{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T03:01:20Z","timestamp":1787022080456,"version":"build-2736575974"},"reference-count":38,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2021,4,2]],"date-time":"2021-04-02T00:00:00Z","timestamp":1617321600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Africa Oxford (AfOx) Collaboration Fellowship Programme"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>\n                    From 2008 to 2018, South Africa permitted the export of captive-bred African lion (\n                    <jats:italic>Panthera leo<\/jats:italic>\n                    ) skeletons to Southeast Asia under CITES Appendix II. Legal exports rose from approximately 50 individuals in 2008 to a maximum of 1,771 skeletons in 2016, and has led to ongoing concerns over possible laundering of non-lion, multiple-source and wild-sourced bones. South Africa is required under its obligations to CITES to employ mechanisms for monitoring and reporting trade, and to limit the potential for illegal trade and laundering of lion and other large felid bones. Monitoring tools for legal trade are critical to compliance with CITES. Here we evaluate the CITES-compliance procedure implemented by South Africa for export of lion bones and identify six essential general points for consideration in the implementation of animal export quota compliance protocols. We provide specific insight into the South African lion bone export monitoring system through: i) outlining the protocols followed; ii) assessing the utility of cranial morphology to identify species; iii) evaluating skeleton consignment weight as a monitoring tool; and iv) presenting molecular (DNA) species assignment and pairwise-comparative sample matching of individuals. We describe irregularities and illicit behaviour detected in the 2017 and 2018 lion bone quotas. Notably, we report that the compliance procedure successfully identified and prevented the attempted laundering of a tiger (\n                    <jats:italic>P<\/jats:italic>\n                    .\n                    <jats:italic>tigris<\/jats:italic>\n                    ) skeleton in 2018. We emphasise the utility of mixed-method protocols for the monitoring of compliance in CITES Appendix II export quota systems.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0249306","type":"journal-article","created":{"date-parts":[[2021,4,2]],"date-time":"2021-04-02T13:31:30Z","timestamp":1617370290000},"page":"e0249306","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":20,"title":["Monitoring compliance of CITES lion bone exports from South Africa"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0698-6512","authenticated-orcid":true,"given":"Vivienne L.","family":"Williams","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1735-5487","authenticated-orcid":true,"given":"Peter G.","family":"Coals","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marli","family":"de Bruyn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincent N.","family":"Naude","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5975-6425","authenticated-orcid":true,"given":"Desir\u00e9 L.","family":"Dalton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antoinette","family":"Kotz\u00e9","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,4,2]]},"reference":[{"key":"pone.0249306.ref001","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1177\/194008291200500302","article-title":"Trade bans: A perfect storm for poaching?","volume":"5","author":"K. Conrad","year":"2012","journal-title":"Trop Conserv Sci"},{"key":"pone.0249306.ref002","author":"VL Williams","year":"2015"},{"key":"pone.0249306.ref003","doi-asserted-by":"crossref","first-page":"e0185996","DOI":"10.1371\/journal.pone.0185996","article-title":"A roaring trade? The legal trade in Panthera leo bones from Africa to East-Southeast Asia","volume":"12","author":"VL Williams","year":"2017","journal-title":"PLoS One"},{"key":"pone.0249306.ref004","article-title":"Born captive: A survey of the lion breeding, keeping and hunting industries in South Africa","author":"VL Williams","year":"2019","journal-title":"PLoS ONE."