On the Front Line: Quantitative Virus Dynamics in Honeybee (Apis mellifera L.) Colonies along a New Expansion Front of the Parasite Varroa destructor
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{"title"=>"On the Front Line: Quantitative Virus Dynamics in Honeybee (Apis mellifera L.) Colonies along a New Expansion Front of the Parasite Varroa destructor", "type"=>"journal", "authors"=>[{"first_name"=>"Fanny", "last_name"=>"Mondet", "scopus_author_id"=>"36604919800"}, {"first_name"=>"Joachim R.", "last_name"=>"de Miranda", "scopus_author_id"=>"7004471310"}, {"first_name"=>"Andre", "last_name"=>"Kretzschmar", "scopus_author_id"=>"7004382851"}, {"first_name"=>"Yves", "last_name"=>"Le Conte", "scopus_author_id"=>"6603929265"}, {"first_name"=>"Alison R.", "last_name"=>"Mercer", "scopus_author_id"=>"7102052083"}], "year"=>2014, "source"=>"PLoS Pathogens", "identifiers"=>{"sgr"=>"84953342785", "pmid"=>"25144447", "pui"=>"607916837", "isbn"=>"1553-7366", "scopus"=>"2-s2.0-84953342785", "doi"=>"10.1371/journal.ppat.1004323", "issn"=>"15537374"}, "id"=>"bb11b461-04c4-30b7-9dd2-7325341aba06", "abstract"=>"Over the past fifty years, annual honeybee (Apis mellifera) colony losses have been steadily increasing worldwide. These losses have occurred in parallel with the global spread of the honeybee parasite Varroa destructor. Indeed, Varroa mite infestations are considered to be a key explanatory factor for the widespread increase in annual honeybee colony mortality. The host-parasite relationship between honeybees and Varroa is complicated by the mite's close association with a range of honeybee viral pathogens. The 10-year history of the expanding front of Varroa infestation in New Zealand offered a rare opportunity to assess the dynamic quantitative and qualitative changes in honeybee viral landscapes in response to the arrival, spread and level of Varroa infestation. We studied the impact of de novo infestation of bee colonies by Varroa on the prevalence and titres of seven well-characterised honeybee viruses in both bees and mites, using a large-scale molecular ecology approach. We also examined the effect of the number of years since Varroa arrival on honeybee and mite viral titres. The dynamic shifts in the viral titres of black queen cell virus and Kashmir bee virus mirrored the patterns of change in Varroa infestation rates along the Varroa expansion front. The deformed wing virus (DWV) titres in bees continued to increase with Varroa infestation history, despite dropping infestation rates, which could be linked to increasing DWV titres in the mites. This suggests that the DWV titres in mites, perhaps boosted by virus replication, may be a major factor in maintaining the DWV epidemic after initial establishment. Both positive and negative associations were identified for several pairs of viruses, in response to the arrival of Varroa. These findings provide important new insights into the role of the parasitic mite Varroa destructor in influencing the viral landscape that affects honeybee colonies.", "link"=>"http://www.mendeley.com/research/front-line-quantitative-virus-dynamics-honeybee-apis-mellifera-l-colonies-along-new-expansion-front", "reader_count"=>114, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>7, "Researcher"=>30, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>8, "Student > Master"=>21, "Other"=>1, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>7, "Researcher"=>30, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>8, "Student > Master"=>21, "Other"=>1, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Environmental Science"=>11, "Biochemistry, Genetics and Molecular Biology"=>3, "Medicine and Dentistry"=>4, "Agricultural and Biological Sciences"=>80, "Neuroscience"=>1, "Veterinary Science and Veterinary Medicine"=>7, "Chemistry"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>80}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>11}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>7}}, "reader_count_by_country"=>{"New Zealand"=>1, "United States"=>3, "Serbia and Montenegro"=>1, "Brazil"=>2, "Mexico"=>2, "Germany"=>2}, "group_count"=>7}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1645863"], "description"=>"<p>Colours indicate the date <i>Varroa</i> was first confirmed in each area. Shaded tones from dark red to light yellow show the progression of the front of <i>Varroa</i> infestation. Control regions where the mite had not yet been detected are presented in white. Black dots indicate the location of the apiaries sampled in each region. The sampling transect crosses the front of infestation.