Evidence for a Novel Marine Harmful Algal Bloom: Cyanotoxin (Microcystin) Transfer from Land to Sea Otters
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{"title"=>"Evidence for a novel marine harmful algal bloom: Cyanotoxin (microcystin) transfer from land to sea otters", "type"=>"journal", "authors"=>[{"first_name"=>"Melissa A.", "last_name"=>"Miller", "scopus_author_id"=>"55553727415"}, {"first_name"=>"Raphael M.", "last_name"=>"Kudela", "scopus_author_id"=>"7003923978"}, {"first_name"=>"Abdu", "last_name"=>"Mekebri", "scopus_author_id"=>"8875047600"}, {"first_name"=>"Dave", "last_name"=>"Crane", "scopus_author_id"=>"7103272028"}, {"first_name"=>"Stori C.", "last_name"=>"Oates", "scopus_author_id"=>"36537773500"}, {"first_name"=>"M. Timothy", "last_name"=>"Tinker", "scopus_author_id"=>"35588232500"}, {"first_name"=>"Michelle", "last_name"=>"Staedler", "scopus_author_id"=>"6506539390"}, {"first_name"=>"Woutrina A.", "last_name"=>"Miller", "scopus_author_id"=>"8552521600"}, {"first_name"=>"Sharon", "last_name"=>"Toy-Choutka", "scopus_author_id"=>"23570200000"}, {"first_name"=>"Clare", "last_name"=>"Dominik", "scopus_author_id"=>"36536769900"}, {"first_name"=>"Dane", "last_name"=>"Hardin", "scopus_author_id"=>"7005216517"}, {"first_name"=>"Gregg", "last_name"=>"Langlois", "scopus_author_id"=>"6701644304"}, {"first_name"=>"Michael", "last_name"=>"Murray", "scopus_author_id"=>"35374023200"}, {"first_name"=>"Kim", "last_name"=>"Ward", "scopus_author_id"=>"36769664800"}, {"first_name"=>"David A.", "last_name"=>"Jessup", "scopus_author_id"=>"7006841976"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"20844747", "doi"=>"10.1371/journal.pone.0012576", "sgr"=>"77958593142", "isbn"=>"1932-6203", "scopus"=>"2-s2.0-77958593142", "issn"=>"19326203", "pui"=>"359838965"}, "id"=>"969dbd5b-4453-334e-8f4f-22e24169aeea", "abstract"=>"\"Super-blooms\" of cyanobacteria that produce potent and environmentally persistent biotoxins (microcystins) are an emerging global health issue in freshwater habitats. Monitoring of the marine environment for secondary impacts has been minimal, although microcystin-contaminated freshwater is known to be entering marine ecosystems. Here we confirm deaths of marine mammals from microcystin intoxication and provide evidence implicating land-sea flow with trophic transfer through marine invertebrates as the most likely route of exposure. This hypothesis was evaluated through environmental detection of potential freshwater and marine microcystin sources, sea otter necropsy with biochemical analysis of tissues and evaluation of bioaccumulation of freshwater microcystins by marine invertebrates. Ocean discharge of freshwater microcystins was confirmed for three nutrient-impaired rivers flowing into the Monterey Bay National Marine Sanctuary, and microcystin concentrations up to 2,900 ppm (2.9 million ppb) were detected in a freshwater lake and downstream tributaries to within 1 km of the ocean. Deaths of 21 southern sea otters, a federally listed threatened species, were linked to microcystin intoxication. Finally, farmed and free-living marine clams, mussels and oysters of species that are often consumed by sea otters and humans exhibited significant biomagnification (to 107 times ambient water levels) and slow depuration of freshwater cyanotoxins, suggesting a potentially serious environmental and public health threat that extends from the lowest trophic levels of nutrient-impaired freshwater habitat to apex marine predators. Microcystin-poisoned sea otters were commonly recovered near river mouths and harbors and contaminated marine bivalves were implicated as the most likely source of this potent hepatotoxin for wild otters. This is the first report of deaths of marine mammals due to cyanotoxins and confirms the existence of a novel class of marine \"harmful algal bloom\" in the Pacific coastal environment; that of hepatotoxic shellfish poisoning (HSP), suggesting that animals and humans are at risk from microcystin poisoning when consuming shellfish harvested at the land-sea interface.", "link"=>"http://www.mendeley.com/research/evidence-novel-marine-harmful-algal-bloom-cyanotoxin-microcystin-transfer-land-sea-otters-6", "reader_count"=>183, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>8, "Librarian"=>2, "Researcher"=>40, "Student > Doctoral Student"=>6, "Student > Ph. D. 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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/831288"], "description"=>"1<p>nd  =  microcystin concentration was below minimum detection limits on liquid chromatography-tandem mass spectrophotometry.</p>", "links"=>[], "tags"=>["microcystin", "concentrations", "microcystin-positive", "otters", "captive"], "article_id"=>501632, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.t001", "stats"=>{"downloads"=>2, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stranding_information_and_microcystin_MCY_concentrations_ppb_wet_weight_for_wild_microcystin_positive_sea_otters_and_captive_controls_/501632", "title"=>"Stranding information and microcystin (MCY) concentrations (ppb wet weight) for wild, microcystin-positive sea otters and captive controls.