Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-22T22:50:01.430Z Has data issue: false hasContentIssue false
  • English
  • Français

Population estimate and morphometry of ovarian preantral follicles from three recently recognized squirrel monkey species: a comparative study

Published online by Cambridge University Press:  23 May 2017

Gerson P. Lopes ,
Regiane R. Santos ,
Débora V. Almeida ,
Adriel B. Brito ,
Helder L. Queiroz  and
Sheyla F. S. Domingues
Gerson P. Lopes
Affiliation:
Federal University of Pará, Postgraduate Program in Animal Science, Belém, Pará, Brazil. Institute for Sustainable Development Mamirauá, Research Group on Ecology of Terrestrial Vertebrates Tefé, Amazonas, Brazil.
Regiane R. Santos*
Affiliation:
Federal University of Pará, Laboratory of Wild Animal Biology and Medicine, BR 316 Km 61, CEP 687406970, Castanhal, Pará, Brazil.
Débora V. Almeida
Affiliation:
Federal University of Pará, Postgraduate Program in Animal Science, Belém, Pará, Brazil.
Adriel B. Brito
Affiliation:
Federal University of Pará, Postgraduate Program in Animal Science, Belém, Pará, Brazil.
Helder L. Queiroz
Affiliation:
Institute for Sustainable Development Mamirauá, Research Group on Ecology of Terrestrial Vertebrates Tefé, Amazonas, Brazil.
Sheyla F. S. Domingues
Affiliation:
Federal University of Pará, Postgraduate Program in Animal Science, Belém, Pará, Brazil.
*
All correspondence to: Regiane R Santos. Federal University of Pará, Laboratory of Wild Animal Biology and Medicine, BR 316 Km 61, CEP 687406970, Castanhal, Pará, Brazil. Email: R.Rodriguesdossantos@pq.cnpq.br
Get access Rights & Permissions [Opens in a new window]

Summary

We describe morphological and morphometrical characteristics of preantral ovarian follicles from three recently recognized Saimiri species: S. macrodon, S. cassiquiarensis and S. vanzolinii; the last one a threatened species. Ovaries from four adult monkeys were evaluated: one pair from a pregnant S. macrodon, two ovarian pairs from S. cassiquiarensis females (one of them pregnant), and one left ovary from a senile S. vanzolinii, applying classical histology. Follicular preantral population was quantified and morphology and morphometry of primordial, primary and secondary follicles were evaluated. Follicular preantral population varied among species, being 347,153 in the ovaries of the S. macrodon, 270,342 and 278,376 in the ovaries of both adult non-pregnant and pregnant S. cassiquiarensis females, and 28,149 in the ovary from a senile S. vanzolinii. Most follicles were at primordial or transition stages, except for the senile S. vanzolinii female, which presented the lowest percentages of primordial and transition follicles when compared with primary and secondary ones. Most preantral follicles (>70%) were morphologically normal in the ovaries from all studied S. macrodon and S. cassiquiarensis females, but the ovary of the senile S. vanzolinii female presented a significant decrease in the percentage of normal follicles (primordial: 61%, transition: 52%, primary: 54%, and secondary: 48%). In general, follicular diameter increased significantly from primordial to transition, and subsequently from primary to secondary follicles.

