Characterization of Bottlenose Dolphin (Tursiops truncatus) Sperm Based on Morphometric Traits
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
PID2019-106380RB-I00/AEI /10.1303/501100011033
Ministerio de Ciencia e Innovación
PubMed
33922110
PubMed Central
PMC8143526
DOI
10.3390/biology10050355
PII: biology10050355
Knihovny.cz E-zdroje
- Klíčová slova
- cetacean, morphology, morphometry, semen, sperm cells,
- Publikační typ
- časopisecké články MeSH
Bottlenose dolphin (Tursiops truncatus) males follow many reproductive strategies to ensure their paternity. However, little is known about the sperm traits, including morphometric features, that contribute to their reproductive success. Our aim was to study dolphin sperm morphometry (a total of 13 parameters) in two adult males to evaluate (i) presumptive sperm subpopulations, (ii) the correlation of sperm morphometry with testosterone levels and (iii) the effect of refrigerated storage on the sperm morphometry. Sperm populations were classified into four principal components (PCs) based on morphometry (>94% of cumulative variance). The PCs clustered into two different sperm subpopulations, which differed between males. Furthermore, the levels of serum testosterone were positively correlated with the length of the midpiece but negatively correlated with head width and the principal piece, flagellum and total sperm lengths. Most of the sperm morphometric parameters changed during the storage period (day 1 vs. day 7), but only the principal piece length was affected by the storage temperature (5 °C vs. 15 °C). This is the first study to identify dolphin sperm subpopulations based on morphometry and the influence of serum testosterone and refrigeration on sperm morphometry.
Biology Department Avanqua Oceanogràfic S L 46013 Valencia Spain
Department of Animal Reproduction INIA 28040 Madrid Spain
Department of Medicine and Surgery Faculty of Veterinary Science 28040 Madrid Spain
Research Department Fundación Oceanogràfic 46013 Valencia Spain
Zobrazit více v PubMed
Valls A., Coll M., Christensen V., Ellison A.M. Keystone species: Toward an operational concept for marine biodiversity conservation. Ecol. Monogr. 2015;85:29–47. doi: 10.1890/14-0306.1. DOI
Bowen W. Role of marine mammals in aquatic ecosystems. Mar. Ecol. Prog. Ser. 1997;158:267–274. doi: 10.3354/meps158267. DOI
López B.D. Bottlenose dolphins and aquaculture: Interaction and site fidelity on the north-eastern coast of Sardinia (Italy) Mar. Biol. 2012;159:2161–2172. doi: 10.1007/s00227-012-2002-x. DOI
Reynolds J.E., Marsh H., Ragen T.J. Marine mammal conservation. Endanger. Species Res. 2009;7:23–28. doi: 10.3354/esr00179. DOI
Pace D., Tizzi R., Mussi B. Cetaceans Value and Conservation in the Mediterranean Sea. J. Biodivers. Endanger. Species. 2015:S1:004. doi: 10.4172/2332-2543.S1.004. DOI
Wells R., Natoli A., Braulik G. Tursiops truncatus (errata version published in 2019) IUCN Red List Threat. Species. 2019;8235:e.T22563A156932432.
Barratclough A., Wells R.S., Schwacke L.H., Rowles T.K., Gomez F.M., Fauquier D.A., Sweeney J.C., Townsend F.I., Hansen L.J., Zolman E.S., et al. Health Assessments of Common Bottlenose Dolphins (Tursiops truncatus): Past, Present, and Potential Conservation Applications. Front. Veter Sci. 2019;6:444. doi: 10.3389/fvets.2019.00444. PubMed DOI PMC
Herrick J.R. Assisted reproductive technologies for endangered species conservation: Developing sophisticated protocols with limited access to animals with unique reproductive mechanisms. Biol. Reprod. 2019;100:1158–1170. doi: 10.1093/biolre/ioz025. PubMed DOI
Kamler J.F., Ballard W.B., Lemons P.R., Mote K. Variation in mating system and group structure in two populations of swift foxes, Vulpes velox. Anim. Behav. 2004;68:83–88. doi: 10.1016/j.anbehav.2003.07.017. DOI
Hayes S.A., Pearse D.E., Costa D.P., Harvey J.T., Le Boeuf B.J., Garza J.C. Mating system and reproductive success in eastern Pacific harbour seals. Mol. Ecol. 2006;15:3023–3034. doi: 10.1111/j.1365-294X.2006.02984.x. PubMed DOI
Whitehead H., Mann J. Female Reproductive Strategies of Cetaceans: Life Histories and Calf Care. In: Mann J., Connor R.C., Whitehead P.T.H., editors. Cetacean Societies: Field Studies of Dolphins and Whales. The University of Chicago Press; Chicago, IL, USA: 2000.
