{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T03:38:02Z","timestamp":1790221082084,"version":"4.1.0"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"1","funder":[{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["#105-2628-B-002-022-MY3"],"award-info":[{"award-number":["#105-2628-B-002-022-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Vet Res"],"published-print":{"date-parts":[[2018,12]]},"DOI":"10.1186\/s12917-018-1389-0","type":"journal-article","created":{"date-parts":[[2018,2,27]],"date-time":"2018-02-27T00:15:36Z","timestamp":1519690536000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["The effects of type I collagenase on the degelification of chimpanzee (Pan troglodytes) semen plug and sperm quality"],"prefix":"10.1186","volume":"14","author":[{"given":"Jane-Fang","family":"Yu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Hua","family":"Lai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tse-En","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Syuan","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Jia","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sheng-Hsiang","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shih-Chien","family":"Chin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Radhika","family":"Joshi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui-Wen","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pei-Shiue","family":"Tsai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,2,27]]},"reference":[{"key":"1389_CR1","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1016\/j.fsigen.2015.03.009","volume":"18","author":"RW Cotton","year":"2015","unstructured":"Cotton RW, Fisher MB. Review: properties of sperm and seminal fluid, informed by research on reproduction and contraception. Forensic Sci Int Genet. 2015;18:66\u201377.","journal-title":"Forensic Sci Int Genet"},{"issue":"10","key":"1389_CR2","doi-asserted-by":"publisher","first-page":"3008","DOI":"10.1111\/evo.12477","volume":"68","author":"S Dhole","year":"2014","unstructured":"Dhole S, Servedio MR. Sperm competition and the evolution of seminal fluid composition. Evolution. 2014;68(10):3008\u201319.","journal-title":"Evolution"},{"key":"1389_CR3","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1186\/s12915-015-0197-2","volume":"13","author":"SA Ramm","year":"2015","unstructured":"Ramm SA, Edward DA, Claydon AJ, Hammond DE, Brownridge P, Hurst JL, Beynon RJ, Stockley P. Sperm competition risk drives plasticity in seminal fluid composition. BMC Biol. 2015;13:87.","journal-title":"BMC Biol"},{"issue":"4","key":"1389_CR4","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0123770","volume":"10","author":"T Yamane","year":"2015","unstructured":"Yamane T, Goenaga J, Ronn JL, Arnqvist G. Male seminal fluid substances affect sperm competition success and female reproductive behavior in a seed beetle. PLoS One. 2015;10(4):e0123770.","journal-title":"PLoS One"},{"issue":"6","key":"1389_CR5","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1084\/jem.76.6.527","volume":"76","author":"C Huggins","year":"1942","unstructured":"Huggins C, Neal W. Coagulation and liquefaction of semen : proteolytic enzymes and citrate in prostatic fluid. J Exp Med. 1942;76(6):527\u201341.","journal-title":"J Exp Med"},{"issue":"1","key":"1389_CR6","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/S0921-4488(00)00142-5","volume":"38","author":"PW Bravo","year":"2000","unstructured":"Bravo PW, Ccallo M, Garnica J. The effect of enzymes on semen viscosity in llamas and alpacas. Small Rumin Res. 2000;38(1):91\u20135.","journal-title":"Small Rumin Res"},{"issue":"2","key":"1389_CR7","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1007\/s00239-002-2463-0","volume":"57","author":"SB Kingan","year":"2003","unstructured":"Kingan SB, Tatar M, Rand DM. Reduced polymorphism in the chimpanzee semen coagulating protein, semenogelin I. J Mol Evol. 2003;57(2):159\u201369.","journal-title":"J Mol Evol"},{"issue":"2\u20133","key":"1389_CR8","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1159\/000064784","volume":"73","author":"AL Dixson","year":"2002","unstructured":"Dixson AL, Anderson MJ. Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol (Basel). 2002;73(2\u20133):63\u20139.","journal-title":"Folia Primatol (Basel)"},{"key":"1389_CR9","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/ajp.1350370102","volume":"37","author":"LG Young","year":"1995","unstructured":"Young LG, Young LG. Effect of liquefaction time on semen parameters in chimpanzee (pan troglodytes) ejaculates. Am J Primatol. 