Keywords

MorphologyMorphometryNeotropicalOvarian folliclesPrimateSaimiri sp.
Type
Research Article
Information
Zygote , Volume 25 , Issue 3 , June 2017 , pp. 279 - 287
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almeida, D.V., Santos, R.R., Scalercio, S.R., Leão, D.L., Haritova, A., Oskam, I.C. & Domingues, S.F. (2012). Morphological and morphometrical characterization, and estimation of population of preantral ovarian follicles from senile common squirrel monkey (Saimiri sciureus). Anim. Reprod. Sci. 134, 210–15.CrossRefGoogle ScholarPubMed
Andrabi, S.M.H. & Maxwell, W.M.C. (2007). A review on reproductive biotechnologies for conservation of endangered mammalian species. Anim. Reprod. Sci. 99, 223–43.CrossRefGoogle ScholarPubMed
Baker, T.G. & Wai, S.O. (1976). Developmental of the ovary and oogenesis. Clin. Obstet. Gynecol. 3, 3–26.Google Scholar
Baldwin, J.D. (1969). The ontogeny of social behaviour of squirrel monkeys (Saimiri sciureus) in a seminatural environment. Fol. Primatol. 11, 161–84.CrossRefGoogle Scholar
Boinski, S. (1992). Monkeys with inflated sex appeal. Nat. Hist. 101, 42–9.Google Scholar
Brand, H.M. (1981). Urinary oestrogen excretion in the female cotton–topped tamarin (Saguinus oedipus oedipus). J. Reprod. Fertil 62, 467–73.CrossRefGoogle ScholarPubMed
Braw-Tal, R. (2002). The initiation of follicle growth: the oocyte or the somatic cells? Mol. Cell Endocrinol. 187, 11–8.CrossRefGoogle ScholarPubMed
Brito, A.B., Santos, R.R., van den Hurk, R., Lima, J.S., Miranda, M.S., Ohashi, O.M. & Domingues, S.F.S. (2013). Short–term culture of ovarian cortical strips from capuchin monkeys (Sapajus apella): a morphological, viability, and molecular study of preantral follicular development in vitro . Reprod. Sci. 20, 990–7.CrossRefGoogle ScholarPubMed
Bysted, B.V., Dieleman, S.J., Hyttel, P. & Greve, T. (2001). Embryonic developmental stages in relation to the LH peak in dogs. J. Reprod. Fertil. 57, 181–6.Google Scholar
Cahill, L.P., Mariana, J.C. & Mauléon, P. (1979). Total follicular populations in ewes of high and low ovulations rates. J. Reprod. Fertil. 55, 27–36.CrossRefGoogle ScholarPubMed
Campbell, C.J., Shideler, S.E., Todd, H.E. & Lasley, B.L. (2001). Fecal analysis of ovarian cycles in female black–headed spider monkeys (Ateles geoffroyi). Am. J. Primatol. 54, 79–89.CrossRefGoogle Scholar
Dixson, A.F. (1983). The owl monkey. In Reproduction in New World Primates (ed. Hearn, J.P.), pp. 69–113. Lancaster: MTP Press.CrossRefGoogle Scholar
Dixson, A.F. (2001). The evolution of neuroendocrine mechanisms regulating sexual behaviour in female primates. Reprod. Fertil. Dev. 13, 599–607.CrossRefGoogle ScholarPubMed
Domingues, S.F.S., Diniz, L.V., Furtado, S.H.C., Ohashi, O.M., Rondina, D. & Silva, L.D.M. (2004). Histological study of capuchin monkey (Cebus apella) ovarian follicles. Acta Amazon. 34, 495–501.CrossRefGoogle Scholar
Erickson, B.H. (1966). Development and senescence of the postnatal bovine ovary. J. Anim. Sci. 25, 800–5.CrossRefGoogle ScholarPubMed
Erickson, B.H., Reynolds, R.A. & Murphree, R.L. (1976). Ovarian characteristics and reproductive performance of the aged cow. Biol Reprod. 15, 555–60.CrossRefGoogle ScholarPubMed
Forman, E.J., Hong, K.H., Ferry, K.M., Tao, X., Taylor, D., Levy, B., Treff, N.R. & Scott, R.T. Jr. (2013). In vitro fertilization with single euploid blastocyst transfer: a randomized controlled trial. Fertil. Steril. 100, 100–7.CrossRefGoogle ScholarPubMed
