Spermatogenesis is seasonal in the large hairy armadillo, Chaetophractus villosus (Dasypodidae, Xenarthra, Mammalia)
Juan P. Luaces A , Luis F. Rossi A , Valeria Merico B , Maurizio Zuccotti C , Carlo A. Redi B D E , Alberto J. Solari A , Maria S. Merani A F and Silvia Garagna B E F
+ Author Affiliations
- Author Affiliations
A Laboratorio de Biología Cromosómica, Facultad de Medicina, UBA, Paraguay 2155 10°P Lab 6, Buenos Aires, Argentina.
B Laboratorio di Biologia dello Sviluppo, Dipartimento di Biologia e Biotecnologie ‘Lazzaro Spallanzani’, Universita’ degli Studi di Pavia, Via Ferrata 9, 27100 Pavia, Italy.
C Sezione di Istologia ed Embriologia, Dipartimento di Medicina Sperimentale, Universita’ degli Studi di Parma, Parma, Italy.
D Fondazione Istituto di Ricovero e Cura a Carattere Scientifico, Policlinico San Matteo, Pavia, Italy.
E Centro di Ingegneria Tissutale e Centro di Eccellenza in Biologia Applicata, Universita’ degli Studi di Pavia, Pavia, Italy.
F Corresponding author. Emails: mmerani@fmed.uba.ar; silvia.garagna@unipv.it
Reproduction, Fertility and Development 25(3) 547-557 https://doi.org/10.1071/RD12127
Submitted: 7 December 2011 Accepted: 20 April 2012 Published: 6 June 2012
Abstract
Very little is known about the distinct reproductive biology of armadillos. Very few studies have investigated armadillo spermatogenesis, with data available only for Euphractus sexcinctus and Dasypus novemcinctus. In the present study, we analysed male germ cell differentiation in the large hairy armadillo Chaetophractus villosus throughout the year, describing a cycle of the seminiferous epithelium made of eight different stages. Evaluation of the testis/body mass ratio, analysis of the architecture of the seminiferous epithelium and the frequency of defective seminiferous tubules allowed identification of a temporal interruption of spermatogenesis during the period between mid-May to July (mid–end autumn) in correlation with very low testosterone levels. Overall, these results suggest that spermatogenesis is seasonal in C. villosus.
Additional keywords: germ cells, reproduction, seminiferous epithelium, Sertoli cells.
References
Abba, A. M., and Superina, M. (2010). The 2009/2010 armadillo Red List assessment. Edentata 11, 135–184.Affanni, J. M., Cervino, C. O., and Marcos, H. J. (2001). Absence of penile erections during paradoxical sleep. Peculiar penile events during wakefulness and slow wave sleep in the armadillo. J. Sleep Res. 10, 219–228.
| Absence of penile erections during paradoxical sleep. Peculiar penile events during wakefulness and slow wave sleep in the armadillo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnkt1Wisw%3D%3D&md5=cd05c5258a5b31b021d3ff11654c6590CAS | 11696075PubMed |
Bansode, F. W., Chowdhury, S. R., and Dhar, J. D. (2003). Seasonal changes in the seminiferous epithelium of rhesus and bonnet monkeys. J. Med. Primatol. 32, 170–177.
| Seasonal changes in the seminiferous epithelium of rhesus and bonnet monkeys.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3ps1Oktg%3D%3D&md5=0823745b8a09f67f21ff5a1e518ca870CAS | 12823627PubMed |
Benítez, I., Aldana Marcos, H. J., and Affanni, J. M. (1994). The encephalon of Chaetophractus villosus. A general view of its most salient features. Comun. Biol. 12, 57–73.
Berg, K. A., Wiger, R., Dahl, E., Torp, T., Farstad, W., Krogenaes, A., McNeilly, A. S., Paulenz, H., and Ropstad, E. (2005). Seasonal changes in spermatogenic activity and in plasma levels of FSH, LH and testosterone, and the effect of immunization against inhibin in the male silver fox (Vulpes vulpes). Anat. Histol. Embryol. 34, 220–224.
Cetica, P. D., Sassaroli, J., Merani, M. S., and Solari, A. J. (1993). Comparative spermatology in Dasypodidae (Priodontes maximus, Chaetophractus villosus and Dasypus hybridus). Biocell 18, 89–103.
