{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T05:54:16Z","timestamp":1789883656410,"version":"4.0.1"},"reference-count":26,"publisher":"Wiley","issue":"2","license":[{"start":{"date-parts":[[2003,2,27]],"date-time":"2003-02-27T00:00:00Z","timestamp":1046304000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Morphology"],"published-print":{"date-parts":[[2003,5]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The unique urogenital anatomy and histology of female spotted hyenas (<jats:italic>Crocuta crocuta Erxleben<\/jats:italic>) was reexamined to identify adaptations of \u201cstructure\u201d that enable\/facilitate urination, mating, and parturition through the clitoris. Unusual features of penile anatomy required for meeting ceremonies and successful mating through a clitoral point of insertion were also examined. As reported previously, the upper urogenital tract of the female spotted hyena is typical of other carnivores and consists of the oviducts, uterine horns, uterine body, and vagina. An anatomically defined cervix is absent, even though a histologically defined transition zone between the uterine body and vagina was demonstrated. Adaptive features of the upper genital tract were a helical\u2010shaped uterine cavity, extensive smooth muscle in the uterus and vagina, and a newly discovered submucosal mucous urogenital gland (SMUG) located immediately caudal to the vagina. The extensive smooth muscle facilitates the expulsion of the large pups at parturition through the recurved birth canal. Secretions of the SMUG provide lubrication and protection for the urogenital mucosa during mating and parturition. Two types of \u201cerections\u201d are suggested by behavioral observations: the common hemodynamic erection required for insertion and thrusting by the male, and phallic \u201cflipping\u201d that commonly occurs earlier in the mating sequence and is sometimes seen during meeting ceremonies. Phallic \u201cflipping\u201d appears to be accomplished by the coordinated contractions of the large ischiocavernosus and retractor muscles acting on the semirigid organ. The extremely thick tunica albuginea and interstitial collagen of the common corporal body of the penis and clitoris gives the flaccid phallus some degree of rigidity even in the resting state in males and nulliparous females. Phallic \u201cflipping\u201d implies a hinge region in which flexibility is the key feature. Such a proximal hinge region of the male and female phallus was defined and was notable for its diminished collagen content. The urogenital sinus traversing the clitoris was specialized for distensibility, thus facilitating receipt of the penis during mating and for passage of the infant to the tip of the glans clitoris, where it emerges at parturition. The morphology of the glans penis is notable for the tapered common corporal body that extends to the distal tip of the glans. This adaptation is suggested to be required for a clitoral (as opposed to a vaginal) point of insertion during mating. Finally, additional segments of erectile tissue devoid of a thick collagenous capsule were demonstrated in the glans penis and glans clitoris, which appear to account for the \u201cpartially\u2010locking\u201d of the male into the female during the late stages of a mating sequence. Taken together, it is evident that the unusual sexual behaviors of the male and female spotted hyenas are facilitated by unique structural modifications of the relevant organs. J. Morphol. 256:205\u2013218, 2003. \u00a9 2003 Wiley\u2010Liss, Inc.<\/jats:p>","DOI":"10.1002\/jmor.10085","type":"journal-article","created":{"date-parts":[[2003,3,18]],"date-time":"2003-03-18T23:01:05Z","timestamp":1048028465000},"page":"205-218","source":"Crossref","is-referenced-by-count":34,"title":["Urogenital system of the spotted hyena (<i>Crocuta crocuta Erxleben<\/i>): A functional histological study"],"prefix":"10.1002","volume":"256","author":[{"given":"Gerald R.","family":"Cunha","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuzhuo","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ned J.","family":"Place","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenhui","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Larry","family":"Baskin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen E.","family":"Glickman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2003,2,27]]},"reference":[{"key":"e_1_2_1_2_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1749-6632.1959.tb44596.x"},{"key":"e_1_2_1_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001430309"},{"key":"e_1_2_1_4_1","first-page":"277","article-title":"The female external genitalia of the spotted hyena","volume":"31","author":"Davis D","year":"1949","journal-title":"Field Zool"},{"key":"e_1_2_1_5_1","first-page":"118","article-title":"Androgens and masculinization of the genitalia in the spotted hyaena (Crocuta crocuta). 