{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T11:07:09Z","timestamp":1788865629152,"version":"build-2803163510"},"reference-count":80,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T00:00:00Z","timestamp":1788825600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T00:00:00Z","timestamp":1788825600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100006450","name":"Bureau of Reclamation","doi-asserted-by":"publisher","award":["R20AC00027"],"award-info":[{"award-number":["R20AC00027"]}],"id":[{"id":"10.13039\/100006450","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Journal of Fish Biology"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    In the San Francisco Estuary, non\u2010native Wakasagi\n                    <jats:italic>Hypomesus nipponensis<\/jats:italic>\n                    hybridize with endemic and endangered Delta Smelt\n                    <jats:italic>H. transpacificus<\/jats:italic>\n                    , and all wild\u2010caught hybrids have a maternal Wakasagi parent. However, the mechanisms that facilitate or impede hybridization and explain sex\u2010biased hybrid asymmetry between these two species remain unclear. We conducted a no\u2010choice spawning experiment, in which wild\u2010caught Wakasagi (WK) and cultured Delta Smelt (DS) spawned naturally in different species\u2010sex combinations: five Delta Smelt females with five Wakasagi males (DS\u2009\u00d7\u2009WK), five Wakasagi females with five Delta Smelt males (WK\u2009\u00d7\u2009DS) and five Wakasagi females with five Wakasagi males (WK\u2009\u00d7\u2009WK). We compared these data to those from a previous study testing DS\u2009\u00d7\u2009DS using the same methods. We quantified the frequency of spawns and attempts, sex ratio of participants and diel timing of behaviours, as well as the fertilization success of resulting eggs. Wakasagi engaged in five times more spawns than Delta Smelt in same\u2010species trials, and spawns were more frequent in WK\u2009\u00d7\u2009DS than in DS\u2009\u00d7\u2009WK trials. Whereas fish in WK\u2009\u00d7\u2009WK trials exhibited mostly diurnal spawns, those in all other crosses exhibited predominantly nocturnal spawns. Eggs resulting from WK\u2009\u00d7\u2009DS trials had lower fertilization success than those in all other crosses. These results did not clearly explain the hybrid asymmetry observed in nature. Nevertheless, our study demonstrated that: 1) Wakasagi exhibited a very high propensity to spawn, which may provide a reproductive advantage over Delta Smelt, 2) Wakasagi showed great plasticity in spawning behaviour, which may facilitate interspecific spawning and 3) all crosses produced fertilized eggs, demonstrating that there are no complete pre\u2010zygotic barriers to hybridization. Ultimately, any level of Delta Smelt spawning activity that includes Wakasagi is wasted reproductive potential, and our study highlights the mechanisms by and degree to which this may occur.\n                  <\/jats:p>","DOI":"10.1111\/jfb.70626","type":"journal-article","created":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T10:11:51Z","timestamp":1788862311000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Spawning behaviour between endemic delta smelt (\n                    <i>Hypomesus transpacificus<\/i>\n                    ) and non\u2010native Wakasagi (\n                    <i>H. nipponensis<\/i>\n                    ) in the San Francisco estuary"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7575-8225","authenticated-orcid":false,"given":"Yi\u2010Jiun Jean","family":"Tsai","sequence":"first","affiliation":[{"name":"Department of Biological and Agricultural Engineering University of California  Davis California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3876-4570","authenticated-orcid":false,"given":"Luke","family":"Ellison","sequence":"additional","affiliation":[{"name":"Department of Biological and Agricultural Engineering University of California  Davis California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3850-3685","authenticated-orcid":false,"given":"Amanda J.","family":"Finger","sequence":"additional","affiliation":[{"name":"Department of Animal Science University of California  Davis California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5502-9984","authenticated-orcid":false,"given":"Evan W.","family":"Carson","sequence":"additional","affiliation":[{"name":"US Fish and Wildlife Service, San Francisco Bay\u2010Delta Fish and Wildlife Office  Sacramento California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5419-0282","authenticated-orcid":false,"given":"Nann A.","family":"Fangue","sequence":"additional","affiliation":[{"name":"Department of Wildlife, Fish and Conservation Biology University of California  Davis California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9618-5887","authenticated-orcid":false,"given":"Tien\u2010Chieh","family":"Hung","sequence":"additional","affiliation":[{"name":"Department of Biological and Agricultural Engineering University of California  Davis California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,8]]},"reference":[{"key":"e_1_2_8_2_1","first-page":"31","article-title":"Establishment of Wakasagi, Hypomesus nipponensis, in the Sacramento\u2010San Joaquin estuary","volume":"84","author":"Aasen