},{"key":"pone.0249306.ref005","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3390\/ani9020052","article-title":"The ethics of human\u2013animal relationships and public discourse: A case study of lions bred for their bones","volume":"9","author":"P Coals","year":"2019","journal-title":"Animals"},{"key":"pone.0249306.ref006","doi-asserted-by":"crossref","first-page":"5085","DOI":"10.3390\/su11185085","article-title":"Deep uncertainty, public reason, the conservation of biodiversity and the regulation of markets for lion skeletons","volume":"11","author":"P Coals","year":"2019","journal-title":"Sustain"},{"key":"pone.0249306.ref007","doi-asserted-by":"crossref","first-page":"e12444","DOI":"10.1111\/conl.12444","article-title":"Lions in the modern arena of CITES","volume":"11","author":"H Bauer","year":"2018","journal-title":"Conserv Lett"},{"key":"pone.0249306.ref008","article-title":"Convention on International Trade in Endangered Species of Wild Fauna and Flora","author":"CITES","year":"2020"},{"key":"pone.0249306.ref009","doi-asserted-by":"crossref","first-page":"e0135144","DOI":"10.1371\/journal.pone.0135144","article-title":"\u201cSkullduggery\u201d: Lions align and their mandibles rock!","volume":"10","author":"VL Williams","year":"2015","journal-title":"PLoS One"},{"key":"pone.0249306.ref010","article-title":"Consideration of Proposals for Amendment of Appendices I and II\u2014Proposal 4","author":"CITES","year":"2016","journal-title":"Seventeenth meeting of the Conference of the Parties"},{"key":"pone.0249306.ref011","article-title":"African populations of Panthera leo","volume":"64","author":"U Breitenmoser","year":"2016","journal-title":"CAT News"},{"key":"pone.0249306.ref012","author":"CITES","year":"2009","journal-title":"Management of nationally established export quotas"},{"key":"pone.0249306.ref013","doi-asserted-by":"crossref","first-page":"179","DOI":"10.3354\/esr00144","article-title":"Wildlife DNA forensics\u2013bridging the gap between conservation genetics and law enforcement","volume":"9","author":"R Ogden","year":"2009","journal-title":"Endanger Species Res"},{"key":"pone.0249306.ref014","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1007\/BF02729016","article-title":"Highly conserved D-loop-like nuclear mitochondrial sequences (Numts) in tiger (Panthera tigris)","volume":"85","author":"W Zhang","year":"2006","journal-title":"J Genet"},{"key":"pone.0249306.ref015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.forsciint.2006.09.013","article-title":"Validation of the barcoding gene COI for use in forensic genetic species identification","volume":"173","author":"N Dawnay","year":"2007","journal-title":"Forensic Sci Int"},{"key":"pone.0249306.ref016","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.forsciint.2007.01.019","article-title":"Identification of mammal species using species-specific DNA pyrosequencing","volume":"173","author":"AO Karlsson","year":"2007","journal-title":"Forensic Sci Int"},{"key":"pone.0249306.ref017","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1111\/j.1556-4029.2007.00553.x","article-title":"Routine forensic use of the mitochondrial 12S ribosomal RNA gene for species identification","volume":"52","author":"T Melton","year":"2007","journal-title":"J Forensic Sci"},{"key":"pone.0249306.ref018","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1520\/JFS14258J","article-title":"Genetic individualization of domestic cats using feline STR loci for forensic applications","volume":"42","author":"M Menotti-Raymond","year":"1997","journal-title":"J Forensic Sci"},{"key":"pone.0249306.ref019","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1006\/geno.1999.5743","article-title":"A genetic linkage map of microsatellites in the domestic cat (Felis catus)","volume":"57","author":"M Menotti-Raymond","year":"1999","journal-title":"Genomics"},{"key":"pone.0249306.ref020","doi-asserted-by":"crossref","first-page":"2996","DOI":"10.1002\/ece3.4757","article-title":"Incomplete estimates of genetic diversity within species: implications for DNA barcoding","volume":"9","author":"JD Phillips","year":"2019","journal-title":"Ecol Evol"},{"key":"pone.0249306.ref021","first-page":"258","article-title":"Estimating relatedness using genetic markers","volume":"43","author":"DC Queller","year":"1989","journal-title":"Evolution (N Y)"},{"key":"pone.0249306.ref022","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fevo.2019.00302","article-title":"Review and interpretation of trends in DNA barcoding","volume":"7","author":"R DeSalle","year":"2019","journal-title":"Front Ecol Evol"},{"key":"pone.0249306.ref023","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3957\/056.044.0107","article-title":"Rapid