Skip to content
Research Article Open access CC BY 4.0

Preliminary Environmental Risk Assessment of Insect Resistant Genetically Modified Maize MON 89034 for Cultivation (EFSA/GMO/BE/2011/90)

Audun Helge Nerland, Aksel Bernhoft, Per Brandtzæg, Merethe Aasmo Finne, Askild Lorentz Holck, Olavi Junttila, Heidi Sjursen Konestabo, Richard Meadow, Kåre M. Nielsen, Ville Erling Sipinen, Hilde-Gunn Opsahl-Sorteberg, Rose Vikse, Åshild Andreassen

European Journal of Nutrition & Food Safety · pp. 47–50 · Published 19 Nov 2019

10.9734/ejnfs/2019/v11i130129

Abstract

The environmental risk assessment of the insect resistant genetically modified maize MON 89034 (Reference EFSA/GMO/BE/2011/90) has been performed by the Panel on Genetically Modified Organisms (GMO) of the Norwegian Scientific Committee for Food Safety (VKM). VKM has been requested by the Norwegian Directorate for Nature Management and the Norwegian Food Safety Authority to issue a preliminary scientific opinion on the safety of the genetically modified maize MON 89034 (Unique identifier MON-89Ø34-3) for cultivation, and submit relevant scientific comments or questions to EFSA on the application EFSA/GMOBE/2011/90. The current submission is intended to complement application EFSA-GMO-NL-2007-37, which was approved by Commission Decision 2009/813/EC of 30 October 2009, authorising the placing on the market of products containing, consisting of, or produced from genetically modified maize MON 89034 (scope import, processing, food and feed).  Maize MON89034 has previously been assessed by the VKM GMO Panel in connection with EFSA´s public hearing of the application EFSA/GMO/NL/2007/37 (VKM 2008a). Preliminary health- and environmental risk assessments of several stacked events, with MON 89034 as one of the parental lines, have also been performed by the VKM GMO Panel (VKM 2009a, b, c; VKM 2010a,b).   The environmental risk assessment of the maize MON 89034 is based on information provided by the applicant in the application EFSA/GMO/BE/2011/90, and scientific comments from EFSA and other member states made available on the EFSA website GMO Extranet. The risk assessment also considered peer-reviewed scientific literature as relevant.     The VKM GMO Panel has evaluated MON 89034 with reference to its intended uses in the European Economic Area (EEA), and according to the principles described in the Norwegian Food Act, the Norwegian Gene Technology Act and regulations relating to impact assessment pursuant to the Gene Technology Act, Directive 2001/18/EC on the deliberate release into the environment of genetically modified organisms, and Regulation (EC) No 1829/2003 on genetically modified food and feed. The Norwegian Scientific Committee for Food Safety has also decided to take account of the appropriate principles described in the EFSA guidelines for the risk assessment of GM plants and derived food and feed (EFSA 2006, 2011a), the environmental risk assessment of GM plants (EFSA 2010), the selection of comparators for the risk assessment of GM plants (EFSA 2011b), and for the post-market environmental monitoring of GM plants (EFSA 2006, 2011c).    The scientific risk assessment of maize MON 89034 include molecular characterisation of the inserted DNA and expression of target proteins, comparative assessment of agronomic and phenotypic characteristics, unintended effects on plant fitness, potential for gene transfer, interactions between the GM plant and target and non-target organisms, effects on biogeochemical processes and evaluations of the post-market environmental plan.   In line with its mandate, VKM emphasised that assessments of sustainable development, societal utility and ethical considerations, according to the Norwegian Gene Technology Act and Regulations relating to impact assessment pursuant to the Gene Technology Act, shall not be carried out by the Panel on Genetically Modified Organisms.    The genetically modified maize MON 89034 was developed to provide protection against certain lepidopteran target pest, including European corn borer (Ostrinia nubilalis) and Mediterranean corn borer (Sesamia nonagrioides). Protection is achieved through expression in the plant of two insecticidal Cry proteins, Cry1A.105 and Cry2Ab2, derived from Bacillus thuringiensis, a common soil bacterium. Cry1A.105, encoded by the cry1A.105 gene, is a chimeric protein made up of different functional domains derived from three wild-type Cry proteins from B. thuringiensis subspecies kurstaki and aizawai.  The Cry2Ab2 protein is encoded by the cry2Ab2 gene derived from B. thuringiensis subspecies kurstaki.    Molecular characterization:   Appropriate analysis of the integration site, including flanking sequence and bioinformatics analysis, has been performed to characterise the transformation event MON 89034. The results of the segregation analysis are consistent with a single site of insertion for the cry1A.105 and cry2Ab2 gene expression cassettes and confirm the results of the molecular characterisation.  