Advertisement

Acta Theriologica

, Volume 53, Issue 1, pp 73–85 | Cite as

Female reproductive responses to photoperiod and male odours in the subterranean rodentCtenomys talarum

  • M. Sol Fanjul
  • Roxana R. Zenuto
Article

Abstract

The tuco-tucoCtenomys talarum Thomas, 1898 is a solitary subterranean rodent that breeds seasonally in coastal sand-dune grasslands from Argentina. We assessed whether short-day photoperiod determines the onset of reproduction by an increase in female’s receptivity and whether male odour interacts with photoperiod as a cue by producing a greater response in receptivity. Receptivity was measured by an increase in the percentage of vaginal epithelial cells, particularly cornified cells. Females were trapped during their non-reproductive season (summer-long days) and randomly assigned to different day-length experimental groups: constant summer (CS), early winter (EW), and natural (NA) photoperiod. We examined the vaginal epithelium using vaginal smears during the first experimental phase (120 days) to test the effect of photoperiod. In the second experimental phase (15 days), we presented the females with male-soiled shavings to test the effect of photoperiod and male odor.Ctenomys talarum females showed some evidence of reproductive responsiveness to photoperiodic cuing. The proportion of epithelial cells peaked earlier in females when winter day-length was advanced than in females under natural photoperiod. Contrary to that expected, male odours did not stimulate female receptivity. These results suggest that, while photoperiod may participate in regulating reproduction, the integration of other environmental and social factors, as well as the identification of bodily conditions that lead to differences in individual response needs further consideration.

