Sheila R. Colla

Climate-associated phenological advances in bee pollinators and bee-pollinated plants

The phenology of many ecological processes is modulated by temperature, making them potentially sensitive to climate change. Mutualistic interactions may be especially vulnerable because of the potential for phenological mismatching if the species involved do not respond similarly to changes in temperature. Here we present an analysis of climate-associated shifts in the phenology of wild bees, the most important pollinators worldwide, and compare these shifts to published studies of bee-pollinated plants over the same time period. We report that over the past 130 y, the phenology of 10 bee species from northeastern North America has advanced by a mean of 10.4 ± 1.3 d. Most of this advance has taken place since 1970, paralleling global temperature increases. When the best available data are used to estimate analogous rates of advance for plants, these rates are not distinguishable from those of bees, suggesting that bee emergence is keeping pace with shifts in host-plant flowering, at least among the generalist species that we investigated.

Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees

Parasites can affect host behavior in subtle but ecologically important ways. In the laboratory, we conducted experiments to determine whether parasitic infection by the intestinal protozoan Crithidia bombi or the tracheal mite Locustacarus buchneri alters the foraging behavior of the bumble bee Bombus impatiens. Using an array of equally rewarding yellow and blue artificial flowers, we measured the foraging rate (flowers visited per minute, flower handling time, and flight time between flowers) and flower constancy (tendency to sequentially visit flowers of the same type) of bees with varying intensities of infection. Bumble bee workers infected with tracheal mites foraged as rapidly as uninfected workers, but were considerably more constant to a single flower type (yellow or blue). In contrast, workers infected with intestinal protozoa showed similar levels of flower constancy, but visited 12% fewer flowers per minute on average than uninfected bees. By altering the foraging behavior of bees, such parasites may influence interactions between plants and pollinators, as well as the reproductive output of bumble bee colonies. Our study is the first to investigate the effects of parasitic protozoa and tracheal mites on the foraging behavior of bumble bees, and provides the first report of Crithidia bombi in commercial bumble bees in North America.

Assessing declines of North American bumble bees (Bombus spp.) using museum specimens

Bumble bees are an important group of wild pollinators in North America and considerable concern has been expressed over declines in their populations. However, before causes for declines can be assessed, it is essential that the geographical and chronological patterns of decline be discovered. Hitherto a lack of assessment of historical data has hindered our efforts to determine which species are most at risk. Here, the status of 21 North American bumble bee species (Hymenoptera: Apidae) occurring in the eastern nearctic biogeographic region is assessed using a specimen-level database from compiled museum and survey records dating back to the late nineteenth century from various institutional collections. Using a combination of measures, bumble bee declines were assessed over their entire native ranges. We report here that half of the selected fauna is in varying levels of decline (especially Bombus ashtoni, B. fervidus, and B. variabilis), with the remaining species exhibiting stable or increasing trends (e.g., B. bimaculatus, B. impatiens, and B. rufocinctus). Suggestions for prioritizing conservation efforts for this important group of pollinators are given.

Evidence for the decline of the western bumble bee (Bombus occidentalis Greene) in British Columbia

