Abstract
Via a non-invasive approach, we aimed to provide comparative data on the presence and relative abundance of progestogen and estrogen metabolites excreted into the urine of Eulemur rubriventer, E. macaco flavifrons and Hapalemur griseus occidentalis and to characterize the patterns of progestogen and estrogen excretion during pregnancy. We found that estrone is the major urinary estrogen in Eulemur macaco flavifrons and Hapalemur griseus occidentalis, while 16α-hydroxyestrone appeared to be the predominant estrogen in the urine of E. rubriventer. Estradiol-17ß was either absent (Hapalemur) or present in very low amounts. HPLC of progestogens had high levels of immunoreactivity in an assay against 5α-pregnane-3α-ol-20-one (5-P-3OH) in each species, though the nature of the progestogens measured by the 5-P-3OH assay differed among species. During pregnancy, 5-P-3OH levels remained relatively low in Eulemur rubriventer, whereas in E. macaco flavifrons and Hapalemur griseus occidentalis, a sustained elevation in levels occurred from mid-pregnancy until the final weeks before parturition. Estrogen excretion differed depending on the sex of the fetus in each species, with only females carrying male infants showing clearly elevated estrogen levels during the last 6–8 weeks of gestation. In conclusion, we demonstrate both species similarities and differences in the metabolism and urinary excretion patterns of reproductive hormones throughout gestation in the Lemuridae. The data not only extend our knowledge on the reproductive physiology of lemurs but also show that more studies on other lemur taxa are needed to provide a broader basis for interspecific comparison.
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Albrecht, E. D., and Pepe, G. J. (1998). Placental steroidogenesis in primate pregnancy. In Knobil, E., and Neill, J. D. (eds.), Encyclopedia of Reproduction, Academic Press, London, pp. 889-898.
Bahr, N. I., Palme, R., Möhle, U., Hodges, J. K., and Heistermann, M. (2000). Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen. Comp. Endocrinol. 117: 427-438.
Bogart, M. H., Kumamoto, A. T., and Lasley, B. L. (1977). A comparison of the reproductive cycle of three species of Lemur. Folia Primatol. 28: 134-143.
Brockman, D. K., and Whitten, P. L. (1996). Reproduction in free-ranging Propithecus verreauxi: Estrus and the relationship between multiple partner matings and fertilization. Am. J. Phys. Anthropol. 100: 57-69.
Butler, H. (1960). Some notes on the breeding cycle of the Senegal galago (Galago senegalensis senegalensis) in the Sudan. Proc. Zool. Soc. Lond. 135: 423-430.
Carosi, M., Heistermann, M., and Visalberghi, E. (1999). Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys. Horm. Behav. 36: 252-265.
Curtis, D. J., Zaramody, A., Green, D. I., and Pickard, A. R. (1999). Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz): An investigation of faecal steroid excretion patterns. In 7th World Conference on Breeding Endangered Species. Linking Zoo and Field Research to Advance Conservation, Poster Abstracts, Cincinnati Zoo and Botanical Garden, USA.
Curtis, D. J., Zaramody, A., Green, D. I., and Pickard, A. R. (2000). Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz). Reprod. Fertil. Dev. 12: 21-29.
Czekala, N. M., Benirschke, K., McClure, H., and Lasley, B. L. (1983). Urinary estrogen excretion during pregnancy in the gorilla (Gorilla gorilla), orangutan (Pongo pygmaeus) and the human (Homo sapiens). Biol. Reprod. 28: 289-294.
Fiess, M., Heistermann, M., and Hodges, J. K. (1999). Patterns of urinary and fecal steroid excretion during the ovarian cycle and pregnancy in the African elephant (Loxodonta africana). Gen. Comp. Endocrinol. 115: 76-89.
Heistermann, M., Finke, M., and Hodges, J. K. (1995). Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am. J. Primatol. 37: 275-284.
Heistermann, M., Tari, S., and Hodges, J. K. (1993). Measurement of fecal steroids for monitoring ovarian function in New World primates, Callitrichidae. J. Reprod. Fertil. 99: 243-251.
Heistermann, M., Trohorsch, B., and Hodges, J. K. (1997). Assessment of ovarian function in the African elephant (Loxodonta africana) by measurement of 5 alpha-reduced progesterone metabolites in serum and urine. Zoo Biol. 16: 273-284.
