{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,27]],"date-time":"2026-05-27T15:03:48Z","timestamp":1779894228565,"version":"3.53.1"},"reference-count":59,"publisher":"Wiley","issue":"22","license":[{"start":{"date-parts":[[2018,10,28]],"date-time":"2018-10-28T00:00:00Z","timestamp":1540684800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2018,10,28]],"date-time":"2018-10-28T00:00:00Z","timestamp":1540684800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000203","name":"U.S. Geological Survey","doi-asserted-by":"publisher","award":["G16AC00106"],"award-info":[{"award-number":["G16AC00106"]}],"id":[{"id":"10.13039\/100000203","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Ecology and Evolution"],"published-print":{"date-parts":[[2018,11]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:label\/>\n                    <jats:p>\n                      Demonstrating disease impacts on the vital rates of free\u2010ranging mammalian hosts typically requires intensive, long\u2010term study. Evidence for chronic pathogens affecting reproduction but not survival is rare, but has the potential for wide\u2010ranging effects. Accurately quantifying disease\u2010associated reductions in fecundity is important for advancing theory, generating accurate predictive models, and achieving effective management. We investigated the impacts of brucellosis (\n                      <jats:italic>Brucella abortus<\/jats:italic>\n                      ) on elk (\n                      <jats:italic>Cervus canadensis<\/jats:italic>\n                      ) productivity using serological data from over 6,000 captures since 1990 in the Greater Yellowstone Ecosystem, USA. Over 1,000 of these records included known age and pregnancy status. Using Bayesian multilevel models, we estimated the age\u2010specific pregnancy probabilities of exposed and na\u00efve elk. We then used repeat\u2010capture data to investigate the full effects of the disease on life history. Brucellosis exposure reduced pregnancy rates of elk captured in mid\u2010 and late\u2010winter. In an average year, we found 60% of exposed 2\u2010year\u2010old elk were pregnant compared to 91% of their na\u00efve counterparts (a 31 percentage point reduction, 89% HPDI\u00a0=\u00a020%\u201342%), whereas exposed 3\u2010 to 9\u2010year\u2010olds were 7 percentage points less likely to be pregnant than na\u00efve elk of their same age (89% HPDI\u00a0=\u00a02%\u201311%). We found these reduced rates of pregnancy to be independent from disease\u2010induced abortions, which afflict a portion of exposed elk. We estimate that the combination of reduced pregnancy by mid\u2010winter and the abortions following mid\u2010winter reduces the reproductive output of exposed female elk by 24%, which affects population dynamics to a similar extent as severe winters or droughts. Exposing hidden reproductive costs of disease is essential to avoid conflating them with the effects of climate and predation. Such reproductive costs cause complex population dynamics, and the magnitude of the effect we found should drive a strong selection gradient if there is heritable resistance.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1002\/ece3.4521","type":"journal-article","created":{"date-parts":[[2018,10,28]],"date-time":"2018-10-28T22:54:59Z","timestamp":1540767299000},"page":"10733-10742","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Hidden cost of disease in a free\u2010ranging ungulate: brucellosis reduces mid\u2010winter pregnancy in elk"],"prefix":"10.1002","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1408-778X","authenticated-orcid":false,"given":"Gavin G.","family":"Cotterill","sequence":"first","affiliation":[{"name":"Department of Wildland Resources Utah State University Logan Utah"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8045-5213","authenticated-orcid":false,"given":"Paul C.","family":"Cross","sequence":"additional","affiliation":[{"name":"U.S. Geological Survey Northern Rocky Mountain Science Center Bozeman Montana"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arthur D.","family":"Middleton","sequence":"additional","affiliation":[{"name":"Department of Environmental Science, Policy and Management University of California Berkeley California"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jared D.","family":"Rogerson","sequence":"additional","affiliation":[{"name":"Wyoming