G. A.","year":"1998","journal-title":"California Fish & Game"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(01)02290-X"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.0022-1112.2006.01002.x"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jcz.2023.11.008"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v067.i01"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10592-018-1048-9"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.15447\/sfews.2005v3iss2art1"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1054-3139(97)80008-2"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1086\/722136"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biocon.2016.10.011"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1006\/anbe.2002.2024"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1111\/jfb.15240"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.32614\/RJ-2017-066"},{"key":"e_1_2_8_15_1","volume-title":"State and federally listed endangered and threatened animals of California","author":"California Natural Diversity Database","year":"2025"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1029\/2012RG000397"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.279.5350.555"},{"key":"e_1_2_8_18_1","first-page":"188","article-title":"Fecundity and reproductive potential of wild female Delta smelt in the upper San Francisco estuary, California","volume":"102","author":"Damon L. J.","year":"2016","journal-title":"California Fish & Game"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.15447\/sfews.2022v20iss3art2"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1602480113"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1002\/aff2.116"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1093\/jhered\/esy035"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1093\/jhered\/ess084"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10592-013-0555-y"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/0044-8486(92)90405-A"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.2307\/1941826"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2000.1173"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.2307\/2404960"},{"key":"e_1_2_8_29_1","volume-title":"An R companion to applied regression","author":"Fox J.","year":"2019"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1111\/fwb.12610"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8649.2010.02566.x"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1577\/M08-062.1"},{"key":"e_1_2_8_33_1","doi-asserted-by":"publisher","DOI":"10.1093\/beheco\/14.2.282"},{"key":"e_1_2_8_34_1","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.1114"},{"key":"e_1_2_8_35_1","unstructured":"Hartig F. Lohse L. &deSouza leite M.(2024).Residual diagnostics for hierarchical (multi\u2010lavel\/mixed) regression models. R package version 0.4.7.http:\/\/florianhartig.github.io\/DHARMa\/"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0016557"},{"key":"e_1_2_8_37_1","doi-asserted-by":"publisher","DOI":"10.2331\/fishsci.64.995"},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-52273-8"},{"key":"e_1_2_8_39_1","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1111\/j.1365-2699.2007.01782.x","article-title":"Evolutionary and biogeographical patterns within the smelt genus Hypomesus in the North Pacific Ocean","volume":"35","author":"Ilves K. L.","year":"2008","journal-title":"Journal of Biogeography"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8649.1991.tb04403.x"},{"key":"e_1_2_8_41_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1444-2906.2001.00275.x"},{"key":"e_1_2_8_42_1","first-page":"87","article-title":"Pond smelt spawning in the inflowing river into Lake Ogawara","volume":"45","author":"Katayama S.","year":"1995","journal-title":"Tohoku Journal of Agricultural Research"},{"key":"e_1_2_8_43_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1007682729460"},{"key":"e_1_2_8_44_1","first-page":"175","article-title":"Variation in migration patterns of pond smelt, Hypomesus nipponensis, in Japan determined by otolith microchemical analysis","volume":"71","author":"Katayama S.","year":"2007","journal-title":"Bulletin of the Japanese Society of Fisheries Oceanography"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02674943"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10641-016-0483-z"},{"key":"e_1_2_8_47_1","doi-asserted-by":"publisher","DOI":"10.1080\/15222055.2015.1007192"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1523-1739.1993.740856.x"},{"key":"e_1_2_8_49_1","unstructured":"Lenth R. V. Banfai B. Bolker B. Buerkner P. Gin\u00e9\u2010V\u00e1squez I. Herve M. Jung M. Love J. Miguez F. Piaskowski J. Riebl H. &Singmann H.