Key words

Ctenomys odours photoperiod subterranean rodents vaginal smears 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Antinuchi C. D. and Busch C. 1992. Burrow structure in the subterranean rodentCtenomys talarum. Zeitschrift für Säugertierkunde 57: 163–168.Google Scholar
  2. Antinuchi C. D., Zenuto R., LunaF., Cutrera A. P., Perisinotti P. and Busch C. 2007. Energy budget in subterranean rodents: Insights from the tuco-tucoCtenomys talarum (Rodentia: Ctenomidae). [In: Essays in honor of Oliver Pearson. D. Kelt, ed]. University of California Publications in Zoology Series. California: 111–139.Google Scholar
  3. Bennett N. C., Faulkes C. G. and Molteno A. J. 2000. Reproduction in subterranean rodents. [In: Life underground: the biology of subterranean rodents. E. A. Lacey, J. L. Patton and G. N. Cameron, eds]. The University of Chicago Press, Chicago, Illinois: 145–182.Google Scholar
  4. Blank J. L. 1992. Phenotypic variation in physiological response to seasonal environments. [In: Mammalian energetics: interdisciplinary views of metabolism and reproduction. T. Tomasi and T. Horton, eds]. Cornell University Press, Ithaca, New York: 186–212.Google Scholar
  5. Breed W. G. 1967. Ovulation in the GenusMicrotus. Nature 214: 826.CrossRefPubMedGoogle Scholar
  6. Bronson F. H. 1989. Mammalian reproductive biology. The University of Chicago Press, Chicago: 1–325.Google Scholar
  7. Bronson F. H. and Perrigo G. 1987. Seasonal regulation of reproduction in muroid rodents. American Zoologist 27: 929–940.Google Scholar
  8. Brown R. E. 1985. The rodents I: effects of odours on reproductive physiology (primer effects). [In: Social odours in mammals. R. E. Brown and D. W. MacDonald, eds.] Clarendon Press, Oxford: Vol. 1: 245–344.Google Scholar
  9. Buffenstein R. 2000. Ecophysiological responses of subterranean rodents to underground habitats. [In: Life underground: the biology of subterranean rodents. E. A. Lacey, J. L. Patton and G. N. Cameron, eds]. The University of Chicago Press, Chicago, Illinois: 62–110.Google Scholar
  10. Busch C. 1989. Metabolic rate and thermoregulation in two species of tuco-tucoCtenomys talarum andCtenomys australis (Caviomorpha: Octodontidae). Comparative Biochemical Physiology 93: 345–347.CrossRefGoogle Scholar
  11. Busch C., Malizia A. I., Scaglia O. A. and Reig O. A. 1989. Spatial distribution and attributes of a population ofCtenomys talarum (Rodentia, Octodontidae). Journal of Mammalogy 70: 204–208.CrossRefGoogle Scholar
  12. Carter C. S., Getz L. L., Gavish L., McDermott J. L. and Arnold P. 1980. Male-related pheromones and the activation of female reproduction in the prairie vole (Microtus ochrogaster). Biology of Reproduction 23: 1038–1045.CrossRefPubMedGoogle Scholar
  13. Cohen-Parsons M. and Carter C. S. 1988. Males increase progestin receptor binding in brain of female voles. Physiology Behavavior 42: 191–197.CrossRefGoogle Scholar
  14. Cutrera A. P. and Antinuchi C. D. 2004. [Fur changes in subterranean rodentCtenomys talarum: posible termal compensatory mechanism]. Revista Chilena de Historia Natural 77: 235–242. [In Spanish with English abstract]CrossRefGoogle Scholar
  15. del Valle J. C., Lohfelt M. I., Comparatore V. M., Cid M. S. and Busch C. 2001. Feeding selectivity and food preference ofCtenomys talarum (tuco-tuco). Zeitschrift für Säugertierkunde 66: 165–173.Google Scholar
  16. Dodge J. C., Kristal M. B. and Badura L. L. 2002. Male-induced estrus synchronization in the female Siberian hamster (Phodopus sungurus sungurus). Physiology and Behavior 77: 227–231.CrossRefPubMedGoogle Scholar
  17. Edmonds K. E., Riggs L. and Stetson M. H. 2003. Food availability and photoperiod affect reproductive development and maintenance in the marsh rice rat (Oryzomys palustris). Physiology and Behavior 78: 41–49.CrossRefPubMedGoogle Scholar
  18. Evans J. M. and Savage T. J. 1970. The collection of vaginal smears from bitches. Veterinary Records 87: 598–599.CrossRefGoogle Scholar
  19. Fanjul M. S. 2006. Regulación ambiental y social de la reproducción en hembras del roedor subterráneoCtenomys talarum. PhD thesis, Universidad Nacional de Mar del Plata, Mar del Plata: 1–116.Google Scholar
  20. Fanjul M. S., Zenuto R. R. and Busch C. 2003. Use of olfaction for sexual recognition in the subterranean rodentCtenomys talarum. Acta Theriologica 48: 35–46.Google Scholar
  21. Fanjul M. S., Zenuto R. R and Busch C. 2006. Seasonality of breeding in wild tuco-tucosCtenomys talarum in relation to climate and food availability. Acta Theriologica 51: 283–293.CrossRefGoogle Scholar
  22. Haim A., Heth G., Pratt H. and Nevo E. 1983. Photoperiodic effects on thermoregulation in a “blind” subterranean mammal. Journal of Experimental Biology 107: 59–64.PubMedGoogle Scholar
  23. Herbst M., Jarvis J. U. M. and Bennett N. C. 2004. A field assessment of reproductive seasonality in the threatened wild Namaqua dune mole-rat (Bathyergus janetta). Journal of Zoology, London 263: 259–268.CrossRefGoogle Scholar
  24. Hoffman R. A., Johnson L. B., Vaughan M. K. and Reiter R. J. 1987. Influence of diet on photoperiod-induced gonadal regression in female hamsters. Growth 51: 385–396.PubMedGoogle Scholar
  25. Horton T. H. and Rowsemitt C. N. 1992. Natural selection and variation in reproductive physiology. [In: Mammalian energetics: interdisciplinary views of metabolism and reproduction. T. Tomasi and T. Horton, eds]. Cornell University Press, Ithaca, New York: 160–185.Google Scholar
  26. Ims R. A. 1990. The ecology and evolution of reproductive synchrony. Tree 5: 135–140.Google Scholar
  27. Jarvis J. U. M. and Bennett N. C. 1990. The evolutionary history, population biology and social structure of African mole-rats: family Bathyergidae. Progress in Clinical and Biological Research 335: 97–128.PubMedGoogle Scholar