</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148032, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.g001", "stats"=>{"downloads"=>7, "page_views"=>189, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Map_illustrating_the_spread_of_Varroa_across_New_Zealand_and_the_location_of_sampling_sites_/1148032", "title"=>"Map illustrating the spread of <i>Varroa</i> across New Zealand and the location of sampling sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645865"], "description"=>"<p>(<b>A</b>) Varroa prevalence. The proportion of colonies where mites could be retrieved (black) versus not retrieved (white) is presented in terms of the sampling site location and number of years <i>Varroa</i> had been detected in the area. A significant increase in <i>Varroa</i> prevalence along the sampling transect is symbolised by the red curve (GLMM, Z = 4.14, p<0.001, 27≤n≤39). (<b>B</b>) <i>Varroa</i> infestation levels according to the number of years of confirmed exposure to <i>Varroa</i>. Number of phoretic mites per 100 bees (27≤n≤39). Stars indicate significant differences between years of infestation (Pairwise post-hoc comparisons, p<0.01).</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148034, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.g002", "stats"=>{"downloads"=>3, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantitative_analysis_of_the_phoretic_Varroa_infestation_/1148034", "title"=>"Quantitative analysis of the phoretic <i>Varroa</i> infestation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645868"], "description"=>"<p>Pathogen prevalence across the front of infestation, in bee samples and <i>Varroa</i> mite samples. The percentage of colonies assigned positive for each of the seven viruses monitored is compared between <i>Varroa</i>-free areas for bee samples (white bars, n = 39), <i>Varroa</i>-infested areas for bee samples (black bars, n = 75), and <i>Varroa</i> mite samples (grey bars, n = 34). Stars indicate significant differences between proportions (Chi-square, p<0.05). Viruses are presented in decreasing order of prevalence. The average pathogen prevalence in bee samples across all regions sampled is indicated on the x-axis below the pathogen acronym.</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148037, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.g003", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Honeybee_virus_prevalence_across_the_Varroa_front_of_infestation_/1148037", "title"=>"Honeybee virus prevalence across the <i>Varroa</i> front of infestation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645870"], "description"=>"<p>(<b>A</b>) Barplot of the eigenvectors of the PCA performed on the variables measured in bees. Variables included in the Principal Component Analysis (PCA) are the titres of 5 viruses (DWV, BQCV, CBPV, KBV, SBV) and the <i>Varroa</i> infestation rate (Var). Numbers above each bar indicate the cumulative percentage of variability explained by the successive eigenvectors. The two principal eigenvectors, represented by black bars, correspond to the axes used to plot the colonies in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004323#ppat-1004323-g004\" target=\"_blank\">Figure 4.B</a>. (<b>B</b>) Scatterplot of colonies analysed by PCA for the titres of 5 viruses plus the <i>Varroa</i> infestation rates in bees (n = 191). The colony values for the two principal components are plotted, with each colony represented by a filled circle. The colonies are clustered by colour and bound by an ellipse according to the number of years since the first detection of <i>Varroa</i>, indicated by the number located at the centre of gravity of each ellipse. The ellipse covers 67% of the samples belonging to the cluster. The colour code is the same as for <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004323#ppat-1004323-g001\" target=\"_blank\">Figure 1</a>. (<b>C</b>) Barplot of the eigenvectors of the PCA performed on variables measured in bees and in <i>Varroa</i>. Variables included in the PCA are the titres of 4 virus species in bees (DWV, BQCV, KBV, SBV), titres of 4 virus species in <i>Varroa</i> (DWV.V, BQCV.V, KBV.V, SBV.V) and the <i>Varroa</i> infestation rates (Var). The numbers above each bar indicate the cumulative percentage of variability explained by the successive eigenvectors. The two principal eigenvectors, represented by the black bars, correspond to the axes used to plot the colonies in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004323#ppat-1004323-g004\" target=\"_blank\">Figure 4.D</a>. (<b>D</b>) Scatterplot of colonies analysed by PCA for virus titres in bees and mites plus the <i>Varroa</i> infestation rates (n = 83). The colony values for the two principal components are plotted, with each colony represented by a filled circle. The colonies are clustered by colour and bound by an ellipse, according to the number of years since the first detection of <i>Varroa</i>. Each ellipse covers 67% of the samples belonging to the cluster.