Received date: 2024-07-18
Accepted date: 2024-10-15
Online published: 2025-06-03
To adapt to cyclical changes in their environment, mammals have developed different reproductive strategies over long periods of evolution. Seasonal changes in spermatogenesis are one of the typical adaptive features of seasonally breeding animals. During the reproductive period, spermatogenic cells at all levels of the testicular spermatogenic epithelium differentiate in an orderly manner to produce a steady stream of spermatozoa, whereas during the nonreproductive period, spermatogenic cell development is blocked and the testis degenerates. Seasonal spermatogenesis is cyclic in response to dynamic changes in hormone levels, a process that is tightly regulated by the photoperiod and the Hypothalamic-Pituitary-Gonadal (HPG) axis. As a major environmental signal regulating seasonal reproduction, photoperiod affects gonadotropin-releasing hormone (GnRH) neuronal activity through melatonin-mediated neurotransmission, which in turn acts on the gonads to regulate testosterone secretion and spermatogonial differentiation. In addition, thyroid hormones play a key role in the animal’s response to light signaling and maintenance of the HPG axis. Within the gonads, spermatogenic cell development in non-reproducing animals exhibits different patterns of blockage, including reduced proliferative activity of spermatogonia, autophagy and spermatocyte apoptosis, and detachment, with testosterone-regulated changes in retinoic acid concentration playing a central role in the blockage of spermatogonial differentiation. This article summarizes the mechanisms by which key environmental factors, the reproductive axis, and the testicular microenvironment synergistically regulate seasonal spermatogenesis in mammals, outlining new findings on the regulation of seasonal reproduction in animals. This paper focuses on a more systematic review of the roles of testosterone- and retinoic acid-regulated testicular microenvironments in seasonal spermatogenesis, with a view to providing reference information for the study of the molecular regulatory mechanisms of both on mammalian seasonal spermatogenesis, as well as an in-depth understanding of the physiology of reproduction and physiological ecology of veterinary species, and the development of techniques for the regulation of animal populations.
Lianhong PAN , Gongxue JIA , Qien YANG , Xumin WANG . Regulation of seasonal spermatogenesis in mammals[J]. ACTA THERIOLOGICA SINICA, 2025 , 45(3) : 271 -282 . DOI: 10.16829/j.slxb.150983
| Allrich R D, Christenson R K, Ford J J, Zimmerman D R. 1983. Pubertal development of the boar: age?related changes in testicular morphology and in vitro production of testosterone and estradiol?17 beta [J]. Biology of Reproduction, 28 (4): 902-909. | |
| An K, Yao B, Kang Y, Bao M, Tan Y, Pu Q, Su J H. 2022. Seasonal expression of gonadotropin genes in the pituitary and testes of male plateau zokor (Eospalax baileyi) [J]. Animals, 12 (6). DOI: 10.3390/ani12060725 . | |
