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Research Article

Test of the invasive pathogen hypothesis of bumble bee decline in North America

Sydney A. Cameron, Haw Chuan Lim, Jeffrey D. Lozier, Michelle A. Duennes, and Robbin Thorp
PNAS April 19, 2016 113 (16) 4386-4391; first published April 4, 2016; https://doi.org/10.1073/pnas.1525266113
Sydney A. Cameron
aDepartment of Entomology, University of Illinois, Urbana, IL 61801;
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  • For correspondence: scameron@life.illinois.edu
Haw Chuan Lim
aDepartment of Entomology, University of Illinois, Urbana, IL 61801;
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Jeffrey D. Lozier
bDepartment of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487;
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Michelle A. Duennes
aDepartment of Entomology, University of Illinois, Urbana, IL 61801;
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Robbin Thorp
cDepartment of Entomology and Nematology, University of California, Davis, CA 95616
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  1. Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved February 26, 2016 (received for review January 3, 2016)

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    Fig. 1.

    Number of specimens screened and prevalence level per time period of Nosema for five target North American bumble bee species and the European B. terrestris (pink, infected bees; blue, uninfected bees; left y axis and bars, number of bees; right y axis and dashed lines, proportion out of the total screened). For species with sufficient sample sizes, results of χ2 tests of independence of proportions are shown above each bar graph. Horizontal lines indicate pairs of time periods in which Nosema prevalence is significantly different at P = 0.05 based on arcsine-transformed prevalence data.

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    Fig. 2.

    Yearly proportion of four declining bumble bee species infected with Nosema (open circles). The size of each circle is proportional on a logarithmic scale to the number of bees screened in a given year. Yearly infection rate data are fitted with a piecewise quasibinomial regression curve and its 95% CI (shaded area). For each species, the change point in time (i.e., year) with SE is indicated by a filled circle, with an error bar on either side. Numbers beside curves are estimated slope parameters for each segment of the piecewise regression (95% slope CI in parentheses). For B. affinis, B. pensylvanicus, and B. occidentalis, Nosema prevalence did not vary with time before the estimated change points (i.e., 95% CI of slope parameters include 0), but the prevalence–time relationship became significantly positive (with 95% CI of slope parameters excluding 0) after the change points.

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    Fig. S1.

    Pie charts showing spatial distributions of infected (red) or uninfected (blue) bumble bees for all five North American study species combined. Bees were collected between 1979 and 1991 (A) and between 1992 and 2011 (B). The largest circle in A represents 157 bees, and the largest circle in B represents 187 bees.

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    Fig. S2.

    Success rate of amplifying the LW Rh gene in bumble bee specimens of different ages. General linear modeling (binomial errors: dependent variable, success rate; independent variable, year of specimen collection) showed that year as an independent variable contributed little to model fit (regression coefficient = 0.0182, P = 0.814). Except for 2004, when only three bees were screened, four bees were screened in each study year.

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    Fig. S3.

    Proportion of four declining bumble bee species infected by Nosema (open circles) based on a less-stringent PCR detection criterion (at least one of three PCRs showed product of correct size on a gel). The size of each circle is proportional on a logarithmic scale to the number of bees screened in a given year. Yearly infection rate data are fitted with a piecewise quasibinomial regression curve and its 95% CI (shaded area). For each species, the change point in time (i.e., year) with SE is indicated by a filled circle, with error bar on either side. Numbers beside curves are estimated slope parameters for each segment of the piecewise regression (95% CI in parentheses). For B. affinis and B. pensylvanicus, the 95% CI of the slope parameter of post-1990 segment does not include 0.

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    Fig. 3.

    Filtered splits phylogenetic network showing relationships among Nosema clades. Clades may contain members that are attributable to known species (e.g., N. apis) that have been previously named in the literature (e.g., Nosema “D”) or newly delineated (e.g., clade 1). For each clade, the number of host individuals (represented both numerically and by size of circle at the tips) and their geographic origins are also shown. Clade memberships can be found in Table S3.

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    Fig. S4.

    Filtered splits phylogenetic network showing node designations. Refer to Table S3 for samples represented by each node.

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    Fig. 4.

    Neighbor-joining tree showing interisolate relationships based on allele frequency data from six genomic loci. Blue text represents North American Bombus species from across the United States; green text represents European B. terrestris taxa from different countries of western Europe.

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    Fig. S5.

    Kernel density plots of ΦST (among-isolate genetic variation), ΦCT (between-group genetic variation), and ΦSC (within-group, among-isolate genetic variation) calculated by hierarchical analysis of molecular variance. The analysis was based on data from six variable loci from 31 N. bombi isolates.

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Pathogen hypothesis of bumble bee decline
Sydney A. Cameron, Haw Chuan Lim, Jeffrey D. Lozier, Michelle A. Duennes, Robbin Thorp
Proceedings of the National Academy of Sciences Apr 2016, 113 (16) 4386-4391; DOI: 10.1073/pnas.1525266113

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Pathogen hypothesis of bumble bee decline
Sydney A. Cameron, Haw Chuan Lim, Jeffrey D. Lozier, Michelle A. Duennes, Robbin Thorp
Proceedings of the National Academy of Sciences Apr 2016, 113 (16) 4386-4391; DOI: 10.1073/pnas.1525266113
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