Skip to main content Accessibility help

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

  • Gerson P. Lopes (a1) (a2), Regiane R. Santos (a3), Débora V. Almeida (a1), Adriel B. Brito (a1), Helder L. Queiroz (a2) and Sheyla F. S. Domingues (a1)...


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.


Corresponding author

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:


Hide All
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.
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.
Baker, T.G. & Wai, S.O. (1976). Developmental of the ovary and oogenesis. Clin. Obstet. Gynecol. 3, 326.
Baldwin, J.D. (1969). The ontogeny of social behaviour of squirrel monkeys (Saimiri sciureus) in a seminatural environment. Fol. Primatol. 11, 161–84.
Boinski, S. (1992). Monkeys with inflated sex appeal. Nat. Hist. 101, 42–9.
Brand, H.M. (1981). Urinary oestrogen excretion in the female cotton–topped tamarin (Saguinus oedipus oedipus). J. Reprod. Fertil 62, 467–73.
Braw-Tal, R. (2002). The initiation of follicle growth: the oocyte or the somatic cells? Mol. Cell Endocrinol. 187, 11–8.
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.
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.
Cahill, L.P., Mariana, J.C. & Mauléon, P. (1979). Total follicular populations in ewes of high and low ovulations rates. J. Reprod. Fertil. 55, 2736.
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, 7989.
Dixson, A.F. (1983). The owl monkey. In Reproduction in New World Primates (ed. Hearn, J.P.), pp. 69113. Lancaster: MTP Press.
Dixson, A.F. (2001). The evolution of neuroendocrine mechanisms regulating sexual behaviour in female primates. Reprod. Fertil. Dev. 13, 599607.
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, 495501.
Erickson, B.H. (1966). Development and senescence of the postnatal bovine ovary. J. Anim. Sci. 25, 800–5.
Erickson, B.H., Reynolds, R.A. & Murphree, R.L. (1976). Ovarian characteristics and reproductive performance of the aged cow. Biol Reprod. 15, 555–60.
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.
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.
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.
Gougeon, A. (1981). Frequent occurrence of multiovular follicles and multinuclear oocytes in the adult human ovary. Fertil. Steril. 35, 417–22.
Gougeon, A. (1996). Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrinol. Rev. 17, 121–55.
Graham, C.E. & Bradley, C.F. (1971). Polyovular follicles in squirrel monkeys after prolonged diethylstilboestrol treatment. J. Reprod. Fertil. 27, 181–5.
Harrison, R.G. (1949). The comparative anatomy of the blood–supply of the mammalian testis. Proc. Zool. Soc. Lond. 119, 325–44.
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, 151.
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.
IUCN Red List of Threatened Species 2008: e.T19839A9023022. Downloaded on 17 November 2016.
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.
Koering, M.J. (1983). Preantral follicle development during the menstrual cycle in the Macaca mulatta ovary. Am. J. Anat. 166, 429–43.
Lang, C.M. (1967). The estrous cycle of the squirrel monkey (Saimiri sciureus). Lab. Anim. Care 17, 442–51.
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.
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, 196201.
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]
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.
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.
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. 3967.
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, 1928.
Potashnik, G., Insler, V., Meizner, I. & Sternberg, M. (1987). Frequency, sequence and side of ovulation in women menstruating normally. Brit. Med. J. 294, 294319.
Pukazhenthi, B. & Wildt, D.E. (2004). Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod. Fertil. Dev. 16, 3346.
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 130:193201.
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.
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, 6874.
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, 93103.
Silva-Santos, K.C. & Seneda, M.M. (2011). Multioocyte follicles in adult mammalian ovaries. Anim. Reprod. 8, 5867.
Smith, B.H. (1989). Dental development as a measure of life history in primates. Evolution 43: 683–8.
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.
Strier, K.B. & Ziegler, T.E. (1994). Insights into ovarian function in wild muriqui monkeys (Brachyteles arachnoides). Am. J. Primatol. 32, 3140.
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, 299310.
Tardif, S.D., Richter, C.B. & Carson, R.L. (1985). Reproductive performance of three species of Callitrichidae. Lab. Anim. Sci. 34, 272–5.
Taube, D. (1980). Age at first pregnancy and reproductive outcome among colony-born squirrel monkeys (Saimiri sciureus, Brazilian). Fol. Primatol. 33, 262–72.
Trevino, H.S. (2007). Seasonality of reproduction in captive squirrel monkeys (Saimiri sciureus). Am. J. Primatol. 69, 1001–12.
Walker, M.L., Anderson, D.C., Herndon, J.G. & Walker, L.C. (2009). Ovarian aging in squirrel monkeys (Saimiri sciureus). Reproduction 138, 793–9.
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.


Related content

Powered by UNSILO

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

  • Gerson P. Lopes (a1) (a2), Regiane R. Santos (a3), Débora V. Almeida (a1), Adriel B. Brito (a1), Helder L. Queiroz (a2) and Sheyla F. S. Domingues (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.