Metabolomics Reveals the Origins of Antimicrobial Plant Resins Collected by Honey Bees
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{"title"=>"Metabolomics Reveals the Origins of Antimicrobial Plant Resins Collected by Honey Bees", "type"=>"journal", "authors"=>[{"first_name"=>"Michael B.", "last_name"=>"Wilson", "scopus_author_id"=>"55887548800"}, {"first_name"=>"Marla", "last_name"=>"Spivak", "scopus_author_id"=>"7005641314"}, {"first_name"=>"Adrian D.", "last_name"=>"Hegeman", "scopus_author_id"=>"6602451948"}, {"first_name"=>"Aaron", "last_name"=>"Rendahl", "scopus_author_id"=>"25723698900"}, {"first_name"=>"Jerry D.", "last_name"=>"Cohen", "scopus_author_id"=>"7410010720"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84885751157", "doi"=>"10.1371/journal.pone.0077512", "sgr"=>"84885751157", "pmid"=>"24204850", "issn"=>"19326203", "pui"=>"370052229"}, "id"=>"989d44d8-aa58-31ba-8fa2-335c0aa05b93", "abstract"=>"The deposition of antimicrobial plant resins in honey bee, Apis mellifera, nests has important physiological benefits. Resin foraging is difficult to approach experimentally because resin composition is highly variable among and between plant families, the environmental and plant-genotypic effects on resins are unknown, and resin foragers are relatively rare and often forage in unobservable tree canopies. Subsequently, little is known about the botanical origins of resins in many regions or the benefits of specific resins to bees. We used metabolomic methods as a type of environmental forensics to track individual resin forager behavior through comparisons of global resin metabolite patterns. The resin from the corbiculae of a single bee was sufficient to identify that resin's botanical source without prior knowledge of resin composition. Bees from our apiary discriminately foraged for resin from eastern cottonwood (Populus deltoides), and balsam poplar (P. balsamifera) among many available, even closely related, resinous plants. Cottonwood and balsam poplar resin composition did not show significant seasonal or regional changes in composition. Metabolomic analysis of resin from 6 North American Populus spp. and 5 hybrids revealed peaks characteristic to taxonomic nodes within Populus, while antimicrobial analysis revealed that resin from different species varied in inhibition of the bee bacterial pathogen, Paenibacillus larvae. We conclude that honey bees make discrete choices among many resinous plant species, even among closely related species. Bees also maintained fidelity to a single source during a foraging trip. Furthermore, the differential inhibition of P. larvae by Populus spp., thought to be preferential for resin collection in temperate regions, suggests that resins from closely related plant species many have different benefits to bees.", "link"=>"http://www.mendeley.com/research/metabolomics-reveals-origins-antimicrobial-plant-resins-collected-honey-bees", "reader_count"=>64, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Librarian"=>2, "Researcher"=>9, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>4, "Student > Bachelor"=>10, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Librarian"=>2, "Researcher"=>9, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>4, "Student > Bachelor"=>10, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>37, "Medicine and Dentistry"=>2, "Design"=>1, "Sports and Recreations"=>1, "Chemistry"=>9, "Social Sciences"=>1, "Computer Science"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>9}, "Social Sciences"=>{"Social Sciences"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>37}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>3}}, "reader_count_by_country"=>{"United States"=>2, "Mexico"=>1, "United Kingdom"=>1, "Germany"=>2}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1252672"], "description"=>"<p>Table arranged by peak appearance in a given species group. The number of samples within a species group in which each peak appears is indicated in the last column. Retention time was rounded to the nearest 0.1 min. Pd  =  <i>P. deltoides</i>, Pf  =  <i>P. fremontii</i>, Pa  =  <i>P. angustifolia</i>, Pb  =  <i>P. balsamifera</i>, Pt  =  <i>P. trichocarpa</i>, dm  =  <i>P. deltoides x maximowiczii</i>. Mass accuracy was 2 ppm. Rt  =  retention time.</p>", "links"=>[], "tags"=>["markers", "terminal", "taxonomic", "nodes"], "article_id"=>828448, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.t003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spectral_markers_of_terminal_taxonomic_nodes_in_Populus_/828448", "title"=>"Spectral markers of terminal taxonomic nodes in <i>Populus</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252670"], "description"=>"<p>Semi-log plot of the antimicrobial activity of resin from six representative <i>Populus spp</i>. individuals against <i>P. larvae</i>, a brood pathogen of honey bees. Antimicrobial activity was evaluated spectrophotmetrically at OD<sub>600</sub> relative to untreated controls. N = 8 replicates per sample per concentration of resin.</p>", "links"=>[], "tags"=>[], "article_id"=>828446, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g010", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_Paenibacillus_larvae_by_Populus_spp_resin_/828446", "title"=>"Inhibition of <i>Paenibacillus larvae</i> by <i>Populus spp.