Rommel S., Pabst D., McLellan W. Reproductive Biology and Phylogeny of Cetacea. CRC Press; Boca Raton, FL, USA: 2007. Functional Anatomy of the Cetacean Reproductive System, with Comparisons to the Domestic Dog; pp. 127–145.
Brook F.M. The Use of Diagnostic Ultrasound in Assessment of the Reproductive Status of the Bottlenose Dolphin, Tursiops Aduncas, in Captivity & Applications in Management of a Controlled Breeding Programme. The Hong Kong Polytechnic University; Hong Kong, China: 1997.
Krützen M., Barré L.M., Connor R.C., Mann J., Sherwin W.B. ‘O father: Where art thou?’—Paternity assessment in an open fission-fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Mol. Ecol. 2004;13:1975–1990. doi: 10.1111/j.1365-294X.2004.02192.x. PubMed DOI
Sánchez-Calabuig M., López-Fernández C., Johnston S., Blyde D., Cooper J., Harrison K., De La Fuente J., Gosálvez J. Effect of Cryopreservation on the Sperm DNA Fragmentation Dynamics of the Bottlenose Dolphin (Tursiops truncatus) Reprod. Domest. Anim. 2015;50:227–235. doi: 10.1111/rda.12474. PubMed DOI
Van Der Horst G., Medger K., Steckler D., Luther I., Bartels P. Bottlenose dolphin (Tursiops truncatus) sperm revisited: Motility, morphology and ultrastructure of fresh sperm of consecutive ejaculates. Anim. Reprod. Sci. 2018;195:309–320. doi: 10.1016/j.anireprosci.2018.06.009. PubMed DOI
Kenagy G.J., Trombulak S.C. Size and Function of Mammalian Testes in Relation to Body Size. J. Mammal. 1986;67:1–22. doi: 10.2307/1380997. DOI
Turner J.P., Clark L.S., Haubold E.M., Worthy G.A.J., Cowan D.F. Organ Weights and Growth Profiles in Bottlenose Dolphins (Tursiops truncatus) from the Northwestern Gulf of Mexico. Aquat. Mamm. 2006;32:46–57. doi: 10.1578/AM.32.1.2006.46. DOI
Mead J.G. Encyclopedia of Marine Mammals. Academic Press; Cambridge, MA, USA: 2018. Shepherd’s Beaked Whale; pp. 853–854.
Van Der Horst G., Maree L. Sperm form and function in the absence of sperm competition. Mol. Reprod. Dev. 2014;81:204–216. doi: 10.1002/mrd.22277. PubMed DOI
Parker G.A. Sperm Competition and Its Evolutionary Consequences in the Insects. Biol. Rev. 1970;45:525–567. doi: 10.1111/j.1469-185X.1970.tb01176.x. DOI
Holt W., Fazeli A. Sperm selection in the female mammalian reproductive tract. Focus on the oviduct: Hypotheses, mechanisms, and new opportunities. Theriogenology. 2016;85:105–112. doi: 10.1016/j.theriogenology.2015.07.019. PubMed DOI
A García-Vázquez F., Gadea J., Matás C., Holt W.V. Importance of sperm morphology during their transport and fertilization in mammals. Asian J. Androl. 2016;18:844–850. doi: 10.4103/1008-682X.186880. PubMed DOI PMC
Vicente-Fiel S., Palacín I., Santolaria P., Yániz J. A comparative study of sperm morphometric subpopulations in cattle, goat, sheep and pigs using a computer-assisted fluorescence method (CASMA-F) Anim. Reprod. Sci. 2013;139:182–189. doi: 10.1016/j.anireprosci.2013.04.002. PubMed DOI
