{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,21]],"date-time":"2026-01-21T14:41:56Z","timestamp":1769006516398,"version":"3.49.0"},"reference-count":59,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2014,11,7]],"date-time":"2014-11-07T00:00:00Z","timestamp":1415318400000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0112382","type":"journal-article","created":{"date-parts":[[2014,11,7]],"date-time":"2014-11-07T18:59:41Z","timestamp":1415386781000},"page":"e112382","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":24,"title":["Sperm Flagellum Volume Determines Freezability in Red Deer Spermatozoa"],"prefix":"10.1371","volume":"9","author":[{"given":"Jos\u00e9 Luis","family":"Ros-Santaella","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"\u00c1lvaro Efr\u00e9n","family":"Dom\u00ednguez-Rebolledo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jos\u00e9 Juli\u00e1n","family":"Garde","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2014,11,7]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1071\/RD9950871","article-title":"Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function","volume":"7","author":"PF Watson","year":"1995","journal-title":"Reprod Fertil Dev"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S0378-4320(00)00099-3","article-title":"The causes of reduced fertility with cryopreserved semen","volume":"60\u201361","author":"PF Watson","year":"2000","journal-title":"Anim Reprod Sci"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"716","DOI":"10.2164\/jandrol.05030","article-title":"Identification of sperm morphometric subpopulations in two different portions of the boar ejaculate and its relation to postthaw quality","volume":"26","author":"FJ Pe\u00f1a","year":"2005","journal-title":"J Androl"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/0093-691X(92)90231-F","article-title":"Effects of cryopreservation procedures on sperm membranes","volume":"38","author":"JE Parks","year":"1992","journal-title":"Theriogenology"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1046\/j.1365-2109.2000.00423.x","article-title":"Changes in the flagellum morphology of intact and frozen\/thawed Siberian sturgeon <italic>Acipenser baerii<\/italic> (Brandt) sperm during motility","volume":"31","author":"R Billard","year":"2000","journal-title":"Aquac Res"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0378-4320(00)00152-4","article-title":"Basic aspects of frozen storage of semen","volume":"62","author":"WV Holt","year":"2000","journal-title":"Anim Reprod Sci"},{"key":"ref7","first-page":"329","article-title":"Staining of stallion spermatozoa with damaged tail membrane after freezing\/thawing","volume":"68","author":"U Domes","year":"2001","journal-title":"Anim Reprod Sci"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1530\/rep.0.1240643","article-title":"Measured effect of collection and cooling conditions on the motility and the water transport parameters at subzero temperatures of equine spermatozoa","volume":"124","author":"RV Devireddy","year":"2002","journal-title":"Reproduction"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1016\/j.theriogenology.2004.09.046","article-title":"New assays for detection and localization of endogenous lipid peroxidation products in living boar sperm after BTS dilution or after freeze-thawing","volume":"63","author":"JF Brouwers","year":"2005","journal-title":"Theriogenology"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"610","DOI":"10.2164\/jandrol.05028","article-title":"Kinematic changes during the cryopreservation of boar spermatozoa","volume":"26","author":"T Cremades","year":"2005","journal-title":"J Androl"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/j.theriogenology.2004.09.018","article-title":"The significance of cooling rates and animal variability for boar sperm cryopreservation: insights from the cryomicroscope","volume":"63","author":"WV Holt","year":"2005","journal-title":"Theriogenology"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1095\/biolreprod66.3.545","article-title":"Identification of amplified restriction fragment length polymorphism markers linked to genes controlling boar sperm viability following cryopreservation","volume":"66","author":"LM Thurston","year":"2002","journal-title":"Biol Reprod"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1530\/rep.1.00296","article-title":"Functional significance of the cell volume for detecting sperm membrane changes and predicting freezability in dog semen","volume":"128","author":"AM Petrunkina","year":"2004","journal-title":"Reproduction"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"662","DOI":"10.2164\/jandrol.106.000489","article-title":"Functional significance of the sperm head morphometric size and shape for determining freezability in iberian red deer (<italic>Cervus elaphus hispanicus<\/italic>) epididymal sperm samples","volume":"27","author":"MC Esteso","year":"2006","journal-title":"J Androl"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/j.theriogenology.2008.01.012","article-title":"Comparison of three staining techniques for the morphometric study of rainbow trout (<italic>Oncorhynchus mykiss<\/italic>) spermatozoa","volume":"69","author":"VM Tuset","year":"2008","journal-title":"Theriogenology"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1098\/rsbl.2006.0449","article-title":"Sperm design and sperm function","volume":"2","author":"AF Malo","year":"2006","journal-title":"Biol Lett"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1186\/1475-2875-7-214","article-title":"Intra-specific variation of sperm length in the malaria vector <italic>Anopheles gambiae<\/italic>: males with shorter sperm have higher reproductive success","volume":"7","author":"MJ Voordouw","year":"2008","journal-title":"Malar J"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1038\/416496a","article-title":"Sperm competition: motility and the midpiece in primates","volume":"416","author":"MJ Anderson","year":"2002","journal-title":"Nature"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1017\/S0952836905007284","article-title":"Sperm competition and the evolution of sperm midpiece volume in mammals","volume":"267","author":"MJ Anderson","year":"2005","journal-title":"J Zool"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/j.anireprosci.2008.09.013","article-title":"Testis size, sperm characteristics and testosterone concentrations in four species of shrews (Mammalia, Soricidae)","volume":"114","author":"RN Parapanov","year":"2009","journal-title":"Anim Reprod Sci"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1098\/rsbl.2009.0635","article-title":"Sperm competition and sperm length influence the rate of mammalian spermatogenesis","volume":"6","author":"SA Ramm","year":"2010","journal-title":"Biol Lett"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1016\/0006-291X(80)91497-7","article-title":"Effects of glycerol on microtubule polymerization kinetics","volume":"97","author":"RA Keates","year":"1980","journal-title":"Biochem Biophys Res Commun"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1095\/biolreprod51.3.414","article-title":"Effects of temperature and restoration of osmotic equilibrium during thawing on the induction of plasma membrane damage in cryopreserved ram spermatozoa","volume":"51","author":"WV Holt","year":"1994","journal-title":"Biol Reprod"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.cryobiol.2011.12.004","article-title":"Cytoskeletal proteins F-actin and \u03b2-dystrobrevin are altered by the cryopreservation process in bull sperm","volume":"64","author":"YE Felipe-P\u00e9rez","year":"2012","journal-title":"Cryobiology"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1095\/biolreprod55.6.1325","article-title":"Surface area and volume measurements for ram and human spermatozoa","volume":"55","author":"MR Curry","year":"1996","journal-title":"Biol Reprod"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"195","DOI":"10.3109\/01485019808994891","article-title":"Postmortem assessment of sperm characteristics of the red deer during the breeding season","volume":"41","author":"JJ Garde","year":"1998","journal-title":"Arch Androl"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"1931","DOI":"10.1016\/j.theriogenology.2006.05.012","article-title":"Cryopreservation of Iberian red deer (<italic>Cervus elaphus hispanicus<\/italic>) epididymal spermatozoa: effects of egg yolk, glycerol and cooling rate","volume":"66","author":"MR Fern\u00e1ndez-Santos","year":"2006","journal-title":"Theriogenology"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1071\/RD09197","article-title":"Improving the effect of incubation and oxidative stress on thawed spermatozoa from red deer by using different antioxidant treatments","volume":"22","author":"AE Dom\u00ednguez-Rebolledo","year":"2010","journal-title":"Reprod Fertil Dev"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/j.1439-0531.2006.00773.x","article-title":"The application of reproductive technologies to natural populations of red deer","volume":"41","author":"JJ Garde","year":"2006","journal-title":"Reprod Domest Anim"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/S0093-691X(01)00561-1","article-title":"Assessment of <italic>in vitro<\/italic> fertility of deer spermatozoa by heterologous IVF with zona-free bovine oocytes","volume":"56","author":"P Comizzoli","year":"2001","journal-title":"Theriogenology"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1002\/j.1939-4640.2001.tb02161.x","article-title":"Lack of significant morphological differences between human X and Y spermatozoa and their precursor cells spermatids exposed to different prehybridization treatments","volume":"22","author":"AM Hossain","year":"2001","journal-title":"J Androl"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1007\/11556121_12","article-title":"Statistical approach to boar semen head classification based on intracellular intensity distribution","volume":"3691","author":"L Sanchez","year":"2005","journal-title":"Computer Analysis of Images and Patterns, Proceedings"},{"key":"ref33","first-page":"350","article-title":"Modular equations and approximations to \u03c0","volume":"45","author":"S Ramanujan","year":"1914","journal-title":"Quart J Pure Appl Math"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1095\/biolreprod.104.036368","article-title":"Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa","volume":"72","author":"AF Malo","year":"2005","journal-title":"Biol Reprod"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"596","DOI":"10.2164\/jandrol.05153","article-title":"Two-step cluster procedure after principal component analysis identifies sperm subpopulations in canine ejaculates and its relation to cryoresistance","volume":"27","author":"I Nu\u00f1ez-Mart\u00ednez","year":"2006","journal-title":"J Androl"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1111\/j.1439-0310.2010.01758.x","article-title":"Using principal components and factor analysis in animal behaviour research: caveats and guidelines","volume":"116","author":"SV Budaev","year":"2010","journal-title":"Ethology"},{"key":"ref37","unstructured":"Bohonak AJ, Linde K (2004) RMA: Software for reduced major axis regression, Java version. Website: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.kimvdlinde.com\/professional\/rma.html\" xlink:type=\"simple\">http:\/\/www.kimvdlinde.com\/professional\/rma.html<\/ext-link>."