RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species
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{"title"=>"RNA viruses in hymenopteran pollinators: Evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species", "type"=>"journal", "authors"=>[{"first_name"=>"Rajwinder", "last_name"=>"Singh", "scopus_author_id"=>"7408228938"}, {"first_name"=>"Abby L.", "last_name"=>"Levitt", "scopus_author_id"=>"37093343200"}, {"first_name"=>"Edwin G.", "last_name"=>"Rajotte", "scopus_author_id"=>"6603394186"}, {"first_name"=>"Edward C.", "last_name"=>"Holmes", "scopus_author_id"=>"55535773400"}, {"first_name"=>"Nancy", "last_name"=>"Ostiguy", "scopus_author_id"=>"6507012856"}, {"first_name"=>"Dennis", "last_name"=>"Vanengelsdorp", "scopus_author_id"=>"16311263600"}, {"first_name"=>"W. Ian", "last_name"=>"Lipkin", "scopus_author_id"=>"7005714572"}, {"first_name"=>"Claude W.", "last_name"=>"Depamphilis", "scopus_author_id"=>"55664042900"}, {"first_name"=>"Amy L.", "last_name"=>"Toth", "scopus_author_id"=>"7202905012"}, {"first_name"=>"Diana L.", "last_name"=>"Cox-Foster", "scopus_author_id"=>"6603060478"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"361059651", "sgr"=>"78650985060", "issn"=>"19326203", "pmid"=>"21203504", "scopus"=>"2-s2.0-78650985060", "doi"=>"10.1371/journal.pone.0014357", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)"}, "id"=>"70d219c3-f6c9-33ed-aee7-2bb8d8bfe1f5", "abstract"=>"Although overall pollinator populations have declined over the last couple of decades, the honey bee (Apis mellifera) malady, colony collapse disorder (CCD), has caused major concern in the agricultural community. Among honey bee pathogens, RNA viruses are emerging as a serious threat and are suspected as major contributors to CCD. Recent detection of these viral species in bumble bees suggests a possible wider environmental spread of these viruses with potential broader impact. It is therefore vital to study the ecology and epidemiology of these viruses in the hymenopteran pollinator community as a whole. We studied the viral distribution in honey bees, in their pollen loads, and in other non-Apis hymenopteran pollinators collected from flowering plants in Pennsylvania, New York, and Illinois in the United States. Viruses in the samples were detected using reverse transcriptase-PCR and confirmed by sequencing. For the first time, we report the molecular detection of picorna-like RNA viruses (deformed wing virus, sacbrood virus and black queen cell virus) in pollen pellets collected directly from forager bees. Pollen pellets from several uninfected forager bees were detected with virus, indicating that pollen itself may harbor viruses. The viruses in the pollen and honey stored in the hive were demonstrated to be infective, with the queen becoming infected and laying infected eggs after these virus-contaminated foods were given to virus-free colonies. These viruses were detected in eleven other non-Apis hymenopteran species, ranging from many solitary bees to bumble bees and wasps. This finding further expands the viral host range and implies a possible deeper impact on the health of our ecosystem. Phylogenetic analyses support that these viruses are disseminating freely among the pollinators via the flower pollen itself. Notably, in cases where honey bee apiaries affected by CCD harbored honey bees with Israeli Acute Paralysis virus (IAPV), nearby non-Apis hymenopteran pollinators also had IAPV, while those near apiaries without IAPV did not. In containment greenhouse experiments, IAPV moved from infected honey bees to bumble bees and from infected bumble bees to honey bees within a week, demonstrating that the viruses could be transmitted from one species to another. This study adds to our present understanding of virus epidemiology and may help explain bee disease patterns and pollinator population decline in general.", "link"=>"http://www.mendeley.com/research/rna-viruses-hymenopteran-pollinators-evidence-intertaxa-virus-transmission-via-pollen-potential-impa", "reader_count"=>276, "reader_count_by_academic_status"=>{"Unspecified"=>6, "Professor > Associate Professor"=>11, "Librarian"=>5, "Researcher"=>56, "Student > Doctoral Student"=>14, "Student > Ph. D. 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Student"=>74, "Student > Postgraduate"=>9, "Other"=>9, "Student > Master"=>47, "Student > Bachelor"=>27, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>15}, "reader_count_by_subject_area"=>{"Unspecified"=>20, "Environmental Science"=>32, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>196, "Medicine and Dentistry"=>5, "Arts and Humanities"=>1, "Veterinary Science and Veterinary Medicine"=>5, "Psychology"=>1, "Social Sciences"=>1, "Computer Science"=>2, "Earth and Planetary Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>196}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Unspecified"=>{"Unspecified"=>20}, "Environmental Science"=>{"Environmental Science"=>32}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>5}}, "reader_count_by_country"=>{"Colombia"=>2, "United States"=>16, "United Kingdom"=>1, "Spain"=>2, "Netherlands"=>1, "Austria"=>2, "Belgium"=>1, "Serbia and Montenegro"=>1, "Poland"=>1, "Mexico"=>2, "South Africa"=>1, "France"=>6, "Chile"=>1}, "group_count"=>9}