Molecular analysis of both self-pollinated and cross-fertilised lines, representing a total of seven different generations, indicates that the inserted DNA is stably transformed and inherited from one generation to the next. No genes that encode resistance to antibiotics are present in the genome of MON 89034 maize. The molecular characterisation confirmed the absence of both the aad and nptII genes, which were used in the cloning and transformation process.   Event MON 89034 and the physical, chemical and functional characteristics of the proteins have previously been evaluated by The VKM Panel on Genetically Modified Organisms, and considered satisfactory (VKM 2008a).   Comparative assessment:   The field trials for comparative assessment of agronomic and phenotypic characteristics of maize MON 89034 in the USA (2004-2005) and Europe (2007), have been performed in accordance with the EFSAs guidelines for risk assessment of genetically modified plants and derived food and feed (EFSA 2010, 2011a). Based on results from the comparative analyses, it is concluded that maize MON 89034 is agronomically and phenotypically equivalent to the conventional counterpart and commercial available reference varieties, with the exception of the lepidopteran-protection trait. The field evaluations support a conclusion of no phenotypic changes indicative of increased plant weed/pest potential of MON 89034 compared to conventional maize. Evaluations of ecological interactions between maize MON 89034 and the biotic and abiotic environment indicate no unintended effects of the introduced trait on agronomic and phenotypic characteristics.    Environmental risk:   There are no reports of the target Lepidopteran species attaining pest status on maize in Norway. Since there are no Bt-based insecticides approved for use in Norway, and lepidopteran pests have not been registered in maize, issues related to resistance evolution in target pests are not relevant at present for Norwegian agriculture.   Published scientific studies show no or negligible adverse effects of Cry1A.105 and Cry2Ab2 proteins on non-target arthropods that live on or in the vicinity of maize plants. Cultivation of maize MON 89034 is not considered to represent a threat to the prevalence of red-listed species in Norway.   Few studies have been published examining potential effects of Cry1A.105 and Cry2Ab toxin on ecosystems in soil, mineralization, nutrient turnover and soil communities. Some field studies have indicated that root exudates and decaying plant material containing Cry proteins may affect population size and activity of rhizosphere organisms (soil protozoa and microorganisms). However, data are only available from short term experiments and predictions of potential long term effects are difficult to deduce. Most studies conclude that effects on soil microorganisms and microbial communities are transient and minor compared to effects caused by agronomic and environmental factors.   Few studies have assessed the impact of Cry proteins on non-target aquatic arthropods and the fate of these proteins in senescent and decaying maize detritus in aquatic environments. Further studies with better experimental design are needed for the assessment of the potential effects of Bt crops on aquatic organisms. However, exposure of non-target organisms to Cry proteins in aquatic ecosystems is likely to be very low, and potential exposure of Bt toxins to non-target organisms in stream ecosystems in Norway is considered to be negligible.    Maize is the only representative of the genus Zea in Europe, and there are no cross-compatible wild or weedy relatives outside cultivation with which maize can hybridise and form backcross progeny. Vertical gene transfer in maize therefore depends on cross-pollination with other conventional or organic maize varieties. In addition, unintended admixture of genetically modified material in seeds represents a possible way for gene flow between different crop cultivations. The risk of pollen flow from maize volunteers is negligible under Norwegian growing conditions.    In addition to the data presented by the applicant, the VKM GMO Panel is not aware of any scientific report of increased establishment and spread of maize MON 89034 and any change in survival (including over-wintering), persistence and invasiveness capacity. Because the general characteristics of maize MON 89034 are unchanged, insect resistance are not likely to provide a selective advantage outside cultivation in Norway.    Since MON 89034 has no altered agronomic and phenotypic characteristics, except for the specific target pest resistance, the VKM GMO Panel is of the opinion that the likelihood of unintended environmental effects due to the establishment and survival of maize MON 89034 will be no different to that of conventional maize varieties in Norway    The environmental risk assessment will be completed and finalized by the VKM Panel on Genetically Modified Organisms when requested additional information from the applicant is available.

