Subfertile effects of quinestrol and levonorgestrel in male rats
Ming Liu A B D , Xinrong Wan A , Yimeng Yin C , Yu-xia Li B , Fei Sun C , Zhibin Zhang A A and Yan-ling Wang B E
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Integrated Management of Pest Insets and Rodents, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Beijing 100101, China.
B State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Beijing 100101, China.
C Life Science College, University of Science and Technology in China, Huangshan Road, Hefei 230027, China.
D Graduate School of Chinese Academy of Sciences, Yuquan Road, Beijing 100049, China.
E Corresponding authors. Emails: wangyl@ioz.ac.cn; zhangzb@ioz.ac.cn
Reproduction, Fertility and Development 24(2) 297-308 https://doi.org/10.1071/RD10221
Published online: 26 September 2011
Abstract
The contraceptive regimen consisting of levonorgestrel and quinestrol (EP-1) has been shown to be effective in several types of wild rodents. In the present study, we investigated the effect of EP-1 and its two components on fertility and spermatogenesis to elucidate the mechanisms underlying its contraceptive effect. Sprague-Dawley rats were treated with 0.33 mg kg–1 quinestrol (E group), 0.67 mg kg–1 levonorgestrel (P group) or their combination (EP group) for 7 days and then killed on Days 21 or 42 after treatment for tissue analysis. On Day 21, the weight of the cauda epididymis decreased significantly, while the weight of the adrenal gland increased significantly in the E and EP groups compared with the weights in the control group. In addition, there was a significant decrease in sperm number in the E and EP groups compared with the control group and there was less staining for the androgen receptor and Wilms’ tumour nuclear protein 1 in the E and EP groups. The primary defects in E- or EP-treated rats were abnormal spermiogenesis, lack of elongating spermatids, and pachytene spermatocyte arrest. Analysis of MutL homologue 1 revealed that EP treatment inhibited chromosome recombination during meiosis, but did not cause obvious genetic abnormalities. These data demonstrate that quinestrol, alone or in combination with levonorgestrel, induces subfertility in male rats mainly by interfering with germ cell differentiation. Thus, EP-1 or E alone may be effective contraceptive regimens for fertility control in rodents.
Additional keywords: fertility control, spermatogenesis, testis.
References
Amory, J. K., Page, S. T., and Bremner, W. J. (2006). Drug insight: recent advances in male hormonal contraception. Nat. Clin. Pract. Endocrinol. Metab. 2, 32–41.| Drug insight: recent advances in male hormonal contraception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Sitro%3D&md5=06c8729ab2fd4d3f87bec263ed85358aCAS | 16932251PubMed |
Anawalt, B. D., Bebb, R. A., Bremner, W. J., and Matsumoto, A. M. (1999). A lower dosage levonorgestrel and testosterone combination effectively suppresses spermatogenesis and circulating gonadotropin levels with fewer metabolic effects than higher dosage combinations. J. Androl. 20, 407–414.
| 1:CAS:528:DyaK1MXktFOiu74%3D&md5=732a5842658cc0ad396841a97fc9b493CAS | 10386821PubMed |
Anawalt, B. D., Amory, J. K., Herbst, K. L., Coviello, A. D., Page, S. T., Bremner, W. J., and Matsumoto, A. M. (2005). Intramuscular testosterone enanthate plus very low dosage oral levonorgestrel suppresses spermatogenesis without causing weight gain in normal young men: a randomized clinical trial. J. Androl. 26, 405–413.
| Intramuscular testosterone enanthate plus very low dosage oral levonorgestrel suppresses spermatogenesis without causing weight gain in normal young men: a randomized clinical trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVWjsrk%3D&md5=6b41734dc49fabf002ac998fec7cdb70CAS | 15867009PubMed |
Anderson, R. A., and Baird, D. T. (2002). Male contraception. Endocr. Rev. 23, 735–762.
| Male contraception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVSntLg%3D&md5=6c2c7ba93be2dbfc9cc9dc7cc822ca74CAS | 12466187PubMed |
Bagatell, C. J., Dahl, K. D., and Bremner, W. J. (1994). The direct pituitary effect of testosterone to inhibit gonadotropin secretion in men is partially mediated by aromatization to estradiol. J. Androl. 15, 15–21.
| 1:CAS:528:DyaK2cXivFSgtLY%3D&md5=0ab010efec6e4fa1e65f0d9829cdb13fCAS | 8188534PubMed |
Bebb, R. A., Anawalt, B. D., Christensen, R. B., Paulsen, C. A., Bremner, W. J., and Matsumoto, A. M. (1996). Combined administration of levonorgestrel and testosterone induces more rapid and effective suppression of spermatogenesis than testosterone alone: a promising male contraceptive approach. J. Clin. Endocrinol. Metab. 81, 757–762.
