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Gestational period and reproductive cycle in Spix's yellow-toothed cavy (Galea spixii Wagler, 1831)

Abstract

Spix's yellow-toothed cavies are rodents displaying high biological and farming potential. Knowledge of cavy reproductive aspects is paramount for satisfactory breeding. This study aimed to determine the gestation length and characterize the reproductive cycle phases of Spix's yellow-toothed cavies, also investigating potential male effects on these processes. The investigated animals were categorized into three groups: Gestational follow-up (G1), with a 5:1 female-to-male enclosure ratio; estrous cycle (G2), with a 5:1 female-to-male ratio with a male confined to a cage; and G3, consisting of five females and no male. Daily colpocytological examinations were performed, with the presence of spermatozoa on the microscopy slides indicative of copulation. G1 females were separated from the male immediately after copulation, with this being considered day "zero" of the pregnancy. G2 and G3 females were evaluated for two complete estrous cycles and qualitatively assessed through vaginal smears. The gestation length of the Spix's yellow-toothed cavies averaged 59 ± 2.24 days, with a continuous polyestrous cycle lasting 14.8 ± 0.73 days in G2 and 14.6 ± 0.75 days in G3. The proestrus phase was characterized by the dominance of parabasal cells, dyes, bacteria, and leukocytes; the estrus phase, by superficial cells with the predominance of anucleate cells with and without the presence of bacteria; the metestrus phase, by parabasal cells and numerous genuine cells, neutrophils, and bacteria; and the diestrus phase, mainly by basal, parabasal, and mutant cells, as well as high amounts of vaginal mucus, neutrophils, and bacteria. The presence of a male cavy significantly influenced diestrus duration, prolonging this phase, which is potentially attributed to female progesterone production effects.

Keywords
Estrous cycle; estrus; Galea spixii; pregnancy; rodent

Resumo

O preá é um roedor com elevado potencial biológico e zootécnico a ser explorado, sendo o conhecimento sobre os aspectos reprodutivos fundamentais para que sua criação seja satisfatória. Objetivou-se determinar a duração da gestação em preás, e a caracterização das fases do ciclo reprodutivo, verificando, se existe influência da presença do macho neste processo. Os animais foram separados em três grupos: Acompanhamento gestacional (G1), 5:1, proporção de fêmea e macho no box; Ciclo estral, 5:1, com o macho preso em gaiola (G2) e cinco fêmeas em outro box sem o macho (G3). O exame colpocitológico ocorreu diariamente, identificado o espermatozoide na lâmina como cópula. As fêmeas do G1 foram separadas assim que copulavam e contadas como dia “zero” da gestação. As fêmeas do G2 e G3 foram avaliadas ao longo de dois ciclos estrais completos, avaliados qualitativamente pelo o esfregaço vaginal. O período de gestação em preás foi de 59±2,24 dias, com um ciclo poliéstrico contínuo, com duração de 14,8±0,73 dias no G2 e 14,6±0,75 dias no G3. O proestro caracterizou-se pelo predomínio de células parabasais, intermediárias, bactérias e leucócitos; o estro, células superficiais, com predomínio das anucleadas com presença ou não de bactérias; metaestro, células parabasais e grande quantidade de células intermediárias, neutrófilos e bactérias; diestro, predomínio de células basais, parabasais e intermediárias e grande quantidade de muco vaginal, neutrófilos e bactérias. A presença do macho influenciou significativamente a duração do diestro, tornando-se mais longa, fato que pode estar atrelado a influência sobre a produção de progesterona na fêmea.

