Ecological Niche Dimensionality and the Evolutionary Diversification of Stick Insects
- Publication Date
- April 02, 2008
- Journal
- PLOS ONE
- Authors
- Patrik Nosil & Cristina P. Sandoval
- Volume
- 3
- Issue
- 4
- Pages
- e1907
- DOI
- https://dx.plos.org/10.1371/journal.pone.0001907
- Publisher URL
- http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0001907
- PubMed
- http://www.ncbi.nlm.nih.gov/pubmed/18382680
- PubMed Central
- http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2270911
- Europe PMC
- http://europepmc.org/abstract/MED/18382680
- Web of Science
- 000260795400032
- Scopus
- 44849096261
- Mendeley
- http://www.mendeley.com/research/ecological-niche-dimensionality-evolutionary-diversification-stick-insects
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CiteULike | Further Information
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Mendeley | Further Information
{"title"=>"Ecological niche dimensionality and the evolutionary diversification of stick insects", "type"=>"journal", "authors"=>[{"first_name"=>"Patrik", "last_name"=>"Nosil", "scopus_author_id"=>"6602157859"}, {"first_name"=>"Cristina P.", "last_name"=>"Sandoval", "scopus_author_id"=>"7005249600"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"351954389", "sgr"=>"44849096261", "issn"=>"19326203", "arxiv"=>"3017", "pmid"=>"18382680", "scopus"=>"2-s2.0-44849096261", "doi"=>"10.1371/journal.pone.0001907", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"007ce9d8-2361-3e8b-9a61-d8e209ea5a7f", "abstract"=>"The degree of phenotypic divergence and reproductive isolation between taxon pairs can vary quantitatively, and often increases as evolutionary divergence proceeds through various stages, from polymorphism to population differentiation, ecotype and race formation, speciation, and post-speciational divergence. Although divergent natural selection promotes divergence, it does not always result in strong differentiation. For example, divergent selection can fail to complete speciation, and distinct species pairs sometimes collapse ('speciation in reverse'). Widely-discussed explanations for this variability concern genetic architecture, and the geographic arrangement of populations. A less-explored possibility is that the degree of phenotypic and reproductive divergence between taxon pairs is positively related to the number of ecological niche dimensions (i.e., traits) subject to divergent selection. Some data supporting this idea stem from laboratory experimental evolution studies using Drosophila, but tests from nature are lacking. Here we report results from manipulative field experiments in natural populations of herbivorous Timema stick insects that are consistent with this 'niche dimensionality' hypothesis. In such insects, divergent selection between host plants might occur for cryptic colouration (camouflage to evade visual predation), physiology (to detoxify plant chemicals), or both of these niche dimensions. We show that divergent selection on the single niche dimension of cryptic colouration can result in ecotype formation and intermediate levels of phenotypic and reproductive divergence between populations feeding on different hosts. However, greater divergence between a species pair involved divergent selection on both niche dimensions. Although further replication of the trends reported here is required, the results suggest that dimensionality of selection may complement genetic and geographic explanations for the degree of diversification in nature.", "link"=>"http://www.mendeley.com/research/ecological-niche-dimensionality-evolutionary-diversification-stick-insects", "reader_count"=>193, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>15, "Librarian"=>1, "Researcher"=>45, "Student > Doctoral Student"=>10, "Student > Ph. D. Student"=>44, "Student > Postgraduate"=>13, "Student > Master"=>19, "Other"=>9, "Student > Bachelor"=>16, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>13}, "reader_count_by_user_role"=>{"Unspecified"=>5, "Professor > Associate Professor"=>15, "Librarian"=>1, "Researcher"=>45, "Student > Doctoral Student"=>10, "Student > Ph. D. Student"=>44, "Student > Postgraduate"=>13, "Student > Master"=>19, "Other"=>9, "Student > Bachelor"=>16, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>13}, "reader_count_by_subject_area"=>{"Unspecified"=>9, "Engineering"=>1, "Environmental Science"=>12, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>159, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Social Sciences"=>2, "Earth and Planetary Sciences"=>4}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>159}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>9}, "Environmental Science"=>{"Environmental Science"=>12}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Reunion"=>1, "Republic of Singapore"=>1, "Colombia"=>2, "Argentina"=>1, "United States"=>6, "Japan"=>3, "United Kingdom"=>2, "Portugal"=>2, "Switzerland"=>1, "Spain"=>2, "India"=>2, "China"=>1, "Brazil"=>5, "Serbia and Montenegro"=>1, "Mexico"=>1, "South Africa"=>2, "France"=>2, "Chile"=>2, "Germany"=>1}, "group_count"=>5}CrossRef