| Combined administration of levonorgestrel and testosterone induces more rapid and effective suppression of spermatogenesis than testosterone alone: a promising male contraceptive approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVyktLw%3D&md5=5fa07780a1e6387efade7a09898c2c8fCAS | 8636300PubMed |
Borg, C. L., Wolski, K. M., Gibbs, G. M., and O’Bryan, M. K. (2010). Phenotyping male infertility in the mouse: how to get the most out of a ‘non-performer’. Hum. Reprod. Update 16, 205–224.
| Phenotyping male infertility in the mouse: how to get the most out of a ‘non-performer’.Crossref | GoogleScholarGoogle Scholar | 19758979PubMed |
Brinkmann, A. O., Leemborg, F. G., Roodnat, E. M., De Jong, F. H., and Van der Molen, H. J. (1980). A specific action of estradiol on enzymes involved in testicular steroidogenesis. Biol. Reprod. 23, 801–809.
| A specific action of estradiol on enzymes involved in testicular steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlehtw%3D%3D&md5=a5156005b8e92b3df7b12a15e7fbddf2CAS | 7448281PubMed |
Couse, J. F., Lindzey, J., Grandien, K., Gustafsson, J., and Korach, K. S. (1997). Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology 138, 4613–4621.
| Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmslGrtr0%3D&md5=ad94737a86ab7f9341082c1d2ab9e827CAS | 9348186PubMed |
Danzo, B. J. (1998). The effects of environmental hormones on reproduction. Cell. Mol. Life Sci. 54, 1249–1264.
| The effects of environmental hormones on reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXns1CnsrY%3D&md5=0ecd4ad115121acf2667b315999434a4CAS | 9849617PubMed |
Delanoe, D., Fougeyrollas, B., Meyer, L., and Thonneau, P. (1984). Androgenisation of female partners of men on medroxyprogesterone acetate/percutaneous testosterone contraception. Lancet 323, 276.
| Androgenisation of female partners of men on medroxyprogesterone acetate/percutaneous testosterone contraception.Crossref | GoogleScholarGoogle Scholar |
D’Souza, R., Gill-Sharma, M. K., Pathak, S., Kedia, N., Kumar, R., and Balasinor, N. (2005). Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats. Mol. Cell. Endocrinol. 241, 41–48.
| Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFelsbg%3D&md5=1efe5e44e026ec07b9554c8e457a58d9CAS | 15936871PubMed |
El-Hefnawy, T., and Huhtaniemi, I. (1998). Progesterone can participate in down-regulation of the luteinizing hormone receptor gene expression and function in cultured murine Leydig cells. Mol. Cell. Endocrinol. 137, 127–138.
| Progesterone can participate in down-regulation of the luteinizing hormone receptor gene expression and function in cultured murine Leydig cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhs1Ggur4%3D&md5=5e29d3b2c316167bd1bf3bdab857c24bCAS | 9605514PubMed |
Ewing, L. L., Desjardins, C., Irby, D. C., and Robaire, B. (1977). Synergistic interaction of testosterone and oestradiol inhibits spermatogenesis in rats. Nature 269, 409–411.
| Synergistic interaction of testosterone and oestradiol inhibits spermatogenesis in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXjt1elug%3D%3D&md5=986d1d37ec2f79302385e7ee1ca92299CAS | 909588PubMed |
Fisher, J. S., Millar, M. R., Majdic, G., Saunders, P. T., Fraser, H. M., and Sharpe, R. M. (1997). Immunolocalisation of oestrogen receptor-alpha within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. J. Endocrinol. 153, 485–495.
| Immunolocalisation of oestrogen receptor-alpha within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1arsLo%3D&md5=017c7037946a3df9319d5543089dc441CAS | 9204003PubMed |
Franca, L. R., Ogawa, T., Avarbock, M. R., Brinster, R. L., and Russell, L. D. (1998). Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol. Reprod. 59, 1371–1377.
| Germ cell genotype controls cell cycle during spermatogenesis in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvVKrtbY%3D&md5=3b8666cbb5385084e027f8d94063158bCAS | 9828180PubMed |
Gill-Sharma, M. K., Dsouza, S., Padwal, V., Balasinor, N., Aleem, M., Parte, P., and Juneja, H. S. (2001). Antifertility effects of estradiol in adult male rats. J. Endocrinol. Invest. 24, 598–607.