Yániz J., Soler C., Santolaria P. Computer assisted sperm morphometry in mammals: A review. Anim. Reprod. Sci. 2015;156:1–12. doi: 10.1016/j.anireprosci.2015.03.002. PubMed DOI
Santolaria P., Soler C., Recreo P., Carretero T., Bono A., Berné J.M., Yániz J.L. Morphometric and kinematic sperm subpopulations in the split ejaculate of normozoospermic men. Asian J. Androl. 2016;18:831. doi: 10.4103/1008-682X.186874. PubMed DOI PMC
Anderson M.J., Nyholt J., Dixson A.F. Sperm competition and the evolution of sperm midpiece volume in mammals. J. Zool. 2005;267:135–142. doi: 10.1017/S0952836905007284. DOI
Bauer M., Breed W.G. Variation of sperm head shape and tail length in a species of Australian hydromyine rodent: The spinifex hopping mouse, Notomys alexis. Reprod. Fertil. Dev. 2006;18:797–805. doi: 10.1071/RD06045. PubMed DOI
Kleven O., Laskemoen T., Lifjeld J.T. Sperm length in sand martinsRiparia riparia: A comment on Helfenstein et al. J. Avian Biol. 2009;40:241–242. doi: 10.1111/j.1600-048X.2009.04766.x. DOI
Lüpold S., Calhim S., Immler S., Birkhead T.R. Sperm morphology and sperm velocity in passerine birds. Proc. R. Soc. B Boil. Sci. 2008;276:1175–1181. doi: 10.1098/rspb.2008.1645. PubMed DOI PMC
García–Vázquez F.A., Hernández-Caravaca I., Yánez-Quintana W., Matas C., Soriano-Úbeda C., Izquierdo-Rico M.J. Morphometry of boar sperm head and flagellum in semen backflow after insemination. Theriogenology. 2015;84:566–574. doi: 10.1016/j.theriogenology.2015.04.011. PubMed DOI
Fitzpatrick J.L., Lüpold S. Sexual selection and the evolution of sperm quality. Mol. Hum. Reprod. 2014;20:1180–1189. doi: 10.1093/molehr/gau067. PubMed DOI
Ramm S. Sperm competition and the evolution of reproductive systems. Mol. Hum. Reprod. 2014;20:1159–1160. doi: 10.1093/molehr/gau076. PubMed DOI
Fleming A.D., Yanagimachi R., Yanagimachi H. Spermatozoa of the Atlantic bottlenosed dolphin, Tursiops truncatus. Reproduction. 1981;63:509–514. doi: 10.1530/jrf.0.0630509. PubMed DOI
Miller D.L., Styer E.L., Decker S.J., Robeck T. Ultrastructure of the spermatozoa from three odontocetes: A killer whale (Orcinus orca), a Pacific white-sided dolphin (Lagenorhynchus obliquidens) and a beluga (Delphinapterus leucas) Anat. Histol. Embryol. 2002;31:158–168. doi: 10.1046/j.1439-0264.2002.00385.x. PubMed DOI
Meisner A.D., Klaus A.V., O’Leary M.A. Sperm head morphology in 36 species of artiodactylans, perissodactylans, and cetaceans (Mammalia) J. Morphol. 2004;263:179–202. doi: 10.1002/jmor.10297. PubMed DOI
Amaral R.S., Da Silva V.M.F., Domingos F.X.V., Martin A.R. Morphology and Ultrastructure of the Amazon River Dolphin (Inia geoffrensis) Spermatozoa. Anat. Rec. Adv. Integr. Anat. Evol. Biol. 2017;300:1519–1523. doi: 10.1002/ar.23585. PubMed DOI