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Scopus | Further Information
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Journal Comments | Further Information
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/be42d6f1-deb9-443c-907e-c9cf5e5b4cb2", "title"=>"Interesting new perspective on insect divergence on hostplants", "body"=>"This is an interesting article where the authors compare divergence at different taxonomic levels: between ecotypes within a species and between different species. The results indicate that niche dimensionality is important in evolutionary divergence of these insects, i. e. the number of niche dimensions along which divergence has taken place. Apparently, colouration differences evolve first, followed by subsequent diversification of host-plant related physiological adaptations. \n\nThe results are suggestive and the study makes good use of an already well-explored system. A criticism raised by some referees is that the number of comparisons are few (only one between-species comparison), which means that the generality of the results needs to be verified in a future study encompassing additional species in a broader phylogenetic framework of these stick insects.", "isRemoved"=>false, "created"=>"2008-04-02T17:29:52Z", "lastModified"=>"2008-04-02T17:29:52Z", "creator"=>{"userId"=>"82923"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001907", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-04-02T17:29:52Z", "replies"=>[]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/93d60d25-fdc6-401e-9e9c-7727aaf76cd2", "title"=>"Referee Comments: Referee 2", "body"=>"Referee 2's Review:\n\nGeneral Comments:\n\nThe manuscript tests the ecological niche dimensionality hypothesis using Timema stick insects. The authors propose that selection for both crypsis (to avoid predation) as well as physiology (to adapt to different host plants) should result in greater divergence between species than selection in just one trait dimension. Data from field experiments (already published experiments and new ones) are used to test this hypothesis using ecotypes of T. cristinae and T. podura, and the species pair T. podura and T. chumash. The results provide evidence in support of the niche dimensionality hypothesis and suggest that the number of traits under selection needs to be taken into account when investigating and trying to explain the variability in the degree of divergence between species.\n\nIn general I think that the manuscript is very tidy and concise, and provides interesting and novel information about the factors that affect the variability in divergence between species. Although the authors only investigate one species pair in detail (which limits the generality of their conclusions), I think that this manuscript will be important in stimulating research in this area.\n\nMinor Comments:\n\nPage 2, Line 21: reference is lacking after '...following speciation...'\nPage 3, Line 26: delete are versus\nPage 5, Line 15: T. podura can be found on Ceanothus as well\nPage 5, Line 29: Comma before respectively\nPage 7, Line 17: result should be results\nDiscussion: The authors are too general in the beginning of the discussion (they start out saying that these findings provide a model of diversification in Timema stick insects), and I feel that the results are extrapolated beyond a level that is appropriate. Specifically, the statement that (line 18 and 19) 'divergent selection on the single dimension of crypsis appears insufficient to complete speciation' should be modified, as the authors base this statement on limited data. It is unknown if other species pairs in this group follow a similar pattern, for example, in situations when predation is more intense or when host plants vary more strongly in chemical composition or morphology.\nPage 8, Line, 25: '...of selection on single niche dimensions does exist...'\nMaterial and Methods, Page 10 and 11: inconsistent writing of dimensions etc. Sometimes the authors add a space and sometimes not (e.g. 12m and 12 m).\nPage 11, Line 5: Add the year to the date\nPage 14, Line 6: BMC??\nPage 15, Line 20: add pages\nPage 16, Line 5: add pages\nPage 17, Line 7: Delete dot after Funk DJ\nPage 17, Line 22: Delete dot after (2005)\nPage 17, Line 30: 2nd should be superscript\nReferences: It would be good to include DOI numbers\nPage 18, Figure 1, Line 2: Add that the host plants are shown too\nPage 19, Figure 1 taxon pairs: The differences in plant morphology are impossible to see. The authors need to use a different photograph here.\nPage 19, Figure 1, Line 4: How were the genealogies derived? A summary of the methods would be necessary.