| 1:CAS:528:DC%2BD3MXotlGhsLk%3D&md5=c521a61151b47caea4774253ae456243CAS | 11686542PubMed |
Hayes, F. J., Seminara, S. B., Decruz, S., Boepple, P. A., and Crowley, W. F., (2000). Aromatase inhibition in the human male reveals a hypothalamic site of estrogen feedback. J. Clin. Endocrinol. Metab. 85, 3027–3035.
| Aromatase inhibition in the human male reveals a hypothalamic site of estrogen feedback.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVKrur4%3D&md5=ec070e31e25981137108e948f08fc148CAS | 10999781PubMed |
Hess, R. A., Bunick, D., Lee, K. H., Bahr, J., Taylor, J. A., Korach, K. S., and Lubahn, D. B. (1997). A role for oestrogens in the male reproductive system. Nature 390, 509–512.
| A role for oestrogens in the male reproductive system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvF2gu74%3D&md5=94154a3483937a2648b6783f677fd677CAS | 9393999PubMed |
Huo X., Wang D., Liang H., Shi D., Zhang H., and Liang J. (2006) . A prelimary study on the anti-fertility effect of two sterilants to clawed jirds (Meriones unguiculatus). Acta Agrestia Sin. 14, 184–187. [In Chinese]
Jackson, R. J., Maguire, D. J., Hinds, L. A., and Ramshaw, I. A. (1998). Infertility in mice induced by a recombinant ectromelia virus expressing mouse zona pellucida glycoprotein 3. Biol. Reprod. 58, 152–159.
| Infertility in mice induced by a recombinant ectromelia virus expressing mouse zona pellucida glycoprotein 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvVSjtQ%3D%3D&md5=b1ea92e2f580a34079a53862eb889bb1CAS | 9472936PubMed |
Janulis, L., Bahr, J. M., Hess, R. A., and Bunick, D. (1996). P450 aromatase messenger ribonucleic acid expression in male rat germ cells: detection by reverse transcription–polymerase chain reaction amplification. J. Androl. 17, 651–658.
| 1:CAS:528:DyaK2sXms1Cqtw%3D%3D&md5=70bba9095dc4caf65850039d6919ba36CAS | 9016395PubMed |
Kamischke, A., Diebacker, J., and Nieschlag, E. (2000). Potential of norethisterone enanthate for male contraception: pharmacokinetics and suppression of pituitary and gonadal function. Clin. Endocrinol. 53, 351–358.
| Potential of norethisterone enanthate for male contraception: pharmacokinetics and suppression of pituitary and gonadal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt1Kls7k%3D&md5=31f5714fc2bea177da5cca259546c6b5CAS |
Laflamme, N., Nappi, R. E., Drolet, G., Labrie, C., and Rivest, S. (1998). Expression and neuropeptidergic characterization of estrogen receptors (ERα and ERβ) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J. Neurobiol. 36, 357–378.
| Expression and neuropeptidergic characterization of estrogen receptors (ERα and ERβ) throughout the rat brain: anatomical evidence of distinct roles of each subtype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVyjs7Y%3D&md5=d733aa39049355dc0493cf689881054aCAS | 9733072PubMed |
Li, H., Papadopoulos, V., Vidic, B., Dym, M., and Culty, M. (1997). Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol: identification of signaling mechanisms involved. Endocrinology 138, 1289–1298.
| Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol: identification of signaling mechanisms involved.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1yltrk%3D&md5=0ef9a68ee6ba12ae84a10ad6ca65e57aCAS | 9048638PubMed |
Liang, H., Huo, X., Wang, D., Shi, D., Zhang, H., and Liang, J. (2006). A preliminary study on the control effect of the sterilant on the population of clawed gerbil. Plant Protect. 32, 45–48.
Liu, M., Qu, J., Yang, M., Wang, Z., Wang, Y.-L., Zhang, Y., and Zhang, Z. (2011). Effects of quinestrol and levonorgestrel on populations of plateau pikas, Ochotona curzoniae, in the Qinghai-Tibetan Plateau. Pest Manag. Sci. 67, in press..