| An K, Yao B, Tan Y, Kang Y, Wang Z, Su J. 2024. Spermatocytes are the terminals of germ cell differentiation in plateau zokor (Eospalax baileyi) during the non?breeding season [J]. Integrative Zoology.DOI: 10.1111/1749-4877.12849 . | |
| Asher G W. 2011. Reproductive cycles of deer [J]. Animal Reproduction Science, 124 (3): 170-175. | |
| Ax R L, Gilbert G R, Shook G E. 1987. Sperm in poor quality semen from bulls during heat stress have a lower affinity for binding hydrogen?3 heparin [J]. Journal of Dairy Science, 70 (1): 195-200. | |
| Baandrup L, Lindschou J, Winkel P, Gluud C, Glenthoj B Y. 2016. Prolonged?release melatonin versus placebo for benzodiazepine discontinuation in patients with schizophrenia or bipolar disorder: A randomised, placebo?controlled, blinded trial [J]. The World Journal of Biological Psychiatry, 17 (7): 514-524. | |
| Barrett P, Ebling F J P, Schuhler S, Wilson D, Ross AW, Warner A, Jethwa P, Boelen A, Visser T J, Ozanne D M, Archer Z A, Mercer J G, Morgan P J. 2007. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction [J]. Endocrinology, 148 (8): 3608-3617. | |
| Beltrán?Frutos E, Seco?Rovira V, Martínez?Hernández J, Ferrer C, Serrano?Sánchez M I, Pastor L M. 2022. Cellular modifications in spermatogenesis during seasonal testicular regression: an update review in mammals [J]. Animals, 12 (13).DOI: 10.3390/ani12131605 . | |
| Bernal J. 2002. Action of thyroid hormone in brain [J]. Journal of Endocrinological Investigation, 25 (3): 268-288. | |
| Bhushan S, Theas M S, Guazzone V A, Jacobo P, Wang M, Fijak M, Meinhardt A, Lustig L. 2020. Immune cell subtypes and their function in the testis [J]. Frontiers in Immunology, 11.DOI: 10.3389/fimmu.2020.583304 . | |
| Blottner S, Sch?n J, Jewgenow K. 2006. Seasonally activated spermatogenesis is correlated with increased testicular production of testosterone and epidermal growth factor in mink (Mustela vison) [J]. Theriogenology, 66 (6): 1593-1598. | |
| Blottner S, Sch?n J, Roelants H. 2007. Apoptosis is not the cause of seasonal testicular involution in roe deer. Cell and Tissue Research, 327 (3): 615-624. | |
| Boufermes R, Belhocine M, Amirat Z, Khammar F. 2021. Assessment of testicular Lhcgr mRNA expression correlated with testis and seminal vesicle activities in the Libyan jird (Meriones libycus, Rodentia: Muridae) during breeding season compared with nonbreeding season [J]. Animals (Basel), 11 (2). DOI: 10.3390/ani11020320 . | |
| Bronson F H. 1990. Mammalian Reproductive Biology [M]. Elsevier BV. | |
| Cao W, Pu P, Wang J, Niu Z, Zhang T, He J, Tang X L, Chen Q. 2020. Suppressed LPS?mediated TLR4 signaling in the plateau zokor (Eospalax baileyi) compared to the bamboo rat (Rhizomys pruinosus) and rat (Rattus norvegicus). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 333 (4): 240-251. | |
| Cecon E, Liu L, Jockers R. 2019. Melatonin receptor structures shed new light on melatonin research [J]. Journal of Pineal Research, 67 (4). DOI: 10.1111/jpi.12606 . | |
| Choi D. 2018. Evolutionary viewpoint on GnRH (gonadotropin‐releasing hormone) in chordata?amino acid and nucleic acid sequences [J]. Development Reproduction, 22 (2): 119-132. | |