  28. Johnson L. B. and Hoffman R. A. 1985. Interaction of diet and photoperiod on growth and reproduction in male golden hamsters. Growth 49: 380–399.PubMedGoogle Scholar
  29. Kenagy G. J. and Barnes B. M. 1984. Environmental and endogenous control of reproductive function in the Great Basin pocket mousePerognatus parvus. Biology of Reproduction 31: 637–645.CrossRefPubMedGoogle Scholar
  30. Lombardi J. 1998. Comparative vertebrate reproduction. Kluwer Academic Publishers, Boston: 1–469.Google Scholar
  31. Lynch G. R., Lynch C. B. and Kliman R. M. 1989. Genetic analyses of photoresponsiveness in the Djungarian hamster,Phodopus sungorus. Journal of Comparative Physiology 164: 475–481.CrossRefPubMedGoogle Scholar
  32. MacFarlane J. D. and Taylor J. M. 1982. Nature of estrus and ovulation inMicrotus townsendii (Bachman). Journal of Mammalogy 63: 104–109.CrossRefGoogle Scholar
  33. Malherbe G. P., Schoeman A. S. and Bennett N. C. 2004. Is the highveld mole-ratCryptomys hottentotus pretoriae (Rodentia: Bathyergidae) an induced or spontaneous ovulator? Journal of Zoology, London 263: 159–165.CrossRefGoogle Scholar
  34. Malizia A. I. and Busch C. 1991. Reproductive parameters and growth in the fossorial rodentCtenomys talarum (Rodentia: Octodontidae). Mammalia 55: 293–305.CrossRefGoogle Scholar
  35. Milligan S. R. 1975. Mating, ovulation and corpus luteum function in the vole,Microtus agrestis. Journal of Reproduction and Fertility 42: 35–44.CrossRefPubMedGoogle Scholar
  36. Pévet P., Heth G., Haim A. and Nevo E. 1984. Photoperiod perception in the blind mole-rat (Spalax ehrenbergi, Nehring). Involvement of the Harderian gland, atrophied eyes and melatonin. Journal of Experimental Zoology 232: 41–50.CrossRefPubMedGoogle Scholar
  37. Rado R., Bronchti G., Wollberg Z. and Terkel J. 1992a. Sensitivity to light of the blind mole rat: behavioral and neuroanatomical study. Israel Journal of Zoology 38: 323–331.Google Scholar
  38. Rado R., Wollberg Z. and Terkel J. 1992b. Dispersal of young mole-rats (Spalax ehrenbergi) from the natal burrow. Journal of Mammalogy 74: 885–890.CrossRefGoogle Scholar
  39. Sawrey D. K. and Dewsbury D. A. 1985. Control of ovulation, vaginal estrus and behavioral receptivity in voles (Microtus). Neuroscience and Biobehavioral Reviews 9: 563–571.CrossRefPubMedGoogle Scholar
  40. Shanas U., Heth G., Nevo E., Shalgi R. and Terkel J. 1995. Reproductive behaviour in the female blind mole rat (Spalax ehrenbergi). Journal of Zoology, London 137: 195–210.CrossRefGoogle Scholar
  41. Stein B. R. 2000. Morphology of subterranean rodents. [In: Life underground: the biology of subterranean rodents. E. A. Lacey, J. L. Patton and G. N. Cameron, eds]. The University of Chicago Press, Chicago, Illinois: 19–61.Google Scholar
  42. Šumbera R., Burda H. and Chitaukali W. N. 2003. Reproductive biology of a solitary subterranean bathyergid rodent, the silvery mole-rat (Heliophobius argenteocinereus). Journal of Mammalogy 84: 278–287.CrossRefGoogle Scholar
  43. Temeles E. J. 1994. The role of neighbors in territorial systems: when are they “dear enemies”? Animal Behavior 47: 339–350.CrossRefGoogle Scholar
  44. Trillmich F. 2000. Effects of low temperature and photo-p eriod on reproduction in the female wild guinea pig (Cavia aperea). Journal of Mammalogy 81: 586–594.CrossRefGoogle Scholar
  45. Turek F. W. and Cambell C. S. 1979. Photoperiodic regulation of neuroendocrine-gonadal activity. Biology of Reproduction 20: 32- 50.PubMedGoogle Scholar
  46. Vandenbergh J. G. 1994. Pheromones and mammalian reproduction. [In: Encyclopedia of reproduction. E. R. Knobil and J. D. Neill, eds]. Academic Press, New York: 349–359.Google Scholar
  47. Weir B. J. 1974. Reproductive characteristics of hystricomorph rodents. Symposium of The Zoological Society of London 34: 265–301.Google Scholar
  48. Zarrow M. X. and Clark J. H. 1968. Ovulation following vaginal stimulation in a spontaneous ovulator and its implications. Journal of Endocrinology 40: 343–352.CrossRefPubMedGoogle Scholar
  49. Zenuto R. R., Antinuchi C. D. and Busch C. 2002a. Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum). Physiological Biochemical Zoology 75: 469–478.CrossRefGoogle Scholar
  50. Zenuto R. R., Estavillo C. and Fanjul M. S. 2007. Familiarity and mating behaviour in the subterranean rodentCtenomys talarum (tuco-tuco). Canadian Journal of Zoology 85: 944–955.CrossRefGoogle Scholar
  51. Zenuto R. R. and Fanjul M. S. 2002. Olfactory discrimination of individual scents in the subterranean rodentCtenomys talarum (tuco-tuco). Ethology 108: 629–641.CrossRefGoogle Scholar
  52. Zenuto R. R., Fanjul M. S. and Busch C. 2004. Subterranean rodentCtenomys talarum (tuco-tuco) use chemical communication during breeding season. Journal of Chemical Ecology 30: 2111–2126.CrossRefPubMedGoogle Scholar
  53. Zenuto R. R., Lacey E. A. and Busch C. 1999. DNA fingerprinting reveals polygyny in the subterranean rodentCtenomys talarum. Molecular Ecology 8: 1529–1532.CrossRefPubMedGoogle Scholar
  54. Zenuto R. R., Vassallo A. I. and Busch C. 2001. A method for studying social and reproductive behavior of subterranean rodents in captivity. Acta Theriologica 46: 161–170.CrossRefGoogle Scholar
  55. Zenuto R. R., Vasallo A. I. and Busch C. 2002b. [Social and reproductive behaviour of the subterranean rodentCtenomys talarum (Rodentia, Ctenomyidae) in semi captivity conditions]. Revista Chilena de Historia Natural 75: 165–177. [In Spanish]CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Bialowieza, Poland 2008

Authors and Affiliations

  • M. Sol Fanjul
    • 1
  • Roxana R. Zenuto
    • 1
  1. 1.Laboratorio de Ecofisiología, Departamento de Biología, Facultad de Ciencias Exactas y NaturalesUniversidad Nacional de Mar del PlataBuenos AiresArgentina

Personalised recommendations