Fukuda, M., Fukuda, K., Andersen, C.Y. & Byskov, A.G. (2000). Right-sided ovulation favours pregnancy more than left–sided ovulation. Hum. Reprod. 15, 1921–6.CrossRefGoogle ScholarPubMed
Gougeon, A. & Chainy, G.B.N. (1987). Morphometric studies of small follicles in ovares of women at different ages. J. Reprod. Fertil. 81, 433–42.CrossRefGoogle Scholar
Gougeon, A. (1981). Frequent occurrence of multiovular follicles and multinuclear oocytes in the adult human ovary. Fertil. Steril. 35, 417–22.CrossRefGoogle ScholarPubMed
Gougeon, A. (1996). Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrinol. Rev. 17, 121–55.CrossRefGoogle ScholarPubMed
Graham, C.E. & Bradley, C.F. (1971). Polyovular follicles in squirrel monkeys after prolonged diethylstilboestrol treatment. J. Reprod. Fertil. 27, 181–5.CrossRefGoogle ScholarPubMed
Harrison, R.G. (1949). The comparative anatomy of the blood–supply of the mammalian testis. Proc. Zool. Soc. Lond. 119, 325–44.CrossRefGoogle Scholar
Hartman, C.G. (1926). Polynuclear ova and polyovular follicles in the opossum and other mammals, with special reference to the problem of fecundity. Am. J. Anat. 37, 1–51.CrossRefGoogle Scholar
Helvacioglu, A., Aksel, S., Yeoman, R.R., Williams, L.E. & Abee, C.R. (1994). Age-related hormonal differences in cycling squirrel monkeys (Saimiri boliviensis boliviensis). Am. J. Primatol. 32, 207–13.CrossRefGoogle ScholarPubMed
IUCN Red List of Threatened Species 2008: e.T19839A9023022. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T19839A9023022.en. Downloaded on 17 November 2016.CrossRefGoogle Scholar
Kendrick, K.M. & Dixson, A.F. (1983). The effect of the ovarian cycle on the sexual behaviour of the common marmoset (Callithrix jacchus). Physiol. Behav. 30, 735–42.CrossRefGoogle ScholarPubMed
Koering, M.J. (1983). Preantral follicle development during the menstrual cycle in the Macaca mulatta ovary. Am. J. Anat. 166, 429–43.CrossRefGoogle ScholarPubMed
Lang, C.M. (1967). The estrous cycle of the squirrel monkey (Saimiri sciureus). Lab. Anim. Care 17, 442–51.Google ScholarPubMed
Lass, A., Croucher, C., Lawrie, H., Margara, R. & Winston, R.M.L. (1997). Right or left ovary–which one is better? Hum. Reprod. 12, 1730–1.CrossRefGoogle ScholarPubMed
Lopes, L.H., Lucci, C.M., Garcia, M.P., Azevedo, R.B. & Báo, S.N. (2006). Light microscopical and ultrastructural characterization of black howler monkey (Alouatta caraya) ovarian follicles. Anat. Hist. Embryol. 35, 196–201.CrossRefGoogle ScholarPubMed
Lopes, G.P., Brito, A.B., Paim, F.P., Santos, R.R., Queiroz, H.L. & Domingues, S.F. (2017). Comparative characterization of the external genitalia and reproductive tubular organs of three species of the genus Saimiri Voigt, 1831 (Primates: Cebidae). Anat. Histol. Embryol. doi: 10.1111/ahe.12246 [Epub ahead of print]CrossRefGoogle ScholarPubMed
Mayor, P., Bowler, M. & Lópezâ–Plana, C. (2013). Functional morphology of the female genital organs in the peruvian red uakari monkey (Cacajao calvus ucayalii). Am. J. Primatol. 75, 545–54.CrossRefGoogle ScholarPubMed
Miller, P.B., Charlenston, J.S., Battaglia, D.E., Klein, N.A. & Soules, M.R. (1999). Morphometric analysis of primordial follicle number in pigtailed monkey ovaries: symmetry and relationship with age. Biol. Reprod. 61, 553–6.CrossRefGoogle ScholarPubMed
Nagle, C.A. & Denari, J.H. (1983). The Cebus monkey (Cebus apella). In: Hearn JP, editor. Reproduction in New World Primates, Lancaster: MTP Press, pp. 39–67.CrossRefGoogle Scholar