| Costoya J A, Hobbs R M, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig K E, Wolgemuth D J, Pandolfi P P. 2004. Essential role of Plzf in maintenance of spermatogonial stem cells [J]. Nature Genetics, 36: 653-659. | |
| Dadhich R K, Real F M, Zurita F, Barrionuevo F J, Burgos M, 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 [J]. Biology of Reproduction, 83 (1): 83-91. | |
| Dardente H, Lomet D, Robert V, Decourt C, Beltramo M, Pellicer?Rubio M T. 2016. Seasonal breeding in mammals: from basic science to applications and back [J]. Theriogenology, 86 (1): 324-332. | |
| De Rooij D G. 2009. The spermatogonial stem cell niche [J]. Microscopy Research and Technique, 72 (8): 580-585. | |
| Desantis S, Ventriglia G, Zizza S, Nicassio M, Valentini L, Di Summa A, Lacalandra G M. 2010. Lectin?binding sites on ejaculated stallion sperm during breeding and non?breeding periods [J]. Theriogenology, 73 (8): 1146-1153. | |
| Dubocovich M L, Markowska M. 2005. Functional MT1 and MT2 melatonin receptors in mammals [J]. Endocrine, 27 (2): 101-110. | |
| Duncan M J, Fang J M, Dubocovich M L. 1990. Effects of melatonin agonists and antagonists on reproduction and body weight in the Siberian hamster [J]. Journal of Pineal Research, 9 (4): 231-242. | |
| El Sabry M I, Almasri O. 2023. Stocking density, ambient temperature, and group size affect social behavior, productivity and reproductivity of goats: a review. Tropical Animal Health and Production, 55 (3).DOI: 10.1007/s11250-023-03598-0 . | |
| Feoktistova N Y, Meschersky I G. 2005.Seasonal changes in desert hamster Phodopus roborovskii breeding activity [J]. Acta Zoologica Sinica, 51 (1): 1-6. | |
| Ferrara N. 2004. Vascular endothelial growth factor: basic science and clinical progress [J]. Endocrine Reviews, 25 (4): 581-611. | |
| Gandara A C P, Drummond?Barbosa D. 2023. Chronic exposure to warm temperature causes low sperm abundance and quality in Drosophila melanogaster [J]. Scientific Reports, 13 (1).DOI: 10.1038/s41598-023-39360-7 . | |
| González C R, Isla M L M, Vitullo A D. 2018. The balance between apoptosis and autophagy regulates testis regression and recrudescence in the seasonal?breeding South American plains vizcacha, Lagostomus maximus Drosophila melanogaster [J]. PLoS ONE, 13 (1). DOI: 10.1371/journal.pone.0191126 . | |
| Griswold M D. 1998. The central role of Sertoli cells in spermatogenesis [J]. Seminars in Cell Development Biology, 9 (4): 411-416. | |
| Hai Y, Hou J, Liu Y, Liu Y, Yang H, Li Z, He Z P. 2014. The roles and regulation of Sertoli cells in fate determinations of spermatogonial stem cells and spermatogenesis [J]. Seminars in Cell and Developmental Biology, 29: 66-75. | |
| Hamer G, De Rooij D G. 2018. Mutations causing specific arrests in the development of mouse primordial germ cells and gonocytes [J]. Biology of Reproduction, 99 (1): 75-86. | |
| Hart L, O’riain M J, Jarvis J U M, Bennett N C. 2006. The pituitary potential for opportunistic breeding in the Cape dune mole?rat, Bathyergus suillus [J]. Physiology & Behavior, 88 (4): 615-619. | |
| Henningsen J B, Gauer F, Simonneaux V. 2016. RFRP Neurons - The doorway to understanding seasonal reproduction in mammals [J]. Front Endocrinol (Lausanne), 7.DOI: 10.3389/fendo.2016. 00036 . | |