Morse, H. C., Leach, D. R., Rowley, M. J., and Heller, C. G. (1973). Effect of cyproterone acetate on sperm concentration, seminal fluid volume, testicular cytology and levels of plasma and urinary ICSH, FSH and testosterone in normal men. J. Reprod. Fertil. 32, 365–378.
| Effect of cyproterone acetate on sperm concentration, seminal fluid volume, testicular cytology and levels of plasma and urinary ICSH, FSH and testosterone in normal men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXktVSls7c%3D&md5=7cc62972ac65a1459341ffacd32011b6CAS | 4692335PubMed |
O’Donnell, L., Robertson, K. M., Jones, M. E., and Simpson, E. R. (2001). Estrogen and spermatogenesis. Endocr. Rev. 22, 289–318.
| Estrogen and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVOgurw%3D&md5=5040d27c2e059cf93d2495f8caa544d5CAS | 11399746PubMed |
Onoda, M., and Hall, P. F. (1981). Inhibition of testicular microsomal cytochrome P-450 (17 alpha-hydroxylase/C-17,20-lyase) by estrogens. Endocrinology 109, 763–767.
| Inhibition of testicular microsomal cytochrome P-450 (17 alpha-hydroxylase/C-17,20-lyase) by estrogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsVCht7o%3D&md5=3b04f6c91f0ecf1ff738595d8a93260eCAS | 6973463PubMed |
Primakoff, P., Lathrop, W., Woolman, L., Cowan, A., and Myles, D. (1988). Fully effective contraception in male and female guinea pigs immunized with the sperm protein PH-20. Nature 335, 543–546.
| Fully effective contraception in male and female guinea pigs immunized with the sperm protein PH-20.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlvVelur8%3D&md5=658fb16430905970a78eb138be08e717CAS | 3419530PubMed |
Rivas, A., Fisher, J. S., McKinnell, C., Atanassova, N., and Sharpe, R. M. (2002). Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology 143, 4797–4808.
| Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1eltLw%3D&md5=5c1d62a2ed42819ffc5cecbe2cf9b61cCAS | 12446607PubMed |
McLachlan, R. I., O’Donnell, L., Stanton, P. G., Balourdos, G., Frydenberg, M., de Kretser, D. M., and Robertson, D. M. (2002). Effects of testosterone plus medroxyprogesterone acetate on semen quality, reproductive hormones, and germ cell populations in normal young men. J. Clin. Endocrinol. Metab. 87, 546–556.
| 1:CAS:528:DC%2BD38XhsVSjur8%3D&md5=295e80ffd858bf40a5eb237186de08baCAS | 11836283PubMed |
Satyaswaroop, P. G., and Gurpide, E. (1978). A direct effect of medroxyprogesterone acetate on 17beta-hydroxysteroid dehydrogenase in adult rat testis. Endocrinology 102, 1761–1765.
| A direct effect of medroxyprogesterone acetate on 17beta-hydroxysteroid dehydrogenase in adult rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXkvVCqtbo%3D&md5=f28e509b2d8b9ca1a134e145f9d92a87CAS | 744049PubMed |
Saunders, P. T., Majdic, G., Parte, P., Millar, M. R., Fisher, J. S., Turner, K. J., and Sharpe, R. M. (1997). Fetal and perinatal influence of xenoestrogens on testis gene expression. Adv. Exp. Med. Biol. 424, 99–110.
| 1:CAS:528:DyaK1cXhsVOqtLc%3D&md5=2b509b33f5fd9f4f3b7d4e0a848b7685CAS | 9361775PubMed |
Saunders, P. T., Fisher, J. S., Sharpe, R. M., and Millar, M. R. (1998). Expression of oestrogen receptor beta (ER beta) occurs in multiple cell types, including some germ cells, in the rat testis. J. Endocrinol. 156, R13–R17.
| Expression of oestrogen receptor beta (ER beta) occurs in multiple cell types, including some germ cells, in the rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVWjsrs%3D&md5=fb2df610496080d90f8dd2038728a450CAS | 9582517PubMed |
Segmuller, B. E., Armstrong, B. L., Dunphy, R., and Oyler, A. R. (2000). Identification of autoxidation and photodegradation products of ethynylestradiol by on-line HPLC–NMR and HPLC–MS. J. Pharm. Biomed. Anal. 23, 927–937.
| Identification of autoxidation and photodegradation products of ethynylestradiol by on-line HPLC–NMR and HPLC–MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtlKjsro%3D&md5=756d9d07e12c7a3f88763c3236e8a810CAS | 11022917PubMed |
Shi, D., Wan, X., Davis, S. A., Pech, R. P., and Zhang, Z. (2002). Simulation of lethal control and fertility control in a demographic model for Brandt’s vole (Microtus brandti). J. Appl. Ecol. 39, 337–348.
| Simulation of lethal control and fertility control in a demographic model for Brandt’s vole (Microtus brandti).Crossref | GoogleScholarGoogle Scholar |
Simoni, M., Khan, S. A., De Geyter, C., and Nieschlag, E. (1989). Stimulatory and inhibitory influences of serum from pregnant women on aromatase activity of immature rat Sertoli cells. Acta Endocrinol. 121, 265–269.