Cetica, P. D., Rahn, I. M., Merani, M. S., and Solari, A. J. (1997). Comparative spermatology in Dasypodidae II (Chaetophractus vellerosus, Zaedyus pichiy, Euphractus sexcinctus, Tolypeutes matacus, Dasypus septemcinctus and Dasypus novemcinctus). Biocell 21, 195–204.
Cetica, P. D., Solari, A. J., Merani, M. S., De Rosas, J. C., and Burgos, M. H. (1998). Evolutionary sperm morphology and morphometry in armadillos. J. Submicrosc. Cytol. Pathol. 30, 309–314.
| 1:STN:280:DyaK1czht1Wjsw%3D%3D&md5=e57efd9713771c8f0e472ae0583aebb8CAS | 9648295PubMed |
Cetica, P. D., Aldana Marcos, H. J., and Merani, M. S. (2005). Morphology of female genital tracts in Dasypodidae (Xenarthra, Mammalia): a comparative survey. Zoomorphology 124, 57–65.
| Morphology of female genital tracts in Dasypodidae (Xenarthra, Mammalia): a comparative survey.Crossref | GoogleScholarGoogle Scholar |
Clarke, J. R. (1981). Physiological problems of seasonal breeding in eutherian mammals. In ‘Oxford Reviews in Reproductive Biology’. (Ed. C. A. Finn.) pp. 244–312. (Clarendon Press: Oxford.)
Clermont, Y. C. (1972). Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198–236.
| 1:STN:280:DyaE38%2FntVSntw%3D%3D&md5=510979757cd70160e28a3f546d986ac3CAS |
Clermont, Y. C., Leblond, P., and Messier, B. (1959). Durée du cycle de l’épithelium séminal du rat. Arch. Anat. Microsc. Morphol. Exp. 48, 37–56.
| 1:CAS:528:DyaF3cXltFWqtg%3D%3D&md5=fbf69e948d3c614cebf3dd2cb892225bCAS |
Dadhich, R. K., Real, F. M., Zurita, F., Barrionuevo, F. J., Burgos, M., and Jiménez, R. (2010). Role of apoptosis and cell proliferation in the testicular dynamics of seasonal breeding mammals: a study in the Iberian mole, Talpa occidentalis. Biol. Reprod. 83, 83–91.
| Role of apoptosis and cell proliferation in the testicular dynamics of seasonal breeding mammals: a study in the Iberian mole, Talpa occidentalis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtLk%3D&md5=084c098316e3a37da6a04aa88f033102CAS | 20357272PubMed |
Domínguez, S., Piezzi, R. S., Scardapane, L., and Guzmán, J. A. (1987). A light and electron microscopic study of the pineal gland of vizcacha (Lagostomus maximus maximus). J. Pineal Res. 4, 211–219.
| A light and electron microscopic study of the pineal gland of vizcacha (Lagostomus maximus maximus).Crossref | GoogleScholarGoogle Scholar | 3598856PubMed |
Dym, M., He, Z., Jiang, J., Pant, D., and Kokkinaki, M. (2009). Spermatogonial stem cells: unlimited potential. Reprod. Fertil. Dev. 21, 15–21.
| Spermatogonial stem cells: unlimited potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislGgt7Y%3D&md5=923e42a378ff9bcecc5c7297e53941e2CAS | 19152741PubMed |
Fuentes, L. B., Caravaca, N., Pelzer, L. E., Scardapane, L. A., Piezzi, R. S., and Guzman, J. A. (1991). Seasonal variations in the testis and epididymis of vizcacha (Lagostomus maximus maximus) Biol. Reprod. 45, 493–497.
| Seasonal variations in the testis and epididymis of vizcacha (Lagostomus maximus maximus)Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387ksVOqtA%3D%3D&md5=2a43a7587e72059eaa16a9a6960da3f8CAS | 1782299PubMed |
Galbreath, G. J. (1985). The evolution of monozygotic polyembryony in Dasypus. In ‘The Evolution and Ecology of Armadillos, Sloths and Vermilinguas’. (Ed. G. G. Montgomery.) pp. 243–246. (Smithsonian Institution Press: Washington.)