O’Brien E., Esteso M., Castaño C., Toledano-Díaz A., Bóveda P., Martínez-Fresneda L., López-Sebastián A., Martínez-Nevado E., Guerra R., Fernández M.L., et al. Effectiveness of ultra-rapid cryopreservation of sperm from endangered species, examined by morphometric means. Theriogenology. 2019;129:160–167. doi: 10.1016/j.theriogenology.2019.02.024. PubMed DOI
Rubio-Guillén J., González D., Garde J., Esteso M., Santos F., Rodríguez-Gil J., Madrid-Bury N., Quintero-Moreno A. Effects of Cryopreservation on Bull Spermatozoa Distribution in Morphometrically Distinct Subpopulations. Reprod. Domest. Anim. 2007;42:354–357. doi: 10.1111/j.1439-0531.2006.00788.x. PubMed DOI
Dorado J., Alcaraz L., Duarte N., Portero J., Acha D., Hidalgo M. Changes in the structures of motile sperm subpopulations in dog spermatozoa after both cryopreservation and centrifugation on PureSperm® gradient. Anim. Reprod. Sci. 2011;125:211–218. doi: 10.1016/j.anireprosci.2011.03.013. PubMed DOI
Esteso M., Santos F., Soler A.J., Montoro V., Quintero-Moreno A., Garde J. The Effects of Cryopreservation on the Morphometric Dimensions of Iberian Red Deer (Cervus elaphus hispanicus) Epididymal Sperm Heads. Reprod. Domest. Anim. 2006;41:241–246. doi: 10.1111/j.1439-0531.2006.00676.x. PubMed DOI
Martí J., Aparicio I., García-Herreros M. Head morphometric changes in cryopreserved ram spermatozoa are related to sexual maturity. Theriogenology. 2011;75:473–481. doi: 10.1016/j.theriogenology.2010.09.015. PubMed DOI
Goeritz F., Quest M., Wagener A., Fassbender M., Broich A., Hildebrandt T., Hofmann R., Blottner S. Seasonal timing of sperm production in roe deer: Interrelationship among changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology. 2003;59:1487–1502. doi: 10.1016/S0093-691X(02)01201-3. PubMed DOI
Immler S., Pryke S.R., Birkhead T.R., Griffith S.C. Pronounced within-Individual Plasticity in Sperm Morphometry across Social Environments. Evolution. 2009;64:1634–1643. doi: 10.1111/j.1558-5646.2009.00924.x. PubMed DOI
Sánchez-Calabuig M.J., García-Vázquez F.A., Laguna-Barraza R., Barros-García C., García-Parraga D., Rizos D., Gutierrez-Adan A., Pérez-Gutíerrez J.F. Bottlenose Dolphin (Tursiops truncatus) Spermatozoa: Collection, Cryopreservation, and Heterologous In Vitro Fertilization. J. Vis. Exp. 2017;2017:e55237. doi: 10.3791/55237. PubMed DOI PMC
Ros-Santaella J.L., Domínguez-Rebolledo Á.E., Garde J.J. Sperm Flagellum Volume Determines Freezability in Red Deer Spermatozoa. PLoS ONE. 2014;9:e112382. doi: 10.1371/journal.pone.0112382. PubMed DOI PMC
Saravia F., Núñez-Martínez I., Morán J., Soler C., Muriel A., Rodríguez-Martínez H., Peña F. Differences in boar sperm head shape and dimensions recorded by computer-assisted sperm morphometry are not related to chromatin integrity. Theriogenology. 2007;68:196–203. doi: 10.1016/j.theriogenology.2007.04.052. PubMed DOI
Kassambara A. Machine Learning Essentials: Practical Guide in R. [(accessed on 1 March 2021)];2018 Available online: https://www.amazon.com/Machine-Learning-Essentials-Practical-Guide/dp/1986406857.