| Hochereau?De Reviers M T, Perreau C, Lincoln G A. 1985. Photoperiodic variations of somatic and germ cell populations in the Soay ram testis [J]. Journal of Reproduction and Fertility, 74 (2): 329-334. | |
| Jockers R, Maurice P, Boutin J A, Delagrange P. 2008. Melatonin receptors, heterodimerization, signal transduction and binding sites: what’s new? [J]. British Journal of Pharmacology, 154 (6): 1182-1195. | |
| Khanehzad M, Abbaszadeh R, Holakuyee M, Modarressi M H, Nourashrafeddin S M. 2021. FSH regulates RA signaling to commit spermatogonia into differentiation pathway and meiosis [J]. Reproductive Biology and Endocrinology, 19 (1).DOI: 10.1186/s12958-020-00686-w . | |
| Lack D L. 2008. The breeding seasons of European birds [J]. Ibis, 92: 288-316. | |
| Lee V H, Lee L T, Chow B K. 2008. Gonadotropin?releasing hormone: regulation of the GnRH gene [J]. Febs Journal, 275 (22): 5458-5478. | |
| Li J H, Yin H B, Wang Q S. 2005. Seasonality of reproduction and sexual activity in female Tibetan macaques (Macaca thibetana) at Huangshan, China [J]. Acta Zoologica Sinica, 51: 365-375. | |
| Li Z W, Sun R Y, Du J Z.1998.Seasonal reproductive cycles in male plateau pika (Ochotona curzoniae) [J]. Acta Theriologica Sinica, 18 (1): 42-49. | |
| Luaces J P, Rossi L F, Merico V, Zuccotti M, Redi C A, Solari A J, Merani M S, Garagna S. 2013. Spermatogenesis is seasonal in the large hairy armadillo, Chaetophractus villosus (Dasypodidae, Xenarthra, Mammalia) [J]. Reproduction, Fertility and Development, 25 (3): 547-557. | |
| Luaces J P, Rossi L F, Sciurano R B, Rebuzzini P, Merico V, Zuccotti M, Merani M S, Garagna S. 2014. Loss of Sertoli?germ cell adhesion determines the rapid germ cell elimination during the seasonal regression of the seminiferous epithelium of the large hairy armadillo Chaetophractus villosus [J]. Biology of Reproduction, 90 (3): 48. | |
| Mayerhofer A, Sinha Hikim A P, Bartke A, Russell L D. 1989. Changes in the testicular microvasculature during photoperiod?related seasonal transition from reproductive quiescence to reproductive activity in the adult golden hamster [J]. Anatomical Record, 224 (4): 495-507. | |
| Meinhardt A, Dejucq?Rainsford N, Bhushan S. 2022. Testicular macrophages: development and function in health and disease [J]. Trends Immunol, 43 (1): 51-62. | |
| Meng X, Lindahl M, Hyv?nen M E, Parvinen M, De Rooij D G, Hess M W, Raatikainen?Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel J G, Westphal H, Saarma M, Sariola H. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF [J]. Science, 287 (5457): 1489-1493. | |
| Mislei B, Bucci D, Malama E, Bollwein H, Mari G. 2020. Seasonal changes in ROS concentrations and sperm quality in unfrozen and frozen?thawed stallion semen [J]. Theriogenology, 144: 89-97. | |
| Morales E, Pastor L M, Ferrer C, Zuasti A, Pallarés J, Horn R, Calvo A, Santamaria L, Canteras M. 2002. Proliferation and apoptosis in the seminiferous epithelium of photoinhibited Syrian hamsters (Mesocricetus auratus). International Journal of Andrology, 25(5): 281-287. | |
