{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T17:05:42Z","timestamp":1781715942171,"version":"3.54.5"},"reference-count":69,"publisher":"Wiley","issue":"6","license":[{"start":{"date-parts":[[2025,7,28]],"date-time":"2025-07-28T00:00:00Z","timestamp":1753660800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Zoo Biology"],"published-print":{"date-parts":[[2025,11]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Species recovery efforts may require establishment of ex situ populations to supply augmentation or reintroduction projects. The Eastern Massasauga (\n                    <jats:italic>Sistrurus catenatus<\/jats:italic>\n                    ) is a small rattlesnake with an ex situ breeding program maintained by a consortium of conservation breeding centres. Small population size in human care has restricted the supply of animals for in situ conservation, thus, the development of improved ex situ breeding protocols was recommended. The objectives of our retrospective study were to (1) describe and compare reproductive traits between two groups of Massasauga litters born in human care: wild\u2010bred litters (i.e., conceived in the wild) and zoo\u2010bred litters, (2) test for factors associated with improved reproductive output in zoo\u2010bred litters, and, (3) make recommendations for standardizing ex situ breeding protocols. Data were collected on Massasauga birth events that occurred from 2000 to 2020 at 13 North American zoos and partner facilities. Six outcomes related to litter size and survival of offspring were compared between zoo\u2010bred (\n                    <jats:italic>n<\/jats:italic>\n                    \u2009=\u200943) and wild\u2010bred litters (\n                    <jats:italic>n<\/jats:italic>\n                    \u2009=\u200951). Odds ratios were used to test for correlations between nine predictor variables and four response variables in zoo\u2010bred litters. We found higher mean litter size and number of live young per litter in wild\u2010bred litters (12 and 10, respectively) compared to zoo\u2010bred litters (6 and 2). Wild\u2010bred litters more often contained live young and less often contained unfertilized ova (98% and 34% of litters, respectively) than did zoo\u2010bred litters (58% and 81%). Experimentation on the effectiveness of alternative mating practices is warranted to improve reproductive output in human care, thereby increasing capacity to support in situ conservation.\n                  <\/jats:p>","DOI":"10.1002\/zoo.70005","type":"journal-article","created":{"date-parts":[[2025,7,28]],"date-time":"2025-07-28T12:54:31Z","timestamp":1753707271000},"page":"572-588","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Reproductive Traits of Zoo\u2010Bred and Wild\u2010Bred Eastern Massasaugas (\n                    <i>Sistrurus catenatus<\/i>\n                    ) at Species Survival Plan\u00ae Conservation Breeding Centres and Other Facilities"],"prefix":"10.1002","volume":"44","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9965-4359","authenticated-orcid":false,"given":"Jonathan D.","family":"Choquette","sequence":"first","affiliation":[{"name":"School of Natural Sciences Laurentian University Sudbury Ontario Canada"},{"name":"Wildlife Preservation Canada (WPC) Guelph Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Trevor E.","family":"Pitcher","sequence":"additional","affiliation":[{"name":"Department of Integrative Biology &amp; Great Lakes Institute for Environmental Research University of Windsor Windsor Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne","family":"Yagi","sequence":"additional","affiliation":[{"name":"8Trees Inc. Fonthill Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Corentin","family":"Fournier","sequence":"additional","affiliation":[{"name":"Wildlife Preservation Canada (WPC) Guelph Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rick","family":"Vos","sequence":"additional","affiliation":[{"name":"Toronto Zoo Toronto Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacqueline D.","family":"Litzgus","sequence":"additional","affiliation":[{"name":"School of Natural Sciences Laurentian University Sudbury Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2025,7,28]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1071\/ZO05010"},{"key":"e_1_2_9_3_1","first-page":"403","volume-title":"The Biology of the Rattlesnakes","author":"Aldridge R. D.","year":"2008"},{"key":"e_1_2_9_4_1","unstructured":"Association of Zoos and Aquariums Eastern Massasauga Rattlesnake Species Survival Plan (AZAEMRSSP).2013.Eastern Massasauga Rattlesnake (Sistrurus catenatus catenatus) Care Manual.Association of Zoos and Aquariums Silver Spring.www.aza.org\/animal-care-manuals."},{"key":"e_1_2_9_5_1","unstructured":"Association of Zoos and Aquariums Snake Advisory Group (AZASAG).2016.Regional Collection Plan 4th ed.Association of Zoos and Aquariums Silver Spring."