Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host
Publication Date
November 27, 2012
Journal
PLOS Biology
Authors
Erik H. Poelman, Maaike Bruinsma, Feng Zhu, Berhane T. Weldegergis, et al
Volume
10
Issue
11
Pages
e1001435
DOI
https://dx.plos.org/10.1371/journal.pbio.1001435
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.1001435
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23209379
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3507920
Europe PMC
http://europepmc.org/abstract/MED/23209379
Web of Science
000311888300017
Scopus
84870279235
Mendeley
http://www.mendeley.com/research/hyperparasitoids-herbivoreinduced-plant-volatiles-locate-parasitoid-host
Events
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Mendeley | Further Information

{"title"=>"Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host", "type"=>"journal", "authors"=>[{"first_name"=>"Erik H.", "last_name"=>"Poelman", "scopus_author_id"=>"55904118000"}, {"first_name"=>"Maaike", "last_name"=>"Bruinsma", "scopus_author_id"=>"56284546500"}, {"first_name"=>"Feng", "last_name"=>"Zhu", "scopus_author_id"=>"55443442800"}, {"first_name"=>"Berhane T.", "last_name"=>"Weldegergis", "scopus_author_id"=>"22942807900"}, {"first_name"=>"Aline E.", "last_name"=>"Boursault", "scopus_author_id"=>"55505895100"}, {"first_name"=>"Yde", "last_name"=>"Jongema", "scopus_author_id"=>"23489019700"}, {"first_name"=>"Joop J A", "last_name"=>"van Loon", "scopus_author_id"=>"7103050745"}, {"first_name"=>"Louise E M", "last_name"=>"Vet", "scopus_author_id"=>"7003530925"}, {"first_name"=>"Jeffrey A.", "last_name"=>"Harvey", "scopus_author_id"=>"55708310400"}, {"first_name"=>"Marcel", "last_name"=>"Dicke", "scopus_author_id"=>"7005100613"}], "year"=>2012, "source"=>"PLoS Biology", "identifiers"=>{"sgr"=>"84870279235", "doi"=>"10.1371/journal.pbio.1001435", "pui"=>"366156149", "pmid"=>"23209379", "scopus"=>"2-s2.0-84870279235", "issn"=>"15449173", "isbn"=>"1545-7885 (Electronic)\\r1544-9173 (Linking)"}, "id"=>"e5b40a6d-1286-35e6-bc1f-3f5fcf984761", "abstract"=>"Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.", "link"=>"http://www.mendeley.com/research/hyperparasitoids-herbivoreinduced-plant-volatiles-locate-parasitoid-host", "reader_count"=>169, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>9, "Librarian"=>1, "Student > Doctoral Student"=>12, "Researcher"=>33, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>7, "Student > Master"=>29, "Other"=>6, "Student > Bachelor"=>20, "Lecturer"=>2, "Professor"=>11}, "reader_count_by_user_role"=>{"Unspecified"=>5, "Professor > Associate Professor"=>9, "Librarian"=>1, "Student > Doctoral Student"=>12, "Researcher"=>33, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>7, "Student > Master"=>29, "Other"=>6, "Student > Bachelor"=>20, "Lecturer"=>2, "Professor"=>11}, "reader_count_by_subject_area"=>{"Unspecified"=>11, "Environmental Science"=>8, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>136, "Neuroscience"=>3, "Veterinary Science and Veterinary Medicine"=>1, "Physics and Astronomy"=>1, "Chemistry"=>3, "Social Sciences"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>3}, "Chemistry"=>{"Chemistry"=>3}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>136}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>11}, "Environmental Science"=>{"Environmental Science"=>8}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>2, "Netherlands"=>1, "United States"=>3, "Japan"=>2, "Italy"=>1, "Mexico"=>1, "Slovakia"=>1, "France"=>1, "Peru"=>1, "Germany"=>3, "India"=>3}, "group_count"=>4}

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/536645"], "description"=>"<p>Plants were either undamaged (red, UD), damaged with two unparasitized <i>Pieris rapae</i> caterpillars (blue, PR), or <i>P. rapae</i> caterpillars parasitized by <i>Cotesia rubecula</i> (orange, PR-CR) or <i>C. glomerata</i> (green, PR-CG). Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "comparisons", "volatile", "blends", "plants", "herbivory", "parasitized", "unparasitized"], "article_id"=>207111, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g005", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PLS_DA_plot_based_on_comparisons_among_volatile_blends_of_Brassica_oleracea_plants_under_herbivory_by_parasitized_or_unparasitized_caterpillars_/207111", "title"=>"PLS-DA plot based on comparisons among volatile blends of <i>Brassica oleracea</i> plants under herbivory by parasitized or unparasitized caterpillars.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:43:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/537130"], "description"=>"<p>Boldface type presents significant effects (α = 0.05) in a GLM model with a binomial distribution.