Hodgen, G. D., Dufau, M. L., Catt, K. J., and Tullner, W. W. (1972). Estrogens, progesterone, and chorionic gonadotropin in pregnant rhesus monkeys. Endocrinology 91: 896-900.
Hodges, J. K., Heistermann, M., Beard, A., and van Aarde, R. J. (1997). Concentrations of progesterone and the 5α-reduced progestins, 5α-pregnane-3,20-dione and 3α-hydroxy-5α-pregnan-20-one, in luteal tissue and circulating blood and their relationship to luteal function in the African elephant, Loxodonta africana. Biol. Reprod. 556: 640-646.
Hodges, J. K., van Aarde, R. J., Heistermann, M., and Hoppen, H.-O. (1994). Progestin content and biosynthetic potential of the corpus luteum of the African elephant (Loxodonta africana). J. Reprod. Fert. 102: 163-168.
Izard, M. K., and Fail, P. A. (1988). Progesterone levels during pregnancy in the greater thick-tailed galago (Galago crassicaudatus). J. Med. Primatol. 17: 125-133.
Jurke, M. H., Czekala, N. M., and Fitch-Snyder, H. (1997). Non-invasive detection and monitoring of estrus, pregnancy and the postpartum period in pygmy loris (Nycticebus pygmaeus) using fecal estrogen metabolites. Am. J. Primatol. 41: 103-115.
Lasley, B. L., Bogart, M. H., and Shideler, S. E. (1979). A comparison of lemur ovarian cycles. In Alexander, N. J. (ed.), Animal Models for Research On Contraception and Fertility, Harper and Row, New York, pp. 417-424.
Maston, G. A., and Ruvolo, M. (2002). Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection. Mol. Biol. Evol. 19: 320-335.
Ostner, J., Heistermann, M. (2003). Endocrine characterization of female reproductive status in wild redfronted lemurs (Eulemur fulvus rufus). Gen. Comp. Endocrinol. 131: 274-283.
Ostner, J., Heistermann, M., and Kappeler, P. M. (2003). Intersexual dominance, masculinized genitals and prenatal steroids: Comparative data from lemurid primates. Naturwissenschaften 90: 141-144.
Perez, L. E., Czekala, N. M., Weissenseel, K. A., and Lasley, B. L. (1988). Excretion of radiolabeled estradiol metabolites in the slow loris (Nycticebus coucang). Am. J. Primatol. 16: 321-330.
Perry, J. M., Izard, M. K., and Fail, P. A. (1992). Observations on reproduction, hormones, copulatory behavior, and neonatal mortality in captive Lemur mongoz (Mongoose Lemur). Zoo Biology. 11: 81-97.
Rowe, N. (1996). The Pictorial Guide to the Living Primate, Pogonias Press, New York.
Schaaf, C. D., and Stuart, M. D. (1983). Reproduction of the mongoose lemur (Lemur mongoz) in captivity. Zoo Biol. 2: 23-38.
Shideler, S. E., Czekala, N. M., Benirschke, K., and Lasley, B. L. (1983). Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus). Biol. Reprod. 28: 963-969.
von Horn, R. N., Resko, J. A. (1977). The reproductive cycle of the ring-tailed lemur (Lemur catta): Sex steroid levels and sexual receptivity under controlled photoperiods. Endocrinology 5: 1579-1586.
Ziegler, T. E., Sholl, S. A., Scheffler, G., Haggerty, M. A., and Lasley, B. L. (1989). Excretion of estrone, estradiol, and progesterone in the urine and feces of the female cotton-top tamarin (Saguinus oedipus oedipus). Am. J. Primatol. 17: 185-195.
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Gerber, P., Moisson, P. & Heistermann, M. Urinary Progestogen and Estrogen Excretion During Pregnancy in Eulemur macaco flavifrons, E. rubriventer, and Hapalemur griseus occidentalis . International Journal of Primatology 25, 449–463 (2004). https://doi.org/10.1023/B:IJOP.0000019161.01299.d7
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DOI: https://doi.org/10.1023/B:IJOP.0000019161.01299.d7