Advertisement

Mammalian Biology

, Volume 79, Issue 4, pp 225–229 | Cite as

Seasonal changes in testosterone levels in wild Mexican cottontails Sylvilagus cunicularius

  • Fernando Aguilar
  • Heiko G. Rödel
  • Jorge Vázquez
  • Letícia Nicolas
  • Luisa Rodríguez-Martínez
  • Amando Bautista
  • Margarita Martínez-GómezEmail author
Original Investigation

Abstract

We studied serum testosterone levels in the endemic Mexican cottontail, Sylvilagus cunicularius, which has been reported to show seasonal breeding. Animals were trapped in the wild and in a field enclosure in the National Park La Malinche in central Mexico over a period of five years. Serum testosterone (T) levels were quantified by ELISA from blood samples. T levels of adult males were lowest around 4 months after the onset of the annual reproductive season and were already high prior to the onset of breeding. As expected, the T levels of adult females were consistently lower than in males, and there were no differences in T level with respect to female reproductive state. There were no detectable sex-specific differences in juveniles and subadults, but there was a marked increase in T levels between juvenile and adult males. Overall, our study clearly reflects and confirms the seasonal breeding strategy of this species, showing high similarities to the much better studied European rabbit.

Keywords

Hormones La Malinche Net traps Reproductive state Seasonal reproduction 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arteaga, L, Bautista, A., Martínez-Gómez, M., Nicolás, L, Hudson, R., 2008. Scent marking, dominance and serum testosterone levels in male domestic rabbits, Physiol. Behav. 94, 510–515.CrossRefGoogle Scholar
  2. Bates, D., Maechler, M., 2010. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-34, http://CRAN.R-project.org/package=lme4Google Scholar
  3. BenSaad, M.M., Baylé, J.D., 1985. Seasonal changes in plasma testosterone, thyroxine, and cortisol levels in wild rabbits (Oryctolagus cuniculus algirus) of Zembra Island, Gen. Comp. Endocrinol. 57, 383–388.CrossRefGoogle Scholar
  4. Ben Saad, M.M., Maurel, D.L., 2004. Reciprocal interaction between seasonal testis and thyroid activity in Zembra Island wild rabbits (Oryctolagus cuniculus): effects of castration, thyroidectomy, temperature and photoperiod, Biol. Reprod. 70, 1001–1009.CrossRefGoogle Scholar
  5. Berger, M., Jean-Faucher, C, deTurckheim, M., Veyssiere, G., Blanc, M.R., Poirier, J.C, Jean, C, 1982. Testosterone, luteinizing hormone (LH) and follicle stimulating hormone (FSH) in plasma of rabbit from birth to adulthood, Correlation with sexual and behavioural development. Acta Endocrinol. 99, 459–465.PubMedGoogle Scholar
  6. Bronson, F.M., Heideman, P.D., 1984. Seasonal regulation of reproduction in mammals, In: Knobil, E., Neill, J.D. (Eds.), The Physiology of Reproduction, vol. 2, 2nd ed. Raven Press, New York, pp. 541–583.Google Scholar
  7. Blottner, S., Faber, D., Roelants, H., 2000. Seasonal variation of testicular activity in European brown hare Lepus europaeus, Acta Theriol. 45, 385–394.CrossRefGoogle Scholar
  8. Blottner, S., Hingst, O., Meyer, H.D., 1996. Seasonal spermatogenesis and testosterone production in roe deer (Capreolus capreolus). J, Reprod. Fertil. 108, 299–305.CrossRefGoogle Scholar
  9. Boyd, I.L., Myhill, D.G., 1987. Seasonal changes, reproduction and fecundity in the wild European rabbit (Oryctolagus cuniculus). J, Zool. 212, 223–233.CrossRefGoogle Scholar
  10. Cavigelli, S.A., Pereira, M.E., 2000. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm, Behav. 37, 246–255.Google Scholar
  11. Ceballos, G.G., Galindo, L.C., 1984. Mamíferos silvestres de la Cuenca de México. Limusa, México, DF.Google Scholar
  12. Cerbón, M.A., Camacho-Arroyo, I., Gamboa-Domínguez, A., González-Mariscal, G., 1996. The rabbit submandibular glands: sexual dimorphism, effects of gonadec-tomy, and variations across the female reproductive cycle, J. Comp. Physiol. A 178, 351–357.CrossRefGoogle Scholar
  13. Cervantes, F.A., Delgado, P., Colmenares, A.L., 2005. Conejos: Sylvilagus cunicularius (Waterhouse, 1984). In: Ceballos, G., Oliva, G. (Eds.), Los Mamíferos Silvestres de México. Comisión Nacional para el Uso y Aprovechamiento de la Biodiversidad y El Fondo de Cultura Económica. Toppan Printing Co., Hong Kong, pp. 842–843.Google Scholar
  14. Cervantes, F.A., Lorenzo, C, Vargas, J., Holmes, T., 1992. Sylvilagus cunicularius. Mamm, Spec. 412, 1–4.Google Scholar
  15. Farabollini, F., 1987. Behavioral and endocrine aspects of dominance and submission in male rabbits, Aggress. Behav. 13, 247–258.CrossRefGoogle Scholar
  16. Faraway, J., 2006. Extending the Linear Model with R. Chapman & Hall/CRC, New York.Google Scholar
  17. González, J., Lara, C, Vázquez, J., Martínez-Gómez, M., 2007. Demography, density, and survival of an endemic and nearthreatened cottontail Sylvilagus cunicularius in central Mexico, Acta Theriol. 52, 299–305.CrossRefGoogle Scholar
  18. González-Mariscal, G., Díaz-Sánchez, V., Melo, A.I., Beyer, C, Rosenblatt, J.S., 1994. Maternal behavior in New Zealand white rabbits: quantification of somatic events, motor patterns and steroid plasma levels, Physiol. Behav. 6, 1081–1089.CrossRefGoogle Scholar
  19. González-Mariscal, G., Jiménez, P., Beyer, C, Rosenblatt, J.S., 2003. Androgens stimulate specific aspects of maternal nest-building and reduce food intake in rabbits, Horm. Behav. 43, 312–317.CrossRefGoogle Scholar
  20. González-Mariscal, G., Melo, A., Zavala, A., Chirino, R., Beyer, C, 1993. Sex steroid regulation of chin-marking behavior in male New Zealand rabbits, Physiol. Behav. 54, 1035–1040.CrossRefGoogle Scholar
  21. Goncalves, H., Alves, P.C., Rocha, A., 2002. Seasonal variation in the reproductive activity of the wild rabbit (Oryctolagus cuniculus algirus) in a Mediterranean ecosystem, Wildl. Res. 29, 165–173.CrossRefGoogle Scholar
  22. Holm, S., 1979. A simple sequential rejective multiple test procedure, Scand.J. Stat. 6, 65–70.Google Scholar
  23. Hudson, R., Rodríguez-Martínez, L., Distel, H., Cordero, C, Altbäcker, V., Martínez-Gómez, M., 2005. A comparison between vegetation and diet records from the wet and dry season in the cottontail rabbit Sylvilagus floridanus at Ixtacuixtla, central Mexico, Acta Theriol. 50, 377–389.CrossRefGoogle Scholar
  24. Kouloumenta, V., Hatziefthimiou, A., Paraskeva, E., Gourgoulianis, K., Molyvdas, P.A., 2007. Sexual dimorphism in airway responsiveness to sex hormones in rabbits. Am. J. Physiol. Lung Cell Mol. Physiol. 293, 516.CrossRefGoogle Scholar
  25. Lincoln, G.A., Kay, R.N., 1979. Effects of season on the secretion of LH and testosterone in intact and castrated red deerstags (Cervus elaphus).J. Reprod, Fertil. 55, 75–80.CrossRefGoogle Scholar