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 23:34:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/830556"], "description"=>"<p>Note spatial association of sea otter strandings with coastal locations of river mouths, harbors, coastal ponds and embayments. Habitat utilization distributions for 4 radio-tagged, microcystin-poisoned otters are plotted as kernel density distributions fit to daily re-sighting locations (red shading, with regions of most intense shading corresponding to the habitats most frequently utilized by affected animals). Locations of freshwater samples collected during a “Super-bloom” of <i>Microcystis</i> in 2007 are indicated by green circles, with numbers that correspond with the microcystin concentrations listed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0012576#pone-0012576-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["monterey", "otters", "microcystin", "intoxication"], "article_id"=>500900, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g004", "stats"=>{"downloads"=>6, "page_views"=>51, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Map_of_Monterey_Bay_showing_distribution_of_sea_otters_dying_due_to_microcystin_intoxication_yellow_circles_/500900", "title"=>"Map of Monterey Bay showing distribution of sea otters dying due to microcystin intoxication (yellow circles).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:31:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/831034"], "description"=>"<p>Note the spatial overlap of all 4 home ranges on the north central Monterey Peninsula near Monterey Harbor (bracket): This harbor appears to be one of several high-risk locations for microcystin poisoning of sea otters, possibly due to prolonged retention of microcystin-contaminated water.</p>", "links"=>[], "tags"=>["ranges", "tagged", "otters", "died", "microcystin"], "article_id"=>501382, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g007", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overlapping_home_ranges_of_4_tagged_southern_sea_otters_that_died_due_to_microcystin_intoxication_/501382", "title"=>"Overlapping home ranges of 4 tagged southern sea otters that died due to microcystin intoxication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:33:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/831144"], "description"=>"1<p>All tanks were flushed continually with clean seawater beginning at 96 H post-exposure.</p>2<p>n = 1 or 2 pooled invertebrates of each species at each sample point, except snails, where n = 7.</p>3<p>nd  =  microcystin concentration was below minimum detection limits on liquid chromatography-tandem mass spectrophotometry.</p>4<p>---  =  not tested.</p>5<p>Average microcystin-LR concentration across the top, middle and bottom of Tank 3 at each time point.</p>", "links"=>[], "tags"=>["lr", "concentrations", "invertebrate", "gastrointestinal", "tissues", "microcystin", "intervals"], "article_id"=>501480, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.t003", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microcystin_LR_concentrations_ppb_wet_weight_in_marine_invertebrate_gastrointestinal_tissues_collected_from_Tank_3_high_microcystin_exposure_tank_at_various_time_intervals_post_exposure_1_/501480", "title"=>"Microcystin LR concentrations (ppb wet weight) in marine invertebrate gastrointestinal tissues collected from Tank 3 (high microcystin exposure tank) at various time intervals post-exposure<sup>1</sup>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 23:34:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/830909"], "description"=>"<p>A.) Gross appearance of normal sea otter liver. B.) Swollen, hemorrhagic liver from a sea otter that died due to microcystin intoxication. C.) Microscopic view of normal sea otter liver, D.) Microscopic appearance of liver from an otter that died due to microcystin intoxication, demonstrating hepatocyte swelling, cytoplasmic vacuolation, necrosis or apoptosis and parenchymal hemorrhage. Small greenish-gold accumulations of bile are apparent at the upper left and center-right portions of the photomicrograph.</p>", "links"=>[], "tags"=>["microscopic", "hepatic", "lesions", "microcystin", "intoxication", "compared"], "article_id"=>501258, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g006", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gross_and_microscopic_hepatic_lesions_of_microcystin_intoxication_in_sea_otters_compared_to_control_livers_/501258", "title"=>"Gross and microscopic hepatic lesions of microcystin intoxication in sea otters, compared to control livers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:33:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/831220"], "description"=>"1<p>All samples from Tank 1 (seawater control) tested negative for microcystin-LR. All 3 tanks were flushed with fresh seawater starting 96 H postexposure).</p>2<p>nd  =  microcystin concentration was below minimum detection limits on liquid chromatography-tandem mass spectrophotometry.</p>", "links"=>[], "tags"=>["concentrations", "seawater", "tanks", "varying", "postexposure"], "article_id"=>501551, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.t002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microcystin_LR_concentrations_ppb_at_the_top_middle_and_bottom_of_seawater_tanks_at_two_exposure_concentrations_Tank_2_and_Tank_3_1_and_varying_postexposure_intervals_/501551", "title"=>"Microcystin-LR concentrations (ppb) at the top, middle, and bottom of seawater tanks at two exposure concentrations (Tank 2 and Tank 3<sup>1</sup>) and varying postexposure intervals.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 23:34:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/830236"], "description"=>"<p>Inset: Sample of surface water collected during a “super-bloom” of <i>Microcystis</i> in Pinto Lake in fall, 2007 (Caution: Nitrile gloves and other appropriate personal protective equipment should be used to prevent dermal contact when collecting environmental samples of <i>Microcystis</i> and microcystins). Main figure: Time-matched microcystin-LA concentrations (ppb) in samples from Pinto Lake, just downstream in Corralitos Creek and the receiving waters of the Pajaro River within 1 km of Monterey Bay. Asterisks (*) indicate sampling locations where <i>Microcystis</i> was detected microscopically.