\nPage 2, Figure 2, 1 Line 4: The term bugs is too general and should be replaced\nPage 23, Figure 3: The graphs showing divergence of populations needs to be improved\n\n**********\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.", "isRemoved"=>false, "created"=>"2008-04-08T00:01:16Z", "lastModified"=>"2008-04-08T00:01:16Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001907", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-04-08T00:01:16Z", "replies"=>[]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/43732758-42dd-46e9-ada3-8dc85f3b7210", "title"=>"Referee Comments: Referee 3", "body"=>"Referee 3's Review:\n\nThis paper investigates the hypothesis that genetic divergence is related to the number of ecological niche dimensions that are subject to divergent selection. The authors perform a series of field experiments on herbivorous Timema stick insects to test the hypothesis with regard to the host plant related niche dimensions crypsis and feeding performance. The tests consists of comparing pairs of ecotypes and closely related species with the hypothesis that different species should differ in more niche dimensions than ecotypes of the same species.\n\nI find the idea as such interesting. However, one must say that the way it is put forward here, it is not a very strong test in a popperian sense. It is hardly surprising that you will find that interspecific divergence is larger, or along more dimensions, than intraspecific divergence. The authors already knew that one of the species in the species pair comparison (T. chumash) does not utilize one of the hosts, so they knew in advance that the treatment that transplants these insects to the non-host will result in poor performance. They also knew in advance that T. podura have the capacity to use both hosts. Hence, even if the principle makes sense, and is indeed interesting, it strikes me as a very blunt test. Haven't they just shown that individuals that are more closely related to each other are more similar than individuals that are more distantly related?\nIn my view, the merit of the paper lies in the general discussion of the problem, but I don't see that the authors have really tested the hypothesis at all. As the authors say, the outcome must not necessarily be as found, but it would have been rather surprising if it wasn't. A more proper test, in my view, would be either a comparative study of multiple species that vary in phylogenetic distance from each other (it would increase the n-value), or better still, a comparison of multiple ecotypes (or just populations) where genetic distance is measured independently.\n\nSome additional comments:\nFirst, I find the text to be unnecessarily hard to follow at times, and it could still do with some polishing. For example, the word \"divergence\" is used abundantly in the text and it is not always clear what type of divergence is meant. Take for example the second paragraph in the introduction, where I count to nine occurrences of various forms of the word (plus one \"differentiation\"). Sometimes the word refers to genetic divergence, sometimes to ecological, geographic or phenotypic divergence.\nAnother example is on page 13, line18: \"Thus, although increased dimensionality of niche divergence may play a causal role in driving divergence ...\" There are many more such examples and I recommend a thorough run through the manuscript to see if other wordings can be used, or to add more modifiers such as \"ecological\".\nThe authors claim to have measured \"actual selection\" (e.g. p 13, line 27), but I think they have measured \"potential selection\", as there is no information on the response to the selection. If, for example, there is no genetic variance for the trait, relative gene frequencies in the population will not change no matter how hard the selection pressure is.\nPage 3, line 25: \"the extent to which divergent drives ...\" Insert \"selection\"\nPage 14, line 12: \"... different types of phenotypic traits that have diverged between the species pairs (e.g., water depth, distance from shore in the lake ...\" Water depth and distance from shore are not phenotypic traits.\nPage 16, line 21: \"Lifetime fecundity was the number of eggs within an enclosure after the final census.\" Is this measure of fecundity not dependent of survival?\n\n**********\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.", "isRemoved"=>false, "created"=>"2008-04-08T00:06:26Z", "lastModified"=>"2008-04-08T00:06:26Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001907", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-04-08T00:06:26Z", "replies"=>[]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/f885f52f-b971-4557-866d-61e878f611e9", "title"=>"Referee Comments: Referee 4", "body"=>"Referee 4's Review:\n\nIn this manuscript the authors use new as well as previously published data on stick insect taxa to test the 'niche dimensionality hypothesis'. This hypothesis states that divergent selection between taxa along multiple niche dimensions promotes the evolution of reproductive isolation. The authors find support for the hypothesis, in that reproductively non-isolated host plant ecotypes of Timena cristinae and of T. podura are exposed to divergent selection mainly on coloration, whereas the two established species T. podura and T. chumash, which differ in their host plants, are exposed to divergent selection on both coloration and on host-plant-related physiology or performance. There is no doubt in my mind that the niche dimensionality hypothesis is potentially important, and thus well worth testing. The reported field experiments on survival and performance on the different host plants are ambitiously planned and seem well executed, adding to the quality of the study. Thus, I am generally in favor of this work, although I also have a number of questions and comments.