2. Effects of prenatal anti\u2010androgens","volume":"113","author":"Drea C","year":"1998","journal-title":"J Reprod Fertil"},{"key":"e_1_2_1_6_1","first-page":"718","volume-title":"Encyclopedia of reproduction","author":"Drea C","year":"1999"},{"key":"e_1_2_1_7_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00170251"},{"key":"e_1_2_1_8_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1096-9861(19961111)375:2<333::AID-CNE11>3.0.CO;2-W"},{"key":"e_1_2_1_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/377584b0"},{"key":"e_1_2_1_10_1","first-page":"501","article-title":"The spotted hyena from Aristotle to The Lion King: reputation is everything","volume":"62","author":"Glickman SE","year":"1995","journal-title":"Soc Res"},{"key":"e_1_2_1_11_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1749-6632.1992.tb22858.x"},{"key":"e_1_2_1_12_1","doi-asserted-by":"publisher","DOI":"10.1530\/jrf.0.1130129"},{"key":"e_1_2_1_13_1","volume-title":"Meeting ceremonies in a colony of juvenile spotted hyenas","author":"Krusko N","year":"1988"},{"key":"e_1_2_1_14_1","volume-title":"The spotted hyaena: a study of predation and social behavior","author":"Kruuk H","year":"1972"},{"key":"e_1_2_1_15_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.2001.0458"},{"key":"e_1_2_1_16_1","doi-asserted-by":"publisher","DOI":"10.1530\/jrf.0.1130105"},{"key":"e_1_2_1_17_1","volume-title":"Histopathologic technic and practical histochemistry","author":"Lillie RD","year":"1965"},{"key":"e_1_2_1_18_1","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1111\/j.1469-7998.1935.tb06254.x","article-title":"The oestrus cycle and intersexuality in the female mole (Talpa europaea Linn.)","volume":"1935","author":"Matthews L","year":"1935","journal-title":"Proc Zool Soc Lond"},{"key":"e_1_2_1_19_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.1939.0004"},{"key":"e_1_2_1_20_1","doi-asserted-by":"publisher","DOI":"10.1530\/jrf.0.0590509"},{"key":"e_1_2_1_21_1","first-page":"135","article-title":"Einige Bilder zur Paarung der Fleckenhy\u00e4ne, Crocutta crocuta","volume":"19","author":"Schneider K","year":"1952","journal-title":"Erxl Zool Garten"},{"key":"e_1_2_1_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-5347(05)67247-3"},{"key":"e_1_2_1_23_1","first-page":"1001","article-title":"Canine reproduction: reproductive organs and related structures of the nonparous, parous, and postpartum bitch","volume":"34","author":"Sokolowski JH","year":"1973","journal-title":"Am J Vet Res"},{"key":"e_1_2_1_24_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod56.5.1301"},{"key":"e_1_2_1_25_1","first-page":"369","article-title":"On the female generative organs of Hyaena crocuta","author":"Watson M","year":"1877","journal-title":"Proc Zool Soc Lond"},{"key":"e_1_2_1_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2028.1968.tb00901.x"},{"key":"e_1_2_1_27_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001150208"}],"container-title":["Journal of Morphology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fjmor.10085","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/jmor.10085","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,17]],"date-time":"2023-11-17T11:25:57Z","timestamp":1700220357000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/jmor.10085"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,2,27]]},"references-count":26,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2003,5]]}},"alternative-id":["10.1002\/jmor.10085"],"URL":"https:\/\/doi.org\/10.1002\/jmor.10085","archive":["Portico"],"relation":{},"ISSN":["0362-2525","1097-4687"],"issn-type":[{"value":"0362-2525","type":"print"},{"value":"1097-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,2,27]]}}}