1995;37:1\u20137.","journal-title":"Am J Primatol"},{"key":"1389_CR10","doi-asserted-by":"publisher","unstructured":"Lima JS, Leao DL, Oliveira KG, Brito AB, Sampaio WV, Santos RR, Queiroz HL, Domingues SF. Seminal coagulation and sperm quality in different social contexts in captive tufted capuchin monkeys (Sapajus apella). Am J Primatol. 2017;79(6). https:\/\/doi.org\/10.1002\/ajp.22643 . Epub 2017 Feb 7.","DOI":"10.1002\/ajp.22643"},{"key":"1389_CR11","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1016\/j.theriogenology.2016.10.024","volume":"89","author":"I Luther","year":"2017","unstructured":"Luther I, Jakop U, Lueders I, Tordiffe A, Franz C, Schiller J, Kotze A, Muller K. Semen cryopreservation and radical reduction capacity of seminal fluid in captive African lion (Panthera leo). Theriogenology. 2017;89:295\u2013304.","journal-title":"Theriogenology"},{"key":"1389_CR12","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1002\/zoo.1430120303","volume":"12","author":"CANT VandeVoort","year":"1993","unstructured":"VandeVoort CANT, Tollner TL, Farichild O. Non-invasive semen collection from an adult orangutan. Zoo Biology. 1993;12:257\u201366.","journal-title":"Zoo Biology"},{"issue":"2","key":"1389_CR13","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1530\/jrf.0.0900347","volume":"90","author":"TL Tollner","year":"1990","unstructured":"Tollner TL, VandeVoort CA, Overstreet JW, Drobnis EZ. Cryopreservation of spermatozoa from cynomolgus monkeys (Macaca fascicularis). J Reprod Fertil. 1990;90(2):347\u201352.","journal-title":"J Reprod Fertil"},{"issue":"3","key":"1389_CR14","doi-asserted-by":"publisher","first-page":"275","DOI":"10.3109\/01485018708988493","volume":"18","author":"TF Kruger","year":"1987","unstructured":"Kruger TF, Ackerman SB, Simmons KF, Swanson RJ, Brugo SS, Acosta AA. A quick, reliable staining technique for human sperm morphology. Arch Androl. 1987;18(3):275\u20137.","journal-title":"Arch Androl"},{"issue":"2","key":"1389_CR15","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1016\/j.fertnstert.2007.03.027","volume":"89","author":"R Henkel","year":"2008","unstructured":"Henkel R, Schreiber G, Sturmhoefel A, Hipler UC, Zermann DH, Menkveld R. Comparison of three staining methods for the morphological evaluation of human spermatozoa. Fertil Steril. 2008;89(2):449\u201355.","journal-title":"Fertil Steril"},{"key":"1389_CR16","first-page":"87","volume":"22","author":"CE Pope YZZ","year":"1991","unstructured":"Pope YZZ CE, Dresser BL. A simple staining method for evaluating acrosomal status of cat spermatozoa. J Zoo Wild Med. 1991;22:87\u201395.","journal-title":"J Zoo Wild Med"},{"issue":"10","key":"1389_CR17","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1023\/A:1020310503143","volume":"19","author":"MH Nasr-Esfahani","year":"2002","unstructured":"Nasr-Esfahani MH, Aboutorabi R, Esfandiari E, Mardani M. Sperm MTT viability assay: a new method for evaluation of human sperm viability. J Assist Reprod Genet. 2002;19(10):477\u201382.","journal-title":"J Assist Reprod Genet"},{"key":"1389_CR18","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/j.anireprosci.2016.08.010","volume":"173","author":"A Santiani","year":"2016","unstructured":"Santiani A, Ugarelli A, Evangelista-Vargas S. Characterization of functional variables in epididymal alpaca (Vicugna pacos) sperm using imaging flow cytometry. Anim Reprod Sci. 2016;173:49\u201355.","journal-title":"Anim Reprod Sci"},{"issue":"3","key":"1389_CR19","doi-asserted-by":"publisher","first-page":"779","DOI":"10.2527\/jas.2011-4311","volume":"90","author":"ML Broekhuijse","year":"2012","unstructured":"Broekhuijse ML, Sostaric E, Feitsma H, Gadella BM. Application of computer-assisted semen analysis to explain variations in pig fertility. J Anim Sci. 2012;90(3):779\u201389.","journal-title":"J Anim Sci"},{"issue":"2","key":"1389_CR20","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1093\/molehr\/gah142","volume":"11","author":"J Laflamme","year":"2005","unstructured":"Laflamme J, Akoum A, Leclerc P. Induction of human sperm capacitation and protein tyrosine phosphorylation by endometrial cells and interleukin-6. Mol Hum Reprod. 2005;11(2):141\u201350.","journal-title":"Mol Hum Reprod"},{"issue":"6","key":"1389_CR21","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1002\/j.1939-4640.1996.tb01852.x","volume":"17","author":"FP Cheng","year":"1996","unstructured":"Cheng FP, Fazeli A, Voorhout WF, Marks A, Bevers MM, Colenbrander B. Use of peanut agglutinin to assess the acrosomal status and the zona pellucida-induced acrosome reaction in stallion spermatozoa. J Androl. 