Maize Zea mays L. genetically modified maize MON 89034 EFSA/GMO/BE/2011/90 insect resistance Cry proteins Cry1A.105 Cry2Ab2 cultivation environmental risk assessment Regulation (EC) No. 1829/2003 Directive 2001/18/EC.

References (109)

  1. 1 Transgenic pollen harms monarch larvae [DOI]
  2. 2 Field Development of Resistance to Bacillus thuringiensis in Diamondback Moth (Lepidoptera: Plutellidae) [DOI]
  3. 3 Mirid Bug Outbreaks in Multiple Crops Correlated with Wide-Scale Adoption of Bt Cotton in China [DOI]
  4. 4 Uptake of Bt‐toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea [DOI]
  5. 5 Coexistence of genetically modified (GM) and non-GM crops in the European Union. A review [DOI]
  6. 6 A Meta-Analysis of Effects of Bt Crops on Honey Bees (Hymenoptera: Apidae) [DOI]
  7. 7 Early Warning of Cotton Bollworm Resistance Associated with Intensive Planting of Bt Cotton in China [DOI]
  8. 8 Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera , a comparative approach [DOI]
  9. 9 Soil Microbial Communities Associated with Bt and Non‐Bt Corn in Three Soils [DOI]
  10. 10 Monitoring and modeling horizontal gene transfer [DOI]
  11. 11 Microbial Populations and Enzyme Activities in Soil In Situ under Transgenic Corn Expressing Cry Proteins from Bacillus thuringiensis [DOI]
  12. 12 Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design [DOI]
  13. 13 Genetically modified crops and aquatic ecosystems: considerations for environmental risk assessment and non-target organism testing [DOI]
  14. 14 Responses of stream macroinvertebrates to Bt maize leaf detritus [DOI]
  15. 15 Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly [DOI]
  16. 16 Dispersion and Deposition of Corn Pollen from Experimental Sources1 [DOI]
  17. 17 An aerobiological framework for assessing cross-pollination in maize [DOI]
  18. 18 The co-existence between transgenic and non-transgenic maize in the European Union: a focus on pollen flow and cross-fertilization [DOI]
  19. 19 Settling speed of corn (Zea mays) pollen [DOI]
  20. 20 Effect of Cry3Bb Transgenic Corn and Tefluthrin on the Soil Microbial Community: Biomass, Activity, and Diversity [DOI]
  21. 21 Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain [DOI]
  22. 22 Effect of volunteers on maize gene flow [DOI]
  23. 23 Increased Frequency of Pink Bollworm Resistance to Bt Toxin Cry1Ac in China [DOI]
  24. 24 Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans [DOI]
  25. 25 Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees [DOI]
  26. 26 Cry3Bb1 protein from Bacillus thuringiensis in root exudates and biomass of transgenic corn does not persist in soil [DOI]
  27. 27 Contact and oral toxicity to honey bees ( Apis mellifera ) of agents registered for use for sweet corn insect control in Ontario, Canada [DOI]
  28. 28 Isolation of Maize from Pollen‐Mediated Gene Flow by Time and Distance [DOI]
  29. 29 Effects of transgenic corn and Cry1Ab protein on the nematode, Caenorhabditis elegans [DOI]
  30. 30 Effects of Bt-corn decomposition on the composition of the soil meso- and macrofauna [DOI]
  31. 31 Determination of insecticidal Cry1Ab protein in soil collected in the final growing seasons of a nine-year field trial of Bt-maize MON810 [DOI]
  32. 32 Preference tests with collembolas on isogenic and Bt-maize [DOI]
  33. 33 Impact of Genetically Modified Crops on Pollinators [DOI]
  34. 34 Distances needed to limit cross-fertilization between GM and conventional maize in Europe [DOI]
  35. 35 Genes without frontiers? [DOI]
  36. 36 Effects of multiple Bt proteins and GNA lectin on in vitro-reared honey bee larvae [DOI]
  37. 37 Ostrinia nubilalisparasitism and the field abundance of non-target insects in transgenicBacillus thuringiensiscorn (Zea mays) [DOI]
  38. 38 Variations in Maize Pollen Emission and Deposition in Relation to Microclimate [DOI]
  39. 39 Consequences for Protaphorura armata (Collembola: Onychiuridae) following exposure to genetically modified Bacillus thuringiensis (Bt) maize and non-Bt maize [DOI]
