Malaria Mosquitoes Attracted by Fatal Fungus
Publication Date
May 01, 2013
Journal
PLOS ONE
Authors
Justin George, Nina E. Jenkins, Simon Blanford, Matthew B. Thomas, et al
Volume
8
Issue
5
Pages
e62632
DOI
https://dx.plos.org/10.1371/journal.pone.0062632
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0062632
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23658757
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3641063
Europe PMC
http://europepmc.org/abstract/MED/23658757
Web of Science
000319167000064
Scopus
84877020532
Mendeley
http://www.mendeley.com/research/malaria-mosquitoes-attracted-fatal-fungus
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Mendeley | Further Information

{"title"=>"Malaria Mosquitoes Attracted by Fatal Fungus", "type"=>"journal", "authors"=>[{"first_name"=>"Justin", "last_name"=>"George", "scopus_author_id"=>"56555777300"}, {"first_name"=>"Nina E.", "last_name"=>"Jenkins", "scopus_author_id"=>"7201534117"}, {"first_name"=>"Simon", "last_name"=>"Blanford", "scopus_author_id"=>"6601979003"}, {"first_name"=>"Matthew B.", "last_name"=>"Thomas", "scopus_author_id"=>"35612365500"}, {"first_name"=>"Thomas C.", "last_name"=>"Baker", "scopus_author_id"=>"7402604731"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84877020532", "doi"=>"10.1371/journal.pone.0062632", "pui"=>"368847444", "pmid"=>"23658757", "scopus"=>"2-s2.0-84877020532", "issn"=>"19326203", "isbn"=>"10.1371/journal.pone.0062632"}, "id"=>"e6cb118a-a695-346f-b6fe-ed4f0bf3caa1", "abstract"=>"Insect-killing fungi such as Beauveria bassiana are being evaluated as possible active ingredients for use in novel biopesticides against mosquito vectors that transmit malaria. Fungal pathogens infect through contact and so applications of spores to surfaces such as walls, nets, or other resting sites provide possible routes to infect mosquitoes in and around domestic dwellings. However, some insects can detect and actively avoid fungal spores to reduce infection risk. If true for mosquitoes, such behavior could render the biopesticide approach ineffective. Here we find that the spores of B. bassiana are highly attractive to females of Anopheles stephensi, a major anopheline mosquito vector of human malaria in Asia. We further find that An. stephensi females are preferentially attracted to dead and dying caterpillars infected with B. bassiana, landing on them and subsequently becoming infected with the fungus. Females are also preferentially attracted to cloth sprayed with oil-formulated B. bassiana spores, with 95% of the attracted females becoming infected after a one-minute visit on the cloth. This is the first report of an insect being attracted to a lethal fungal pathogen. The exact mechanisms involved in this behavior remain unclear. Nonetheless, our results indicate that biopesticidal formulations comprising B. bassiana spores will be conducive to attraction and on-source visitation by malaria vectors.", "link"=>"http://www.mendeley.com/research/malaria-mosquitoes-attracted-fatal-fungus", "reader_count"=>53, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>8, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>8, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>5, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>35, "Design"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemical Engineering"=>1, "Chemistry"=>1, "Social Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>35}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>5}, "Chemical Engineering"=>{"Chemical Engineering"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "Mexico"=>1, "United Kingdom"=>1, "Germany"=>1, "Indonesia"=>1, "India"=>1}, "group_count"=>4}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1050813"], "description"=>"<p><b>A)</b> Percentage of females attracted to 50 mg of dried spores of <i>B. bassiana, M. anisopliae,</i> or <i>Penicillium</i> spp. placed on a filter paper disc (dark bars) versus a blank disc (light bars) (N = 60 females in each comparison); <b>B)</b> Percentage of females attracted to the arm containing <i>B. bassiana</i> spores (dark bars) compared to the arm containing spores of either <i>M. anisopliae</i> or <i>Penicillium</i> (light bars) (N = 60 females in each comparison). Brackets denote ±95% binomial confidence intervals (C.I.). Asterisks indicate significant differences between attraction to treatment choice-pairs (Chi-square 2×2 test of independence; **P≤0.01; ***P≤0.001).</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "fungal", "spores"], "article_id"=>695650, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dried_fungal_spores_of_B_bassiana_and_M_anisopliae_are_attractive_to_female_An_stephensi_but_spores_of_B_bassiana_are_more_attractive_than_those_of_M_anisopliae_or_Penicillium_spp_/695650", "title"=>"Dried fungal spores of <i>B. bassiana</i> and <i>M. anisopliae</i> are attractive to female <i>An. stephensi</i>, but spores of <i>B. bassiana</i> are more attractive than those of <i>M. anisopliae</i> or <i>Penicillium</i> spp.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050814"], "description"=>"<p>Following attraction to the caterpillars, the females land and probe them, sometimes engorging on caterpillar haemolymph (unpublished data). <b>A</b>) A healthy, uninfected <i>H. subflexa</i> 4<sup>th</sup>-instar caterpillar. <b>B</b>) Several dead, sporulating <i>H. subflexa</i> caterpillars that had attracted <i>An. stephensi</i> females.