Palavras-chave
Ciclo estral; estro; Galea spixii; gestação; roedor

1. Introduction

Rodents exhibit a wide variety of shapes and sizes, with particularities identifiable by their teeth, skull, and jaw. This enables these animals to carry out specific feeding, tunnel digging, and seed dispersal activities, validating their importance in many ecosystems(11 Brasil. Ministério da Saúde. Manual de controle de roedores. 2002., 22 Wolff JO, Sherman PW. Rodent Societies: An Ecological Evolutionary Perspective. Chicago: The University of Chicago Press; 2007.). Some particular life habits and reproductive diversities constitute a challenge for scientists who employ rodent species in experiments(33 Upham NS, Patterson BD. Diversification and biogeography of the Neotropical caviomorph lineage Octodontoidea (Rodentia: Hystricognathi). Molecular Phylogenetics and Evolution. 2012;63(2):417-29. https://doi.org/10.1016/j.ympev.2012.01.020
https://doi.org/10.1016/j.ympev.2012.01....
). However, several genetic, ecological, demographic, and physiological studies have applied rodents as experimental models, due to their simple management and breeding(22 Wolff JO, Sherman PW. Rodent Societies: An Ecological Evolutionary Perspective. Chicago: The University of Chicago Press; 2007.).

Cavies, encompassing rodents belonging to the family Caviidae, exhibit an elongated body, dark gray dorsal surface, and white belly. This species has achieved commercial interest due to its high farming potential, which may be explored in the near future(44 Oliveira GB, Rodrigues MN, Sousa RDS, Moura CEB, Miglino MA, Oliveira MF. Origin of the lumbosacral plexus in Galea spixii (Wagler, 1831) (Rodentia, Caviidae). Biotemas. 2014; 15;27(4):107. https://doi.org/10.5007/2175-7925.2014v27n4p107
https://doi.org/10.5007/2175-7925.2014v2...
, 55 Oliveira GB, Santos AC, Oliveira REM, Câmara FVC, Bezerra FVF, Araújo Júnior HN, Silva AVN, Oliveira MF. Artérias mesentéricas cranial e caudal do preá (Galea spixii). Acta Scientiae Veterinariae, 2015; 21;43(1):1-8. https://www.ufrgs.br/actavet/43/PUB%201297.pdf
https://www.ufrgs.br/actavet/43/PUB%2012...
). Captive cavy breeding has been carried out with the aim of furthering knowledge of this species and its maintenance requirements. Reproductive aspects, especially concerning reproductive periods and estrous cycles, are paramount in this context(66 Pinheiro MJP, Andrade SA, Cunha JN. Preservação e exploração de animais silvestres nativos: preá, cutia e mocó. Caatinga, 1989; 6(1):28-49. https://periodicos.ufersa.edu.br/caatinga/article/view/2534/4991
https://periodicos.ufersa.edu.br/caating...
, 77 Roberts M, Maliniak E, Deal M. The reproductive biology of the rock cavy, Kerodon rupestris in captivity: a study of reproductive adaptation in a tropic specialist. Mammalia, 1984; 48(2):252-266. https://doi.org/10.1515/mamm.1984.48.2.253
https://doi.org/10.1515/mamm.1984.48.2.2...
).

Vaginal cytology is a practical and non-invasive method used to obtain reproductive data(88 Bastos LV, Guimarães DA, Luz-Ramos RS, Ferreira ACS, Ohashi OM. Aspectos da citologia vaginal durante o ciclo estral de Agouti paca criada em cativeiro. Revista Brasileira de Reprodução. 2003; 27(2):294-295., 99 Marcondes FK, Bianchi FJ, Tanno AP. Determination of the estrous cycle phases of rats: some helpful considerations. Brazilian Journal of Biology [Internet]. 2002; 62(4A):609-14. https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1519-69842002000400008&lng=en&nrm=iso&tlng=en
https://www.scielo.br/scielo.php?script=...
), where smears and staining are performed with Giemsa, Methylene Blue, and Shorr dyes, constituting a relatively quick and efficient method(1010 Barbosa LP, Rodrigues MV, Neves MM, Morais DB, Melo BED, Balarini MK, Coelho CDP, Cínthia M. Caracterização da colpocitologia em capivaras (Hydrochoerus hydrochaeris). Revista Brasileira de Saúde e Produção Animal, 2007; 8(4):258-266. https://repositorio.ufba.br/bitstream/ri/1928/1/762-2976-2-PB.pdf
https://repositorio.ufba.br/bitstream/ri...
). Morphological and quantitative cell patterns are evaluated post-staining to assess the integrity of the female reproductive system(1111 Goldman JM, Murr AS, Cooper RL. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Research Part B: Developmental and Reproductive Toxicology. 2007;80(2):84-97. https://onlinelibrary.wiley.com/doi/full/10.1002/bdrb.20106.
https://onlinelibrary.wiley.com/doi/full...
, 1212 Lohmiller JJ, Swing SP. Reproduction and breeding. In: Suckow MA, Weisbroth SH, Franklin CL. The Laboratory Rat. Elsevier; 2005.). In this context, this study aimed to determine the duration of pregnancy and characterize the reproductive cycle phases of female cavies. The potential influence of males in this process was also evaluated.