</p>", "links"=>[], "tags"=>["freshwater", "contamination", "microcystins"], "article_id"=>500564, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g001", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tracing_freshwater_contamination_by_microcystins_from_land_to_sea_/500564", "title"=>"Tracing freshwater contamination by microcystins from land-to-sea.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:29:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/830740"], "description"=>"<p>A.) Wild southern sea otter (<i>Enhydra lutris nerei</i>s) consuming a clam in Elkhorn Slough, Monterey Bay. B.) Diffuse icterus of oral mucous membranes of an otter poisoned by microcystin, due to severe hepatic damage and elevated plasma bilirubin. C.) Severe icterus of cartilage at the costochondral junction in a sea otter that died due to microcystin intoxication.</p>", "links"=>[], "tags"=>["detection", "otter", "tissues", "was", "linked", "bivalve"], "article_id"=>501078, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g005", "stats"=>{"downloads"=>4, "page_views"=>117, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microcystin_detection_in_sea_otter_tissues_was_linked_to_bivalve_consumption_liver_damage_and_icterus_/501078", "title"=>"Microcystin detection in sea otter tissues was linked to bivalve consumption, liver damage and icterus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:32:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/830419"], "description"=>"<p>Comparison of microcystin (MCY-LR) detection in fresh water using intermittent “grab” sampling (sample periods indicated by black circles) and SPATT (solid line indicating weekly averaged toxin values) in Pinto Lake, demonstrating the higher sensitivity of SPATT for microcystin detection. Grab samples were collected at the beginning of each weekly SPATT deployment, and from the same sample location, so each 7-day integrated SPATT deployment is bracketed by two grab samples.</p>", "links"=>[], "tags"=>["microcystin", "detection", "samples", "adsorption", "toxin", "tracking"], "article_id"=>500762, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g003", "stats"=>{"downloads"=>5, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variation_in_microcystin_detection_between_conventional_8220_grab_8221_samples_and_Solid_Phase_Adsorption_Toxin_Tracking_SPATT_/500762", "title"=>"Variation in microcystin detection between conventional “grab” samples and Solid Phase Adsorption Toxin Tracking (SPATT).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:30:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/830326"], "description"=>"<p>SPATT adsorption characteristics for microcystin were tested in the laboratory using Pinto Lake water amended with a known quantity of microcystin-LR. A control sample (open symbols) showed no change in microcystin concentration over time; In contrast, SPATT HP20 resin-based samplers (solid symbols: error bars represent standard deviation of 3 replicates) show rapid microcystin adsorption, with near-total depletion of microcystins from a controlled volume of water within <24 hours.</p>", "links"=>[], "tags"=>["adsorption", "toxin", "tracking", "sampler", "characteristics", "freshwater"], "article_id"=>500668, "categories"=>["Neuroscience", "Marine Biology", "Cancer", "Virology", "Microbiology", "Inorganic Chemistry"], "users"=>["Melissa A. Miller", "Raphael M. Kudela", "Abdu Mekebri", "Dave Crane", "Stori C. Oates", "M. Timothy Tinker", "Michelle Staedler", "Woutrina A. Miller", "Sharon Toy-Choutka", "Clare Dominik", "Dane Hardin", "Gregg Langlois", "Michael Murray", "Kim Ward", "David A. Jessup"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012576.g002", "stats"=>{"downloads"=>4, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evaluation_of_Solid_Phase_Adsorption_Toxin_Tracking_SPATT_sampler_adsorption_characteristics_for_freshwater_microcystins_/500668", "title"=>"Evaluation of Solid Phase Adsorption Toxin Tracking (SPATT) sampler adsorption characteristics for freshwater microcystins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 23:30:06"}

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  • {"unique-ip"=>"21", "full-text"=>"20", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"16", "full-text"=>"14", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"18", "full-text"=>"24", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
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  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"16", "full-text"=>"14", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"25", "full-text"=>"27", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"31", "full-text"=>"33", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"27", "full-text"=>"34", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"15", "full-text"=>"14", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"28", "full-text"=>"29", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"24", "full-text"=>"23", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"43", "full-text"=>"53", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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Relative Metric

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