</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "females", "released", "groups", "dead-sporulating"], "article_id"=>695651, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g002", "stats"=>{"downloads"=>3, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Photographs_of_typical_An_stephensi_females_when_released_in_groups_in_the_presence_of_either_live_A_or_dead_sporulating_B_H_subflexa_caterpillars_/695651", "title"=>"Photographs of typical <i>An. stephensi</i> females when released in groups in the presence of either live (A) or dead-sporulating (B) <i>H. subflexa</i> caterpillars.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050816"], "description"=>"<p>Percentage (dark bars) of individually tested <i>An. stephensi</i> females that flew upwind in the Y-tube in response to sporulating cadavers of: (left) <i>H. subflexa</i>; (center) <i>M. sexta</i>: and (right) <i>An. stephensi</i> females that had died following <i>B. bassiana</i> infection. Light bars indicate attraction to the alternate Y-tube arm containing uninfected dead caterpillars or mosquitoes. Brackets denote ±95% binomial confidence intervals (C.I.). Asterisks indicate significant differences between attraction to treatment choice-pairs (Chi-square 2×2 test of independence; ***P≤0.001; N = 60).</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "cadavers", "females", "uninfected"], "article_id"=>695653, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g003", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_B_bassiana_sporulating_insect_cadavers_are_more_attractive_to_An_stephensi_females_than_uninfected_cadavers_/695653", "title"=>"<i>B. bassiana</i>-sporulating insect cadavers are more attractive to <i>An. stephensi</i> females than uninfected cadavers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050817"], "description"=>"<p>N = 46 and 47 females out of 60 tested that contacted the sporulating vs. the healthy-live caterpillars, respectively. Brackets denote ±95% binomial confidence intervals (C.I.). Asterisks indicate a significant difference of infection (***P≤0.001, Chi-square 2×2 test of independence).</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "females", "infected", "spore-laden", "mosquitoes", "contacting", "sporulating", "caterpillars", "uninfected", "exhibited", "sporulation"], "article_id"=>695654, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g004", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_An_stephensi_females_become_infected_with_B_bassiana_following_contact_with_spore_laden_caterpillars_74_34_46_of_mosquitoes_contacting_the_sporulating_caterpillars_vs_8_4_47_contacting_the_uninfected_caterpillars_exhibited_B_bassiana_sporulation_after_de/695654", "title"=>"<b><i>An. stephensi</i></b> females become infected with <i>B. bassiana</i> following contact with spore-laden caterpillars.74% (34/46) of mosquitoes contacting the sporulating caterpillars vs. 8% (4/47) contacting the uninfected caterpillars exhibited <i>B. bassiana</i> sporulation after death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050818"], "description"=>"<p>(Left) percentage of female <i>An. stephensi</i> flying upwind to cadavers of 4<sup>th</sup>-instar <i>H. subflexa</i> caterpillars that were infected with <i>B. bassiana</i> but not sporulating (dark bars) or were uninfected (light bars). (Center) percentage of females flying upwind to cadavers of <i>H. subflexa</i> caterpillars that either exhibited <i>B. bassiana</i> spores (dark bars) or were uninfected (light bars). (Right) percentage flying upwind to <i>B. bassiana</i>-infected but non-sporulating live <i>H. subflexa</i> caterpillars (dark bars) compared to uninfected live caterpillars (light bars). (***P<0.001; Chi-square 2×2 test of independence; N = 90).</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "females", "attracted", "y-tube", "experiments", "caterpillars", "uninfected", "sporulating"], "article_id"=>695655, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g005", "stats"=>{"downloads"=>3, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_An_stephensi_females_are_significantly_more_attracted_in_Y_tube_choice_experiments_to_B_bassiana_infected_caterpillars_than_to_uninfected_caterpillars_whether_they_are_alive_or_dead_sporulating_or_non_sporulating_/695655", "title"=>"<i>An. stephensi</i> females are significantly more attracted in Y-tube choice experiments to <i>B. bassiana</i>-infected caterpillars than to uninfected caterpillars, whether they are alive or dead, sporulating or non-sporulating.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050820"], "description"=>"<p>Photographs of <i>An. stephensi</i> females on sporulating and non-sporulating caterpillar cadavers after having flown upwind to them in the Y-tube olfactometer assays: A) female probing infected non-sporulating cadavers of <i>Heliothis subflexa</i> (B) female probing infected sporulating cadavers of <i>Heliothis subflexa</i> C) female probing infected sporulating cadaver of <i>Manduca sexta.