The crucial ecosystem service provided by native pollinators has been recentlyregarded as threatened globally (e.g., Biesmeijer et al. 2006, Klein et al. 2007, NRC2007). Bees (Hymenoptera: Apoidea) are a speciose taxon containing a large portionof native pollinating insects. As in many invertebrate groups, baseline data andnatural history knowledge for most bee species is highly deficient. As a result,important pollinators may undergo drastic declines unnoticed (Buchmann &Nabhan 1996).Bumble bees (Bombus spp.) are among the best studied bee taxa as they are large,colorful and relatively easy to identify (Kearns & Thomson 2001). The declines ofsome species have been documented globally (Williams & Osborne 2009) but thedeclines in western Canada have been largely anecdotal. In particular, NorthAmerican members of the subgenus Bombus sensu strictu have declined rapidlythroughout their native ranges (reviewed in Evans et al. 2008). While the decline ofB. franklini in southwestern U.S.A. and B. affinis in eastern North America havebeen well documented and quantified (Thorp & Shepherd 2005, Colla & Packer2008, Grixti et al. 2009), there are few baseline data for comparing previous andcurrent abundances of B. occidentalis, the Western Bumblebee. Here we provide acomparison of the relative abundance of B. occidentalis after 20 years in the FraserValley of British Columbia, Canada.In 2003 and 2004, a study on the abundance and diversity of wild bees incommercial highbush blueberry and cranberry fields was performed (Ratti et al.2008, Ratti 2006). The study was located in the Fraser Valley of British Columbiawhere a total twelve sites were surveyed using sweep nets and pan traps (Ratti et al.2008, Ratti 2006). Collected specimens were identified by C. Ratti with vouchersbeing confirmed by T. Griswold and deposited in the Packer Collection at YorkUniversity, Toronto, Ontario, Canada and the USDA-ARS Bee Biology andSystematics Laboratory, Logan, Utah. Similar surveys were performed in variousberry fields and natural vegetation in the same region in the early 1980s (Winston &Graf 1982, MacKenzie & Winston 1984). While the exact same sampling methodswere not used for both time periods, the recent study (Ratti 2006) sampled more sitesand used an additional sampling method (pan trapping in addition to sweep netting).This indicates that differences noted in B. occidentalis abundance are not the result oflower sampling effort during the more recent time period.Bombus occidentalis was the second most abundant bumble bee in blueberry fieldsin 1981 (27% of collected bumble bees) (Winston & Graf 1982), and it was the secondmost common Bombus species, overall, collected in berry fields and naturalvegetation (approx 22%) in 1982 (MacKenzie & Winston 1984). In 2003–2004, thisspecies represented less than 1% of the Bombus collected (26 individuals of the 2738total). Likewise B. occidentalis was the most abundant bee (55% of bumble bees, 312individuals) in cranberry fields in 1982 and second most abundant bee in 1981 (41%of bumble bees, 104 individuals) (MacKenzie & Winston 1984, Winston & Graf

Questioning public perception, conservation policy, and recovery actions for honeybees in North America

Global pollinator declines have resulted in an increasing number of policies and actions to help bee populations. In North America, there is strong public engagement, but also growing controversies over how to address declines. This is fueled by complex scientific evidence across species, habitat types, geographic regions, as well as intense lobbying by NGOs, beekeeping, agro-chemical and farming industries. Policy and conservation initiatives often focus on the Western Honeybee, Apis mellifera Linnaeus, a domesticated species not native to North America. Although losses of managed honeybee colonies are recorded annually, we argue that honeybee losses are not a conservation problem, but instead a domesticated animal management issue. By focusing attention on honeybees, policies and subsequent resources may undermine native bee conservation and have negative impacts ecologically and socially. This article is protected by copyright. All rights reserved

Conservation Genomics of the Declining North American Bumblebee Bombus terricola Reveals Inbreeding and Selection on Immune Genes

The yellow-banded bumblebee Bombus terricola was common in North America but has recently declined and is now on the IUCN Red List of threatened species. The causes of B. terricola’s decline are not well understood. Our objectives were to create a partial genome and then use this to estimate population data of conservation interest, and to determine whether genes showing signs of recent selection suggest a specific cause of decline. First, we generated a draft partial genome (contig set) for B. terricola, sequenced using Pacific Biosciences RS II at an average depth of 35×. Second, we sequenced the individual genomes of 22 bumblebee gynes from Ontario and Quebec using Illumina HiSeq 2500, each at an average depth of 20×, which were used to improve the PacBio genome calls and for population genetic analyses. The latter revealed that several samples had long runs of homozygosity, and individuals had high inbreeding coefficient F, consistent with low effective population size. Our data suggest that B. terricola’s effective population size has decreased orders of magnitude from pre-Holocene levels. We carried out tests of selection to identify genes that may have played a role in ameliorating environmental stressors underlying B. terricola’s decline. Several immune-related genes have signatures of recent positive selection, which is consistent with the pathogen-spillover hypothesis for B. terricola’s decline. The new B. terricola contig set can help solve the mystery of bumblebee decline by enabling functional genomics research to directly assess the health of pollinators and identify the stressors causing declines.