Citation: Cardoso, D.d.L.;
Guimarães, D.A.d.A.; Mayor, P.;
Ferreira, M.A.P.; Coutinho, L.N.;
Monteiro, F.O.B. Follicular Atresia,
Cell Proliferation, and Anti-Mullerian
Hormone in Two Neotropical
Primates (Aotus nancymae and Sapajus
macrocephalus). Animals 2023, 13, 1051.
https://doi.org/10.3390/
ani13061051
Academic Editor: Giuseppina Basini
Received: 7 December 2022
Revised: 29 December 2022
Accepted: 7 February 2023
Published: 14 March 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
animals
Article
Follicular Atresia, Cell Proliferation, and Anti-Mullerian
Hormone in Two Neotropical Primates (Aotus nancymae and
Sapajus macrocephalus)
Deise de Lima Cardoso
1,2
, Diva Anélie de Araújo Guimarães
1
, Pedro Mayor
2,3
,
Maria Auxiliadora Pantoja Ferreira
1
, Leandro Nassar Coutinho
2
and Frederico Ozanan Barros Monteiro
2,
*
1
Programa de pós-graduação em Ciência Animal, Universidade Federal do Pará, Rua Augusto Corrêa 01,
Belém 66075-110, Brazil
2
Programa de Pós-Graduação em Saúde e Produção Animal na Amazônia, Universidade Federal Rural
da Amazônia, Av. Perimetral 2501, Belém 66077-830, Brazil
3
Departament de Sanitat i Anatomia Animals, Facultat de Veterinària, Campus de la UAB,
Universidade Autónoma de Barcelona, Plaça Cívica, 08193 Barcelona, Spain
* Correspondence: frederico.monteiro@ufra.edu.br; Tel.: +55-(91)-99181-9493
Simple Summary: Reproductive processes in Neotropical primates are still poorly understood.
Complications arising in these processes may result in a compromised reproductive condition for a
significant portion of these species. We evaluated the follicular atresia, cell proliferation, and anti-
Mullerian hormone presence in two Neotropical primates, and in three sexual phases (follicular, luteal,
and gestational). Our results contribute to a greater understanding of the ovary morphofunctional
processes that act in follicular selection, recruitment, and degeneration in these species.
Abstract: This study evaluated the follicular atresia, cell proliferation, and anti-Mullerian hormone
action in Aotus nancymae and Sapajus macrocephalus during three sexual phases (follicular, luteal, and
gestational). Follicular quantification and immunolocalization of Caspase-3 protein, B-cell lymphoma
2 (BCL-2), proliferating cell nuclear antigen (PCNA), and anti-Mullerian hormone (AMH) were
performed. A significant difference in the quantification between preantral and antral follicles, with a
progressive decrease in the antrals, was identified. Protein and hormonal markers varied significantly
between follicle cell types (A. nancymae p = 0.001; S. macrocephalus, p = 0.002). Immunostaining in
the preantral and antral follicles was present in all sexual phases; for Caspase-3, in granulosa cells,
oocytes, and stroma; for BCL-2, in granulosa cells, oocytes, and theca; and for PCNA and AMH, in
oocytes and granulosa cells. The immunostaining for Caspase-3 was more expressive in the preantral
follicles (follicular phase, p < 0.05), while that for BCL-2 and PCNA was more expressive in the antral
follicles of the follicular phase. The AMH was more expressive in the primary and antral follicles of
nonpregnant females, in both the follicular and luteal phases. Our results contribute to understanding
the ovarian follicular selection, recruitment, and degeneration of these species.
Keywords: owl monkey; night monkey; capuchin monkey; ovary; folliculogenesis; apoptosis
1. Introduction
In recent years, there has been an increase in reproductive studies focusing on owl or
night monkeys (Aotus spp.) [1–6] and capuchin monkeys (Sapajus spp. and Cebus spp.) [4,7,8].
There are behavioral differences between the primates, such as their mating systems. Owl
monkeys are monogamous [9], while capuchin monkeys are polygamous [10]. Their shared
reproductive characteristics include the presence of a menstrual cycle [4] and the ability to
easily reproduce in captivity [11]. In both species, it has been observed that during follicular
maturation, granulosa cells, theca cells, and oocytes develop a process of cellular death,
Animals 2023, 13, 1051. https://doi.org/10.3390/ani13061051 https://www.mdpi.com/journal/animals