Historical changes in northeastern US bee 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 bees 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 species 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 (Hymenoptera: 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 taxonomy 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 Coelioxys 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 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.