Garagna, S., Zuccotti, M., Searle, J., and Redi, C. A. (1989). Histological description of the seminiferous epithelium cycle in the common shrew (Sorex araneus L.). Boll. Zool. 56, 299–303.
| Histological description of the seminiferous epithelium cycle in the common shrew (Sorex araneus L.).Crossref | GoogleScholarGoogle Scholar |
Godinho, H. P., Cardoso, F. M., Coser, A. M. L., Machado, A. B. M., and Nogueira, J. C. (1977). Biologia reproductiva de machos Dasypus novemcinctus. Cienc. Cult. 29, 793.
Grassé, P. P. (1955). Ordre des Édentés. Formes actualles. Sousordre des Xénarthres. In ‘Traité de Zoologie, Mammiféres: Les Ordres: Anatomie, Éthologie, Systématique’. (Ed. P. Grassé.) pp. 1182–1266. (Masson & Cie: Paris.)
Haider, S. G., Passia, D., Servos, G., and Hettwer, H. (1986). Electron microscopic evidence for deep invaginations of the lamina propria towards the seminiferous tubule lumen in a patient with varicocele. Int. J. Androl. 9, 27–37.
| Electron microscopic evidence for deep invaginations of the lamina propria towards the seminiferous tubule lumen in a patient with varicocele.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28zgtlSrsQ%3D%3D&md5=14650de08172a7f015212939e6e74446CAS | 3744585PubMed |
Johnson, L. (1991). Seasonal differences in equine spermatocytogenesis. Biol. Reprod. 44, 284–291.
| Seasonal differences in equine spermatocytogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7otlSrtQ%3D%3D&md5=7880609703140a7b9bec067926f5e78fCAS | 2009330PubMed |
Kaneko, K., Akiya, Y., Sato, H., Tanaka, A., Aoki, H., Miyoshi, M., Abukawa, T., Mochizuki, M., and Kawakami, S. (2009). Seasonal influence on testicular function of male raccoons, Procyon lotor. Anim. Reprod. Sci. 112, 283–292.
Kuwahara, S., Mizukami, T., Omura, M., Hagihara, M., Iinuma, Y., Shimizu, Y., Tamada, H., Tsukamoto, Y., Nishida, T., and Sasaki, F. (2000). Seasonal changes in the hypothalamo–pituitary–testes axis of the Japanese wood mouse (Apodemus speciosus). Anat. Rec 260, 366–372.
| Seasonal changes in the hypothalamo–pituitary–testes axis of the Japanese wood mouse (Apodemus speciosus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FntFCmuw%3D%3D&md5=9a7bc6a2f5839371af991b9ffd35e9f4CAS | 11074401PubMed |
Leblond, C. P., and Clermont, Y. (1952). Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann. N. Y. Acad. Sci. 55, 548–573.
| Definition of the stages of the cycle of the seminiferous epithelium in the rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2c%2FlvFSgtg%3D%3D&md5=af70bc7678c8e715e9405e1e3198f623CAS | 13139144PubMed |
Lincoln, G. (1979). Photoperiod control of seasonal breeding in the cat: participation of the cranial sympathetic nervous system. J. Endocrinol. 82, 135–147.
| Photoperiod control of seasonal breeding in the cat: participation of the cranial sympathetic nervous system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXmtVygs7Y%3D&md5=0584cc37ab045ece00042827ec8e8a16CAS | 479729PubMed |
Loughry, W. J., Prodöhl, C. M., Mc Donought, J. C., and Avise, J. C. (1998). Polyembryony in armadillos: an unusual feature of the female nine-banded armadillo’s reproductive tract may explain why her litters consist of four genetically identical offspring. Am. Sci. 86, 274–279.
| Polyembryony in armadillos: an unusual feature of the female nine-banded armadillo’s reproductive tract may explain why her litters consist of four genetically identical offspring.Crossref | GoogleScholarGoogle Scholar |
Luaces, J. P., Ciuccio, M., Rossi, L. F., Faletti, A. G., Cetica, P. D., Casanave, E. B., and Merani, M. S. (2011a). Seasonal changes in ovarian steroid hormone concentrations in the large hairy armadillo (Chaetophractus villosus) and the crying armadillo (Chaetophractus vellerosus). Theriogenology 75, 796–802.
| Seasonal changes in ovarian steroid hormone concentrations in the large hairy armadillo (Chaetophractus villosus) and the crying armadillo (Chaetophractus vellerosus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1CmsLo%3D&md5=7ae3bfe19e7f4f7f40cf34a29a5a6d01CAS | 21247625PubMed |
Luaces, J. P., Rossi, L. F., Aldana Marcos, H. J., and Merani, M. S. (2011b). The rete mirabile of the tail, an effective site for sampling sterile blood from armadillos (Dasypodidae, Xenarthra). Int. J. Zool. 78, 63–69.