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  • {"files"=>["https://ndownloader.figshare.com/files/404355", "https://ndownloader.figshare.com/files/404396"], "description"=>"<div><p>Although overall pollinator populations have declined over the last couple of decades, the honey bee (<em>Apis mellifera</em>) malady, colony collapse disorder (CCD), has caused major concern in the agricultural community. Among honey bee pathogens, RNA viruses are emerging as a serious threat and are suspected as major contributors to CCD. Recent detection of these viral species in bumble bees suggests a possible wider environmental spread of these viruses with potential broader impact. It is therefore vital to study the ecology and epidemiology of these viruses in the hymenopteran pollinator community as a whole. We studied the viral distribution in honey bees, in their pollen loads, and in other non-<em>Apis</em> hymenopteran pollinators collected from flowering plants in Pennsylvania, New York, and Illinois in the United States. Viruses in the samples were detected using reverse transcriptase-PCR and confirmed by sequencing. For the first time, we report the molecular detection of picorna-like RNA viruses (deformed wing virus, sacbrood virus and black queen cell virus) in pollen pellets collected directly from forager bees. Pollen pellets from several uninfected forager bees were detected with virus, indicating that pollen itself may harbor viruses. The viruses in the pollen and honey stored in the hive were demonstrated to be infective, with the queen becoming infected and laying infected eggs after these virus-contaminated foods were given to virus-free colonies. These viruses were detected in eleven other non-<em>Apis</em> hymenopteran species, ranging from many solitary bees to bumble bees and wasps. This finding further expands the viral host range and implies a possible deeper impact on the health of our ecosystem. Phylogenetic analyses support that these viruses are disseminating freely among the pollinators via the flower pollen itself. Notably, in cases where honey bee apiaries affected by CCD harbored honey bees with Israeli Acute Paralysis virus (IAPV), nearby non-<em>Apis</em> hymenopteran pollinators also had IAPV, while those near apiaries without IAPV did not. In containment greenhouse experiments, IAPV moved from infected honey bees to bumble bees and from infected bumble bees to honey bees within a week, demonstrating that the viruses could be transmitted from one species to another. This study adds to our present understanding of virus epidemiology and may help explain bee disease patterns and pollinator population decline in general.</p></div>", "links"=>[], "tags"=>["rna", "viruses", "hymenopteran", "inter-taxa", "pollen"], "article_id"=>139905, "categories"=>["Ecology", "Science Policy", "Cancer", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.s001", "https://dx.doi.org/10.1371/journal.pone.0014357.s002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/RNA_Viruses_in_Hymenopteran_Pollinators_Evidence_of_Inter_Taxa_Virus_Transmission_via_Pollen_and_Potential_Impact_on_Non_Apis_Hymenopteran_Species/139905", "title"=>"RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-<em>Apis</em> Hymenopteran Species", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-12-22 02:45:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/810080"], "description"=>"<p>Incoming foragers with pollen pellets were collected in 2005; pollen pellets removed, tagged with identifier, and frozen at −80°C. Some foragers (1–8) were kept for 24 hrs at 34°C, 50% relative humidity and fed sugar water; others (9–12) were frozen immediately upon collection. After freezing, all foragers were divided into two regions, head plus prothorax that have salivary glands <b>(H/T1)</b> and the remainder of body lacking salivary glands <b>(T2,3/A)</b>. Pollen pellets and forager body regions were extracted for detection of deformed wing virus (DWV), sacbrood virus (SBV), and actin mRNA (forager only). Actin mRNA was used as an internal control for methods and loading. Red box indicates three foragers that lack detections of DWV but had pollen pellets with detectable DWV. The red star (lane 3) indicates a forager with heavy DWV infection in Head/Prothorax but no detectable DWV in her pollen pellets. Size of DWV reaction = 424 bp, SBV reaction = 693 bp and Actin reaction = 514 bp.</p>", "links"=>[], "tags"=>["viral", "pollen", "pellets", "corresponding", "forager", "dissected", "regions", "salivary", "secretions"], "article_id"=>480426, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_viral_presence_in_pollen_pellets_and_their_corresponding_forager_with_her_body_dissected_into_two_regions_with_or_without_salivary_glands_to_determine_if_salivary_secretions_of_the_forager_are_associated_with_virus_in_pollen_pellets_/480426", "title"=>"Comparison of viral presence in pollen pellets and their corresponding forager with her body dissected into two regions with or without salivary glands, to determine if salivary secretions of the forager are associated with virus in pollen pellets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:07:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/810169"], "description"=>"<p>For both the foragers and their pollen pellets, Venn diagrams depict the percentage of DWV (Deformed wing virus in red), SBV (Sacbrood virus in yellow), BQCV (Black queen cell virus in blue), or virus-free samples (white). Overlapping colored circles indicate samples wherein more than one virus was detected. Total percentages of these viruses in either foragers or pollen pellets are given in the middle of the figure. N = sample size.