| Muteka S P, Chimimba C T, Bastos A D S, Bennett N C. 2020. Photoperiodic effects on the male gonads of the Namibian gerbil, Gerbilliscus cf. leucogaster from central Namibia [J]. Mammalian Biology, 100 (2): 165-171. | |
| Nishiwaki?Ohkawa T, Yoshimura T. 2016. Molecular basis for regulating seasonal reproduction in vertebrates [J]. Journal of Endocrinology, 229 (3): R117-R127. | |
| Oatley J M, Brinster R L. 2012. The germline stem cell niche unit in mammalian testes [J]. Physiological Reviews, 92 (2): 577-595. | |
| Okubo K, Nagahama Y. 2008. Structural and functional evolution of gonadotropin?releasing hormone in vertebrates [J]. Acta Physiologica (Oxf), 193 (1): 3-15. | |
| Pastor L M, Zuasti A, Ferrer C, Bernal?Ma?as C M, Morales E, Beltrán?Frutos E, Seco?Rovira V. 2011. Proliferation and apoptosis in aged and photoregressed mammalian seminiferous epithelium, with particular attention to rodents and humans [J]. Reproduction in Domestic Animals, 46 (1): 155-164. | |
| Paul C, Teng S, Saunders P T. 2009. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death [J]. Biology of Reproduction, 80 (5): 913-919. | |
| Pérez?Crespo M, Pintado B, Gutiérrez?Adán A. 2008. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice [J]. Molecular Reprodction and Development, 75 (1): 40-47. | |
| Phillips B T, Gassei K, Orwig K E. 2010. Spermatogonial stem cell regulation and spermatogenesis [J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 365 (1546): 1663-1678. | |
| Raucci F, Di Fiore M M. 2007. The c?kit receptor protein in the testis of green frog Rana esculenta: seasonal changes in relationship to testosterone titres and spermatogonial proliferation [J]. Reproduction, 133 (1): 51-60. | |
| Ravel C, Jaillard S. 2011. La cellule de sertoli [J]. Morphologie, 95 (311): 151-158. | |
| Roelants H, Schneider F, G?ritz F, Streich J, Blottner S. 2002. Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c?kit receptor, in relation to follicle?stimulating hormone, luteinizing hormone, and testosterone [J]. Biology of Reproduction, 66 (2): 305-312. | |
| Sailer B L, Sarkar L J, Bjordahl J A, Jost L K, Evenson D P. 1997. Effects of heat stress on mouse testicular cells and sperm chromatin structure [J]. Journal of Andrology, 18 (3): 294-301. | |
| Savoy?Moore R T, Swartz K H. 1987. Several GnRH stimulation frequencies differentially release FSH and LH from isolated, perfused rat anterior pituitary cells [J]. Advances in Experimental Medicine and Biology, 219: 641-645. | |
| Sch?n J, G?ritz F, Streich J, Blottner S. 2004. Histological organization of roe deer testis throughout the seasonal cycle: variable and constant components of tubular and interstitial compartment [J]. Anatomy and Embryology (Berl), 208 (2): 151-159. | |
| Seco?Rovira V, Beltrán?Frutos E, Ferrer C, Sáez F J, Madrid J F, Pastor L M. 2014. The death of sertoli cells and the capacity to phagocytize elongated spermatids during testicular regression due to short photoperiod in Syrian hamster (Mesocricetus auratus) [J]. Biology of Reproduction, 90 (5): 107. | |
| Setchell B P. 1978. The Mammalian Testis [M]. Cornell University Press, Ithaca. | |