McCusker, G. J. (1985). Testicular cycles in the common long-nosed armadillo Dasypus novemcinctus, in north central Texas. In ‘The Evolution and Ecology of Armadillos, Sloths and Vermilinguas’ (Ed. G. G. Montgomery.) pp. 255–260. (Smithsonian Institution Press: Washington.)
Menendez-Pelaez, A., and Buzzell, R. (1992). Harderian gland indoles. In ‘Harderian glands’. (Eds S. M. Webb, R. A. Hoffman, M. L. Puig-Domingo and R. J. Reiter.) pp. 219–234. (Springer: Berlin.)
Nowak, R. M. (1999). Order Xenarthra. In ‘Walker’s Mammals of the World’. (Ed. R. M. Nowak.) pp. 149–168. (Hopkins Fulfillment Service: Baltimore.)
Oakberg, E. F. (1956). A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am. J. Anat. 99, 391–413.
| A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2s%2FkvV2ltw%3D%3D&md5=a2c31ea833dfe34b75856a6089936f57CAS | 13402725PubMed |
Peppler, R. D. (2008). Reproductive biology of the nine-banded armadillo. In ‘Biology of Xenarthra’. (Eds S. F. Vizcaíno and W. J. Loughry.) pp. 151–159. (University Press of Florida: Gainesville.)
Redi, C. A., Garagna, S., Heth, G., and Nevo, E. (1986). Descriptive kinetics of spermatogenesis in four chromosomal species of the Spalax ehrenbergi superspecies in Israel. J. Exp. Zool. 238, 81–88.
| Descriptive kinetics of spermatogenesis in four chromosomal species of the Spalax ehrenbergi superspecies in Israel.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL283is1Sntg%3D%3D&md5=597a7e1e9eaf2f5ad45aa1a56a8b1e12CAS | 3711819PubMed |
Reiter, R. J. (1986). The pineal gland pubertal development in mammals: a state of the art assessment. In ‘The Pineal Gland during Development’. (Eds I. D. Gupta and R. J. Reiter.) pp. 100–116. (Croom Helm: London.)
Rossi, L. F., Luaces, J. P., Aldana Marcos, H. J., Cetica, P. D., Gachen, G., Pérez Jimeno, G., and Merani, M. S. (2011). Female reproductive tract of the lesser anteater (Tamandua tetradactyla, Myrmecophagidae, Xenarthra). Anatomy and histology. J. Morphol. 272, 1307–1313.
| Female reproductive tract of the lesser anteater (Tamandua tetradactyla, Myrmecophagidae, Xenarthra). Anatomy and histology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbgvVCrsA%3D%3D&md5=5840c82de447b03b6c00d66479f8f133CAS | 21732404PubMed |
Sato, T., Tachiwana, T., Takata, K., Tay, T. W., Ishii, M., Nakamura, R., Kimura, S., Kanai, Y., Kurohmaru, M., and Hayashi, Y. (2005). Testicular dynamics in Syrian hamsters exposed to both short photoperiod and low ambient temperature. Anat. Histol. Embryol. 34, 220–224.
| Testicular dynamics in Syrian hamsters exposed to both short photoperiod and low ambient temperature.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MzksVGrsQ%3D%3D&md5=824ec27a33dfa93adca1208adfea970fCAS | 15996122PubMed |
Schön, J., Göritz, F., Streich, J., and Blottner, S. (2004). Histological organization of roe deer testis throughout the seasonal cycle: variable and constant components of tubular and interstitial compartment. Anat. Embryol. 208, 151–159.
| Histological organization of roe deer testis throughout the seasonal cycle: variable and constant components of tubular and interstitial compartment.Crossref | GoogleScholarGoogle Scholar | 15118912PubMed |
Sheng, X., Zhang, H., Zhang, W., Song, M., Zhang, M., Li, B., Weng, Q., Watanabe, G., and Taya, K. (2008). Seasonal changes in spermatogenesis and immunolocalization of inhibin/activin subunits in the wild male ground squirrel (Citellus dauricus Brandt). J. Reprod. Dev. 54, 460–464.
| Seasonal changes in spermatogenesis and immunolocalization of inhibin/activin subunits in the wild male ground squirrel (Citellus dauricus Brandt).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhslOltbY%3D&md5=0dc4ba1eb6860e813494eb0a5f9fdae6CAS | 18818485PubMed |
Storrs, E. E. (1989). Reproduction delay in the common long-nosed armadillo, Dasypus novemcinctus. In ‘Advances in Neotropical Mammalogy’. (Eds K. H. Redford and J. F. Eisenberg.) pp. 535–548. (The Sandhill Crane Press: Gainesville.)