\n\n1. Because the study only involves one species pair, for which there seems to be limited information about their evolutionary relationship, it can at best provide rather weak and circumstantial evidence in favor of the hypothesis. The authors are clearly aware of this, and do not extend their interpretations in an unreasonable way. However, I am still a bit dissatisfied with the almost complete lack of mention of the phylogenetic history of host plant relationships in Timena, and in in particular with the lack of this kind of discussion for the podura/chumash species pair. Is feeding on either Ceanothus or Adenostoma primitive in Timena, and which plant was the likely host of the ancestor of T. podura and T. chumash? This kind of information would be needed to evaluate whether currently observed interspecific differences in host-plant performance are at all likely to be involved as causal agents for the evolution of reproductive isolation. On this crucial matter, the authors have rather little to say. I think they should either admit that nothing is known about the phylogenetic history of host use, or provide whatever information there is on the subject.\n\n2. The authors report a greater magnitude of divergence in stripe-body brightness contrast between species than between ecotypes (bottom p. 7 and Fig. 1). Looking at Fig. 1, I was a bit surprised by this, since there appears to be a more distinctive dorsal stripe on the T. chumash image than on the image of the Ceanothus ecotype of T. cristinae (Fig. 1A), whereas Fig. 1B seems to suggest an almost absence of a dorsal stripe on T. chumash. The images are of course just of single specimens, but a possible explanation may be found in the data on hue and saturation in Table 1, where it seems that T. chumash indeed has a more pronounced dorsal stripe than the C ecotype of T. cristinae. In view of this, is it really fair to emphasize (p. 7, lines 27-28) a greater interspecific divergence in coloration? Is there any strong basis for such a view? I am also a bit uncertain about including morphological data in Table 1, or at least putting this data into the same PC analysis. Why not perform the PC analysis only on coloration, which would seem to be most directly related to crypsis on the host plant?\n\n3. I am a bit confused by the T. chumash data in Fig. 2A. The two bars do not sum to 100% (the bar with 4 individuals seems too tall).\n\n4. Table 2 is very big, and I do not think it is necessary to include it (on the other hand, it does not do any harm).\n\n5. In responding and adjusting to previous comments, the authors have introduced a slightly defensive tone into their writing. This is perhaps not a big problem, but in my view it is more important to be clear about the strength or weakness of the test of the niche dimensionality hypothesis that has been conducted. I think the present results are mainly suggestive, and the role of divergent selection along multiple niche dimensions as a causal factor for the evolution of reproductive isolation is not at all established, or even directly supported, in this study.\n\n**********\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.", "isRemoved"=>false, "created"=>"2008-04-08T20:34:27Z", "lastModified"=>"2008-04-08T20:34:27Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001907", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-04-08T20:34:27Z", "replies"=>[]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/b7272b1c-e7d6-4ff6-8780-8f7d93a7108f", "title"=>"Response to user rating", "body"=>"In general, I totally agree with the comments associated with the user rating posted by ErikiLund. Our study did examine only a few taxon pairs, and thus we were careful to explicitly acknowledge this point in several places in our article. Data from additional taxon pairs is indeed highly desirable.\r\n\r\nThat said, I want to point out that generating the types of data presented in the article is difficult, even for a single taxon pair. In particular, isolating how many niche dimensions are subject to divergent selection in the wild requires manipulative experiments in nature, experiments that not only measure selection, but also isolate the actual agents of natural selection.\r\n\r\nIn short - further replication is required, but the existing data does support the niche dimensionality idea, using the required morphological, genetic, and experimental data.\r\n", "isRemoved"=>false, "created"=>"2008-04-16T18:33:45Z", "lastModified"=>"2008-04-16T18:33:45Z", "creator"=>{"userId"=>"158841"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001907", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-04-16T18:33:45Z", "replies"=>[]}
