{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T22:33:57Z","timestamp":1792708437348,"version":"4.5.0"},"reference-count":55,"publisher":"National Academy of Sciences","issue":"10","license":[{"start":{"date-parts":[[2015,2,23]],"date-time":"2015-02-23T00:00:00Z","timestamp":1424649600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.pnas.org\/site\/misc\/userlicense.xhtml"}],"funder":[{"DOI":"10.13039\/501100004963","name":"Seventh Framework Programme","doi-asserted-by":"publisher","award":["302329"],"award-info":[{"award-number":["302329"]}],"id":[{"id":"10.13039\/501100004963","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000781","name":"EC | European Research Council","doi-asserted-by":"publisher","award":["324249"],"award-info":[{"award-number":["324249"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2015,3,10]]},"abstract":"<jats:title>Significance<\/jats:title>\n                  <jats:p>\n                    The second plague pandemic in medieval Europe started with the Black Death epidemic of 1347\u20131353 and killed millions of people over a time span of four centuries. It is commonly thought that after its initial introduction from Asia, the disease persisted in Europe in rodent reservoirs until it eventually disappeared. Here, we show that climate-driven outbreaks of\n                    <jats:italic>Yersinia pestis<\/jats:italic>\n                    in Asian rodent plague reservoirs are significantly associated with new waves of plague arriving into Europe through its maritime trade network with Asia. This association strongly suggests that the bacterium was continuously reimported into Europe during the second plague pandemic, and offers an alternative explanation to putative European rodent reservoirs for how the disease could have persisted in Europe for so long.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1412887112","type":"journal-article","created":{"date-parts":[[2015,2,25]],"date-time":"2015-02-25T17:27:01Z","timestamp":1424885221000},"page":"3020-3025","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":245,"title":["Climate-driven introduction of the Black Death and successive plague reintroductions into Europe"],"prefix":"10.1073","volume":"112","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0452-623X","authenticated-orcid":false,"given":"Boris V.","family":"Schmid","sequence":"first","affiliation":[{"name":"Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0316 Oslo, Norway;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ulf","family":"B\u00fcntgen","sequence":"additional","affiliation":[{"name":"Dendroecology, Landscape Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape, CH-8903 Birmensdorf, Switzerland;"},{"name":"Oeschger Centre for Climate Change Research, University of Bern, CH-3012 Bern, Switzerland;"},{"name":"Global Change Research Centre AS CR, v.v.i., CZ-60300 Brno, Czech Republic; and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"W. Ryan","family":"Easterday","sequence":"additional","affiliation":[{"name":"Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0316 Oslo, Norway;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Ginzler","sequence":"additional","affiliation":[{"name":"Dendroecology, Landscape Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape, CH-8903 Birmensdorf, Switzerland;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lars","family":"Wall\u00f8e","sequence":"additional","affiliation":[{"name":"Department of Physiology, Institute of Basic Medical Sciences, University of Oslo, NO-0372 Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara","family":"Bramanti","sequence":"additional","affiliation":[{"name":"Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0316 Oslo, Norway;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nils Chr.","family":"Stenseth","sequence":"additional","affiliation":[{"name":"Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0316 Oslo, Norway;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2015,2,23]]},"reference":[{"key":"e_1_3_3_1_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1001134"},{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1003349"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.0050003"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1093\/clinids\/6.6.866"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.2307\/204499"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1038\/35038073"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1002160"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1015946108"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0602447103"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1461-0248.2012.01767.x"},{"key":"e_1_3_3_11_2","first-page":"1963","article-title":"Climatically driven synchrony of gerbil populations allows large-scale plague outbreaks","volume":"274","author":"Kausrud KL","year":"2007","unstructured":"KL Kausrud, , Climatically driven synchrony of gerbil populations allows large-scale plague outbreaks. Proc Biol Sci 274, 1963\u20131969 (2007).","journal-title":"Proc Biol Sci"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(98)01498-0"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-0587.2002.250304.x"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature07053"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsbl.2014.0302"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0950268808000940"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1473-3099(09)70104-5"},{"key":"e_1_3_3_18_2","first-page":"393","volume-title":"The Pamphleteer","author":"Granville AB","year":"1825","unstructured":"AB Granville, A. B. Granville\u2019s letter on the quarantine bill. The Pamphleteer (Sherwood and Co., London) Vol 25, 393\u2013403 (1825)."},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.meegid.2012.11.016"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jas.2012.12.007"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.3201\/eid0809.010536"},{"key":"e_1_3_3_22_2","volume-title":"The Flowering of the Middle Ages (The Great Civilizations)","author":"Evans J","year":"1967","unstructured":"J Evans The Flowering of the Middle Ages (The Great Civilizations) (Thames & Hudson Ltd, London, 1967)."