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "induction", "parasitoid", "cocoons", "contained", "hyperparasitoid"], "article_id"=>207607, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.t003", "stats"=>{"downloads"=>3, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_plant_induction_treatment_on_the_fraction_of_primary_parasitoid_cocoons_per_plant_that_contained_any_hyperparasitoid_in_the_field_/207607", "title"=>"The effect of plant induction treatment on the fraction of primary parasitoid cocoons per plant that contained any hyperparasitoid in the field.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 19:46:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/536526"], "description"=>"<p>Preference of the hyperparasitoid <i>Lysibia nana</i> for herbivore-induced plant volatiles was tested by using a full factorial design of two-choice olfactometer tests including pair-wise comparisons of the treatments: undamaged plants (white bars), <i>Pieris rapae</i> damaged plants (light grey), plants damaged by <i>Pieris rapae</i> caterpillars parasitized by <i>Cotesia glomerata</i> (dark grey bars), or plants damaged by <i>Pieris rapae</i> caterpillars parasitized by <i>C. rubecula</i> (black bars). The two lowest pairs of bars show the preference of <i>L. nana</i> for plants treated with caterpillar regurgitant. The first pair shows hyperparasitoid preference when plants are artificially damaged and regurgitant of unparasitized (light grey) or parasitized (dark grey) caterpillars was applied. The second and lowest pair shows that hyperparasitoids do not respond to the application of regurgitant without artificially damaging the plant. Numbers between brackets indicate the number of wasps that made a choice within 10 min from the start of the experiment versus the total number of wasps tested. * <i>p</i><0.05, ** <i>p</i><0.001. Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "hyperparasitoids", "herbivore-induced"], "article_id"=>206997, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g004", "stats"=>{"downloads"=>5, "page_views"=>85, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Preference_of_hyperparasitoids_for_herbivore_induced_plant_volatiles_/206997", "title"=>"Preference of hyperparasitoids for herbivore-induced plant volatiles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:43:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/536725"], "description"=>"<p>Percentage of <i>Cotesia glomerata</i> (CG, left) and <i>C. rubecula</i> (CR, right) cocoon clutches hyperparasitized on plants that had been induced with herbivory by unparasitized or parasitized caterpillars of <i>P. rapae</i>. <i>Pieris rapae</i> (PR), <i>P. rapae</i> parasitized by <i>C. glomerata</i> (PR-CG), <i>P. rapae</i> parasitized by <i>C. rubecula</i> (PR-CR), and undamaged (UD). Letters indicate significant differences between treatment groups (GLM, <i>p</i><0.05). Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "volatiles", "mediate", "hyperparasitism"], "article_id"=>207203, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g006", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Herbivore_induced_plant_volatiles_mediate_hyperparasitism_in_the_field_/207203", "title"=>"Herbivore-induced plant volatiles mediate hyperparasitism in the field.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/536818"], "description"=>"<p>Primary and hyperparasitoid wasps were reared from cocoons of the gregarious <i>Cotesia glomerata</i> (left) and solitary <i>C. rubecula</i> (right) that had been collected from <i>Brassica oleracea</i> during three field seasons. Colors indicate the different parasitoid species; the white segment of the bars depicts the primary parasitoids (a) <i>C. glomerata</i> and (b) <i>C. rubecula</i>; colored bar segments represent the most abundant hyperparasitoids: <i>Acrolyta nens</i> (1, blue bar), <i>Lysibia nana</i> (2, orange bar), <i>Pteromalus semotus</i> (3, yellow bar), <i>Mesochorus gemellus</i> (4, red bar), and <i>Baryscapus galactopus</i> (5, green bar). Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "abundance", "parasitoids", "hyperparasitoids", "parasitoid", "cocoons"], "article_id"=>207284, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g007", "stats"=>{"downloads"=>4, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_abundance_of_primary_parasitoids_and_hyperparasitoids_from_primary_parasitoid_cocoons_in_the_field_/207284", "title"=>"Relative abundance of primary parasitoids and hyperparasitoids from primary parasitoid cocoons in the field.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:44:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/536442"], "description"=>"<p><i>Lysibia nana</i> preference (top bar) for gregarious broods of <i>Cotesia glomerata</i> (grey) or solitary cocoons of <i>C. rubecula</i> (white) in a Petri dish bioassay. <i>Lysibia nana</i> preference (lower bar) for gregarious broods of <i>Cotesia glomerata</i> (grey) or the same number of cocoons of <i>C. rubecula</i> (white). Numbers between brackets indicate the fraction of wasps that responded to cocoons within 10 min from the start of the experiment. * <i>p</i><0.05, ** <i>p</i><0.001. Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "responses", "parasitoid"], "article_id"=>206913, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g003", "stats"=>{"downloads"=>4, "page_views"=>74, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysibia_nana_responses_in_choice_tests_with_primary_parasitoid_cocoons_/206913", "title"=>"<i>Lysibia nana</i> responses in choice tests with primary parasitoid cocoons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:42:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/536905"], "description"=>"<p>Boldface type presents significant effects at <i>p</i><0.001 in a GLM model with a binomial distribution.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "hyperparasitism", "experiments", "carried"], "article_id"=>207376, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.t004", "stats"=>{"downloads"=>5, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_Cotesia_species_and_year_on_the_fraction_of_hyperparasitism_in_field_experiments_carried_out_in_3_consecutive_years_/207376", "title"=>"The effect of <i>Cotesia</i> species and year on the fraction of hyperparasitism in field experiments carried out in 3 consecutive years.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 19:45:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/537013"], "description"=>"<p>Values indicate mean ± SD.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "clutch", "cocoons", "rearing", "corresponding", "fitness-related", "hyperparasitoid"], "article_id"=>207481, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.t001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fresh_weight_and_clutch_size_of_cocoons_of_two_Cotesia_species_collected_from_a_laboratory_rearing_or_from_the_field_and_the_corresponding_fitness_related_traits_in_the_hyperparasitoid_Lysibia_nana_/207481", "title"=>"Fresh weight and clutch size of cocoons of two <i>Cotesia</i> species collected from a laboratory rearing or from the field, and the corresponding fitness-related traits in the hyperparasitoid <i>Lysibia nana</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 19:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/536365"], "description"=>"<p><i>Lysibia nana</i> dry mass plotted against the mass of the <i>Cotesia</i> cocoon before <i>L. nana</i> had parasitized the cocoon. Orange symbols represent wasps emerging from <i>C. glomerata</i> cocoons, and black symbols those emerging from <i>C. rubecula</i> cocoons. Females are represented by dots, and males by triangles. Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "pupae", "parasitoid"], "article_id"=>206839, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g002", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Performance_of_Lysibia_nana_on_pupae_of_two_parasitoid_species_/206839", "title"=>"Performance of <i>Lysibia nana</i> on pupae of two parasitoid species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:42:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/536214"], "description"=>"<p>The gregarious primary parasitoid <i>Cotesia glomerata</i> (CG) and the solitary <i>C. rubecula</i> (CR) attack caterpillars of <i>Pieris</i> (PR) butterflies, which are in turn attacked by several hyperparasitoids: <i>Acrolyta nens</i> (1), <i>Lysibia nana</i> (2), <i>Pteromalus semotus</i> (3), <i>Mesochorus gemellus</i> (4), and <i>Baryscapus galactopus</i> (5). Hyperparasitoids at the fourth trophic level find their primary parasitoid host at the third trophic level via information derived from the plant at the first trophic level. Larvae of primary parasitoids that develop in their herbivorous host at the second trophic level inflict changes in their herbivore host, and the combination of herbivore and parasitoid (parasitized herbivores) inflict changes in plant volatile emission (I). These changes in plant volatile emission are used by hyperparasitoids as a cue of host presence (II). Photograph credit: Tibor Bukovinszky.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "four-trophic-level"], "article_id"=>206692, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.g001", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_study_system_of_the_four_trophic_level_community_on_Brassica_oleracea_plants_/206692", "title"=>"Experimental study system of the four-trophic-level community on <i>Brassica oleracea</i> plants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 19:41:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/536950"], "description"=>"<p>The numbers represent individual cocoons of the two parasitoids from which either a primary parasitoid or a hyperparasitoid emerged.