Brock G., Pihur V., Datta S., Datta S. clValid: AnRPackage for Cluster Validation. J. Stat. Softw. 2008;25:1–22. doi: 10.18637/jss.v025.i04. DOI
Cerdeira J., Sánchez-Calabuig M., Pérez-Gutiérrez J., Hijon M., Castaño C., Santiago-Moreno J. Cryopreservation effects on canine sperm morphometric variables and ultrastructure: Comparison between vitrification and conventional freezing. Cryobiology. 2020;95:164–170. doi: 10.1016/j.cryobiol.2020.03.007. PubMed DOI
Cucho H., Alarcón V., Ordóñez C., Ampuero E., Meza A., Soler C. Puma (Puma concolor) epididymal sperm morphometry assessed by the ISAS®v1 CASA-Morph system. Asian J. Androl. 2016;18:879–881. doi: 10.4103/1008-682X.187584. PubMed DOI PMC
Esteso M., Rodríguez E., Toledano-Díaz A., Castaño C., Pradiee J., López-Sebastián A., Santiago-Moreno J. Descriptive analysis of sperm head morphometry in Iberian ibex (Capra pyrenaica): Optimum sampling procedure and staining methods using Sperm-Class Analyzer®. Anim. Reprod. Sci. 2015;155:42–49. doi: 10.1016/j.anireprosci.2015.01.014. PubMed DOI
García-Herreros M., Leal C.L.V. Sperm morphometry: A tool for detecting biophysical changes associated with viability in cryopreserved bovine spermatozoa. Andrologia. 2013;46:820–822. doi: 10.1111/and.12141. PubMed DOI
Buendía P., Soler C., Paolicchi F., Gago G., Urquieta B., Sánchez F.P., Bustos-Obregón E. Morphometric characterization and classification of alpaca sperm heads using the Sperm-Class Analyzer® computer-assisted system. Theriogenology. 2002;57:1207–1218. doi: 10.1016/S0093-691X(01)00724-5. PubMed DOI
Villaverde-Morcillo S., Soler A., Esteso M., Castaño C., Miñano-Berna A., Gonzalez F., Santiago-Moreno J. Immature and mature sperm morphometry in fresh and frozen-thawed falcon ejaculates. Theriogenology. 2017;98:94–100. doi: 10.1016/j.theriogenology.2017.04.051. PubMed DOI
Santiago-Moreno J., Esteso M.C., Pradieé J., Castano C., Toledano-Díaz A., O’Brien E., López-Sebastián A., Martinez-Nevado E., Delclaux M., Fernandez-Morán J., et al. Giant panda (Ailuropoda melanoleuca) sperm morphometry and function after repeated freezing and thawing. Andrologia. 2015;48:470–474. doi: 10.1111/and.12468. PubMed DOI
Urióstegui-Acosta M., Hernández-Ochoa I., Sánchez-Gutiérrez M., Piña-Guzmán B., Rafael-Vázquez L., Solís-Heredia M., Martínez-Aguilar G., Quintanilla-Vega B. Methamidophos alters sperm function and DNA at different stages of spermatogenesis in mice. Toxicol. Appl. Pharmacol. 2014;279:391–400. doi: 10.1016/j.taap.2014.06.017. PubMed DOI
Sheldon B. Promiscuity: An Evolutionary History of Sperm Competition and Sexual Conflict. Anim. Behav. 2000;60:704. doi: 10.1006/anbe.2000.1533. DOI
O’Brien J.K., Robeck T.R. Development of sperm sexing and associated assisted reproductive technology for sex preselection of captive bottlenose dolphins (Tursiops truncatus) Reprod. Fertil. Dev. 2006;18:319–329. doi: 10.1071/RD05108. PubMed DOI
Robeck T.R., O’Brien J.K. Effect of Cryopreservation Methods and Precryopreservation Storage on Bottlenose Dolphin (Tursiops truncatus) Spermatozoa1. Biol. Reprod. 2004;70:1340–1348. doi: 10.1095/biolreprod.103.025304. PubMed DOI
Robeck T., Steinman K., Yoshioka M., Jensen E., O’Brien J., Katsumata E., Gili C., McBain J., Sweeney J., Monfort S. Estrous cycle characterisation and artificial insemination using frozen–thawed spermatozoa in the bottlenose dolphin (Tursiops truncatus) Reproduction. 2005;129:659–674. doi: 10.1530/rep.1.00516. PubMed DOI
Anderson M.J., Dixson A.F. Sperm competition: Motility and the midpiece in primates. Nature. 2002;416:496. doi: 10.1038/416496a. PubMed DOI
Peña F.J., Saravia F., García-Herreros M., Núñezmartínez I., Tapia J.A., Wallgren M., Rodriguez-Martinez H., Johannisson A. Identification of Sperm Morphometric Subpopulations in Two Different Portions of the Boar Ejaculate and Its Relation to Postthaw Quality. J. Androl. 2005;26:716–723. doi: 10.2164/jandrol.05030. PubMed DOI
Urbano M., Ortiz I., Dorado J., Hidalgo M. Identification of sperm morphometric subpopulations in cooled-stored canine sperm and its relation with sperm DNA integrity. Reprod. Domest. Anim. 2017;52:468–476. doi: 10.1111/rda.12935. PubMed DOI
Robles-Gómez L., Fuentes-Albero M.D.C., Huerta-Retamal N., Sáez-Espinosa P., García-Párraga D., Romero A., Gómez-Torres M.J. Lectin spatial immunolocalization during in vitro capacitation in Tursiops truncatus spermatozoa. Anim. Reprod. 2020;17:e20190083. doi: 10.21451/1984-3143-AR2019-0083. PubMed DOI PMC