2. Material and methods

Cavies were obtained from the Wild Animal Multiplication Center (CEMAS) at Universidade Federal Rural do Semi-Árido (UFERSA), registered at the Brazilian IBAMA as a scientific breeding site under number 1478912. All experiments were approved by an Institutional Research Committee (approval no. 23091.010264/2015-90).

Five non-pregnant cavy females (Group 1, G1) were allocated in 5.0 m x 4.0 m enclosures and differentiated by painting their fur with hair dye in different anatomical regions. After a 10-day adaptation period, one male was added to the group, and daily vaginal cytology tests were carried out to detect the presence of sperm and the beginning of the gestational period 24 h after encountering the male gamete. Pregnant females were separated from the group and transferred to a male-free enclosure for pregnancy monitoring.

Estrous cycle analyses were performed on ten females, five of which were maintained in an enclosure containing a male trapped in a cage (Group 2, G2), preventing fertilization, whereas the other five were maintained in an enclosure with no males (Group 3, G3). Estrous cycles were determined daily employing vaginal colpocytology smears dyed with Instant-Prov rapid panoptic dye (New Prov®) according to the manufacturer’s recommendations.

The first cycle day for females maintained in the presence of a male was considered the estrus, in which females exhibit a swollen vulva and cytological smears present mostly superficial cells. Concerning the other female group, macroscopic vulva aspects and vaginal cytology were analyzed to assess estrogenic phase features. Several microscopic fields were analyzed in each stained cytological slide, and anucleate scales, nucleated superficial cells, and intermediate, parabasal, and basal cells were counted up to a total of 100 cells. Leukocytes, bacteria, and mucus filaments were qualitatively observed through crosses, with one, two, and three crosses being associated with low, moderate, and high amounts, respectively. In total, two complete cycles were monitored for each animal.

Cell typing data were subjected to an Analysis of Variance (ANOVA) applying the least squares method (1313 Da Silva RG. Manual de procedimentos em análise por quadrados mínimos. FUNEP, Jaboticabal. 1993.) employing general linear models available in Statistical Analysis System (SAS) software(1414 SAS Institute. Statistical Analysis System. SAS User’s guide, version 8. SAS Institute Inc., Cary, North Carolina, USA. 1999.) to determine male presence and estrous cycle phase effects. Data were expressed as means ± standard errors at a p<0.05 significance level and subjected to the Shapiro-Wilk normality test (p=0.1528).

The ANOVA was based on the following mathematical model:

Y i j k = μ + M i + F j + I i j + ε i j k

Where Yijk is colpocytological analysis k performed in experimental group i during phase j of the estrous cycle; μ is the overall mean; Mi comprises the fixed effect of treatment i (i=male absent, male present); Fj is the fixed effect of phase j of the estrous cycle (j=proestrus, estrus, metestrus, diestrus); Iij is the nested effect of phase j of the estrous cycle within treatment i; and ɛijk is the residual effect that includes all other variation sources not considered in the model.

Potential male effects concerning the length of each estrous cycle phase were determined by Student's T test using SAS software. Data normality was first verified by the Shapiro-Wilk test, followed by a homoscedasticity of variances test. Non-normally distributed data were transformed into decimal base logarithms.

