Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Relationship between delayed embryonic development and metabolic factors and fat deposition in fruit bat Cynopterus sphinx

Arnab Banerjee A , K.J. Meenakumari A and Amitabh Krishna A B
+ Author Affiliations
- Author Affiliations

A Department of Zoology, Banaras Hindu University, Varanasi, 221 005, India.

B Corresponding author. Email: akrishna_ak@yahoo.co.in

Reproduction, Fertility and Development 19(5) 626-633 https://doi.org/10.1071/RD06160
Submitted: 7 December 2006  Accepted: 16 April 2007   Published: 31 May 2007

Abstract

The present study was undertaken in the fruit bat Cynopterus sphinx, which breeds twice in quick succession at Varanasi, India. Its gestation period varies significantly in the two successive pregnancies of the year owing to delayed embryonic development during the first (winter) pregnancy. The primary aim of the present study was to determine the role of metabolic factors in delayed embryonic development in the fruit bat C. sphinx. Variation in bodyweight, fat deposition, oxygen (O2) consumption rate, basal metabolic rate (BMR), body temperature (Tb) and hepatic succinate dehydrogenase (SDH) activity, along with circulating levels of thyroid hormones (tri-iodothyronine and thyroxine), were examined as metabolic factors during the two successive pregnancies in C. sphinx. The increase in bodyweight observed in November was due to accumulation of white adipose tissue in the posterior abdominal region. A significant decline in O2 consumption rate, BMR, Tb and SDH activity was found in early winter in November–December, which coincides closely with the period of fat accumulation and with the period of delayed embryonic development in C. sphinx. A significantly higher O2 consumption rate, BMR, Tb and SDH activity was noted during the second pregnancy in, when embryonic development was relatively faster. Thyroid hormone levels were high during the period of embryonic delay compared with levels during the remaining months. The results of the present study suggest that the delayed embryonic development in C. sphinx during early winter may be due to a low O2 consumption rate, BMR, Tb and SDH activity in November–December. The energy saved by suppressing embryonic development in this species may be advantageous for fat accumulation. Increased thyroid hormone levels during the early winter period might facilitate fat accumulation in C. sphinx.

Additional keywords: basal metabolic rate, body temperature, O2 consumption, succinate dehydrogenase.


Acknowledgements

This study was supported by grants to AK from The Department of Science and Technology, New Delhi.


References

Abhilasha, , and Krishna, A. (1996). High androgen production by ovarian thecal interstitial cells: a mechanism for delayed ovulation in a tropical vespertilionid bat, Scotophilus heathi. J. Reprod. Fertil. 106, 207–211.
PubMed | Bartholomew G. A. (1972). Aspects of timing and periodicity of heterothermy. In ‘Hibernation and Hypothermia: Perspective And Challenges’. (Eds F. E. South, J. P. Hannon, J. R. Willis, E. T. Pengelley and N. R. Alpert.) pp. 663–680. (Elsevier: New York.)

Bradshaw, G. V. R. (1962). Reproductive cycle of the California leaf-nosed bat, Macrotus californicus. Science 136, 645–646.
Crossref | GoogleScholarGoogle Scholar | Decuypere E., Kuhn E. R., and Chadwick A. (1985). Rhythms in circulating prolactin and thyroid hormones in the early postnatal life of the domestic fowl: influence of fasting and feeding on thyroid rhythmicity. In ‘The Endocrine System and the Environment’. (Eds B. K. Follet, S. Ishi and A. Chandola.) pp. 189–200. (Japan Society Press: Tokyo.)

Eisentraut, M. (1937). Die wirkung niedriger Temperaturen auf die Embryonalentwicklung bie Fleder mäusen. Biol. Zentralbl. 57, 59–74.
Lowry, O. H., Rosenbough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–267.

Magnus, T. H. , and Henderson, N. E. (1988). Thyroid hormone resistance in hibernating ground squirrels, Spermophilus richardsoni. Gen. Comp. Endocrinol. 69, 352–360.
Crossref | GoogleScholarGoogle Scholar | PubMed | McNab B. K. (1987). The reproduction of marsupial and eutherian mammals in relation to energy expenditure. Symp. Zool. Soc. London 57 29–39.

Mead, R. A. (1993). Embryonic diapause in vertebrates. J. Exp. Zool. 266, 629–641.
Crossref | GoogleScholarGoogle Scholar | PubMed | Myant N. B. (1964). The thyroid and reproduction in mammals. In ‘The Thyroid Gland’. (Eds R. Pitt-Rivers and J. Trotter.) (Butterworth: London.)

Nony, P. A., Scallet, A. C. Rountree, R. L., Ye, X., and Binienda, Z. (1999). 3-Nitropropionic acid (3-NPA) produces hypothermia and inhibits histochemical labeling of succinate dehydrogenase (SDH) in rat brain. Metab. Brain Dis. 14, 83–94.

Parimi, P. S. , Croniger, C. M. , Leahy, P. , Hanson, R. W. , and Kalhan, S. C. (2003). Effect of reduced maternal inspired oxygen on hepatic glucose metabolism in the rat fetus. Pediatr. Res. 53, 325–332.
PubMed | Racey P. A. (1982). Ecology of bat reproduction. In ‘Ecology of Bats’. (Ed. T. H. Kuntz.) pp. 57–104. (Plenum Press: New York and London.)

Racey, P. A. , and Swift, S. M. (1981). Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. J. Reprod. Fertil. 61, 123–129.
PubMed |

Rasweiler, J. J. , and Badwaik, N. K. (1997). Delayed development in the short-tailed fruit bat, Carollia perspicillata. J. Reprod. Fertil. 109, 7–20.
PubMed |

Scallet, A. C. , Haley, R. L. , Scallet, D. M. , Duhart, H. M. , and Binienda, Z. K. (2003). 3-Nitropropionic acid inhibition of succinate dehydrogenase (complex II) activity in cultured chinese hamster ovary cells: antagonism by l-carnitine. Ann. N.Y. Acad. Sci. 993, 305–312.
PubMed |

Schreihofer, D. , Amico, J. , and Cameron, J. (1993). Reversal of fasting-induced suppression of luteinizing hormone (LH) secretion in male rhesus monkeys by intragastric nutrient infusion: evidence for rapid stimulation of LH by nutritional signals. Endocrinology 132, 1890–1897.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shanbhag, B. A. , Saidapur, S. K. , and Radder, R. S. (2003). Lowering body temperature induces embryonic diapause during prolonged egg retention in the lizard, Calotes versicolor. Naturwissenschaften 90, 33–35.
PubMed |

Singh, U. P. , Krishna, A. , and Bhatnagar, K. P. (2002). Seasonal changes in thyroid activity in the female sheath tailed bat, Taphozous longimanus (Chiroptera: emballonuridae). Acta Biol. Hung. 53, 267–278.
Crossref | GoogleScholarGoogle Scholar | PubMed |

van der Laarse, W. J. , Diegenbach, P. C. , and Elzinga, G. (1989). Maximum rate of oxygen consumption and quantitative histochemistry of succinate dehydrogenase in single muscle fibres of Xenopus laevis. J. Muscle Res. Cell Motil. 10, 221–228.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wimsatt, W. A. (1969). Some interrelations of reproduction and hibernation in mammals. Symp. Soc. Exp. Biol. 23, 511–559.
PubMed |