</p>", "links"=>[], "tags"=>["65", "pollen", "foragers"], "article_id"=>480529, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proportion_of_virus_species_detected_in_65_honey_bee_pollen_foragers_versus_their_pollen_pellets_/480529", "title"=>"Proportion of virus species detected in 65 honey bee pollen foragers versus their pollen pellets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:08:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/810271"], "description"=>"<p>Virus was detected in extracts of supernatants and homogenates after various washings of an aliquot of combined pollen pellets, in either Trizol or PBS+ (1M PBS, 0.05% Tween, 2% Polyvinylpyrrolodone) followed by SDS (Sodium Dodecyl Sulfate). Standard size ladders (L) are shown at beginning and end of gel images. Size marker of 500 bp is indicated by * on the ladder. Lane loadings are indicated below the gel image. Size of DWV reaction = 424 bp and BQCV reaction  = 700 bp.</p>", "links"=>[], "tags"=>["dwv", "bqcv"], "article_id"=>480630, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Determination_of_how_DWV_and_BQCV_are_associated_with_pollen_/480630", "title"=>"Determination of how DWV and BQCV are associated with pollen.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:10:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/810392"], "description"=>"<p>DWV- and SBV-free colonies were installed into new equipment in an isolated apiary near State College, Pennsylvania in the spring of 2005. Colonies in the <b>Control</b> treatment were each fed sugar water and artificial pollen, plus given a washed frame. In the <b>Bee Bread</b> or stored pollen treatment, colonies were each given a frame of bee bread with detectable DWV and sugar water. In the <b>Honey</b> treatment, colonies were each given a frame of capped honey with detectable DWV and artificial pollen diet. No SBV was detected in the workers or eggs from the queens in the colonies or the frames of honey or stored pollen prior to experiment. Egg samples (4 samples of 5 eggs each; 20 eggs total per colony) were collected weekly from each of four colonies (colony numbers listed on right of figure) in three treatment groups, at time of feeding and for five additional weeks. Eggs were extracted and used for detection of DWV, SBV and actin mRNA (present in 100% samples, not shown). Detection of actin mRNA in the honey bees is used as an internal control for extraction efficiency.</p>", "links"=>[], "tags"=>["dwv", "infectivity", "stored", "pollen", "detection", "sbv", "eggs"], "article_id"=>480741, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Test_of_DWV_infectivity_in_stored_pollen_and_honey_and_detection_of_SBV_movement_from_outside_source_through_transmission_of_DWV_and_SBV_to_eggs_by_queens_/480741", "title"=>"Test of DWV infectivity in stored pollen and honey and detection of SBV movement from outside source through transmission of DWV and SBV to eggs by queens.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:12:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/810549"], "description"=>"<p>An unrooted maximum likelihood phylogenetic tree of DWV (based on 1230-nt from the capsid) was generated using a region of the structural proteins of the virus. The support for the indicated branching topology was evaluated by using bootstrap re-sampling of the sequences 1,000 times. Nodes supported by bootstrap values over 70 are given. Strains are annotated by genus, species, identification-label, country of isolation, and year of isolation. Blue =  virus from honey bee, red =  virus from pollen pellet, and green =  virus from non-<i>Apis</i> hymenopteran pollinators. Forager/pollen pellet pairs are indicated by common symbols following the sample label.</p>", "links"=>[], "tags"=>["dwv", "sequences", "pollen", "hymenopteran"], "article_id"=>480912, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_comparison_of_DWV_sequences_detected_in_honey_bee_foragers_pollen_pellets_and_non_Apis_hymenopteran_pollinators_/480912", "title"=>"Phylogenetic comparison of DWV sequences detected in honey bee foragers, pollen pellets, and non-<i>Apis</i> hymenopteran pollinators.