growth rates of lion (Panthera leo) populations in small, fenced reserves in South Africa: a management dilemma","volume":"44","author":"SM Miller","year":"2014","journal-title":"S Afr J Wildl Res"},{"key":"pone.0249306.ref024","article-title":"Determination of the 2019","author":"M. Pickover","year":"2019","journal-title":"lion bone quota"},{"key":"pone.0249306.ref025","article-title":"R: A language and environment for statistical computing","author":"Core Team","year":"2019"},{"key":"pone.0249306.ref026","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s12686-018-1060-x","article-title":"A tale of the traded cat: development of a rapid real-time PCR diagnostic test to distinguish between lion and tiger bone","volume":"12","author":"DL Dalton","year":"2020","journal-title":"Conserv Genet Resour."},{"key":"pone.0249306.ref027","first-page":"96","article-title":"Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species","volume":"270","author":"PDN Hebert","year":"2003","journal-title":"Proc R Soc B Biol Sci"},{"key":"pone.0249306.ref028","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s004140000134","article-title":"Species identification by means of the cytochrome b gene","volume":"114","author":"W Parson","year":"2000","journal-title":"Int J Legal Med"},{"key":"pone.0249306.ref029","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"SF Altschul","year":"1990","journal-title":"J Mol Biol"},{"key":"pone.0249306.ref030","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1093\/genetics\/155.2.945","article-title":"Inference of population structure using multilocus genotype data","volume":"155","author":"JK Pritchard","year":"2000","journal-title":"Genetics"},{"key":"pone.0249306.ref031","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.1093\/genetics\/164.4.1567","article-title":"Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies","volume":"164","author":"D Falush","year":"2003","journal-title":"Genetics"},{"key":"pone.0249306.ref032","doi-asserted-by":"crossref","first-page":"1322","DOI":"10.1111\/j.1755-0998.2009.02591.x","article-title":"Inferring weak population structure with the assistance of sample group information","volume":"9","author":"MJ Hubisz","year":"2009","journal-title":"Mol Ecol Resour"},{"key":"pone.0249306.ref033","doi-asserted-by":"crossref","first-page":"1801","DOI":"10.1093\/bioinformatics\/btm233","article-title":"CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure","volume":"23","author":"M Jakobsson","year":"2007","journal-title":"Bioinformatics"},{"key":"pone.0249306.ref034","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1046\/j.1471-8286.2003.00566.x","article-title":"DISTRUCT: A program for the graphical display of population structure","volume":"4","author":"NA Rosenberg","year":"2004","journal-title":"Mol Ecol Notes"},{"key":"pone.0249306.ref035","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1111\/j.1365-294X.2007.03089.x","article-title":"Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment","volume":"16","author":"ST Kalinowski","year":"2007","journal-title":"Mol Ecol"},{"key":"pone.0249306.ref036","first-page":"1280","article-title":"An exact test for population differentiation","volume":"49","author":"M Raymond","year":"1995","journal-title":"Evolution (N Y)"},{"key":"pone.0249306.ref037","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1111\/j.1471-8286.2005.01155.x","article-title":"GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research","volume":"6","author":"R Peakall","year":"2006","journal-title":"Mol Ecol Notes"},{"key":"pone.0249306.ref038","doi-asserted-by":"crossref","first-page":"13486","DOI":"10.1073\/pnas.0803076105","article-title":"Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified","volume":"105","author":"H Song","year":"2008","journal-title":"Proc Natl Acad Sci U S A"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0249306","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,1]],"date-time":"2023-11-01T11:59:13Z","timestamp":1698839953000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0249306"}},"subtitle":[],"editor":[{"given":"Kuo-Hsiang","family":"Hung","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,4,2]]},"references-count":38,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4,2]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0249306","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,2]]}}}