Nagle, C.A., Digiano, L., Paul, N., Terlato, M., Quiroga, S. & Mendizabal, A.F. (1994), Interovarian communication for the control of follicular growth and corpus luteum function in the Cebus monkey. Am. J. Primatol. 34, 19–28.CrossRefGoogle ScholarPubMed
Potashnik, G., Insler, V., Meizner, I. & Sternberg, M. (1987). Frequency, sequence and side of ovulation in women menstruating normally. Brit. Med. J. 294, 294–319.CrossRefGoogle ScholarPubMed
Pukazhenthi, B. & Wildt, D.E. (2004). Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod. Fertil. Dev. 16, 33–46.CrossRefGoogle ScholarPubMed
Reynaud, K., Fontbonne, A., Marseloo, N., Thoumire, S., Chebrout, M., de Lesegno, C.V. & Chastant–Maillard, S. (2005). In vivo meiotic resumption, fertilization and early embryonic development in the bitch. Reproduction 130:193–201.CrossRefGoogle ScholarPubMed
Scaramuzzi, R.J., Adams, N.R., Baird, D.T., Campbell, B.K., Downing, J.A., Findlay, J.K., Henderson, K.M., Martin, G.B., McNatty, K.P., McNeilly, A.S. & Tsonis, C.G. (1993). A model for follicle selection and the determination of ovulation rate in the ewe. Reprod. Fertil. Dev. 5, 459–78.CrossRefGoogle Scholar
Scalercio, S.R.R.A., Brito, A.B., Domingues, S.F.S., Santos, R.R. & Amorim, C.A. (2014). Immunolocalization of growth, inhibitory, and proliferative factors involved in initial ovarian folliculogenesis from adult common squirrel monkey (Saimiri collinsi). Reprod. Sci. 22, 68–74.CrossRefGoogle ScholarPubMed
Schiml, P.A., Mendoza, S.P., Saltzman, W., Lyons, D.M. & Mason, W.A. (1999). Annual physiological changes in individually housed squirrel monkeys (Saimiri sciureus). Am. J. Primatol. 47, 93–103.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Silva-Santos, K.C. & Seneda, M.M. (2011). Multioocyte follicles in adult mammalian ovaries. Anim. Reprod. 8, 58–67.Google Scholar
Smith, B.H. (1989). Dental development as a measure of life history in primates. Evolution 43: 683–8.CrossRefGoogle ScholarPubMed
Stankiewicz, T., Błaszczyk, B. & Udała, J. (2009). A study on the occurrence of polyovular follicles in porcine ovaries with particular reference to intrafollicular hormone concentrations, quality of oocytes and their in vitro fertilization. Anat. Hist. Embryol. 38, 233–9.CrossRefGoogle Scholar
Strier, K.B. & Ziegler, T.E. (1994). Insights into ovarian function in wild muriqui monkeys (Brachyteles arachnoides). Am. J. Primatol. 32, 31–40.CrossRefGoogle ScholarPubMed
Strier, K.B. & Ziegler, T.E. (1997). Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys (Brachyteles arachnoides). Am. J. Primatol. 42, 299–310.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Tardif, S.D., Richter, C.B. & Carson, R.L. (1985). Reproductive performance of three species of Callitrichidae. Lab. Anim. Sci. 34, 272–5.Google Scholar
Taube, D. (1980). Age at first pregnancy and reproductive outcome among colony-born squirrel monkeys (Saimiri sciureus, Brazilian). Fol. Primatol. 33, 262–72.CrossRefGoogle Scholar
Trevino, H.S. (2007). Seasonality of reproduction in captive squirrel monkeys (Saimiri sciureus). Am. J. Primatol. 69, 1001–12.CrossRefGoogle ScholarPubMed
Walker, M.L., Anderson, D.C., Herndon, J.G. & Walker, L.C. (2009). Ovarian aging in squirrel monkeys (Saimiri sciureus). Reproduction 138, 793–9.CrossRefGoogle ScholarPubMed
Wolf, R.C., O'Connor, R.F. & Robinson, J.A. (1977). Cyclic changes in plasma progestins and estrogens in squirrel monkeys. Biol. Reprod. 27, 228– 31.CrossRefGoogle Scholar