nuda -0.0136 0.0031 0.0000 71 2009 Macropis patellata -0.0304 0.0054 0.0000 32 1991 Megachile brevis -0.0093 0.0035 0.0081 137 2011 Megachile frigida -0.0116 0.0038 0.0023 48 2011 Megachile inermis -0.0302 0.0053 0.0000 32 2004 -0.0230 0.0038 0.0000 188 2011 Megachile melanophaea -0.0206 0.0072 0.0050 52 2011 Megachile relativa -0.0093 0.0031 0.0023 75 2011 Melissodes druriella -0.0113 0.0026 0.0000 103 2010 Osmia atriventris -0.0079 0.0023 0.0005 136 2011 Osmia lignaria -0.0225 0.0038 0.0000 130 2010 -0.0201 0.0035 0.0000 61 2011 Stable species Agapostemon splendens 0.0073 0.0044 0.0978 49 2011 Andrena algida -0.0013 0.0047 0.7794 35 2006 Andrena alleghaniensis 0.0049 0.0032 0.1281 85 2011 Andrena arabis -0.0032 0.0042 0.4417 154 2003 Andrena asteris -0.0058 0.0034 0.0906 62 2008 Andrena braccata 0.0002 0.0031 0.9588 80 2010 Andrena bradleyi -0.0027 0.0028 0.3297 97 2011 Andrena ceanothi -0.0014 0.0047 0.7577 35 2006 Andrena commoda -0.0019 0.0034 0.5641 67 2008 Andrena cressonii -0.0012 0.0021 0.5733 253 2011 Andrena dunningi -0.0045 0.0029 0.1285 85 2011 Andrena erythronii -0.0030 0.0042 0.4690 42 2006 Andrena forbesii -0.0014 0.0022 0.5191 285 2011 Andrena fragilis -0.0023 0.0029 0.4244 92 2011 Andrena frigida -0.0003 0.0031 0.9273 79 2011 Andrena hippotes 0.0024 0.0028 0.3833 229 2011 Andrena hirticincta -0.0048 0.0028 0.0868 259 2011 Andrena imitatrix -0.0017 0.0021 0.4244 285 2011 Andrena mandibularis -0.0039 0.0034 0.2418 65 2010 Andrena melanochroa -0.0057 0.0041 0.1674 42 2002 Andrena milwaukeensis -0.0009 0.0036 0.7948 151 2011 Andrena miranda -0.0056 0.0031 0.0737 74 2011 Andrena miserabilis -0.0032 0.0018 0.0758 422 2011 Andrena nasonii -0.0016 0.0020 0.4015 532 2011 Andrena nigrihirta 0.0043 0.0051 0.3971 34 2002 Andrena nivalis -0.0031 0.0030 0.3104 156 2010 Andrena perplexa 0.0023 0.0034 0.5003 143 2011 Andrena persimulata -0.0006 0.0045 0.8941 39 2000 Andrena platyparia -0.0020 0.0038 0.5981 96 2010 Andrena robertsonii 0.0032 0.0033 0.3428 129 2009 Andrena rugosa 0.0020 0.0029 0.4894 272 2011 Andrena simplex -0.0033 0.0040 0.4054 47 2010 Andrena spiraeana 0.0031 0.0028 0.2652 106 2011 Andrena thaspii -0.0002 0.0036 0.9507 132 2011 Andrena vicina -0.0026 0.0019 0.1734 429 2011 Andrena virginiana -0.0011 0.0043 0.7965 41 2006 Andrena ziziae -0.0066 0.0042 0.1104 41 2011 Anthophora terminalis -0.0006 0.0034 0.8711 67 2011 Bombus sandersoni -0.0035 0.0034 0.3177 119 2009 Coelioxys sayi -0.0015 0.0033 0.6588 133 2011 Colletes americanus 0.0036 0.0028 0.1916 110 2010 Colletes inaequalis -0.0030 0.0020 0.1319 190 2011 Colletes kincaidii -0.0064 0.0043 0.1329 39 1976 Colletes simulans 0.0004 0.0027 0.8699 179 2010 Epeolus pusillus -0.0074 0.0047 0.1143 32 2009 Heriades carinata 0.0013 0.0034 0.7042 69 2011 Hoplitis pilosifrons 0.0000 0.0040 0.9982 50 2011 Hoplitis producta 0.0025 0.0034 0.4585 73 2011 affinis * -0.0020 0.0035 0.5716 61 2010 Hylaeus mesillae -0.0029 0.0020 