| 1:CAS:528:DyaL1MXmtV2gsrs%3D&md5=62f00bcfc48239e1ed02d1ac64c8b738CAS | 2549754PubMed |
Spearow, J. L., Doemeny, P., Sera, R., Leffler, R., and Barkley, M. (1999). Genetic variation in susceptibility to endocrine disruption by estrogen in mice. Science 285, 1259–1261.
| Genetic variation in susceptibility to endocrine disruption by estrogen in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Sisrw%3D&md5=a700f8a6fc9578c2f05829daaa8605b1CAS | 10455051PubMed |
Sun, F., Oliver-Bonet, M., Liehr, T., Starke, H., Ko, E., Rademaker, A., Navarro, J., Benet, J., and Martin, R. H. (2004). Human male recombination maps for individual chromosomes. Am. J. Hum. Genet. 74, 521–531.
| Human male recombination maps for individual chromosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitV2gs7w%3D&md5=e6df7ade28ac446dce238ed717caa297CAS | 14973780PubMed |
Vader, J. S., van Ginkel, C. G., Sperling, F. M. G. M., de Jong, J., de Boer, W., de Graaf, J. S., van der Most, M., and Stokman, P. G. W. (2000). Degradation of ethinyl estradiol by nitrifying activated sludge. Chemosphere 41, 1239–1243.
| Degradation of ethinyl estradiol by nitrifying activated sludge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksF2nt7s%3D&md5=562873db505c26f70ee0de36d8f1a640CAS | 10901253PubMed |
van Pelt, A. M., de Rooij, D. G., van der Burg, B., van der Saag, P. T., Gustafsson, J. A., and Kuiper, G. G. (1999). Ontogeny of estrogen receptor-beta expression in rat testis. Endocrinology 140, 478–483.
| Ontogeny of estrogen receptor-beta expression in rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtFWrug%3D%3D&md5=184192135e31796de0e29a0f63469d49CAS | 9886860PubMed |
Wan X., Shi Y., Bao X., Guan Q., Yu C., Wang G., Liu W., Zhang Z., Zhong W., Jiao Y., and Hasi Q. (2006). Effect of the contraceptive compound (EP-1) on reproduction of the djungarian hamster (Phodopus campbelli) in the typical steppe. Acta Theriol. Sin. 26, 392–397. [In Chinese]
Wang, R. S., Yeh, S., Tzeng, C. R., and Chang, C. (2009). Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr. Rev. 30, 119–132.
| Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice.Crossref | GoogleScholarGoogle Scholar | 19176467PubMed |
Zhang Z. (2000a). Advance of immunocontraception in vertebrate pest management. Acta Theriol. Sin. 20, 130–134. [In Chinese]
Zhang, Z. (2000b). Mathematical models of wildlife management by contraception. Ecol. Model. 132, 105–113.
| Mathematical models of wildlife management by contraception.Crossref | GoogleScholarGoogle Scholar |
Zhang, Z., Liao, L., Wang, S., Cao, X., Wang, F., Wang, C., Zhang, J., Wan, X., and Zhong, W. (2004). Effect of a contraceptive compound (EP-1) on fertility of female Brandt’s voles, gray hamsters and mid-day gerbils. Acta Zool. Sin. 50, 341–347.
Zhang, Z., Wang, Y., Wang, S., Wang, F., Cao, X., and Zhang, J. (2005). Effect of a contraceptive compound on reproduction of greater long-tailed hamsters (Tscherskia triton) in experimental enclosures. Acta Theriol. Sin. 25, 269–272.
Zhang, Z., Zhao, M., Cao, X., Wang, Y., Wang, F., and Zhang, J. (2006). Effects of a contraceptive compound (EP-1) on reproductive organs of male greater long-tailed hamsters (Tscherskia triton). Acta Theriol. Sin. 26, 300–302.
Zhao, M., Liu, M., Li, D., Wan, X., Hinds, L. A., Wang, Y., and Zhang, Z. (2007). Anti-fertility effect of levonorgestrel and quinestrol in Brandt’s voles (Lasiopodomys brandtii). Integr. Zool. 2, 260–268.
| Anti-fertility effect of levonorgestrel and quinestrol in Brandt’s voles (Lasiopodomys brandtii).Crossref | GoogleScholarGoogle Scholar | 21396043PubMed |
Zhong, W., Wang, M., and Wan, X. (1999). Ecological management of Brandt’s vole (Microtus brandti) in Inner Mongolia, China. In ‘Ecologically-based Management of Rodent Pests’. (Eds G. Singleton, L. Hinds, H. Leirs and Z. Zhang.) pp. 199–214. (Australian Centre for International Agricultural Research: Canberra.)