</i> resin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252667"], "description"=>"<p>PCA scores plot of resin ‘fingerprints’ from individual <i>P. balsamifera</i> plants collected throughout the growing season. 43.99% of the total variation in the data set is shown. N = 4 individuals in May, N = 5 individuals in June, August, and October.</p>", "links"=>[], "tags"=>[], "article_id"=>828443, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Seasonal_variation_in_P_balsamifera_/828443", "title"=>"Seasonal variation in <i>P. balsamifera</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252660"], "description"=>"<p>Base-peak negative-ion chromatogram (“fingerprints”) of resin collected from individual <i>Pinus spp</i>. within 2 miles of the study apiary.</p>", "links"=>[], "tags"=>["metabolite", "studied"], "article_id"=>828436, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Resin_metabolite_diversity_of_studied_Pinus_sp_Pine_/828436", "title"=>"Resin metabolite diversity of studied <i>Pinus sp</i>. (Pine).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252654"], "description"=>"<p>Top-down view of standard beekeeping equipment displaying a resin forager with red resin attached to her hind legs. Managed honey bees deposit resin mainly at the hive entrance, inner cover, and on top of the movable frames.</p>", "links"=>[], "tags"=>["resin"], "article_id"=>828433, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g001", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Honey_bee_resin_collection_/828433", "title"=>"Honey bee resin collection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252674"], "description"=>"<div><p>The deposition of antimicrobial plant resins in honey bee, <i>Apis mellifera</i>, nests has important physiological benefits. Resin foraging is difficult to approach experimentally because resin composition is highly variable among and between plant families, the environmental and plant-genotypic effects on resins are unknown, and resin foragers are relatively rare and often forage in unobservable tree canopies. Subsequently, little is known about the botanical origins of resins in many regions or the benefits of specific resins to bees. We used metabolomic methods as a type of environmental forensics to track individual resin forager behavior through comparisons of global resin metabolite patterns. The resin from the corbiculae of a single bee was sufficient to identify that resin's botanical source without prior knowledge of resin composition. Bees from our apiary discriminately foraged for resin from eastern cottonwood (<i>Populus deltoides</i>), and balsam poplar (<i>P. balsamifera</i>) among many available, even closely related, resinous plants. Cottonwood and balsam poplar resin composition did not show significant seasonal or regional changes in composition. Metabolomic analysis of resin from 6 North American <i>Populus spp</i>. and 5 hybrids revealed peaks characteristic to taxonomic nodes within <i>Populus</i>, while antimicrobial analysis revealed that resin from different species varied in inhibition of the bee bacterial pathogen, <i>Paenibacillus larvae</i>. We conclude that honey bees make discrete choices among many resinous plant species, even among closely related species. Bees also maintained fidelity to a single source during a foraging trip. Furthermore, the differential inhibition of <i>P. larvae</i> by <i>Populus spp</i>., thought to be preferential for resin collection in temperate regions, suggests that resins from closely related plant species many have different benefits to bees.</p></div>", "links"=>[], "tags"=>["reveals", "origins", "antimicrobial", "resins"], "article_id"=>828450, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512", "stats"=>{"downloads"=>6, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Metabolomics_Reveals_the_Origins_of_Antimicrobial_Plant_Resins_Collected_by_Honey_Bees_/828450", "title"=>"Metabolomics Reveals the Origins of Antimicrobial Plant Resins Collected by Honey Bees", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252669"], "description"=>"<p>PCA scores plot of resin ‘fingerprints’ from 11 different <i>Populus spp.</i> and hybrids grown under greenhouse conditions. Pure species are indicated by closed shapes, while hybrids are indicated by open shapes. 49.11% of the total variation in the data set is shown. d x m  =  <i>P. deltoides x maximowiczii</i> (N = 8), d x n = <i>P. deltoides x nigra</i> (N = 4), d x t = <i>P. deltoides x trichocapra</i> (N = 6), t x d = <i>P. trichocarpa x deltoides</i> (N = 5), (t x d) x d = <i>P. (trichocarpa x deltoides) x deltoides</i> (N = 14). N = 6 for <i>P. deltoides</i> and <i>P. nigra</i>, N = 12 for <i>P. fremontii</i>, N = 14 for <i>P. trichocarpa</i>, N = 18 for <i>P. angustifolia</i>, N = 5 for <i>P. balsamifera</i>.</p>", "links"=>[], "tags"=>["differences"], "article_id"=>828445, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g009", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Compositional_differences_in_Populus_spp_resin_/828445", "title"=>"Compositional differences in <i>Populus spp.