  40. 40 A qualitative multi-attribute model for assessing the impact of cropping systems on soil quality [DOI]
  41. 41 Origin and taxonomic status of the Palearctic population of the stem borer Sesamia nonagrioides (Lefèbvre) (Lepidoptera: Noctuidae) [DOI]
  42. 42 Effects ofBacillus thuringiensisδ-endotoxins Cry1Ab and Cry1Ac on the coccinellid beetle,Cheilomenes sexmaculatus(Coleoptera, Coccinellidae) under direct and indirect exposure conditions [DOI]
  43. 43 Soil microbial and faunal responses to herbicide tolerant maize and herbicide in two soils [DOI]
  44. 44 Effects of Bt-maize material on the life cycle of the land snail Cantareus aspersus [DOI]
  45. 45 Effects of Transgenic Bt Rice on Growth, Reproduction, and Superoxide Dismutase Activity of Folsomia candida (Collembola: Isotomidae) in Laboratory Studies [DOI]
  46. 46 Quantification of Bt-protein digestion and excretion by the primary decomposerPorcellio scaber,fed with two Bt-corn varieties [DOI]
  47. 47 Feeding, oviposition and survival of Liriomyza trifolii (Diptera: Agromyzidae) on Bt and non-Bt cottons [DOI]
  48. 48 Revue bibliographique sur la dispersion des transgènes à partir du maïs génétiquement modifié [DOI]
  49. 49 The life parameters of a parasitoidMicroplitis mediator(Hymenoptera: Braconidae), reared on cotton bollwormHelicoverpa armigera(Hübner) with Cry1Ac diet [DOI]
  50. 50 Supplementary Report from the Danish Working Group on the co-existence of genetically modified crops with conventional and organic crops: update of the 2003 Report.
  51. 51 The environmental consequences of adopting conservation tillage in Europe: reviewing the evidence [DOI]
  52. 52 Economic, Ecological, Food Safety, and Social Consequences of the Deployment of Bt Transgenic Plants [DOI]
  53. 53 Insect resistance to Bt crops: evidence versus theory [DOI]
  54. 54 Fate and effects of insect-resistant Bt crops in soil ecosystems [DOI]
  55. 55 Maize Pollen Longevity and Distance Isolation Requirements for Effective Pollen Control [DOI]
  56. 56 Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) [DOI]
  57. 57 Transgenic Bt plants decompose less in soil than non-Bt plants [DOI]
  58. 58 Persistence and biological activity in soil of the insecticidal proteins from Bacillus thuringiensis, especially from transgenic plants [DOI]
  59. 59 Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape [DOI]
  60. 60 Definition and feasibility of isolation distances for transgenic maize cultivation [DOI]
  61. 61 Effects of Activated Bt Transgene Products (Cry1Ab, Cry3Bb) on Immature Stages of the Ladybird Adalia bipunctata in Laboratory Ecotoxicity Testing [DOI]
  62. 62 A mathematical model of exposure of non-target Lepidoptera toBt-maize pollen expressing Cry1Ab within Europe [DOI]
  63. 63 Specificity and efficacy of purified Bacillus thuringiensis proteins against agronomically important insects [DOI]
  64. 64 Assessing the survival of transgenic plant DNA in the human gastrointestinal tract [DOI]
  65. 65 GM crops : The global economic and environmental impact-The first nine years 1996-2004
  66. 66 Ingested foreign (phage M13) DNA survives transiently in the gastrointestinal tract and enters the bloodstream of mice [DOI]
  67. 67 Detection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize [DOI]
  68. 68 Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.) [DOI]
  69. 69 Decomposition of transgenic Bacillus thuringiensis maize by microorganisms and woodlice Porcellio scaber (Crustacea: Isopoda) [DOI]
  70. 70 Soil Microbial and Faunal Community Responses to Bt Maize and Insecticide in Two Soils [DOI]
  71. 71 Post-harvest gene escape and approaches for minimizing it. [DOI]
  72. 72 Rapid decomposition of maize detritus in agricultural headwater streams [DOI]
  73. 73 Selection for Cry1F resistance in the European corn borer and cross‐resistance to other Cry toxins [DOI]
  74. 74 Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates [DOI]
  75. 75 Exposure and Nontarget Effects of TransgenicBtCorn Debris in Streams [DOI]
  76. 76 Effect of Bacillus thuringiensis Transgenic Corn for Lepidopteran Control on Nontarget Arthropods [DOI]