Game and Fish Department Pinedale Wyoming"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8671-3842","authenticated-orcid":false,"given":"Brandon M.","family":"Scurlock","sequence":"additional","affiliation":[{"name":"Wyoming Game and Fish Department Pinedale Wyoming"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0705-7117","authenticated-orcid":false,"given":"Johan T.","family":"du Toit","sequence":"additional","affiliation":[{"name":"Department of Wildland Resources Utah State University Logan Utah"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2018,10,28]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1461-0248.2005.00879.x"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10393-017-1235-z"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0178780"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0102330"},{"key":"e_1_2_8_6_1","volume-title":"Coexisting with large carnivores: Lessons from greater yellowstone","author":"Clark T.","year":"2013"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1002\/jwmg.917"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.2193\/0084-0173(2004)155[1:EOSNAP]2.0.CO;2"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2017.0093"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1135918"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1890\/08-2062.1"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1890\/06-1603"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2664.2008.01589.x"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1002\/jwmg.883"},{"key":"e_1_2_8_15_1","unstructured":"Dean R. Gocke M. Holz B. Kilpatrick S. Kreeger T. Scurlock B. \u2026Werbelow S.(2004).Elk feedgrounds in Wyoming. Wyoming Game and Fish Department (Unpublished Report). Cheyenne Wyoming USA. Retrieved fromhttps:\/\/wgfd.wyo.gov\/WGFD\/media\/content\/PDF\/Wildlife\/WY_ELKFEEDGROUNDS.pdf"},{"key":"e_1_2_8_16_1","first-page":"301","volume-title":"Animal brucellosis","author":"Enright F.","year":"1990"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1002\/jwmg.908"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.1111\/geb.12290"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.2193\/2006-201"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-37.1.110"},{"key":"e_1_2_8_21_1","unstructured":"Galloway N. L. Monello R. J. Brimeyer D. Cole E. &Hobbs N. T.(2017).Model forecasting of the impacts of chronic wasting disease on the Jackson elk herd. Retrieved fromhttps:\/\/www.researchgate.net\/profile\/Eric_Cole4\/publication\/312435900_Model_Forecasting_of_the_Impacts_of_CWD_on_the_Jackson_Elk_Herd\/links\/587d20c308aed3826af00c3b.pdf"},{"key":"e_1_2_8_22_1","first-page":"255","volume-title":"Terrestrial ecology","author":"Geremia C.","year":"2008"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365-2656.12356"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1098\/rsif.2016.0156"},{"key":"e_1_2_8_25_1","doi-asserted-by":"crossref","unstructured":"Hobbs N.T. Geremia C. Treanor J. Wallen R. White P. J. Hooten M. B. &Rhyan J. C.(2015).State\u2010space modeling to support management of brucellosis in the Yellowstone bison population. Ecological Monographs 85(4) 525\u2010556.https:\/\/doi.org\/10.1890\/14-1413.1","DOI":"10.1890\/14-1413.1"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1000210"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/cobi.12152"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40588-017-0052-z"},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1890\/05-0038"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms11448"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1002\/wsb.734"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1071\/PC940107"},{"key":"e_1_2_8_33_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2012.0224"},{"key":"e_1_2_8_34_1","unstructured":"McElreath R.(2016).Rethinking: Statistical rethinking book package. (Version 1.59)."