</i></p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "females", "sporulating", "non-sporulating", "caterpillar", "cadavers", "having", "flown", "upwind", "y-tube", "olfactometer", "probing", "infected", "cadaver"], "article_id"=>695657, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g006", "stats"=>{"downloads"=>5, "page_views"=>123, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Photographs_of_An_stephensi_females_on_sporulating_and_non_sporulating_caterpillar_cadavers_after_having_flown_upwind_to_them_in_the_Y_tube_olfactometer_assays_A_female_probing_infected_non_sporulating_cadavers_of_Heliothis_subflexa_B_female_probing_infe/695657", "title"=>"Photographs of <i>An. stephensi</i> females on sporulating and non-sporulating caterpillar cadavers after having flown upwind to them in the Y-tube olfactometer assays: A) female probing infected non-sporulating cadavers of <i>Heliothis subflexa</i> (B) female probing infected sporulating cadavers of <i>Heliothis subflexa</i> C) female probing infected sporulating cadaver of <i>Manduca sexta.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050821"], "description"=>"<p>GLM was used to examine the difference between treatments (Uninfected and <i>Beauveria</i> infected, N = 7).</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "metabolic", "produced", "infected", "uninfected", "instar", "caterpillars", "days", "killed"], "article_id"=>695658, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g007", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Basal_Metabolic_Rate_BMR_measurements_showing_the_mean_S_E_amount_of_CO_2_ml_CO_2_hr_gram_of_body_weight_produced_by_infected_and_uninfected_Heliothis_subflexa_fourth_instar_caterpillars_during_the_days_after_infection_before_they_were_killed_by_Beauveri/695658", "title"=>"Basal Metabolic Rate (BMR) measurements showing the mean (± S.E.) amount of CO<sub>2</sub> (ml CO<sub>2</sub>/hr/gram of body weight) produced by infected and uninfected <i>Heliothis subflexa</i> fourth instar caterpillars during the days after infection, before they were killed by <i>Beauveria bassiana</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1050822"], "description"=>"<p>Females collected from the <i>B. bassiana</i>-sprayed cloth following a 1-minute contact duration exhibited a significantly higher rate of <i>B. bassiana</i> infection (95%) than did females allowed a 1-minute contact period (0%) with the oil-only-sprayed cloth. Brackets denote ±95% binomial confidence intervals. Asterisks indicate significant differences between landing on, and infection by, the treatment choice-pairs (Chi-square 2×2 test of independence; ***P<0.001; N = 95 mosquitoes tested for each treatment).</p>", "links"=>[], "tags"=>["Pest control", "ecology", "Behavioral ecology", "Chemical ecology", "Evolutionary ecology", "Evolutionary biology", "Animal behavior", "sprayed", "oil-formulated", "spores", "causes", "females", "upwind", "oil-only-sprayed"], "article_id"=>695659, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Justin George", "Nina E. Jenkins", "Simon Blanford", "Matthew B. Thomas", "Thomas C. Baker"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062632.g008", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cloth_sprayed_with_oil_formulated_spores_of_B_bassiana_causes_An_stephensi_females_to_fly_upwind_and_land_on_it_Left_dark_bars_more_than_on_an_oil_only_sprayed_cloth_Left_light_bars_/695659", "title"=>"Cloth sprayed with oil-formulated spores of <i>B. bassiana</i> causes <i>An. stephensi</i> females to fly upwind and land on it (Left; dark bars), more than on an oil-only-sprayed cloth (Left; light bars).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-01 01:34:19"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"14", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"18", "full-text"=>"16", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"5", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
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  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
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  • {"unique-ip"=>"12", "full-text"=>"18", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"15", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"14", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"20", "full-text"=>"22", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"15", "full-text"=>"17", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"10", "full-text"=>"14", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"10", "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"=>"6"}
  • {"unique-ip"=>"19", "full-text"=>"17", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"19", "full-text"=>"22", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"20", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"13", "full-text"=>"16", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"40", "full-text"=>"48", "pdf"=>"3", "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

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[275, 472, 605, 720, 822, 921, 1013, 1106, 1200, 1289, 1378, 1459, 1531]}, {"subject_area"=>"/Biology and life sciences/Mycology", "average_usage"=>[318, 546, 681, 824, 962, 1073, 1181, 1310, 1465, 1570, 1678, 1771, 1864]}, {"subject_area"=>"/Medicine and health sciences/Epidemiology", "average_usage"=>[263, 452, 568, 671, 758, 847, 921, 1023, 1101, 1187, 1264, 1340, 1394]}, {"subject_area"=>"/Medicine and health sciences/Infectious diseases", "average_usage"=>[297, 523, 655, 765, 866, 971, 1070, 1159, 1256, 1337, 1424, 1496, 1568]}]}
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