</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148039, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.g004", "stats"=>{"downloads"=>2, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Principal_component_analyses_of_pathogen_titres_in_honeybee_and_Varroa_samples_/1148039", "title"=>"Principal component analyses of pathogen titres in honeybee and <i>Varroa</i> samples.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645872"], "description"=>"<p>(<b>A</b>) DWV titres in bees (Log<sub>10</sub> DWV copies/bee) according to the number of years of exposure to <i>Varroa</i>. A significant increase in the level of viral infestation was detected along the sampling transect (GLMM, t = 3.78, p<0.001, 30≤n≤41). (<b>B</b>) DWV titres in <i>Varroa</i> (Log<sub>10</sub> DWV copies/mite) according to the number of years of confirmed exposure to <i>Varroa</i>. A significant increase in the level of viral infestation was detected along the sampling transect (GLMM, t = 4.55, p<10<sup>−5</sup>). (<b>C</b>) BQCV titres in bees (Log<sub>10</sub> BQCV copies/bee) according to the number of years of exposure to <i>Varroa</i>. A significant increase in the level of viral infestation was detected along the sampling transect (GLMM, t = 3.35, p<0.001, 30≤n≤41). (<b>D</b>) KBV titres in bees (Log<sub>10</sub> KBV copies/bee) according to the number of years of exposure to <i>Varroa</i>. (<b>E</b>) SBV titres in bees (Log<sub>10</sub> SBV copies/bee) according to the number of years of exposure to <i>Varroa</i>. (<b>F</b>) CBPV titres in bees (Log<sub>10</sub> CBPV copies/bee) according to the number of years of exposure to <i>Varroa</i>.</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148041, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.g005", "stats"=>{"downloads"=>3, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Virus_titres_in_honeybees_and_Varroa_mites_along_the_Varroa_front_of_expansion_/1148041", "title"=>"Virus titres in honeybees and <i>Varroa</i> mites along the <i>Varroa</i> front of expansion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645873"], "description"=>"<p>The contingency tables were derived through comparing the observed incidence of co-infection with the expected values derived from the individual prevalences of each virus. For significant non-random associations (bold; p<0.05) is also indicated whether the association is positive (+), i.e. a higher incidence of co-infection than expected, or negative (−), i.e. a lower incidence of co-infection than expected.</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148042, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.t001", "stats"=>{"downloads"=>3, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Contingency_tables_showing_the_contingency_Chi_square_values_for_non_random_association_of_pairs_of_viruses_in_colonies_in_the_Varroa_free_areas_upper_section_n_39_and_in_the_Varroa_infested_areas_lower_section_n_75_/1148042", "title"=>"Contingency tables showing the contingency Chi-square values for non-random association of pairs of viruses in colonies in the <i>Varroa</i>-free areas (upper section, n = 39) and in the <i>Varroa</i>-infested areas (lower section, n = 75).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645874"], "description"=>"<p>For the <i>Varroa</i>-infested region, separate comparisons were made for the virus prevalences and co-infection in bee samples and in mite samples (n = 41). The contingency tables were derived through comparing the observed incidence of co-infection with the expected values derived from the individual prevalences in bees and mites. For significant non-random associations (bold; p<0.05) is also indicated whether the association is positive (+), i.e. a higher incidence of co-infection than expected, or negative (−), i.e. a lower incidence of co-infection than expected.</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148043, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.t002", "stats"=>{"downloads"=>6, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Contingency_table_analyses_for_virus_co_prevalence_in_both_bees_and_mite_samples_/1148043", "title"=>"Contingency table analyses for virus co-prevalence in both bees and mite samples.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645875"], "description"=>"<p>Regression analyses were performed to compare the overall titres of each of the five viruses measured on bee samples (Virus titres in bees) with either the overall level of infestation by <i>Varroa</i> (<i>Varroa</i> infestation levels) or with the overall titres of each of the five viruses measured on <i>Varroa</i> samples (Virus titres in mites). Regressions were run on Log<sub>10</sub> transformed data. R-squared with associated p-values<0.05 are indicated in bold. All significant regressions presented positive correlations (r>0).