Bakker T.C.M., Hollmann M., Mehlis M., Zbinden M. Functional variation of sperm morphology in sticklebacks. Behav. Ecol. Sociobiol. 2014;68:617–627. doi: 10.1007/s00265-013-1676-5. DOI
García-Vázquez F.A., Hernández-Caravaca I., Matás C., Soriano-Úbeda C., Abril-Sánchez S., Izquierdo-Rico M.J. Morphological study of boar sperm during their passage through the female genital tract. J. Reprod. Dev. 2015;61:407–413. doi: 10.1262/jrd.2014-170. PubMed DOI PMC
Firman R.C., Cheam L.Y., Simmons L.W. Sperm competition does not influence sperm hook morphology in selection lines of house mice. J. Evol. Biol. 2011;24:856–862. doi: 10.1111/j.1420-9101.2010.02219.x. PubMed DOI
Maroto-Morales A., García-Álvarez O., Ramón M., Martínez-Pastor F., Fernández-Santos M.R., Soler A.J., Garde J.J. Current status and potential of morphometric sperm analysis. Asian J. Androl. 2016;18:863–870. doi: 10.4103/1008-682X.187581. PubMed DOI PMC
Gu N.-H., Zhao W.-L., Wang G.-S., Sun F. Comparative analysis of mammalian sperm ultrastructure reveals relationships between sperm morphology, mitochondrial functions and motility. Reprod. Biol. Endocrinol. 2019;17:1–12. doi: 10.1186/s12958-019-0510-y. PubMed DOI PMC
Schroeder J.P., Keller K.V. Seasonality of serum testosterone levels and sperm density inTursiops truncatus. J. Exp. Zool. 1989;249:316–321. doi: 10.1002/jez.1402490310. PubMed DOI
Ruiz-Díaz S., Luongo C., Fuentes-Albero M., Abril-Sánchez S., Sánchez-Calabuig M., Barros-García C., De La Fe C., García-Galán A., Ros-Santaella J., Pintus E., et al. Effect of temperature and cell concentration on dolphin (Tursiops truncatus) spermatozoa quality evaluated at different days of refrigeration. Anim. Reprod. Sci. 2020;212:106248. doi: 10.1016/j.anireprosci.2019.106248. PubMed DOI
Gomendio M., Malo A.F., Garde J., Roldan E.R.S. Sperm traits and male fertility in natural populations. Reproduction. 2007;134:19–29. doi: 10.1530/REP-07-0143. PubMed DOI
Lavara R., Vicente J., Baselga M. Genetic variation in head morphometry of rabbit sperm. Theriogenology. 2013;80:313–318. doi: 10.1016/j.theriogenology.2013.04.015. PubMed DOI
Hirai M., Boersma A., Hoeflich A., Wolf E., Foll J., Aumüller T.R., Braun J. Objectively measured sperm motility and sperm head morphometry in boars (Sus scrofa): Relation to fertility and seminal plasma growth factors. J. Androl. 2001;22:104–110. PubMed
Marco-Jiménez F., Vicente J.-S., Lavara R., Balasch S., Viudes-De-Castro M.-P. Poor Prediction Value of Sperm Head Morphometry for Fertility and Litter Size in Rabbit. Reprod. Domest. Anim. 2009;45:e118–e123. doi: 10.1111/j.1439-0531.2009.01532.x. PubMed DOI
Vernocchi V., Morselli M.G., Consiglio A.L., Faustini M., Luvoni G.C. DNA fragmentation and sperm head morphometry in cat epididymal spermatozoa. Theriogenology. 2014;82:982–987. doi: 10.1016/j.theriogenology.2014.07.014. PubMed DOI
Phetudomsinsuk K., Sirinarumitr K., Laikul A., Pinyopummin A. Morphology and head morphometric characters of sperm in Thai native crossbred stallions. Acta Veter Scand. 2008;50:41. doi: 10.1186/1751-0147-50-41. PubMed DOI PMC
Martí J., Aparicio I., Leal C., García-Herreros M. Seasonal dynamics of sperm morphometric subpopulations and its association with sperm quality parameters in ram ejaculates. Theriogenology. 2012;78:528–541. doi: 10.1016/j.theriogenology.2012.02.035. PubMed DOI
Cardullo R.A., Baltz J.M. Metabolic regulation in mammalian sperm: Mitochondrial volume determines sperm length and flagellar beat frequency. Cell Motil. Cytoskelet. 1991;19:180–188. doi: 10.1002/cm.970190306. PubMed DOI
Fawcett D.W. The mammalian spermatozoon. Dev. Biol. 1975;44:394–436. doi: 10.1016/0012-1606(75)90411-X. PubMed DOI
Fisher H.S., Jacobs-Palmer E., Lassance J.-M., Hoekstra H.E. The genetic basis and fitness consequences of sperm midpiece size in deer mice. Nat. Commun. 2016;7:13652. doi: 10.1038/ncomms13652. PubMed DOI PMC
González Villalobos D., Quintero-Moreno A., Garde López-Brea J.J., Esteso M.C., Rocío Fernández-Santos M., Rubio-Guillén J., Mejía Silva W., González Marval Y., León Atencio G., Bohórquez Corona R. Morphometry characterization of boar sperm head with computer assisted analysis (preliminary results) Rev. Cient. Fac. Cienc. Vet. La Univ. Del Zulia. 2008;18:570–577.