0.1468 187 2011 Lasioglossum acuminatum 0.0092 0.0054 0.0854 35 2010 Lasioglossum coeruleum 0.0013 0.0035 0.7098 65 2011 Lasioglossum coriaceum 0.0002 0.0022 0.9262 163 2011 Lasioglossum divergens 0.0030 0.0050 0.5434 34 2002 Lasioglossum lineatulum 0.0057 0.0041 0.1633 108 2011 Lasioglossum macoupinense 0.0002 0.0036 0.9477 60 2011 Lasioglossum nymphaearum 0.0035 0.0028 0.2020 220 2011 Lasioglossum oenotherae 0.0033 0.0050 0.5121 34 2011 Lasioglossum smilacinae * -0.0026 0.0039 0.5065 49 2011 Lasioglossum vierecki -0.0061 0.0044 0.1670 37 2011 Lasioglossum zephyrum -0.0018 0.0023 0.4454 222 2011 Megachile centuncularis -0.0074 0.0042 0.0767 95 2011 Megachile gemula 0.0026 0.0031 0.4005 89 2011 Megachile mendica -0.0014 0.0027 0.5918 354 2011 Megachile pugnata -0.0070 0.0042 0.0900 41 2011 Megachile texana -0.0014 0.0056 0.8099 92 2011 Melissodes bimaculata -0.0039 0.0037 0.2865 118 2011 Melissodes desponsa 0.0026 0.0056 0.6512 90 2010 Nomada articulata 0.0046 0.0029 0.1137 102 2011 Nomada denticulata 0.0038 0.0045 0.3961 42 2011 Nomada illinoensis * -0.0025 0.0049 0.6058 31 2011 Osmia bucephala 0.0016 0.0034 0.6499 69 2011 Osmia pumila 0.0020 0.0030 0.5070 187 2011 Perdita octomaculata -0.0050 0.0049 0.3078 30 2010 Pseudopanurgus andrenoides 0.0075 0.0047 0.1106 43 2009 aroniae 0.0067 0.0051 0.1897 36 2011 Sphecodes confertus 0.0008 0.0033 0.8187 74 2010 Sphecodes dichrous -0.0038 0.0039 0.3293 49 2011 Sphecodes ranunculi -0.0033 0.0039 0.4009 49 2007 Increasing species Agapostemon sericeus 0.0054 0.0024 0.0222 264 2011 Agapostemon texanus 0.0101 0.0045 0.0263 50 2011 Agapostemon virescens 0.0052 0.0026 0.0480 351 2011 Andrena carolina 0.0095 0.0033 0.0044 91 2010 Andrena nuda 0.0174 0.0041 0.0000 81 2011 Andrena pruni 0.0220 0.0039 0.0000 103 2011 Andrena rufosignata 0.0099 0.0038 0.0088 72 2011 Andrena tridens 0.0136 0.0056 0.0154 37 2011 Augochlora pura 0.0057 0.0024 0.0200 328 2011 Augochlorella aurata 0.0042 0.0021 0.0466 536 2011 Augochloropsis metallica 0.0064 0.0025 0.0086 154 2011 Bombus bimaculatus 0.0090 0.0016 0.0000 503 2011 Bombus citrinus 0.0148 0.0027 0.0000 293 2011 Bombus griseocollis 0.0245 0.0031 0.0000 340 2011 Bombus impatiens 0.0067 0.0013 0.0000 1288 2011 Bombus perplexus 0.0063 0.0013 0.0000 386 2011 Calliopsis andreniformis 0.0073 0.0029 0.0117 113 2011 calcarata * 0.0194 0.0030 0.0000 302 2011 Ceratina dupla (sensu lato) * 0.0151 0.0036 0.0000 181 2011 Ceratina strenua 0.0130 0.0046 0.0056 126 2011 philadelphi 0.0124 0.0058 0.0326 33 2011 Colletes thoracicus 0.0217 0.0039 0.0000 105 2011 Halictus confusus 0.0041 0.0015 0.0059 400 2011 Halictus ligatus 0.0073 0.0017 0.0000 713 2011 Halictus parallelus 0.1022 0.0253 0.0001 35 2010 Hylaeus modestus * 0.0149 0.0025 0.0000 197 2011 Lasioglossum anomalum 0.0270 0.0079 0.0006 31 2009 Lasioglossum bruneri 0.0254 0.0054 0.0000 61 2011 Lasioglossum cressonii 0.0060 0.0017 0.0003 330 2011 Lasioglossum ephialtum * 0.0283 0.0048 0.0000 87 2011 Lasioglossum foxii 0.0118 0.0032 0.0003 104 2011 Lasioglossum fuscipenne 0.0195 0.0042 0.0000 82 2011 Lasioglossum mitchelli * 0.0088 0.0042 0.0371 56 2011 Lasioglossum nigroviride 0.0155 0.0045 0.0006 61 2011 Lasioglossum oblongum * 0.0239 0.0052 0.0000 62 2011 Lasioglossum obscurum * 0.0193 0.0059 0.0011 41 2011 Lasioglossum pectorale 0.0070 0.0027 0.0118 192 2011 Lasioglossum quebecense 0.0133 0.0031 0.0000 123 2011 Lasioglossum subviridatum * 0.0409 0.0143 0.0049 71 2010 Lasioglossum tegulare * 0.0140 0.0037 0.0001 88 2011 Lasioglossum versans 0.0127 0.0038 0.0009 77 2011 Lasioglossum versatum 0.0488 0.0040 0.0000 277 2011 Lasioglossum weemsi * 0.0234 0.0068 0.0006 36 2011 0.0105 0.0040 0.0094 64 2011 Megachile petulans 0.0289 0.0069 0.0000 44 2010 Nomada bella * 0.0468 0.0095 0.0000 45 2010 Nomada cressonii * 0.0062 0.0026 0.0168 138 2011 Nomada imbricata * 0.0098 0.0044 0.0263 53 2011 Nomada luteoloides 0.0205 0.0044 0.0000 77 2011 Nomada maculata 0.0138 0.0052 0.0083 132 2011 Nomada pygmaea * 0.0178 0.0035 0.0000 108 2011 Sphecodes coronus 0.0109 0.0042 0.0089 61 2010 Sphecodes davisii 0.0113 0.0044 0.0109 55 2010 Sphecodes heraclei 0.0304 0.0066 0.0000 51 2010 Xylocopa virginica 0.0063 0.0029 0.0316 228 2011 Exotic species Andrena wilkella -0.0045 0.0023 0.0499 608 2011 Anthidium manicatum 0.1549 0.0248 0.0000 36 2011 Anthidium oblongatum 0.0749 0.0137 0.0000 59 2011 Chelostoma campanularum 2 2002 Chelostoma rapunculi 6 2004 Hoplitis anthocopoides 0.0020 0.0149 0.8926 54 2004 Hylaeus hyalinatus 13 2011 Hylaeus leptocephalus 0.0142 0.0051 0.0060 42 2011 Hylaeus punctatus 7 2011 Hylaeus purpurissatus 1 1999 Lasioglossum leucozonium 0.0191 0.0045 0.0000 72 2011 Lasioglossum zonulum 22 2011 Megachile apicalis 1 2009 Megachile concinna 18 2010 0.0302 0.0049 0.0000 105 2011 Megachile sculpturalis 0.0913 0.0142 0.0000 36 2011 Osmia caerulescens -0.0273 0.0050 0.0000 74 1998 Osmia cornifrons 0.1095 0.0227 0.0000 32 2011 Osmia taurus 2 2009 Pseudoanthidium nanum 4 2009 Low sample size species Andrena accepta 2 1933 Andrena aliciae 11 1967 Andrena atlantica 3 2003 Andrena banksi 2 2000 Andrena barbara 9 2010 Andrena chromotricha 12 1997 Andrena clarkella 18 2003 Andrena confederata 7 2011 Andrena cornelli 25 2010 Andrena daeckei 2 1969 Andrena dimorpha 1 1923 Andrena duplicata 1 1967 Andrena fenningeri 4 1982 Andrena fulvipennis 6 2000 Andrena gardineri 1 1917 Andrena helianthi 24 2000 Andrena heraclei 5 2010 Andrena hilaris 16 2011 Andrena ilicis 6 2006 Andrena illini 1 1916 Andrena illinoiensis 1 1916 Andrena kalmiae 2 2010 Andrena krigiana 23 2011 Andrena mariae 13 2000 Andrena morrisonella 17 2011 Andrena neonana 10 2009 Andrena nida 5 2000 Andrena nigrae 15 2002 Andrena peckhami 1 1974 Andrena personata 8 1975 Andrena phaceliae 1 1917 Andrena rehni 7 1945 Andrena rudbeckiae 2 2005 Andrena runcinatae 13 2008 Andrena sayi 1 1916 Andrena violae 