1996;17(6):674\u201382.","journal-title":"J Androl"},{"issue":"5","key":"1389_CR22","first-page":"46","volume":"46","author":"JM Schexnider","year":"2007","unstructured":"Schexnider JM, Baker DG, Hasselschwert DL. Semen evaluation for verification of azoospermia after vasectomy in chimpanzees (pan troglodytes). J Am Assoc Lab Anim Sci. 2007;46(5):46\u20139.","journal-title":"J Am Assoc Lab Anim Sci"},{"issue":"5\u20136","key":"1389_CR23","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1387\/ijdb.082583bg","volume":"52","author":"BM Gadella","year":"2008","unstructured":"Gadella BM, Tsai PS, Boerke A, Brewis IA. Sperm head membrane reorganisation during capacitation. The International journal of developmental biology. 2008;52(5\u20136):473\u201380.","journal-title":"The International journal of developmental biology"},{"issue":"22","key":"1389_CR24","doi-asserted-by":"publisher","first-page":"4471","DOI":"10.1242\/dev.090613","volume":"140","author":"M Okabe","year":"2013","unstructured":"Okabe M. The cell biology of mammalian fertilization. Development. 2013;140(22):4471\u20139.","journal-title":"Development"},{"key":"1389_CR25","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1002\/ajp.1350180402","volume":"18","author":"KGS Gould","year":"1989","unstructured":"Gould KGS, R.P. Improved methods for freeze preservation of chimpanzee sperm. Am J Primatol. 1989;18:275\u201384.","journal-title":"Am J Primatol"},{"issue":"4","key":"1389_CR26","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1086\/415144","volume":"61","author":"FB de Waal","year":"1986","unstructured":"de Waal FB. The integration of dominance and social bonding in primates. Q Rev Biol. 1986;61(4):459\u201379.","journal-title":"Q Rev Biol"},{"issue":"4","key":"1389_CR27","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1159\/000156255","volume":"46","author":"FB de Waal","year":"1986","unstructured":"de Waal FB, Luttrell LM. The similarity principle underlying social bonding among female rhesus monkeys. Folia Primatol (Basel). 1986;46(4):215\u201334.","journal-title":"Folia Primatol (Basel)"},{"issue":"3","key":"1389_CR28","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.anireprosci.2012.10.005","volume":"136","author":"PW Bravo","year":"2013","unstructured":"Bravo PW, Alarcon V, Baca L, Cuba Y, Ordonez C, Salinas J, Tito F. Semen preservation and artificial insemination in domesticated south American camelids. Anim Reprod Sci. 2013;136(3):157\u201363.","journal-title":"Anim Reprod Sci"},{"issue":"2","key":"1389_CR29","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1016\/S0749-0720(15)30560-0","volume":"10","author":"PW Bravo","year":"1994","unstructured":"Bravo PW, Johnson LW. Reproductive physiology of the male camelid. Vet Clin North Am Food Anim Pract. 1994;10(2):259\u201364.","journal-title":"Vet Clin North Am Food Anim Pract"},{"issue":"3","key":"1389_CR30","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1080\/014850199262562","volume":"43","author":"PW Bravo","year":"1999","unstructured":"Bravo PW, Pacheco C, Quispe G, Vilcapaza L, Ordonez C. Degelification of alpaca semen and the effect of dilution rates on artificial insemination outcome. Arch Androl. 1999;43(3):239\u201346.","journal-title":"Arch Androl"},{"issue":"1","key":"1389_CR31","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.anireprosci.2009.06.005","volume":"118","author":"S Giuliano","year":"2010","unstructured":"Giuliano S, Carretero M, Gambarotta M, Neild D, Trasorras V, Pinto M, Miragaya M. Improvement of llama (Lama glama) seminal characteristics using collagenase. Anim Reprod Sci. 2010;118(1):98\u2013102.","journal-title":"Anim Reprod Sci"},{"issue":"1","key":"1389_CR32","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1016\/S0015-0282(16)60797-5","volume":"52","author":"BA Keel","year":"1989","unstructured":"Keel BA, Webster BW. Semen analysis data from fresh and cryopreserved donor ejaculates: comparison of cryoprotectants and pregnancy rates. Fertil Steril. 1989;52(1):100\u20135.","journal-title":"Fertil Steril"},{"issue":"6 Pt 1","key":"1389_CR33","doi-asserted-by":"publisher","first-page":"1597","DOI":"10.1016\/0002-9378(92)91548-O","volume":"166","author":"LL Subak","year":"1992","unstructured":"Subak LL, Adamson GD, Boltz NL. Therapeutic donor insemination: a prospective randomized trial of fresh versus frozen sperm. Am J Obstet Gynecol. 