},{"issue":"2","key":"e_1_2_8_35_1","doi-asserted-by":"crossref","first-page":"274","DOI":"10.2460\/ajvr.1988.49.02.274","article-title":"Histopathologic findings in Brucella abortus\u2010infected, pregnant goats","volume":"49","author":"Meador V. P.","year":"1988","journal-title":"American Journal of Veterinary Research"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.2307\/3803048"},{"key":"e_1_2_8_37_1","doi-asserted-by":"publisher","DOI":"10.1890\/11-2298.1"},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.1111\/ele.12133"},{"key":"e_1_2_8_39_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1707807114"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-018-0616-1"},{"key":"e_1_2_8_41_1","volume-title":"Revisiting brucellosis in the Greater Yellowstone Area","author":"National Academies of Sciences, Engineering, and Medicine","year":"2017"},{"key":"e_1_2_8_42_1","volume-title":"Brucellosis in the Greater Yellowstone Area","author":"National Research Council","year":"1998"},{"issue":"3","key":"e_1_2_8_43_1","first-page":"695","article-title":"Accuracy of pregnancy detection by serum protein (PSPB) in elk","volume":"25","author":"Noyes J. H.","year":"1997","journal-title":"Wildlife Society Bulletin (1973\u20102006)"},{"key":"e_1_2_8_44_1","unstructured":"Oldemeyer J. Robbins R. &Smith B.(1990).Effect of feeding level on elk weights and reproductive success at the National Elk Refuge. In Proceedings of the western states and provinces elk workshop (RL Callas DC Koch and ER Loft eds.) (pp.64\u201368).California Fish and Game Department Eureka CA. Retrieved fromhttp:\/\/www.wafwa.org\/Documents%20and%20Settings\/37\/Site%20Documents\/Working%20Groups\/Elk%20Workshops\/1990%20Eureka%20CA%20Elk%20Workshop\/1990%20Eureka%20CA%20Elk%20Workshop\/Effect%20of%20Feeding%20Level%20on%20Elk%20Weights%20and%20Reproductive%20Succ.pdf"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2007.1068"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.1002\/jwmg.792"},{"key":"e_1_2_8_47_1","volume-title":"R: A language and environment for statistical computing","author":"R Core Team","year":"2016"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.2193\/2005-608"},{"key":"e_1_2_8_49_1","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-45.3.729"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1890\/11-0907.1"},{"key":"e_1_2_8_51_1","doi-asserted-by":"publisher","DOI":"10.2192\/1537-6176(2006)17[63:DOGBIT]2.0.CO;2"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-46.2.442"},{"key":"e_1_2_8_53_1","unstructured":"Stan Development Team(2017).Stan modeling language users guide and reference manual (Version 2.17.0). Retrieved fromhttp:\/\/mc-stan.org"},{"key":"e_1_2_8_54_1","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-14.3.280"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11222-016-9696-4"},{"issue":"2","key":"e_1_2_8_56_1","first-page":"75","article-title":"Abortions and infertility in livestock due to brucellosis in Himachal Pradesh, India","volume":"70","author":"Verma S.","year":"2000","journal-title":"Veterinarski Arhiv"},{"key":"e_1_2_8_57_1","first-page":"3571","article-title":"Asymptotic equivalence of Bayes cross validation and Widely Applicable Information Criterion in singular learning theory","volume":"11","author":"Watanabe S.","year":"2010","journal-title":"Journal of Machine Learning Research"},{"key":"e_1_2_8_58_1","doi-asserted-by":"publisher","DOI":"10.1890\/09-2123.1"},{"key":"e_1_2_8_59_1","doi-asserted-by":"publisher","DOI":"10.1002\/9780470344880.ch17"},{"key":"e_1_2_8_60_1","doi-asserted-by":"publisher","DOI":"10.1890\/ES14-00013.1"}],"container-title":["Ecology and Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fece3.4521","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ece3.4521","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/ece3.4521","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/am-pdf\/10.1002%2Fece3.4521","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ece3.4521","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ece3.4521","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T22:10:59Z","timestamp":1775254259000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/ece3.4521"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,10,28]]},"references-count":59,"journal-issue":{"issue":"22","published-print":{"date-parts":[[2018,11]]}},"alternative-id":["10.1002\/ece3.4521"],"URL":"https:\/\/doi.org\/10.1002\/ece3.4521","archive":["Portico"],"relation":{},"ISSN":["2045-7758","2045-7758"],"issn-type":[{"value":"2045-7758","type":"print"},{"value":"2045-7758","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,10,28]]},"assertion":[{"value":"2018-06-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-08-19","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-10-28","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}