},{"key":"ref38","first-page":"44","article-title":"Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success","volume":"14","author":"MJ Gage","year":"2004","journal-title":"Curr Biol"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"1759","DOI":"10.1098\/rspb.1999.0843","article-title":"Sperm mobility determines the outcome of sperm competition in the domestic fowl","volume":"266","author":"TR Birkhead","year":"1999","journal-title":"Proc R Soc B-Biol Sci"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1093\/oxfordjournals.humrep.a136891","article-title":"The value of sperm swimming speed measurements in assessing the fertility of human frozen semen","volume":"4","author":"WV Holt","year":"1989","journal-title":"Hum Reprod"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/j.1439-0531.2007.00876.x","article-title":"Interrelationship between plasma membrane integrity mitochondrial membrane potential and DNA fragmentation in cryopreserved bovine spermatozoa","volume":"43","author":"H Bollwein","year":"2008","journal-title":"Reprod Domest Anim"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.anireprosci.2012.09.001","article-title":"Reduced glutathione and Trolox (vitamin E) as extender supplements in cryopreservation of red deer epididymal spermatozoa","volume":"135","author":"L Anel-L\u00f3pez","year":"2012","journal-title":"Anim Reprod Sci"},{"key":"ref43","first-page":"2","article-title":"Semen quality tests and their relationship to fertility","author":"RG Saacke","year":"1972","journal-title":"Proceedings of the Fourth Technical Conference on Artificial Insemination and Reproduction National Association of Animal Breeders"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.anireprosci.2013.02.007","article-title":"Fertility of cryopreserved ovine semen is determined by sperm velocity","volume":"138","author":"E Del Olmo","year":"2013","journal-title":"Anim Reprod Sci"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1530\/rep.0.1230315","article-title":"Importance of cooling rate and animal variability for boar sperm cryopreservation: insights from the cryomicroscope","volume":"123","author":"A Medrano","year":"2002","journal-title":"Reproduction"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1530\/jrf.0.0530389","article-title":"Ultrastructural injury to human spermatozoa after freezing and thawing","volume":"53","author":"DM Woolley","year":"1978","journal-title":"J Reprod Fertil"},{"key":"ref47","first-page":"135","article-title":"Cryodamage to plasma membrane integrity in head and tail regions of human sperm","volume":"2","author":"WJ Zhu","year":"2000","journal-title":"Asian J Androl"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1016\/S0093-691X(99)00207-1","article-title":"Evaluation of sperm tail membrane integrity by light microscopy","volume":"52","author":"S Nagy","year":"1999","journal-title":"Theriogenology"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"1280","DOI":"10.1016\/j.theriogenology.2011.10.033","article-title":"Toxicity of glycerol for the stallion spermatozoa: effects on membrane integrity and cytoskeleton, lipid peroxidation and mitochondrial membrane potential","volume":"77","author":"B Mac\u00edas Garc\u00eda","year":"2012","journal-title":"Theriogenology"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/j.cryobiol.2007.03.004","article-title":"Ultrastructural observations of cryoinjury in kangaroo spermatozoa","volume":"54","author":"RV McClean","year":"2007","journal-title":"Cryobiology"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1530\/rep.1.00047","article-title":"Requirement for an intact cytoskeleton for volume regulation in boar spermatozoa","volume":"127","author":"AM Petrunkina","year":"2004","journal-title":"Reproduction"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0093-691X(03)00184-5","article-title":"Role of potassium channels, the sodium-potassium pump and the cytoskeleton in the control of dog sperm volume","volume":"61","author":"AM Petrunkina","year":"2004","journal-title":"Theriogenology"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1095\/biolreprod.107.060533","article-title":"The macaque sperm actin cytoskeleton reorganizes in response to osmotic stress and contributes to morphological defects and decreased motility","volume":"77","author":"LM Correa","year":"2007","journal-title":"Biol Reprod"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"706","DOI":"10.2164\/jandrol.106.001669","article-title":"Calmodulin and CaMKII in the sperm principal piece: evidence for a motility-related calcium\/calmodulin pathway","volume":"28","author":"K Schlingmann","year":"2007","journal-title":"J Androl"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/0012-1606(75)90411-X","article-title":"The mammalian spermatozoon","volume":"44","author":"DW Fawcett","year":"1975","journal-title":"Dev Biol"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1242\/jcs.102.2.249","article-title":"The flagellar beat of rat sperm is organized by the interaction of two functionally distinct populations of dynein bridges with a stable central axonemal partition","volume":"102","author":"CB Lindemann","year":"1992","journal-title":"J Cell Sci"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1071\/RD05120","article-title":"Moving to the beat: a review of mammalian sperm motility regulation","volume":"18","author":"RM Turner","year":"2006","journal-title":"Reprod Fertil Dev"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1002\/mrd.1080420407","article-title":"Identification of a unique mu-class glutathione S-transferase in mouse spermatogenic cells","volume":"42","author":"KD Fulcher","year":"1995","journal-title":"Mol Reprod Dev"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1002\/jez.1402300316","article-title":"Partially irreversible cold-induced lipid phase transitions in mammalian sperm plasma membrane domains; freeze fracture study","volume":"230","author":"WV Holt","year":"1984","journal-title":"J Exp Zool"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0112382","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,18]],"date-time":"2023-07-18T00:02:57Z","timestamp":1689638577000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0112382"}},"subtitle":[],"editor":[{"given":"Chris D.","family":"Wood","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2014,11,7]]},"references-count":59,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2014,11,7]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0112382","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,11,7]]}}}