(2025).Emmeans: Estimated marginal means aka least\u2010squares means. R package version 1.11.2\u20138.https:\/\/CRAN.R-project.org\/package=emmeans"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1080\/15222055.2012.751942"},{"key":"e_1_2_8_51_1","volume-title":"Interagency ecological program annual workshop. Poster presentation","author":"Macfarlane C.","year":"2026"},{"key":"e_1_2_8_52_1","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1525\/9780520926516-016","volume-title":"Inland fishes of California: Revised and expanded","author":"Moyle P. B.","year":"2002"},{"key":"e_1_2_8_53_1","doi-asserted-by":"publisher","DOI":"10.15447\/sfews.2016v14iss2art6"},{"key":"e_1_2_8_54_1","first-page":"44","article-title":"Spawning behavior of Wakasagi in inflowing rivers of Lake Kawaguchiko","volume":"35","author":"Okazaki T.","year":"2011","journal-title":"Report of Yamanashi Prefectural Fishing Technology Center"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1006\/gcen.1993.1014"},{"key":"e_1_2_8_56_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biocon.2018.05.019"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11355-021-00462-x"},{"key":"e_1_2_8_58_1","unstructured":"R Core Team. (2025).R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria.https:\/\/www.R-project.org\/"},{"key":"e_1_2_8_59_1","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1146\/annurev.ecolsys.27.1.83","article-title":"Extinction by hybridization and introgression","volume":"27","author":"Rhymer J. M.","year":"1996","journal-title":"Annual Review of Ecology and Systematics"},{"key":"e_1_2_8_60_1","volume-title":"RStudio: Integrated development environment","author":"RStudio Team","year":"2025"},{"key":"e_1_2_8_61_1","first-page":"141","article-title":"Spawning ecology of anadromous Wakasagi, Hypomesus nipponensis inhabiting Hei River in Iwate, Japan","volume":"51","author":"Sasaki T.","year":"2003","journal-title":"Suisanzoshoku"},{"key":"e_1_2_8_62_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.2019"},{"key":"e_1_2_8_63_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.2089"},{"key":"e_1_2_8_64_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1016642723238"},{"key":"e_1_2_8_65_1","doi-asserted-by":"publisher","DOI":"10.15447\/sfews.2014v9iss2art2"},{"key":"e_1_2_8_66_1","doi-asserted-by":"publisher","DOI":"10.51492\/cfwj.cesasi.7"},{"key":"e_1_2_8_67_1","doi-asserted-by":"publisher","DOI":"10.1577\/1548-8659(1998)127<0417:BIAAOP>2.0.CO;2"},{"key":"e_1_2_8_68_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12237-021-01030-0"},{"key":"e_1_2_8_69_1","doi-asserted-by":"publisher","DOI":"10.15447\/sfews.2023v21iss3art2"},{"key":"e_1_2_8_70_1","doi-asserted-by":"crossref","first-page":"5936","DOI":"10.1111\/are.15472","article-title":"Validating the use of sodium hypochlorite for egg detachment and photograph\u2010based egg counting in Delta smelt","volume":"52","author":"Tsai Y.\u2010J. J.","year":"2021","journal-title":"Aquaculture Research"},{"key":"e_1_2_8_71_1","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1002\/naaq.10182","article-title":"Characterization of spawning behavior in cultured Delta smelt (Hypomesus transpacificus)","volume":"83","author":"Tsai Y.\u2010J. J.","year":"2021","journal-title":"North American Journal of Aquaculture"},{"key":"e_1_2_8_72_1","doi-asserted-by":"publisher","DOI":"10.1002\/naaq.10247"},{"key":"e_1_2_8_73_1","unstructured":"US Fish and Wildlife Service California Department of Water Resources US Bureau of Reclamation California Department of Fish and Wildlife &University of California Davis. (2020).Delta Smelt Supplementation Strategy. 55 p.https:\/\/water.ca.gov\/\u2010\/media\/DWR\u2010Website\/Web\u2010Pages\/Programs\/State\u2010Water\u2010Project\/Files\/DEIR\u2010Long\u2010Term\u2010Ops\/2024\/App2E_Delta\u2010Smelt\u2010Supplementation\u2010Strategy_508.pdf"},{"key":"e_1_2_8_74_1","first-page":"12854","article-title":"Endangered and threatened wildlife and plants: Determination of threatened status of the delta smelt","volume":"58","author":"US Fish and Wildlife Service","year":"1993","journal-title":"Federal Register"},{"key":"e_1_2_8_75_1","doi-asserted-by":"crossref","DOI":"10.1007\/978-0-387-21706-2","volume-title":"Modern applied statistics with S","author":"Venables W. N.","year":"2002"},{"key":"e_1_2_8_76_1","doi-asserted-by":"publisher","DOI":"10.1093\/beheco\/ars086"},{"key":"e_1_2_8_77_1","first-page":"141","article-title":"Introduction of pond smelt from Japan into California","volume":"48","author":"Wales J. H.","year":"1962","journal-title":"California Fish & Game"},{"key":"e_1_2_8_78_1","volume-title":"Tracy fish facilities studies","author":"Wang J. C. S.","year":"2007"},{"key":"e_1_2_8_79_1","doi-asserted-by":"publisher","DOI":"10.1111\/eth.12394"},{"key":"e_1_2_8_80_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0034802"},{"key":"e_1_2_8_81_1","doi-asserted-by":"publisher","DOI":"10.1093\/beheco\/ari058"}],"container-title":["Journal of Fish Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/jfb.70626","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/jfb.70626","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/jfb.70626","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T10:11:56Z","timestamp":1788862316000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/jfb.70626"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,8]]},"references-count":80,"alternative-id":["10.1111\/jfb.70626"],"URL":"https:\/\/doi.org\/10.1111\/jfb.70626","archive":["Portico"],"relation":{},"ISSN":["0022-1112","1095-8649"],"issn-type":[{"value":"0022-1112","type":"print"},{"value":"1095-8649","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,8]]},"assertion":[{"value":"2026-03-17","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-08-17","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-08","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"jfb.70626"}}