Counter
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- {"month"=>"4", "year"=>"2008", "pdf_views"=>"261", "xml_views"=>"92", "html_views"=>"1328"}
- {"month"=>"5", "year"=>"2008", "pdf_views"=>"39", "xml_views"=>"39", "html_views"=>"278"}
- {"month"=>"6", "year"=>"2008", "pdf_views"=>"23", "xml_views"=>"1", "html_views"=>"174"}
- {"month"=>"7", "year"=>"2008", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"110"}
- {"month"=>"8", "year"=>"2008", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"103"}
- {"month"=>"9", "year"=>"2008", "pdf_views"=>"5", "xml_views"=>"2", "html_views"=>"131"}
- {"month"=>"10", "year"=>"2008", "pdf_views"=>"32", "xml_views"=>"1", "html_views"=>"148"}
- {"month"=>"11", "year"=>"2008", "pdf_views"=>"17", "xml_views"=>"0", "html_views"=>"118"}
- {"month"=>"12", "year"=>"2008", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"80"}
- {"month"=>"1", "year"=>"2009", "pdf_views"=>"16", "xml_views"=>"0", "html_views"=>"98"}
- {"month"=>"2", "year"=>"2009", "pdf_views"=>"18", "xml_views"=>"0", "html_views"=>"93"}
- {"month"=>"3", "year"=>"2009", "pdf_views"=>"17", "xml_views"=>"3", "html_views"=>"106"}
- {"month"=>"4", "year"=>"2009", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"38"}
- {"month"=>"5", "year"=>"2009", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"42"}
- {"month"=>"6", "year"=>"2009", "pdf_views"=>"15", "xml_views"=>"1", "html_views"=>"54"}
- {"month"=>"7", "year"=>"2009", "pdf_views"=>"16", "xml_views"=>"1", "html_views"=>"63"}
- {"month"=>"8", "year"=>"2009", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"48"}
- {"month"=>"9", "year"=>"2009", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"79"}
- {"month"=>"10", "year"=>"2009", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"60"}
- {"month"=>"11", "year"=>"2009", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"72"}
- {"month"=>"12", "year"=>"2009", "pdf_views"=>"70", "xml_views"=>"1", "html_views"=>"57"}
- {"month"=>"1", "year"=>"2010", "pdf_views"=>"45", "xml_views"=>"0", "html_views"=>"74"}
- {"month"=>"2", "year"=>"2010", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"70"}
- {"month"=>"3", "year"=>"2010", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"50"}
- {"month"=>"4", "year"=>"2010", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"83"}
- {"month"=>"5", "year"=>"2010", "pdf_views"=>"19", "xml_views"=>"1", "html_views"=>"101"}
- {"month"=>"6", "year"=>"2010", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"62"}
- {"month"=>"7", "year"=>"2010", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"8", "year"=>"2010", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"43"}
- {"month"=>"9", "year"=>"2010", "pdf_views"=>"10", "xml_views"=>"1", "html_views"=>"68"}
- {"month"=>"10", "year"=>"2010", "pdf_views"=>"15", "xml_views"=>"1", "html_views"=>"92"}
- {"month"=>"11", "year"=>"2010", "pdf_views"=>"16", "xml_views"=>"0", "html_views"=>"69"}
- {"month"=>"12", "year"=>"2010", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"54"}
- {"month"=>"1", "year"=>"2011", "pdf_views"=>"12", "xml_views"=>"5", "html_views"=>"66"}
- {"month"=>"2", "year"=>"2011", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"3", "year"=>"2011", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"69"}
- {"month"=>"4", "year"=>"2011", "pdf_views"=>"17", "xml_views"=>"0", "html_views"=>"63"}
- {"month"=>"5", "year"=>"2011", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"49"}
- {"month"=>"6", "year"=>"2011", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"37"}
- {"month"=>"7", "year"=>"2011", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"45"}
- {"month"=>"8", "year"=>"2011", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"37"}
- {"month"=>"9", "year"=>"2011", "pdf_views"=>"6", "xml_views"=>"2", "html_views"=>"58"}
- {"month"=>"10", "year"=>"2011", "pdf_views"=>"14", "xml_views"=>"0", "html_views"=>"89"}
- {"month"=>"11", "year"=>"2011", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"95"}
- {"month"=>"12", "year"=>"2011", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"54"}
- {"month"=>"1", "year"=>"2012", "pdf_views"=>"18", "xml_views"=>"0", "html_views"=>"76"}
- {"month"=>"2", "year"=>"2012", "pdf_views"=>"16", "xml_views"=>"0", "html_views"=>"79"}
- {"month"=>"3", "year"=>"2012", "pdf_views"=>"17", "xml_views"=>"0", "html_views"=>"100"}
- {"month"=>"4", "year"=>"2012", "pdf_views"=>"15", "xml_views"=>"1", "html_views"=>"81"}
- {"month"=>"5", "year"=>"2012", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"6", "year"=>"2012", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"55"}
- {"month"=>"7", "year"=>"2012", "pdf_views"=>"14", "xml_views"=>"0", "html_views"=>"52"}