| Sharma T P, Nett T M, Karsch F J, Phillips D J, Lee J S, Herkimer C, et al. 2012. Neuroendocrine control of FSH secretion: IV. Hypothalamic control of pituitary FSH?regulatory proteins and their relationship to changes in FSH synthesis and secretion [J]. Biology of Reproduction, 86 (6). DOI: 10.1095/biolreprod.111.098442 . | |
| Shinomiya A, Shimmura T, Nishiwaki?Ohkawa T, Yoshimura T. 2014. Regulation of seasonal reproduction by hypothalamic activation of thyroid hormone [J]. Front Endocrinol (Lausanne), 5.DOI: 10.3389/fendo.2014.00012 . | |
| Shiraishi K, Takihara H, Matsuyama H. 2010. Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress?mediated apoptosis [J]. World Journal of Urology, 28 (3): 359-364. | |
| Sieme H, Troedsson M H T, Weinrich S, Klug E. 2004. Influence of exogenous GnRH on sexual behavior and frozen/thawed semen viability in stallions during the non?breeding season [J]. Theriogenology, 61 (1): 159-171. | |
| Smith L B, Walker W H. 2014. The regulation of spermatogenesis by androgens [J]. Seminars in Cell & Developmental Biolog, 30: 2-13. | |
| Sofikitis N, Giotitsas N, Tsounapi P, Baltogiannis D, Giannakis D, Pardalidis N. 2008. Hormonal regulation of spermatogenesis and spermiogenesis [J]. Journal of Steroid Biochemistry and Molecular Biology, 109 (3-5): 323-330. | |
| Stevenson T J, Ball G F. 2011. Information theory and the neuropeptidergic regulation of seasonal reproduction in mammals and birds [J]. Proceedings of the Royal Society B: Biological Sciences, 278 (1717): 2477-2485. | |
| Subash S K, Kumar P G. 2021. Spermatogonial stem cells: a story of self?renewal and differentiation [J]. Frontiers in Bioscience (Landmark Ed), 26 (1): 163-205. | |
| Sumida T S, Cheru N T, Hafler D A. 2024. The regulation and differentiation of regulatory T cells and their dysfunction in autoimmune diseases [J]. Nature Reviews Immunology, 24 (7): 503-517. | |
| Tamarkin L, Baird C J, Almeida O F. 1985. Melatonin: a coordinating signal for mammalian reproduction? [J]. Science, 227 (4688): 714-720. | |
| Tiba T, Takahashi M, Igura M, Kita I. 1992. Enhanced proliferation of undifferentiated spermatogonia after treatment of short photoperiod exposure in the Syrian hamster, Mesocricetus auratus [J]. Anatomia Histologia Embryologia, 21 (1): 9-22. | |
| Viguie? C, Battaglia D F, Krasa H B, Thrun L A, Karsch F J. 1999. Thyroid hormones act primarily within the brain to promote the seasonal inhibition of luteinizing hormone secretion in the Ewe [J]. Endocrinology, 140 (3): 1111-1117. | |
| Von Gall C, Stehle J H, Weaver D R. 2002. Mammalian melatonin receptors: molecular biology and signal transduction [J]. Cell and Tissue Research, 309 (1): 151-162. | |
| Wang J H, Zhang L, Zhang P J, Sun B J. 2024a. Physiological processes through which heatwaves threaten fauna biodiversity [J]. The Innovation Life, 2 (2). DOI: https://doi.org/10.59717/j.xinn-life.2024.100069 | |
| Wang Y J, Duo H R, Li S, Zhang X Q, Tao H P, Fang Y G, Jia G X, Yang Q E. 2024b. Functional regulation of testosterone underlying state transition in seasonal spermatogenesis of plateau pika (Ochotona curzoniae) [J]. Journal of Mammalogy, 105 (5):1105-1116. | |