},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1006\/hbeh.2002.1793"},{"key":"e_1_2_9_7_1","volume-title":"Modelling Habitat Suitability and Population Demographics of The Eastern Massasauga Rattlesnake in Managed Lands in Southwestern Michigan","author":"Bailey R. L.","year":"2010"},{"key":"e_1_2_9_8_1","first-page":"8","article-title":"A Successful Breeding of Sistrurus catenatus catenatus","volume":"11","author":"Beek H.","year":"1991","journal-title":"Litteratura Serpentium"},{"key":"e_1_2_9_9_1","first-page":"97","article-title":"Reproductive Biology of the Neotropical Rattlesnake Crotalus Durissus From Northeastern Brazil: A Test of Phylogenetic Conservatism of Reproductive Patterns","volume":"22","author":"Barros V. A.","year":"2012","journal-title":"Herpetological Journal"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1201\/b10879-6"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.21682"},{"key":"e_1_2_9_12_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-0706.2000.890310.x"},{"key":"e_1_2_9_13_1","unstructured":"Bronsgeest H.1992: \u201cBreeding Results:Sistrurus catenatus tergeminus\u2014western Massasauga.\u201d Litteratura Serpentium121:23."},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1420-9101.2006.01256.x"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.1655\/0733-1347(2002)016[0026:GRASIA]2.0.CO;2"},{"key":"e_1_2_9_16_1","first-page":"275","article-title":"Breeding Results: Sistrurus miliarius barbouri (F2)","volume":"9","author":"Drent J.","year":"1989","journal-title":"Litteratura Serpentium"},{"key":"e_1_2_9_17_1","volume-title":"Ecology of the eastern massasauga (Sistrurus catenatus catenatus) From Carlyle Lake, Clinton County, Illinois","author":"Dreslik M. J.","year":"2005"},{"key":"e_1_2_9_18_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1748-1090.1977.tb00871.x"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1201\/b10879-15"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1017\/CBO9780511817359"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.2307\/1436215"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0172011"},{"key":"e_1_2_9_23_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.21460"},{"key":"e_1_2_9_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2021.105435"},{"key":"e_1_2_9_25_1","unstructured":"IUCN\/SSC.2013.Guidelines for Reintroductions and Other Conservation Translocations. Version 1.0. IUCN Species Survival Commission Gland Switzerland.www.iucn.org\/resources#resource_types-resource_type_publication."},{"key":"e_1_2_9_26_1","unstructured":"IUCN\/SSC.2014.IUCN Species Survival Commission Guidelines on the Use of Ex Situ Management for Species Conservation. Version 2.0. IUCN Species Survival Commission Gland Switzerland.www.iucn.org\/resources#resource_types-resource_type_publication."},{"key":"e_1_2_9_27_1","unstructured":"IUCN\/SSC.2023.Position Statement on the Role of Botanic Gardens Aquariums and Zoos in Species Conservation. IUCN Species Survival Commission Gland Switzerland.www.iucn.org\/resources#resource_types-resource_type_publication."},{"key":"e_1_2_9_28_1","doi-asserted-by":"publisher","DOI":"10.1670\/0022-1511(2007)41[451:MMABSA]2.0.CO;2"},{"key":"e_1_2_9_29_1","first-page":"71","volume-title":"Proceedings of the 12th International Herpetological Symposium on Captive Propagation and Husbandry","author":"Johnson B.","year":"1988"},{"key":"e_1_2_9_30_1","unstructured":"Johnson B. andM.Wright.1999.Second International Symposium and Workshop on the Conservation of the Eastern Massasauga Rattlesnake Sistrurus catenatus catenatus: Population and Habitat Management Issues in Urban Bog Prairie and Forested Ecosystems 2\u20133 October 1998 Toronto Zoo Toronto ON Canada."},{"key":"e_1_2_9_31_1","volume-title":"The Eastern Massasauga Rattlesnake: A Handbook for Land Managers","author":"Johnson G.","year":"2000"},{"key":"e_1_2_9_32_1","doi-asserted-by":"publisher","DOI":"10.1093\/condor\/duy007"},{"key":"e_1_2_9_33_1","volume-title":"Rattlesnakes: Their Habits, Life Histories, and Influence on Mankind","author":"Klauber L. M.","year":"1997"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.1201\/b10879-9"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/0016-6480(87)90061-X"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1748-1090.1979.tb00519.x"},{"key":"e_1_2_9_37_1","doi-asserted-by":"publisher","DOI":"10.2307\/1445921"},{"key":"e_1_2_9_38_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-3207(95)00067-4"},{"key":"e_1_2_9_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2005.02505.x"},{"key":"e_1_2_9_40_1","unstructured":"Mulkerin D.2017.AZA Regional Studbook Eastern Massasauga Rattlesnake (Sistrurus catenatus catenatus). Lincoln Park Zoo Chicago."},{"key":"e_1_2_9_41_1","unstructured":"NatureServe.2024.NatureServe Network Biodiversity Location Data accessed Through NatureServe Explorer[web application]. NatureServe Arlington VA USA. Accessed August 26 2024.www.explorer.natureserve.org\/."},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1163\/156853881X00285"},{"key":"e_1_2_9_43_1","unstructured":"Prior K. R.Black K.Cedar et al.2001.National Recovery Plan for the Eastern Massasauga. Eastern Massasauga Recovery Team Canadian Wildlife Service Toronto ON Canada."},{"key":"e_1_2_9_44_1","unstructured":"R Core Team.2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna Austria.https:\/\/www.R-project.org\/."