- {"month"=>"8", "year"=>"2012", "pdf_views"=>"9", "xml_views"=>"5", "html_views"=>"43"}
- {"month"=>"9", "year"=>"2012", "pdf_views"=>"9", "xml_views"=>"2", "html_views"=>"83"}
- {"month"=>"10", "year"=>"2012", "pdf_views"=>"18", "xml_views"=>"0", "html_views"=>"68"}
- {"month"=>"11", "year"=>"2012", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"55"}
- {"month"=>"12", "year"=>"2012", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"37"}
- {"month"=>"1", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"60"}
- {"month"=>"2", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"45"}
- {"month"=>"3", "year"=>"2013", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"58"}
- {"month"=>"4", "year"=>"2013", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"88"}
- {"month"=>"5", "year"=>"2013", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"58"}
- {"month"=>"6", "year"=>"2013", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"41"}
- {"month"=>"7", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"50", "html_views"=>"37"}
- {"month"=>"8", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"3", "html_views"=>"31"}
- {"month"=>"9", "year"=>"2013", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"67"}
- {"month"=>"10", "year"=>"2013", "pdf_views"=>"9", "xml_views"=>"1", "html_views"=>"78"}
- {"month"=>"11", "year"=>"2013", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"57"}
- {"month"=>"12", "year"=>"2013", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"48"}
- {"month"=>"1", "year"=>"2014", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"50"}
- {"month"=>"2", "year"=>"2014", "pdf_views"=>"19", "xml_views"=>"0", "html_views"=>"58"}
- {"month"=>"3", "year"=>"2014", "pdf_views"=>"14", "xml_views"=>"3", "html_views"=>"72"}
- {"month"=>"4", "year"=>"2014", "pdf_views"=>"13", "xml_views"=>"2", "html_views"=>"114"}
- {"month"=>"5", "year"=>"2014", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"51"}
- {"month"=>"6", "year"=>"2014", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"32"}
- {"month"=>"7", "year"=>"2014", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"35"}
- {"month"=>"8", "year"=>"2014", "pdf_views"=>"6", "xml_views"=>"2", "html_views"=>"33"}
- {"month"=>"9", "year"=>"2014", "pdf_views"=>"11", "xml_views"=>"2", "html_views"=>"72"}
- {"month"=>"10", "year"=>"2014", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"82"}
- {"month"=>"11", "year"=>"2014", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"77"}
- {"month"=>"12", "year"=>"2014", "pdf_views"=>"12", "xml_views"=>"2", "html_views"=>"60"}
- {"month"=>"1", "year"=>"2015", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"45"}
- {"month"=>"2", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"35"}
- {"month"=>"3", "year"=>"2015", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"55"}
- {"month"=>"4", "year"=>"2015", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"89"}
- {"month"=>"5", "year"=>"2015", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"73"}
- {"month"=>"6", "year"=>"2015", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"38"}
- {"month"=>"7", "year"=>"2015", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"32"}
- {"month"=>"8", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"34"}
- {"month"=>"9", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"35"}
- {"month"=>"10", "year"=>"2015", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"11", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"41"}
- {"month"=>"12", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"59"}
- {"month"=>"1", "year"=>"2016", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"30"}
- {"month"=>"2", "year"=>"2016", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"25"}
- {"month"=>"3", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"4", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"49"}
- {"month"=>"5", "year"=>"2016", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"59"}
- {"month"=>"6", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"41"}
- {"month"=>"7", "year"=>"2016", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"8", "year"=>"2016", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"62"}
- {"month"=>"9", "year"=>"2016", "pdf_views"=>"14", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"10", "year"=>"2016", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"76"}
- {"month"=>"11", "year"=>"2016", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"12", "year"=>"2016", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"51"}
- {"month"=>"1", "year"=>"2017", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"48"}
- {"month"=>"2", "year"=>"2017", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"3", "year"=>"2017", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"85"}
- {"month"=>"4", "year"=>"2017", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"57"}
- {"month"=>"5", "year"=>"2017", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"46"}