11 2010 Andrena wellesleyana 8 1975 Andrena wheeleri 20 2000 Andrena ziziaeformis 18 2003 Anthidiellum notatum 24 2007 Anthophora abrupta 15 2000 Anthophora bomboides 5 1999 Anthophora ursina 5 1988 Anthophora walshii 3 2011 Augochlorella persimilis 2 1963 Augochloropsis sumptuosa 7 1934 Bombus fernaldae 12 2011 Bombus fraternus 5 1921 Bombus insularis 2 1995 Bombus rufocinctus 16 2007 Calliopsis nebraskensis 6 1966 ipomoeae 1 1964 Ceratina mikmaqi 1 2011 Coelioxys alternata 3 2005 Coelioxys funeraria 7 1934 Coelioxys galactiae 1 1919 Coelioxys germana 21 2010 Coelioxys hunteri 1 1933 Coelioxys immaculata 6 2011 Coelioxys moesta 20 2006 Coelioxys porterae 13 2011 Coelioxys sodalis 4 1973 Colletes bradleyi 1 1923 Colletes consors 1 1973 Colletes latitarsis 13 2011 Colletes nudus 9 2010 Colletes productus 14 2011 Colletes solidaginis 9 2010 Colletes speculiferus 8 2008 Dianthidium simile 1 1925 Dufourea monardae 1 2008 Dufourea novaeangliae 11 2011 pilosulus 9 1928 Epeolus autumnalis 12 2007 Epeolus banksi 1 1919 Epeolus bifasciatus 9 1982 Epeolus canadensis 5 1962 Epeolus ilicis 1 1976 Epeolus lectoides 17 2010 Eucera atriventris 14 1932 Eucera hamata 1 2011 Habropoda laboriosa 29 2010 Halictus poeyi 1 1998 Heriades variolosa 7 2007 Holcopasites calliopsidis 25 2006 Holcopasites illinoiensis 12 1964 Hoplitis albifrons 7 1981 Hoplitis spoliata 23 2006 Hoplitis truncata 12 2011 Hylaeus annulatus 25 2007 Hylaeus basalis 9 1966 Hylaeus illinoisensis 2 2005 Hylaeus nelumbonis 2 2007 Hylaeus saniculae 5 1979 Hylaeus schwarzii 3 2002 Hylaeus sparsus 3 1934 Hylaeus verticalis 5 2004 Lasioglossum abanci 5 2009 Lasioglossum achilleae 1 1969 Lasioglossum admirandum 8 2011 Lasioglossum albipenne 9 2011 Lasioglossum arantium 1 1973 Lasioglossum athabascense 24 2004 Lasioglossum atwoodi 1 1998 Lasioglossum callidum 26 2011 Lasioglossum cattellae 11 2009 Lasioglossum comagenense 2 2002 Lasioglossum coreopsis 5 2010 Lasioglossum dreisbachi 5 1998 Lasioglossum dubitatum 1 1936 Lasioglossum ellisiae 6 2011 Lasioglossum fattigi 1 2007 Lasioglossum forbesii 2 1966 Lasioglossum foveolatum 3 1969 Lasioglossum georgeickworti 10 2005 Lasioglossum gotham 14 2010 Lasioglossum illinoense 27 2011 Lasioglossum katherineae 9 2002 Lasioglossum laevissimum 25 2003 Lasioglossum lionotum 13 2009 Lasioglossum marinum 29 2011 Lasioglossum michiganense 2 2003 Lasioglossum nelumbonis 12 2003 Lasioglossum nymphale 3 1982 Lasioglossum paradmirandum 7 2003 Lasioglossum pectinatum 1 2006 Lasioglossum planatum 2 2002 Lasioglossum platyparium 5 2011 Lasioglossum pruinosum 5 2003 Lasioglossum rozeni 2 2010 Lasioglossum rufitarse 19 2002 Lasioglossum simplex 1 1916 Lasioglossum sopinci 5 1976 Lasioglossum subversans 1 1925 Lasioglossum taylorae 1 1959 Lasioglossum tenax 2 1968 Lasioglossum timothyi 4 2010 Lasioglossum trigeminum 6 2011 Lasioglossum viridatum 18 2008 Megachile addenda 27 2007 Megachile exilis 8 2011 Megachile