3. Results

Cavy pregnancies lasted about 59 days, with a standard error of 2.24 for the five analyzed females, which gave birth from one (20%) to two offspring (80%). Females exhibited a continuous polyestrous sexual cycle, averaging 14.8 ± 0.73 days (12-16) (n=5) for females maintained with a male (G2) and 14.6 ± 0.75 days (13-17) (n=5) for the group maintained in the absence of a male (G3). No statistically significant differences (p>0.05) were detected between groups (Table 1).

Table 1
Male cavy influence on female estrous cycle phase length (means ± standard errors, days).

On the other hand, when comparing each cycle phase to its respective duration and to the two experimental groups, the findings indicate that the presence of a male cavy significantly influenced the diestrus phase, which was longer in G2 (4.0 ± 0.63 days) compared to G3 (2.4 ± 0.24 days) (Table 1).

Concerning estrous cycle cellular patterns, vaginal squamous cells were observed in the decreasing maturity order of polygonal anucleate superficial cells (anucleate scales), exhibiting a delimited eosinophilic cytoplasm, with no nucleus, often found as granulations resulting from karyorrhexis (nuclear fragmentation) (Figure 1B, 1C and 1D), polygonal nucleated superficial cells with well-defined cytoplasmic limits, a slightly basophilic or eosinophilic cytoplasm and a small nucleus containing finely granular (Figure 1B) or markedly condensed (nuclear pyknosis) chromatin (Figure 1D), intermediate round to polygonal cells, a basophilic cytoplasm, poorly defined cell boundaries, a small nucleusn (albeit larger than in superficial cells), and finely granular chromatin (Figures 1A, 1E, 1F, 1G, 1H, and 1I), round basophilic parabasal cells with a moderate nucleus/cytoplasm ratio (Figure 1A, 1E, 1F, 1G, 1H, and 1I), and small round markedly basophilic basal cells with a high nucleus/cytoplasm ratio (Figure 1G, 1H, and 1I).

Figure 1
Estrous cycle phases in female cavies. Proestrus - A: Parabasal (black arrows) and intermediate (red arrows) cells, bacteria (black arrowhead), and a neutrophil (yellow arrowhead). Estrus (B, C and D) - B: Nucleated surface cells (arrows) and bacteria (arrowhead); C: Desquamation of superficial cells, presence of bacteria, and absence of leukocytes; D: Anucleate superficial cells and superficial cell containing a pyknotic nucleus (arrow). Metaestrus (E and F) - E: Parabasal cells (dashed ellipse), intermediate cells (arrows), and bacteria (arrowhead); F: Predominance of intermediate cells, parabasal cells, bacteria, and leukocytes (dashed ellipse). Diestrus (G, H and I) - G: Intermediate cells (arrows) and basal cells (dashed ellipse); H: Basal cells (deep) and bacteria (dashed ellipse); I: Mucus filaments (arrow) and binucleate intermediate cell (*).

Cavy estrous cycle phases were identified by applying these cellular patterns. The beginning of the cycle is termed proestrus, characterized by mostly parabasal and intermediate cells and the presence of bacteria and leukocytes (Figure 1A). The end of this period was similar to the estrogenic phase. The estrus phase exhibited numerous superficial cells, many times exceeding 80% of the total cell counts. Nucleated superficial cells exhibited a finely granular chromatin (Figure 1B). Nucleated scales were predominant compared to nucleated superficial scales (Figure 1B, 1C, and 1D). No leukocytes were detected in this phase, and bacteria were present in low amounts, in some cases not detected (Figure 1D).

Numerous intermediate cells, neutrophils, and bacteria were observed in the metestrus phase, followed by a standard number of parabasal cells (Figure 1E and 1F). The end of this cycle is characterized by the diestrus phase, composed mostly of basal, parabasal, and intermediate cells. Vaginal smears in the diestrus phase appear “dirty”, due to the intense production of vaginal mucus and high amounts of neutrophils and bacteria (Figure 1G, 1H, and 1I).