</p>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148044, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004323.t003", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_the_regression_analyses_/1148044", "title"=>"Results of the regression analyses.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-08-21 04:13:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1645877", "https://ndownloader.figshare.com/files/1645878"], "description"=>"<div><p>Over the past fifty years, annual honeybee (<i>Apis mellifera</i>) colony losses have been steadily increasing worldwide. These losses have occurred in parallel with the global spread of the honeybee parasite <i>Varroa destructor</i>. Indeed, <i>Varroa</i> mite infestations are considered to be a key explanatory factor for the widespread increase in annual honeybee colony mortality. The host-parasite relationship between honeybees and <i>Varroa</i> is complicated by the mite's close association with a range of honeybee viral pathogens. The 10-year history of the expanding front of <i>Varroa</i> infestation in New Zealand offered a rare opportunity to assess the dynamic quantitative and qualitative changes in honeybee viral landscapes in response to the arrival, spread and level of <i>Varroa</i> infestation. We studied the impact of <i>de novo</i> infestation of bee colonies by <i>Varroa</i> on the prevalence and titres of seven well-characterised honeybee viruses in both bees and mites, using a large-scale molecular ecology approach. We also examined the effect of the number of years since <i>Varroa</i> arrival on honeybee and mite viral titres. The dynamic shifts in the viral titres of black queen cell virus and Kashmir bee virus mirrored the patterns of change in <i>Varroa</i> infestation rates along the <i>Varroa</i> expansion front. The deformed wing virus (DWV) titres in bees continued to increase with <i>Varroa</i> infestation history, despite dropping infestation rates, which could be linked to increasing DWV titres in the mites. This suggests that the DWV titres in mites, perhaps boosted by virus replication, may be a major factor in maintaining the DWV epidemic after initial establishment. Both positive and negative associations were identified for several pairs of viruses, in response to the arrival of <i>Varroa</i>. These findings provide important new insights into the role of the parasitic mite <i>Varroa destructor</i> in influencing the viral landscape that affects honeybee colonies.</p></div>", "links"=>[], "tags"=>["Quantitative Virus Dynamics", "mite Varroa destructor", "Varroa infestation rates", "Varroa infestation", "New Expansion Front", "Varroa expansion front", "Varroa mite infestations", "honeybee parasite Varroa destructor", "Varroa infestation history", "Parasite Varroa destructor", "honeybee colony mortality", "DWV titres", "Kashmir bee virus", "queen cell virus"], "article_id"=>1148046, "categories"=>["Biological Sciences"], "users"=>["Fanny Mondet", "Joachim R. de Miranda", "André Kretzschmar", "Yves Le Conte", "Alison R. Mercer"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004323.s001", "https://dx.doi.org/10.1371/journal.ppat.1004323.s002"], "stats"=>{"downloads"=>15, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/On_the_Front_Line_Quantitative_Virus_Dynamics_in_Honeybee_Apis_mellifera_L_Colonies_along_a_New_Expansion_Front_of_the_Parasite_Varroa_destructor_/1148046", "title"=>"On the Front Line: Quantitative Virus Dynamics in Honeybee (<i>Apis mellifera</i> L.) Colonies along a New Expansion Front of the Parasite <i>Varroa destructor</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-08-21 04:13:36"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
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  • {"unique-ip"=>"34", "full-text"=>"26", "pdf"=>"16", "abstract"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
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  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"29", "full-text"=>"33", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"16", "full-text"=>"19", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"19", "full-text"=>"19", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"2", "cited-by"=>"1", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"25", "full-text"=>"23", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"14", "full-text"=>"11", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"15", "full-text"=>"13", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
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  • {"unique-ip"=>"17", "full-text"=>"10", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"20", "full-text"=>"24", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
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Relative Metric

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