frugalis 1 1914 Megachile inimica 18 2011 Megachile montivaga 19 2010 Megachile mucida 2 1998 Megachile rugifrons 2 2002 Megachile xylocopoides 1 2007 Melecta pacifica 1 1910 Melissodes agilis 24 2010 Melissodes apicata 4 2009 Melissodes communis 2 1970 Melissodes denticulata 18 2011 Melissodes dentiventris 9 1933 Melissodes illata 17 2008 Melissodes nivea 8 1935 Melissodes subillata 25 2009 Melissodes trinodis 16 2009 Melitta americana 15 2009 Melitta eickworti 8 1987 Melitta melittoides 25 2011 Nomada armatella 2 1920 Nomada australis 15 2007 Nomada banksi 2 2005 Nomada bethunei 1 1917 Nomada ceanothi 3 1978 Nomada composita 3 2007 Nomada cuneata 20 2010 Nomada depressa 9 2010 Nomada electa 19 2009 Nomada gracilis 3 2009 Nomada integerrima 1 1916 Nomada lehighensis 11 2003 Nomada lepida 22 2010 Nomada louisianae 1 1931 Nomada luteola 14 2010 Nomada obliterata 4 1998 Nomada orba 1 1929 Nomada ovata 24 2010 Nomada parva 11 2009 Nomada perplexa 15 2009 Nomada placida 4 1917 Nomada rubicunda 1 1911 Nomada sayi 22 2006 Nomada tiftonensis 5 2011 Nomada ulsterensis 1 1941 Nomada valida 1 1976 Nomada vegana 1 2006 Nomada vicina 24 2008 Nomada vincta 2 1933 Nomada xanthura 18 2011 Nomia nortoni 1 1922 Osmia albiventris 18 2008 Osmia chalybea 8 2009 Osmia collinsiae 2 1950 Osmia conjuncta 14 1958 Osmia distincta 19 2007 Osmia felti 3 2001 Osmia georgica 6 2011 Osmia inermis 1 2003 Osmia inspergens 15 2007 Osmia proxima 1 2004 Osmia simillima 17 2009 Osmia tersula 1 1987 Osmia virga 7 2006 Panurginus potentillae 7 1987 Paranthidium jugatorium 4 2002 Perdita bequaerti 3 1921 Perdita boltoniae 1 1911 Perdita bradleyi 5 2001 Perdita novaeangliae 8 1993 Perdita swenki 1 2007 Pseudopanurgus compositarum 16 2006 Pseudopanurgus labrosus 3 1977 Pseudopanurgus nebrascensis 9 2007 Pseudopanurgus pauper 7 1934 Ptilothrix bombiformis 12 2011 Sphecodes atlantis 27 2011 Sphecodes autumnalis 13 2008 Sphecodes banksii 6 2004 Sphecodes carolinus 1 1918 Sphecodes clematidis 2 2002 Sphecodes cressonii 23 2004 Sphecodes fattigi 2 2003 Sphecodes illinoensis 4 2001 Sphecodes johnsonii 24 2008 Sphecodes levis 24 2009 Sphecodes mandibularis 26 2011 Sphecodes minor 20 2009 Sphecodes pimpinellae 8 2008 Sphecodes prosphorus 5 1972 * Species particularly difficult to identify in at least one sex; results for these should be interpreted with caution. ** Presence-absence GLM output. Table S2. Phylogenetic signal (lambda) of each evaluated trait and its significance. Phylogenetic correlations between discrete traits were calculated using the Geiger package and continuous variables with the phytools package in R.

Trait Lambda p-value Estimate (relative change) 0.24 <0.001 Nest place 0.94 <0.001 Sociality 0.82 <0.001 Parasitism 0.95 <0.001 Diet breadth 0.54 <0.001 Body size 0.88 <0.001 Phenological range 0.72 <0.001 Phenological mean 0.40 <0.001 Latitude range 0.47 <0.001 Max latitude 0.14 0.07 Min latitude 0.32 <0.001