1992;166(6 Pt 1):1597\u2013604. discussion 1604-1596","journal-title":"Am J Obstet Gynecol"},{"issue":"3","key":"1389_CR34","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1093\/humupd\/dmp048","volume":"16","author":"TG Cooper","year":"2010","unstructured":"Cooper TG, Noonan E, von Eckardstein S, Auger J, Baker HW, Behre HM, Haugen TB, Kruger T, Wang C, Mbizvo MT, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update. 2010;16(3):231\u201345.","journal-title":"Hum Reprod Update"},{"issue":"3","key":"1389_CR35","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1021\/pr100745u","volume":"10","author":"I Batruch","year":"2011","unstructured":"Batruch I, Lecker I, Kagedan D, Smith CR, Mullen BJ, Grober E, Lo KC, Diamandis EP, Jarvi KA. Proteomic analysis of seminal plasma from normal volunteers and post-vasectomy patients identifies over 2000 proteins and candidate biomarkers of the urogenital system. J Proteome Res. 2011;10(3):941\u201353.","journal-title":"J Proteome Res"},{"issue":"5","key":"1389_CR36","doi-asserted-by":"publisher","first-page":"R40","DOI":"10.1186\/gb-2006-7-5-r40","volume":"7","author":"B Pilch","year":"2006","unstructured":"Pilch B, Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 2006;7(5):R40.","journal-title":"Genome Biol"},{"issue":"1","key":"1389_CR37","doi-asserted-by":"publisher","first-page":"e79","DOI":"10.1111\/j.1439-0531.2010.01641.x","volume":"46","author":"AM Kareskoski","year":"2011","unstructured":"Kareskoski AM, del Alamo MM, Guvenc K, Reilas T, Calvete JJ, Rodriguez-Martinez H, Andersson M, Katila T. Protein composition of seminal plasma in fractionated stallion ejaculates. Reprod Domest Anim. 2011;46(1):e79\u201384.","journal-title":"Reprod Domest Anim"},{"issue":"4","key":"1389_CR38","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1002\/pmic.201400032","volume":"15","author":"A Holland","year":"2015","unstructured":"Holland A, Ohlendieck K. Comparative profiling of the sperm proteome. Proteomics. 2015;15(4):632\u201348.","journal-title":"Proteomics"},{"issue":"1","key":"1389_CR39","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/j.theriogenology.2014.08.010","volume":"83","author":"O Kawase","year":"2015","unstructured":"Kawase O, Cao S, Xuan X. Sperm membrane proteome in wild Japanese macaque (Macaca fuscata) and sika deer (Cervus nippon). Theriogenology. 2015;83(1):95\u2013102.","journal-title":"Theriogenology"},{"key":"1389_CR40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.anireprosci.2016.08.008","volume":"173","author":"CJ Li","year":"2016","unstructured":"Li CJ, Wang D, Zhou X. Sperm proteome and reproductive technologies in mammals. Anim Reprod Sci. 2016;173:1\u20137.","journal-title":"Anim Reprod Sci"},{"issue":"3","key":"1389_CR41","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1530\/REP-14-0500","volume":"149","author":"A Swegen","year":"2015","unstructured":"Swegen A, Curry BJ, Gibb Z, Lambourne SR, Smith ND, Aitken RJ. Investigation of the stallion sperm proteome by mass spectrometry. Reproduction. 2015;149(3):235\u201344.","journal-title":"Reproduction"}],"container-title":["BMC Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-018-1389-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,1]],"date-time":"2024-07-01T15:35:25Z","timestamp":1719848125000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcvetres.biomedcentral.com\/articles\/10.1186\/s12917-018-1389-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,2,27]]},"references-count":41,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2018,12]]}},"alternative-id":["1389"],"URL":"https:\/\/doi.org\/10.1186\/s12917-018-1389-0","relation":{},"ISSN":["1746-6148"],"issn-type":[{"value":"1746-6148","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,2,27]]},"assertion":[{"value":"7 September 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 February 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 February 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Ethics approval and sample collections were performed and supervised by the approved veterinarians throughout the study. Material collections from the animals followed the regulation and approval of animal welfare committee of Taipei Zoo (protocol#10601) and was monitored under the guidance of the animal welfare committee of Taipei Zoo. Consent was obtained for the samples to be collected at the Taipei Zoo.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"All authors declare no conflict of interests that could prejudice the impartiality of the research reported.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Publisher\u2019s Note"}}],"article-number":"58"}}