| Wang J J, Wang Y, Zhu M Y, Zhang F W, Sheng X, Zhang H L, Han Y Y, Yuan Z R, Weng Q. 2017. Seasonal expression of luteinizing hormone receptor and follicle stimulating hormone receptor in testes of the wild ground squirrels (Citellus dauricus Brandt) [J]. Acta Histochemica, 119 (7): 727-732. | |
| Wang R S, Yeh S, Tzeng C R, Chang C. 2009. Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell?specific androgen receptor knockout mice [J]. Endocrine Reviews, 30 (2): 119-132. | |
| Wang Y J, Jia G X, Yan R G, Guo S C, Tian F, Ma J B, Zhang R N, Li C, Zhang L Z, Du Y R, Yang Q E. 2019. Testosterone?retinoic acid signaling directs spermatogonial differentiation and seasonal spermatogenesis in the plateau pika (Ochotona curzoniae). Theriogenology, 123: 74-82. | |
| Yamamura T, Yasuo S, Hirunagi K, Ebihara S, Yoshimura T. 2006. T(3) implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail [J]. Cell and Tissue Research, 324 (1): 175-179. | |
| Yuan J, Zhao X, Hu Y, Sun H, Gong G, Huang X, Chen X B, Xia M Y, Sun C, Huang Q L, Sun Y, Kong W, Kong W J. 2018. Autophagy regulates the degeneration of the auditory cortex through the AMPK?mTOR?ULK1 signaling pathway [J]. International Journal of Molecular Medicine, 41 (4): 2086-2098. | |
| Zhang X N, Tao H, Li S, Wang Y J, Wu S X, Pan B, Yang Q E. 2022. Ldha?dependent metabolic programs in sertoli cells regulate spermiogenesis in mouse testis [J]. Biology, 11 (12).DOI: 10.3390/biology11121791 . | |
| Zhang X, Zhao Z, Vasilieva N, Khrushchova A, Wang D. 2015. Effects of short photoperiod on energy intake, thermogenesis, and reproduction in desert hamsters (Phodopus roborovskii) [J]. Integrative Zoology, 10 (2): 207-215. | |
| 于永梅. 2002. 季节性繁殖动物生殖的影响研究 [J]. 上海畜牧兽医通讯, (3): 16-17. | |
| 王玉军, 贾功雪, 王婷, 王秀蓉, 刘忠浩, 都玉蓉, 马建滨. 2020. 光周期—褪黑素信号调控高原鼠兔精原细胞分化和季节性精子发生 [J]. 兽类学报, 40 (1): 54-63. | |
| 田允波, 李琦华. 1990. 公羊繁殖机能的季节性变化研究 [J]. 内蒙古畜牧科学, 1990 (4): 11-15. | |
| 朱翔杰, 周冰峰, 郑秀娟, 王青, 徐新建, 巨骞, 于瀛龙, 夏晓翠. 2011. 季节环境变化对中华蜜蜂形态遗传标记的影响 [J]. 中国蜂业, 62 (Z1): 3-6. | |
| 伊卜拉伊木·胡达拜尔迪, 郭金亮, 孙贝贝, 李伟, 石长青. 2016. 外源性褪黑激素对非繁殖季节和田羊睾丸曲细精管组织结构的影响 [J]. 中国草食动物科学, 36 (1): 19-21. | |
| 刘辉, 崔定中. 2001. 绵羊睾丸内分泌细胞的季节变化 [J]. 新疆农业科学, 2001 (S1): 55-57. | |
| 安晓宇, 王玉军, 李永昌, 贾功雪, 杨其恩. 2020. 高原鼢鼠精子发生的形态学特征和关键调控因子探究 [J]. 兽类学报, 40 (5): 435-445. | |
| 严慧娟, 王巍, 易军, 牛李丽, 屈羽, 陈昂, 蒲阳, 邓家波, 钟燕, 余建秋. 2018. 豚鹿几种激素的季节性变化模式研究 [J]. 四川动物, 37 (1): 62-66. | |
| 李晓婷, 朱万龙, 刘鑫, 刘春燕, 王政昆. 2011. 中缅树鼩能量代谢的季节变化 [J]. 兽类学报, 31 (3): 291-298. | |
| 杨颖, 陈黎, 卢立志. 2017. 松果体调控动物季节性繁殖概述 [J]. 农业生物技术学报, 25 (7): 1086-1101. | |
| 张晓茜, 贾功雪, 王玉军, 宋玉坤, 阿布力孜·吾斯曼. 2022. 高原鼠兔褪黑素受体在下丘脑-垂体-性腺轴中的表达分析 [J]. 动物学杂志, 57 (3): 350-358. | |
| 郑生武. 1980. 中华鼢鼠的繁殖研究 [J]. 动物学研究, (4): 465-473. | |
| 姚宝辉. 2023.雄性高原鼢鼠 (Eospalax baileyi) 生殖抑制的分子调控机制研究 [D]. 兰州: 甘肃农业大学博士学位论文. | |
| 姚蔚, 王德华, 张学英. 2017. 哺乳动物季节性繁殖的内源年生物钟及光敏神经环路研究进展 [J]. 动物学杂志, 52 (4): 717-725. | |
| 夏东坡, 李进华, 朱勇, 陈燃, 孙丙华. 2008. 野生黄山短尾猴雄性睾酮的季节性变化 [J]. 兽类学报, 28 (3): 287-292. | |
| 彭少麟, 李勤奋, 任海. 2002. 全球气候变化对野生动物的影响 [J]. 生态学报, 22 (7): 1153-1159. | |
| 魏海军, 张志明. 2001. 狐繁殖的季节性及其调控机制 [J]. 特种经济动植物, (4): 3-4. |
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