Suescun, M. O., Campo, S., Rivarola, M. A., González-Echeverria, F., Scorticati, C., Ghirlanda, J., Tezón, J., Blaquier, J. A., and Calandra, R. S. (1981). Testosterone, dihydrotestosterone, and zinc concentrations in human testis and epididymis. Arch. Androl. 7, 297–303.
| Testosterone, dihydrotestosterone, and zinc concentrations in human testis and epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XivV2nsw%3D%3D&md5=4e376e240b4f3fdce8b80e8e52de48efCAS | 7316603PubMed |
Suescun, M. O., Calandra, R. S., and Lustig, L. (1994). Alterations of testicular function after induced autoimmune orchitis in rats. J. Androl. 15, 442–448.
| 1:STN:280:DyaK2M7msVehtw%3D%3D&md5=1563b2bc2e4cf3d8258af6d0bd894848CAS | 7860424PubMed |
Superina, M., and Jahn, G. A. (2009). Seasonal reproduction in male pichis Zaedyus pichiy (Xenarthra: Dasypodidae) estimated by fecal androgen metabolites and testicular histology. Anim. Reprod. Sci. 112, 283–292.
| Seasonal reproduction in male pichis Zaedyus pichiy (Xenarthra: Dasypodidae) estimated by fecal androgen metabolites and testicular histology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktFCqs78%3D&md5=39ba263f789ed643d89292e4a57b5f02CAS | 18555622PubMed |
Superina, M., Carreño, N., and Jahn, G. A. (2009). Characterization of seasonal reproduction patterns in female pichis Zaedyus pichiy (Xenarthra: Dasypodidae) estimated by fecal sex steroid metabolites and ovarian histology. Anim. Reprod. Sci. 116, 358–369.
| Characterization of seasonal reproduction patterns in female pichis Zaedyus pichiy (Xenarthra: Dasypodidae) estimated by fecal sex steroid metabolites and ovarian histology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlWns77F&md5=2fc1aab54a6fe1bdf3ade88f59d8df21CAS | 19304417PubMed |
Tähkä, K. M., Teräväinen, T., Pankakoski, E., and Jalkanen, M. (1989). The testes of moles (Talpa europaea) retain a considerable microsomal capacity for androgen synthesis during seasonal regression. Gen. Comp. Endocrinol. 76, 301–309.
| The testes of moles (Talpa europaea) retain a considerable microsomal capacity for androgen synthesis during seasonal regression.Crossref | GoogleScholarGoogle Scholar | 2531692PubMed |
Torres, C. N., Godinho, H. P., and Setchell, B. P. (1981). Frequency and duration of the stages of the cycle of the seminiferous epithelium of the nine-banded armadillo (Dasypus novemcinctus). J. Reprod. Fertil. 61, 335–340.
| Frequency and duration of the stages of the cycle of the seminiferous epithelium of the nine-banded armadillo (Dasypus novemcinctus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7ksFShtg%3D%3D&md5=14e09c2396eb9abd37befb0602b50412CAS | 7205779PubMed |
Torres, C. N., Godinho, H. P., and Machado, A. B. M. (1983). Seasonal variation in spermatogenesis in the nine-banded armadillo from south-eastern Brazil. Anim. Reprod. Sci. 6, 135–141.
| Seasonal variation in spermatogenesis in the nine-banded armadillo from south-eastern Brazil.Crossref | GoogleScholarGoogle Scholar |
Wetzel, R. M. (1985). Taxonomy and distribution of armadillos, Dasypodidae. In ‘The Evolution and Ecology of Armadillos, Sloths and Vermilinguas’. (Eds G. G. Montgomery.) pp. 23–46. (Smithsonian Institution Press: Washington.)