  26. Martiniaková, M., Omelka, R., Grosskopf, B., Sirotkin, A.V., Chrenek, P., 2008. Sex-related variation in compact bone microstructure of the femoral diaphysis in juvenile rabbits. Acta Vet. Scand. 50, 15.CrossRefGoogle Scholar
  27. Mooring, M.S., Patton, M.L., Lance, V.A., Hall, B.M., Schaad, E.W., Fortin, S.S., Jella, J.E., McPeak, K.M., 2004. Fecal androgens of bison bulls during the rut, Horm. Behav. 46, 392–398.CrossRefGoogle Scholar
  28. Mykytowycz, R., 1965. Further observations on the territorial function and histology of the submandibular cutaneous (chin) glands in the rabbit, Oryctolagus cuniculus (L.), Anim. Behav. 13, 400–408.CrossRefGoogle Scholar
  29. Nelson, R.J., 2005. The endocrine system. In: Nelson, R.J. (Ed.), An Introduction to Behavioral Endocrinology. , 3rd ed. Sinauer Associates, Inc., Sunderland, MA, USA, pp. 35–95.Google Scholar
  30. R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0 http://www.R-project.orgGoogle Scholar
  31. Rödel, H.G., Bora, A., Kaetzke, P., Khaschei, M., Hutzelmeyer, H.D., Zapka, M., von Holst, D., 2005. Timing of breeding and reproductive performance of female European rabbits in response to wintertemperature and body mass, Can. J. Zool. 83, 935–942.CrossRefGoogle Scholar
  32. Sánchez, C, Windfield, J.C, Fernández, J.A., 2005. Biodiv. Parque Nacional Malinche, vol. 1., pp. 101–137.Google Scholar
  33. Schradin, C, 2008. Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent, Horm. Behav. 53, 573–579.CrossRefGoogle Scholar
  34. Sempéré, J., Mauget, R., Bubenik, G.A., 1992. Influence of photoperiod on the seasonal pattern of secretion of luteinizing hormone and testosterone and on the antler cycle in roe deer (Capreolus capreolus). J, Reprod. Fertil. 95, 693–700.CrossRefGoogle Scholar
  35. Silván, G., Illera, J.C, Martín, J., Manjón, R., Illera, M., 1990. Variaciones fotoperiódicas de las concentraciones plasmáticas de testosterona en conejo, Rev. Esp. Fisiol. 46, 177–182.PubMedGoogle Scholar
  36. Vázquez, J., Martínez Chacón, A.J., Hudson, R., Rodríguez-Martínez, L, Martínez-Gómez, M., 2007a. Seasonal reproduction in Mexican cottontail rabbits Sylvilagus cunicularius in La Malinche National Park, central México. ActaTheriol. 52, 361–369.Google Scholar
  37. Vázquez, J., Rodríguez, M.L., Bautista, A., Hudson, R., Martínez-Gómez, M., 2007b. Evaluación de una nueva trampa para capturar conejos silvestres (Sylvilagus cunicularius y S. floridanus). Rev. Mex. Mastozool. 11, 34–46.Google Scholar
  38. von Holst, D., Hutzelmeyer, H., Kaetzke, P., Khaschei, M., Schönheiter, R., 1999. Social rank, stress, fitness, and life expectancy in wild rabbits, Naturwissenschaften 86, 388–393.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2014

Authors and Affiliations

  • Fernando Aguilar
    • 1
  • Heiko G. Rödel
    • 2
  • Jorge Vázquez
    • 3
  • Letícia Nicolas
    • 3
  • Luisa Rodríguez-Martínez
    • 3
  • Amando Bautista
    • 3
  • Margarita Martínez-Gómez
    • 3
    • 4
    Email author
  1. 1.Universidad Autónoma de TlaxcalaMexico
  2. 2.Université Paris 13, Sorbonne Paris CitéLaboratoire d’Ethologie Expérimental et ComparéeVilletaneuseFrance
  3. 3.Centro Tlaxcala de Biología de la ConductaUniversidad Autónoma de TlaxcalaMexico
  4. 4.Departamento de Biología Celulary FisiologíaInstituto de Investigaciones BiomédicasUNAMMexico

Personalised recommendations