Morales B., Quintero-Moreno A., Osorio-Meléndez C., Rubio-Guillén J. Valoración de la biometría de la cabeza del espermatozoide mediante análisis computarizado en semen de cerdo recién colectado y refrigerado. Rev. Fac. Agron. 2012;29:413–431.
Gravance C.G., Vishwnath R., Pitt C., Garner L., Casey J. Effects of Cryopreservation on Bull sperm head morphometry. J. Androl. 1998;19:704–709. PubMed
Esteso M.C., Fernández-Santos M.R., Soler A.J., Garde J.J. Head dimensions of cryopreserved red deer spermatozoa are affected by thawing procedure. Cryo Lett. 2003;24:260–267. PubMed
Villaverde-Morcillo S., García-Sánchez R., Castaño C., Rodríguez E., Gonzalez F., Esteso M., Santiago-Moreno J. Characterization of Natural Ejaculates and Sperm Cryopreservation in a Golden Eagle (Aquila chrysaetus) J. Zoo Wildl. Med. 2015;46:335–338. doi: 10.1638/2013-0293R1.1. PubMed DOI
Thomas C.A., Garner D.L., DeJarnette J.M., Marshall C.E. Effect of Cryopreservation on Bovine Sperm Organelle Function and Viability as Determined by Flow Cytometry. Biol. Reprod. 1998;58:786–793. doi: 10.1095/biolreprod58.3.786. PubMed DOI
Núñez-Martinez I., Morán J.M., Peña F.J. Identification of sperm morphometric subpopulations in the canine ejaculate: Do they reflect different subpopulations in sperm chromatin integrity? Zygote. 2007;15:257–266. doi: 10.1017/S0967199407004248. PubMed DOI
Utsuno H., Oka K., Yamamoto A., Shiozawa T. Evaluation of sperm head shape at high magnification revealed correlation of sperm DNA fragmentation with aberrant head ellipticity and angularity. Fertil. Steril. 2013;99:1573–1580.e1. doi: 10.1016/j.fertnstert.2013.01.100. PubMed DOI
Álvarez M., García-Macías V., Martínez-Pastor F., Martínez F., Borragán S., Mata M., Garde J., Anel L., De Paz P. Effects of cryopreservation on head morphometry and its relation with chromatin status in brown bear (Ursus arctos) spermatozoa. Theriogenology. 2008;70:1498–1506. doi: 10.1016/j.theriogenology.2008.06.097. PubMed DOI
Charpentier G., Fournier F., Behue N., Marlot D., Brulé G., Parker G.A., Begon M.E. Sperm competition games: Sperm size and number under gametic control. Proc. R. Soc. B Boil. Sci. 1993;253:255–262. doi: 10.1098/rspb.1993.0111. PubMed DOI
Du Plessis S.S., Agarwal A., Mohanty G., Van Der Linde M. Oxidative phosphorylation versus glycolysis: What fuel do spermatozoa use? Asian J. Androl. 2015;17:230–235. doi: 10.4103/1008-682X.135123. PubMed DOI PMC