Enucleated and superficial nucleated scales (59.42 ± 1.48% and 15.84 ± 0.79, respectively) represented over 70% of the total cell counts in the estrus phase, while deep cells (parabasal and basal), averaging 30.65 ± 1.06% and 18.67 ± 0.87%, respectively, constituted almost half of all identified cells in the diestrus phase. Similar cell types, on the other hand, were observed in the proestrus and metestrus phases, with the predominance of superficial nucleated cells in the proestrus phase and intermediate cells in the metestrus phase (Figure 2).

Figure 2
Different cell types determined in each cavy estrous cycle phase by colpocytological analyses.

Enucleated scales were significantly influenced (p<0.05) by male cavy treatments and different between estrous cycle phases (Figure 3). A significant difference between treatments was observed in the proestrus phase, with G2 females (35.05 ± 1.97%) displaying higher amounts of enucleated scales compared to G3 females (18.00 ± 2.28%). During the estrus phase, both treatments exhibited the highest averages, 59.19 ± 2.21% for G2 females and 59.65 ± 1.97% for G3 females. G2 females exhibited lower amounts of enucleated scales in the diestrus phase (14.55 ± 1.97%). No significant enucleated scale differences between the proestrus (18.00 ± 2.28%) and diestrus (8.33 ± 2.55%) phases were observed for G3 females.

Figure 3
Effects of the presence of a male cavy on enucleated scales determined by colpocytology during different female estrous cycle phases. * The same lowercase letters within each experimental group (male present, male absent) indicate no differences from each other by the Tukey test (p<0.05). ** The same upercase letters within each phase of the estrous cycle (proestrus, estrus, metestrus, diestrus) indicate no differences from each other by the Tukey test (p<0.05).

Significant (p<0.05) interactions between treatments and estrous cycle phase were also observed for intermediate cells (Figure 4). During the proestrus phase, G3 females exhibited significantly higher intermediate cell amounts (48.73 ± 2.17%) compared to G2 females (37.85 ± 1.88%). No significant differences, however, were observed between the proestrus and metestrus phases in G3 females (46.34 ± 1.65%), with the lowest counts observed in the estrus phase (18.45 ± 1.88%). Likewise, no significant differences were observed between the proestrus (37.85 ± 1.88%), metestrus (44.05 ± 1.98%), and diestrus (30.75 ± 1.88%) phases for G2 females, with the lowest counts noted for the estrus phase (20.69 ± 2.10%).

Figure 4
Effects of the presence of a male cavy on intermediate cells as determined by colpocytology during different female estrous cycle phases. * The same lowercase letters within each experimental group (male present, male absent) indicate no differences from each other by the Tukey test (p<0.05). ** The same uppercase letters within each phase of the estrous cycle (proestrus, estrus, metestrus, diestrus) indicate no differences from each other by the Tukey test (p<0.05).

Significant effects between estrous cycle phases (p<0.05) were noted for nucleated superficial, parabasal, and basal cells. Significantly higher nucleated superficial cell counts were observed during the proestrus and estrus phases when compared to the metestrus and diestrus phases (Figure 5). The lowest counts for both parabasal (4.10 ± 0.97%) and basal (0.72 ± 0.79%) cells were noted in the estrus phase. The diestrus phase, on the other hand, was characterized by the highest parabasal (30.65 ± 1.06%) and basal cell (18.66 ± 0.86%) counts. Parabasal cell counts did not differ between the proestrus (13.03 ± 0.99%) and metestrus (16.23 ± 0.89%) phases (Figure 5).

Figure 5
Average nucleated superficial, parabasal, and basal cell counts as determined by colpocytology during different female estrous cycle phases. * The same lowercase letters within each cell type (nucleated surface, parabasal and basal) indicate no differences from each other by the Tukey test (p<0.05).