},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.2307\/2424761"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.5735\/086.045.0106"},{"key":"e_1_2_9_47_1","first-page":"347","article-title":"Female Reproduction in the Western Diamond\u2010Backed Rattlesnake, Crotalus atrox (Serpentes: Viperidae), From Arizona","volume":"54","author":"Rosen P. C.","year":"2002","journal-title":"Texas Journal of Science"},{"key":"e_1_2_9_48_1","first-page":"91","volume-title":"Proceedings of the 14th International Herpetological Symposium on Captive Propagation and Husbandry","author":"Ross R. A.","year":"1990"},{"key":"e_1_2_9_49_1","volume-title":"The Snakes of Ontario: Natural History, Distribution and Status","author":"Rowell J. C.","year":"2012"},{"key":"e_1_2_9_50_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.2041-210x.2012.00250.x"},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1111\/acv.12151"},{"key":"e_1_2_9_52_1","volume-title":"Statistics: A first course","author":"Sanders D. H.","year":"2001"},{"key":"e_1_2_9_53_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0282845"},{"key":"e_1_2_9_54_1","volume-title":"Breeding and Keeping Snakes","author":"Schmidt D.","year":"1995"},{"key":"e_1_2_9_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.anireprosci.2015.10.012"},{"key":"e_1_2_9_56_1","first-page":"181","article-title":"Care and Breeding of Sistrurus miliaris barbouri, the Barbours Pygmy Rattlesnake","volume":"10","author":"Smetsers P.","year":"1990","journal-title":"Litteratura Serpentium"},{"key":"e_1_2_9_57_1","unstructured":"Species360.2021. Population Overview Report forSistrurus catenatus\/Massasauga. For Period From 17 Mar 2001 to 17 Mar 2021. Species360 ZIMS version 2.25.5. Printed 2021\/03\/17 at Toronto Zoo Toronto ON Canada."},{"key":"e_1_2_9_58_1","first-page":"160","article-title":"Multiple Paternity in Three Wild Populations of Eastern Massasauga (Sistrurus catenatus)","volume":"11","author":"Stedman A. L.","year":"2016","journal-title":"Herpetological Conservation and Biology"},{"key":"e_1_2_9_59_1","first-page":"227","article-title":"Explaining Odds Ratios","volume":"19","author":"Szumilas M.","year":"2010","journal-title":"Journal of the Canadian Academy of Child and Adolescent Psychiatry = Journal de l'Academie canadienne de psychiatrie de l'enfant et de l'adolescent"},{"key":"e_1_2_9_60_1","unstructured":"Szymanski J.1998.Status Assessment for the Eastern Massasauga (Sistrurus c. catenatus).US Fish and Wildlife Service Fort Snelling.www.fws.gov\/sites\/default\/files\/documents\/2024-04\/908.pdf."},{"key":"e_1_2_9_61_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00442-005-0056-x"},{"key":"e_1_2_9_62_1","first-page":"121","volume-title":"Rattlesnakes of Arizona, Volume 2: Behaviour, Venom and Evolution","author":"Taylor E. N.","year":"2017"},{"key":"e_1_2_9_63_1","doi-asserted-by":"publisher","DOI":"10.1002\/ece3.3193"},{"key":"e_1_2_9_64_1","doi-asserted-by":"publisher","DOI":"10.1655\/HERPETOLOGICA-D-10-00052.1"},{"key":"e_1_2_9_65_1","unstructured":"U.S. Fish and Wildlife Service (USFWS) and Canadian Wildlife Service (CWS).2001.Conserving Borderline Species: A Partnership Between the United States and Canada. Issued Jointly by the U.S. Department of the Interior Fish and Wildlife Service and Environment Canada Canadian Wildlife Service Ottawa ON Canada.www.publications.gc.ca\/site\/eng\/home.html."},{"key":"e_1_2_9_66_1","doi-asserted-by":"publisher","DOI":"10.1016\/0016-6480(87)90078-5"},{"key":"e_1_2_9_67_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.21713"},{"key":"e_1_2_9_68_1","doi-asserted-by":"publisher","DOI":"10.2307\/2420721"},{"key":"e_1_2_9_69_1","first-page":"7","article-title":"Developmental Irregularities Observed in a Viviparous Species During a Population Growth Spurt","volume":"13","author":"Yagi A.","year":"2024","journal-title":"Canadian Herpetologist"},{"key":"e_1_2_9_70_1","first-page":"24","article-title":"The Young and the Restless: Postpartum Breeding and Early Onset Sexual Maturity in an Isolated Northern Population of Massasauga Rattlesnakes","volume":"8","author":"Yagi A. R.","year":"2018","journal-title":"Canadian Herpetologist"}],"container-title":["Zoo Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/zoo.70005","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T09:51:43Z","timestamp":1765014703000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/zoo.70005"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,28]]},"references-count":69,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2025,11]]}},"alternative-id":["10.1002\/zoo.70005"],"URL":"https:\/\/doi.org\/10.1002\/zoo.70005","archive":["Portico"],"relation":{},"ISSN":["0733-3188","1098-2361"],"issn-type":[{"value":"0733-3188","type":"print"},{"value":"1098-2361","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,28]]},"assertion":[{"value":"2025-04-01","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-07-02","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-07-28","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}