</i> resin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252668"], "description"=>"<p>PCA scores plot of resin ‘fingerprints’ from <i>P. deltoides</i> plants collected throughout the growing season. 40.86% of the total variation in the data set is shown. N = 2 individuals in May, N = 5 individuals in June, N = 9 individuals in July (from near Jamestown, ND), N = 5 individuals in August, N = 5 individuals in October.</p>", "links"=>[], "tags"=>[], "article_id"=>828444, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g008", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Seasonal_variation_in_P_deltoides_/828444", "title"=>"Seasonal variation in <i>P. deltoides</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252665"], "description"=>"<p>(Top) Example of a <i>P. deltoides</i> resin metabolite ‘fingerprint’. (Bottom) PCA scores plot of resin ‘fingerprints’ from individual resin-producing plants and honey bee resin foragers. Points represent the spectral composition of a biological sample. Points that are closer together have more spectral peaks in common than with points that are farther apart. 54.35% of the total variation in the data set is shown. Hybrid poplars were sampled once in June, while <i>P. deltoides</i> (Eastern cottonwood) and <i>P. balsamifera</i> (balsam poplar) once in June and once in July. N = 25 for resin from foraging bees, N = 11 for <i>P. balsamifera</i>, N = 16 for <i>P. deltoides</i> (9 from near Jamestown, ND), and N = 5 for each poplar hybrid population.</p>", "links"=>[], "tags"=>["bees", "resin"], "article_id"=>828441, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g006", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Honey_bees_collect_resin_from_P_balsamifera_and_P_deltoides_/828441", "title"=>"Honey bees collect resin from <i>P. balsamifera</i> and <i>P. deltoides</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252663"], "description"=>"<p>Base-peak negative-ion chromatogram (“fingerprints”) of resin collected from individual <i>Picea spp</i>. within 2 miles of the study apiary.</p>", "links"=>[], "tags"=>["metabolite", "studied"], "article_id"=>828439, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Resin_metabolite_diversity_of_studied_Picea_sp_Spruce_/828439", "title"=>"Resin metabolite diversity of studied <i>Picea sp</i>. (Spruce).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252664"], "description"=>"<p>Base-peak negative-ion chromatogram (“fingerprints”) of resin collected from other conifers within 2 miles of the study apiary.</p>", "links"=>[], "tags"=>["metabolite", "studied"], "article_id"=>828440, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Resin_metabolite_diversity_of_other_studied_conifers_/828440", "title"=>"Resin metabolite diversity of other studied conifers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252673"], "description"=>"<p>Table describes the concentration at which the bee pathogen, <i>Paenibacillus larvae</i>, was inhibited by resin collected from local plants in a spectrophotometric growth assay completely (≤ 1% OD<sub>600</sub> of untreated controls).</p>", "links"=>[], "tags"=>["pathogen"], "article_id"=>828449, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_pathogen_growth_by_local_resins_/828449", "title"=>"Inhibition of pathogen growth by local resins.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252655"], "description"=>"<p>Base-peak negative-ion chromatogram (“fingerprints”) of resin collected from individual <i>Populus spp</i>. (poplar) and <i>Aesculus hippocastanum</i> (horse chestnut) within 2 miles of the study apiary.</p>", "links"=>[], "tags"=>["metabolite", "studied"], "article_id"=>828434, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.g002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Resin_metabolite_diversity_of_studied_angiosperms_/828434", "title"=>"Resin metabolite diversity of studied angiosperms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-18 04:06:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1252671"], "description"=>"<p>Table arranged by peak appearance in a given sample group. The number of samples within a month group in which each peak appears is indicated in the last column. Retention time was rounded to the nearest 0.1 min. Mass accuracy was 5–10 ppm. Rt = retention time.</p>", "links"=>[], "tags"=>["peaks", "late-season", "indicators"], "article_id"=>828447, "categories"=>["Biological Sciences"], "users"=>["Michael B. Wilson", "Marla Spivak", "Adrian D. Hegeman", "Aaron Rendahl", "Jerry D. Cohen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077512.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spectral_peaks_representing_late_season_indicators_in_P_balsamifera_and_P_deltoides_/828447", "title"=>"Spectral peaks representing late-season indicators in <i>P. balsamifera</i> and <i>P. deltoides</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-18 04:06:37"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"23", "full-text"=>"19", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
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Relative Metric

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