- {"month"=>"6", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"1", "html_views"=>"58"}
- {"month"=>"7", "year"=>"2017", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"38"}
- {"month"=>"8", "year"=>"2017", "pdf_views"=>"10", "xml_views"=>"3", "html_views"=>"32"}
- {"month"=>"9", "year"=>"2017", "pdf_views"=>"12", "xml_views"=>"2", "html_views"=>"53"}
- {"month"=>"10", "year"=>"2017", "pdf_views"=>"4", "xml_views"=>"1", "html_views"=>"64"}
- {"month"=>"11", "year"=>"2017", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"52"}
- {"month"=>"12", "year"=>"2017", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"33"}
- {"month"=>"1", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"2", "html_views"=>"39"}
- {"month"=>"2", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"2", "html_views"=>"42"}
- {"month"=>"3", "year"=>"2018", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"46"}
- {"month"=>"4", "year"=>"2018", "pdf_views"=>"11", "xml_views"=>"1", "html_views"=>"20"}
- {"month"=>"5", "year"=>"2018", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"6", "year"=>"2018", "pdf_views"=>"6", "xml_views"=>"1", "html_views"=>"16"}
- {"month"=>"7", "year"=>"2018", "pdf_views"=>"1", "xml_views"=>"3", "html_views"=>"10"}
- {"month"=>"8", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"18"}
- {"month"=>"9", "year"=>"2018", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"10", "year"=>"2018", "pdf_views"=>"9", "xml_views"=>"1", "html_views"=>"27"}
- {"month"=>"11", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"24"}
- {"month"=>"12", "year"=>"2018", "pdf_views"=>"12", "xml_views"=>"1", "html_views"=>"7"}
- {"month"=>"1", "year"=>"2019", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"17"}
- {"month"=>"2", "year"=>"2019", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"3", "year"=>"2019", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"4", "year"=>"2019", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"24"}
- {"month"=>"5", "year"=>"2019", "pdf_views"=>"18", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"6", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"22"}
- {"month"=>"7", "year"=>"2019", "pdf_views"=>"7", "xml_views"=>"4", "html_views"=>"11"}
- {"month"=>"8", "year"=>"2019", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"20"}
- {"month"=>"9", "year"=>"2019", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"11"}
- {"month"=>"10", "year"=>"2019", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"11", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"16"}
- {"month"=>"12", "year"=>"2019", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"4"}
PMC Usage Stats | Further Information
- {"month"=>"1", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"12", "year"=>"2010", "pdf"=>"9", "unique-ip"=>"18", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"2", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "unique-ip"=>"14", "pdf"=>"10", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"17", "year"=>"2010", "pdf"=>"11", "unique-ip"=>"21", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"16", "unique-ip"=>"18", "pdf"=>"10", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"11", "year"=>"2010", "pdf"=>"4", "unique-ip"=>"10", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"7", "unique-ip"=>"12", "pdf"=>"10", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"7", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"7", "year"=>"2010", "pdf"=>"5", "unique-ip"=>"9", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"8", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"11", "unique-ip"=>"16", "pdf"=>"10", "year"=>"2010", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"9", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"8", "year"=>"2010", "pdf"=>"4", "unique-ip"=>"11", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"10", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"13", "unique-ip"=>"19", "pdf"=>"5", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"11", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"8", "year"=>"2010", "pdf"=>"0", "unique-ip"=>"7", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"12", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "unique-ip"=>"6", "pdf"=>"4", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"1", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"3", "year"=>"2011", "pdf"=>"0", "unique-ip"=>"3", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"2", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"7", "unique-ip"=>"12", "pdf"=>"5", "year"=>"2011", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "year"=>"2011", "pdf"=>"3", "unique-ip"=>"7", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"9", "unique-ip"=>"12", "pdf"=>"7", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"8", "year"=>"2011", "pdf"=>"1", "unique-ip"=>"10", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
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Relative Metric
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