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:15:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/810728"], "description"=>"<p>An unrooted maximum likelihood phylogenetic tree of BQCV (based on 687-nt from Capsid/3′UTR) was generated using a region of the structural proteins of the virus. The support for the indicated branching topology was evaluated by using bootstrap re-sampling of the sequences 1,000 times. Nodes supported by bootstrap values over 70 are given. Strains were annotated by genus, species, identification label, country of isolation and year of isolation. Blue =  virus from honey bee, red =  virus from pollen pellet, and green =  virus from non-<i>Apis</i> hymenopteran pollinators. Forager/pollen pellet pairs are indicated by common symbols following the sample label.</p>", "links"=>[], "tags"=>["bqcv", "sequences", "pollen", "hymenopteran"], "article_id"=>481081, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_comparison_of_BQCV_sequences_detected_in_honey_bee_foragers_pollen_pellets_and_non_Apis_hymenopteran_pollinators_/481081", "title"=>"Phylogenetic comparison of BQCV sequences detected in honey bee foragers, pollen pellets, and non-<i>Apis</i> hymenopteran pollinators.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:18:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/810878"], "description"=>"<p>An unrooted maximum likelihood phylogenetic tree of IAPV (based on 771-nt for capsid region) was generated using a region of the structural proteins of the virus. The support for the indicated branching topology was evaluated by using bootstrap re-sampling of the sequences 1,000 times. Nodes supported by bootstrap values over 70 are given. Strains were annotated by genus, species, identification label, country of isolation and year of isolation. Green =  virus from non-<i>Apis</i> hymenopteran pollinators; Black  =  virus sequences from original isolation and honey bees from CCD-affected operations <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0014357#pone.0014357-CoxFoster1\" target=\"_blank\">[16]</a>. Non-<i>Apis</i> hymenopteran pollinators collected from same local are indicated by common symbol following sample label.</p>", "links"=>[], "tags"=>["iapv", "sequences", "honeybees", "hymenopteran", "pollinators"], "article_id"=>481234, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_comparison_of_IAPV_sequences_detected_in_honeybees_and_non_Apis_hymenopteran_pollinators_collected_near_IAPV_apiaries_/481234", "title"=>"Phylogenetic comparison of IAPV sequences detected in honeybees and non-<i>Apis</i> hymenopteran pollinators collected near IAPV(+) apiaries.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-22 00:20:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/810988"], "description"=>"<p>IAPV: Israeli acute paralysis virus; DWV: Deformed wing virus.</p><p>SBV: Sacbrood virus; BQCV: Black queen cell virus.</p><p>KBV: Kashmir bee virus; PA: state of Pennsylvania, USA.</p><p>NY: state of New York, USA; IL: state of Illinois, USA.</p><p>CCD: Colony collapse disorder; n =  Total number of individuals tested.</p><p>−Negative for virus;</p><p>+Positive for virus, (# of samples with virus).</p><p>*Represented by the individual detected with maximum number of co-infecting viruses.</p>", "links"=>[], "tags"=>["viruses", "hymenopteran", "pollinators", "flowering", "plants", "york", "illinois", "october"], "article_id"=>481337, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RNA_viruses_detected_in_non_Apis_hymenopteran_pollinators_collected_from_flowering_plants_in_Pennsylvania_New_York_and_Illinois_from_May_to_October_2007_/481337", "title"=>"RNA viruses detected in non-<i>Apis</i> hymenopteran pollinators collected from flowering plants in Pennsylvania, New York and Illinois from May to October 2007.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-12-22 00:22:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/811040"], "description"=>"<p>DWV: Deformed wing virus.</p><p>SBV: Sacbrood virus.</p><p>BQCV: Black queen cell virus.</p><p>*Number of individual foragers and their pollen pellets in category are indicated in parentheses.</p><p>+Positive for virus.</p><p>−Negative for virus.</p>", "links"=>[], "tags"=>["rna", "viruses", "foragers", "corresponding", "pollen", "pellets", "hives", "apiaries", "pennsylvania", "june", "september"], "article_id"=>481391, "categories"=>["Ecology", "Science Policy", "Infectious Diseases", "Virology", "Evolutionary Biology", "Medicine"], "users"=>["Rajwinder Singh", "Abby L. Levitt", "Edwin G. Rajotte", "Edward C. Holmes", "Nancy Ostiguy", "Dennis vanEngelsdorp", "W. Ian Lipkin", "Claude W. dePamphilis", "Amy L. Toth", "Diana L. Cox-Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014357.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prevalence_of_RNA_viruses_in_honey_bee_foragers_and_their_corresponding_pollen_pellets_collected_from_multiple_hives_and_apiaries_in_central_Pennsylvania_from_June_to_September_2007_/481391", "title"=>"Prevalence of RNA viruses in honey bee foragers and their corresponding pollen pellets collected from multiple hives and apiaries in central Pennsylvania from June to September 2007.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-12-22 00:23:11"}

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  • {"unique-ip"=>"59", "full-text"=>"59", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"77", "full-text"=>"85", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

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