  77. 77 Effects of Bt corn pollen on honey bees: emphasis on protocol development [DOI]
  78. 78 Exposure and effects assessments of Bt-maize on non-target organisms (gastropods, microarthropods, mycorrhizal fungi) in microcosms [DOI]
  79. 79 Consumption of Bt Maize Pollen Expressing Cry1Ab or Cry3Bb1 Does Not Harm Adult Green Lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae) [DOI]
  80. 80 Decomposition processes under Bt (Bacillus thuringiensis) maize: Results of a multi-site experiment [DOI]
  81. 81 Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae) [DOI]
  82. 82 Decomposition dynamics and structural plant components of genetically modified Bt maize leaves do not differ from leaves of conventional hybrids [DOI]
  83. 83 Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae) [DOI]
  84. 84 Tritrophic Interactions of TransgenicBacillus thuringiensisCorn,Anaphothrips obscurus(Thysanoptera: Thripidae), and the PredatorOrius majusculus(Heteroptera: Anthocoridae) [DOI]
  85. 85 Evaluation of effects of transgenic Bt maize on microarthropods in a European multi-site experiment [DOI]
  86. 86 Larvicidal toxins fromBacillusthuringiensissubspp.kurstaki,morrisoni(straintenebrionis), andisraelensishave no microbicidal or microbiostatic activity against selected bacteria, fungi, and algae in vitro [DOI]
  87. 87 Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea [DOI]
  88. 88 Impact of insecticidal proteins expressed in transgenic plants on bumblebee microcolonies [DOI]
  89. 89 Susceptibility of Dipel-Resistant and -Susceptible Ostrinia nubilalis (Lepidoptera: Crambidae) to Individual Bacillus thuringiensis Protoxins [DOI]
  90. 90 Earthworms of different functional groups affect the fate of the Bt-toxin Cry1Ab from transgenic maize in soil [DOI]
  91. 91 Environmental risk assessment for the small tortoiseshell Aglais urticae and a stacked Bt‐maize with combined resistances against Lepidoptera and Chrysomelidae in central European agrarian landscapes [DOI]
  92. 92 Current state of genetically modified plant impact on target and non-target fungi [DOI]
  93. 93 Ingestion and excretion of two transgenic Bt corn varieties by slugs [DOI]
  94. 94 Assessment of the influence of field size on maize gene flow using SSR analysis [DOI]
  95. 95 Putative effects of Cry1Ab to larvae of Adalia bipunctata - reply to Hilbeck et al. (2012) [DOI]
  96. 96 A method to search for optimal field allocations of transgenic maize in the context of co-existence [DOI]
  97. 97 Influence of transgenic Bacillus thuringiensis corn-fed prey on prey preference of immature Chrysoperla carnea (Neuroptera: Chrysopidae) [DOI]
  98. 98 Outcrossing and coexistence of genetically modified with (genetically) unmodified crops: a case study of the situation in the Netherlands [DOI]
  99. 99 Effects of Bacillus thuringiensis Cry Toxins on Developmental and Reproductive Characteristics of the Predator Orius albidipennis (Hemiptera: Anthocoridae) Under Laboratory Conditions [DOI]
  100. 100 The presence of Bacillus thuringiensis (Bt) protein in earthworms Eisenia fetida has no deleterious effects on their growth and reproduction [DOI]
  101. 101 Field-Evolved Insect Resistance to Bt Crops: Definition, Theory, and Data [DOI]
  102. 102 Cry1Ab Protein Does Not Persist in Soil After 3 Years of Sustained Bt Corn Use [DOI]
  103. 103 Effects of dietary transgenic Bt corn pollen on larvae ofApis melliferaandGalleria mellonella [DOI]
  104. 104 Effects of Bacillus thuringiensis Toxins in Transgenic Cotton and Potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Orbatidae) [DOI]
  105. 105 Subacute Effects of Cry1AbBtCorn Litter on the EarthwormEisenia fetidaand the SpringtailFolsomia candida [DOI]
  106. 106 Genetically modified maize: pollen movement and crop co- existence
  107. 107 Release, persistence, and biological activity in soil of insecticidal proteins from Bacillus thuringiensis [DOI]
  108. 108 Ecological Impact of Genetically Modified Organisms
  109. 109 Faglig grunnlag for handlingsplan for heroringvinge Coenonympha hero