},{"key":"e_1_3_3_23_2","first-page":"162","article-title":"The second plague pandemic and its recurrences in the Middle East: 1347-1894","volume":"22","author":"Dols MW","year":"1979","unstructured":"MW Dols, The second plague pandemic and its recurrences in the Middle East: 1347-1894. J Econ Soc Hist Orient 22, 162\u2013189 (1979).","journal-title":"J Econ Soc Hist Orient"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1205750110"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0002166"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1185188"},{"key":"e_1_3_3_27_2","first-page":"1","article-title":"Wet climate and transportation routes accelerate spread of human plague","volume":"281","author":"Lei X","year":"2014","unstructured":"X Lei, , Wet climate and transportation routes accelerate spread of human plague. Proc R Soc Lond B Biol Sci 281, 1\u20139 (2014).","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.puhe.2006.12.011"},{"key":"e_1_3_3_29_2","first-page":"275","article-title":"Plague in camels and its prevention in the USSR","volume":"23","author":"Fedorov VN","year":"1960","unstructured":"VN Fedorov, Plague in camels and its prevention in the USSR. Bull World Health Organ 23, 275\u2013281 (1960).","journal-title":"Bull World Health Organ"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.13173\/jasiahist.47.1.0001"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0025727300072100"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0008401"},{"key":"e_1_3_3_33_2","unstructured":"F Braun St\u00e4dtesystem und Urbanisierung im Ostseeraum in der fr\u00fchen Neuzeit: Wirtschaft Baukultur und historische Informationssysteme: Beitr\u00e4ge des wissenschaftlichen Kolloquiums in Wismar vom 4. und 5. September 2003 (LIT Munster Germany). German. (2004)."},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1093877"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1029\/2005GL023424"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1603\/ME10155"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1186\/1756-3305-4-191"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0025727300072094"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.2307\/4587908"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature10549"},{"key":"e_1_3_3_41_2","doi-asserted-by":"crossref","unstructured":"JJN Biraben Les hommes et la peste en France et dans les pays europ\u00e9ens et m\u00e9diterran\u00e9ens (Mouton Paris-La Haye). French. (1976).","DOI":"10.3917\/popu.p1975.30n6.1144"},{"key":"e_1_3_3_42_2","unstructured":"V Atanasiu C Priol A Tournieroux E Ornato Yersinia. Georeferences for places of plague occurrence in Europe 1347-1600 . Available at www.bernstein.oeaw.ac.at\/atlas\/yersinia-description.pdf. (2008)."},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1093\/cid\/cis723"},{"key":"e_1_3_3_44_2","first-page":"244","article-title":"Reconsiderations on plague in early modern Russia, 1500-1800","volume":"34","author":"Alexander JT","year":"1986","unstructured":"JT Alexander, Reconsiderations on plague in early modern Russia, 1500-1800. Jahrb Gesch Osteur 34, 244\u2013254 (1986).","journal-title":"Jahrb Gesch Osteur"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1080\/10408410500496763"},{"key":"e_1_3_3_46_2","first-page":"377","article-title":"La peste noire \u00e0 Constantinople de 1348 \u00e0 1466 [Black Death in Constantinople (1343-1466)]","volume":"11","author":"Congourdeau M-H","year":"1999","unstructured":"M-H Congourdeau, La peste noire \u00e0 Constantinople de 1348 \u00e0 1466 [Black Death in Constantinople (1343-1466)]. Med Secoli 11, 377\u2013389, French. (1999).","journal-title":"Med Secoli"},{"key":"e_1_3_3_47_2","unstructured":"G Marien The Black Death in early Ottoman territories: 1347\u20131550. PhD dissertation (Bilkent University Ankara Turkey). (2009)."},{"key":"e_1_3_3_48_2","first-page":"45","article-title":"The smoothing spline: A new approach to standardizing forest interior tree-ring width series for dendroclimatic studies","volume":"41","author":"Cook ER","year":"1981","unstructured":"ER Cook, K Peters, The smoothing spline: A new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree-Ring Bulletin 41, 45\u201353 (1981).","journal-title":"Tree-Ring Bulletin"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1177\/095968369700700314"},{"key":"e_1_3_3_50_2","first-page":"89","article-title":"Adjusting variance for sample-size in tree-ring chronologies and other regional mean timeseries","volume":"15","author":"Osborn TJ","year":"1997","unstructured":"TJ Osborn, KR Briffa, PD Jones, Adjusting variance for sample-size in tree-ring chronologies and other regional mean timeseries. Dendrochronologia 15, 89\u201399 (1997).","journal-title":"Dendrochronologia"},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1029\/2007GL030571"},{"key":"e_1_3_3_52_2","volume-title":"Power and Profit: The Merchant in Medieval Europe","author":"Spufford P","year":"2002","unstructured":"P Spufford Power and Profit: The Merchant in Medieval Europe (Thames & Hudson, London, 2002)."},{"key":"e_1_3_3_53_2","unstructured":"TM Ciolek 1999-present. Old World Trade Routes (OWTRAD) Project. Canberra: www.ciolek.com\u2014Asia Pacific Research Online. Available at www.ciolek.com\/owtrad.html. Accessed February 16 2014. (1999)."},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.3406\/remmm.1985.2071"},{"key":"e_1_3_3_55_2","unstructured":"RWF Gross Historical Atlas of Eurasia 3rd Ed. Available at productforums.google.com\/forum\/#!msg\/gec-history-illustrated-moderated\/9UrX_lQEzYE\/ORYfbWZhPuEJ. Accessed July 11 2013. (2012)."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.pnas.org\/syndication\/doi\/10.1073\/pnas.1412887112","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1412887112","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,7]],"date-time":"2024-06-07T08:04:37Z","timestamp":1717747477000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1412887112"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,2,23]]},"references-count":55,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2015,3,10]]}},"alternative-id":["10.1073\/pnas.1412887112"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1412887112","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,2,23]]},"assertion":[{"value":"2015-02-23","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}