</p>1<p><i>Baryscapus galactopus</i> is a gregarious hyperparasitoid that develops with on average eight individuals in a single <i>C. rubecula</i> cocoon. The numbers for <i>B. galactopus</i> represent individual <i>Cotesia</i> cocoons that were hyperparasitized by <i>B. galactopus</i> (and thus on average produced eight hyperparasitoids). The number of cocoons of the gregarious <i>C. glomerata</i> that were hyperparasitized was calculated by dividing the total number of emerging <i>B. galactopus</i> by eight.</p>2<p>Number indicates the collected number of cocoon clutches, from which 25,170 <i>C. glomerata</i> wasps emerged.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "hyperparasitoid", "wasps", "cocoons", "3-year"], "article_id"=>207425, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.t005", "stats"=>{"downloads"=>9, "page_views"=>58, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyperparasitoid_species_and_the_number_of_hyperparasitoid_wasps_emerging_from_Cotesia_glomerata_and_C_rubecula_cocoons_collected_during_a_3_year_survey_/207425", "title"=>"Hyperparasitoid species and the number of hyperparasitoid wasps emerging from <i>Cotesia glomerata</i> and <i>C. rubecula</i> cocoons collected during a 3-year survey.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 19:45:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/537079"], "description"=>"<p>Only those compounds have been included that were present in all replicates of at least one treatment. Amounts of individual compounds are given as average peak area (SE) per litre of trapped air per gram shoot biomass. Variable Importance in the Projection (VIP) scores for the PLS-DA are given. Bold face type scores are higher than 1 and are most influential for separation of the treatments. Differences among treatments for compounds with VIP score >1 based on Mann–Whitney U pair wise comparisons are indicated with superscript letters.</p>*<p>(E)-DMNT = (E)-4,8-dimethylnona-1,3,7-triene.</p>", "links"=>[], "tags"=>["ecology", "Behavioral ecology", "Chemical ecology", "Community Ecology", "Plant ecology", "Terrestrial ecology", "Zoology", "Entomology", "compounds", "headspace", "uninfested", "infested", "caterpillars", "unparasitized", "parasitized"], "article_id"=>207538, "categories"=>["Biological Sciences"], "users"=>["Erik H. Poelman", "Maaike Bruinsma", "Feng Zhu", "Berhane T. Weldegergis", "Aline E. Boursault", "Yde Jongema", "Joop J. A. van Loon", "Louise E. M. Vet", "Jeffrey A. Harvey", "Marcel Dicke"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001435.t002", "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Volatile_compounds_detected_in_the_headspace_of_Brassica_oleracea_uninfested_control_or_infested_with_two_caterpillars_of_Pieris_rapae_that_were_either_unparasitized_or_parasitized_with_Cotesia_rubecula_or_C_glomerata_/207538", "title"=>"Volatile compounds detected in the headspace of <i>Brassica oleracea</i>, uninfested (control), or infested with two caterpillars of <i>Pieris rapae</i> that were either unparasitized or parasitized with <i>Cotesia rubecula</i> or <i>C. glomerata</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 19:46:08"}

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  • {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"22", "full-text"=>"16", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
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  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"6", "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"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"17", "full-text"=>"14", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"19", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"18", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"16", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"19", "full-text"=>"20", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"16", "full-text"=>"17", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"16", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"15", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"15", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"23", "full-text"=>"20", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"30", "full-text"=>"28", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"28", "full-text"=>"25", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"24", "full-text"=>"23", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"16", "full-text"=>"21", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"18", "full-text"=>"21", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

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