Cited by 11

Laboratory tests with Lepidoptera to assess non-target effects of Bt maize pollen: analysis of current studies and recommendations for a standardised design

A. Lang, Marina S. Lee, M. Dolek · Environmental Sciences Europe · 2019

Assessment of genetically modified maize MON 89034 × 1507 × MON 88017 × 59122 × DAS‐40278‐9 and subcombinations independently of their origin for food and feed uses, import and processing under Regulation (EC) No 1829/2003 (application EFSA‐GMO‐NL‐2013‐113)

H. Naegeli, J. Bresson, T. Dalmay · EFSA journal. European Food Safety Authority · 2019

Characterization of scientific studies usually cited as evidence of adverse effects of GM food/feed

M. A. Sánchez, W. Parrott · Plant Biotechnology Journal · 2017

Prospects of genetic modified maize crop in Africa

A. Mwamahonje, L. Mrosso · 2016

Potential exposure of butterflies in protected habitats by Bt maize cultivation: A case study in Switzerland

A. Lang, B. Oehen, J. Ross · 2015

Safety Evaluation of Stacked Genetically Modified Corn Event (MON89034 × MON88017) Using Zebrafish as an Animal Model

Ahmed M. Rayan, Fikru Nigussie, L. Abbott · 2015

Tempest in a Tea Pot: How did the Public Conversation on Genetically Modified Crops Drift so far from the Facts?

D. Goldstein · Journal of Medical Toxicology · 2014

Translational research: from pot to plot.

H. Nelissen, M. Moloney, D. Inzé · Plant Biotechnology Journal · 2014

Feeding Study with Bt Corn (MON810: Ajeeb YG) on Rats: Biochemical Analysis and Liver Histopathology

E. Abdo, O. Barbary,, Omayma El-Sayed Shaltout · 2014

Genetically modified farm animals and fish in agriculture: A review

F. Forabosco, M. Lõhmus, L. Rydhmer · 2013

Related research

Article metrics

Real usage data collected on this platform.

92

Page views

0

PDF downloads

30

Outbound clicks

11

Citations

Views over time

Views by country

Approximate, from request IP at view time — not citizenship or institution. Countries with fewer than 5 views are grouped as "Other".

Traffic sources

Referring site, by host.

Views and downloads exclude known bots/crawlers. Citations combines this platform's own DOI-resolved index with each external source's own reported total — see Cited by above for individually listed citing works. Last refreshed 0 seconds ago.