4. Discussion

Murine rodent assessments reveal a short luteal phase, agreeing with the hypothesis that implantation occurs early in the uterine horns. This has motivated gestational period characterization assessments, suggesting an initial blastocyst development in overlapping pregnancies in which females are still breastfeeding the previous litter. Herein, cavy pregnancies were evaluated for less than 10 days, contrasting with the length of non-overlapping pregnancies reported for other rodents, such as Calomys musculinus (21 days), Calomys laucha (21 days), Microtus ochorogaster (21 days), and Akodon molinae (25 days), all South American sigmodontine rodents, and Peromyscus maniculatus bairdii (25 days), a North American sigmodontine rodent(1515 Buzzio OL, Koninckx A, Carreno NB, Castro-Vazquez A. Embryo implantation during the short luteal phase of the corn mouse, Calomys musculinus, and the apparent lack of a lactional diapause in South American murid rodents. Reproduction, 2001; 1;815-23. https://dx.doi.org/10.1530/rep.0.1210815
https://dx.doi.org/10.1530/rep.0.1210815...
).

Additionally, the information converged regarding the gestation duration estimates of the species Clethrionomys glareolus, Mus musculus, and Rattus norvegicus, which were 19, 20, and 22 days, respectively(1616 Richmond M, Conaway CH. Induced ovulation and oestrus in Microtus ochrogaster. Journal of Reproduction and Fertility. 1969: Supplement 6: 357-376., 1717 Clarke JR, Hellwing S. Fertility of the post-partum bank vole (Clethrionomys glareolus). Journal of Reproduction and Fertility. 1983; 68(1): 241-246. https://doi.org/10.1530/jrf.0.0680241
https://doi.org/10.1530/jrf.0.0680241...
), and agoutis around 104 to 120 days(1818 Lange RR, Schmidt EMS. Rodentia: roedores silvestres. In: Cubas ZS, Silva JCR, Catão-Dias JL. Tratado de animais selvagens Medicina Veterinaria. Sao Paulo (Brasil) Editora Roca; 2014.). Under natural conditions, cavy gestations last 48 days(66 Pinheiro MJP, Andrade SA, Cunha JN. Preservação e exploração de animais silvestres nativos: preá, cutia e mocó. Caatinga, 1989; 6(1):28-49. https://periodicos.ufersa.edu.br/caatinga/article/view/2534/4991
https://periodicos.ufersa.edu.br/caating...
, 1919 Lacher TE. The comparative social behavior of Kerodon rupestris and Galea spixii and the evolution of behavior in the Caviidae. Bulletin of Carnegie Museum of Natural History. 1981; 17:1-71. https://doi.org/10.5962/p.228596
https://doi.org/10.5962/p.228596...
, 2020 Mares MA, Streilein KE, De La Rosa MP. Nonsynchronous Molting in Three Genera of Tropical Rodents from the Brazilian Caatinga (Thrichomys, Galea, and Kerodon). 1982; 63(3):484- 8. https://doi.org/10.2307/1380447
https://doi.org/10.2307/1380447...
), which has been employed as the reference in Galea spixii placentation studies(2121 Oliveira MF, Mess A, Ambrosio CE, Dantas CAG, Favaron PO, Miglino MA. Chorioallantoic Placentation in Galea spixii (Rodentia, Caviomorpha, Caviidae). Reproductive Biology and Endocrinology. 2008; 6(1). https://doi.org/10.1186/1477-7827-6-39
https://doi.org/10.1186/1477-7827-6-39...
). This contrasts with our results, in which the gestation length was determined as being about 59 days for this species in captivity.

The determined cervicovaginal desquamative type profiles reflect the endocrine dynamics associated with mammalian reproductive cycles. Qualitative and quantitative cell estrous cycle analyses and their associated figurative elements can, therefore, be employed to efficiently predict fertile cavy periods and, consequently, reproductive disorders(2222 Moxon R, Copley D, England GCW. Quality assurance of canine vaginal cytology: A preliminary study. Theriogenology. 2010; 74(3):479-85. https://doi.org/10.1016/j.theriogenology.2010.02.031
https://doi.org/10.1016/j.theriogenology...
).

In this regard, one study characterized the cavy estrous cycle employing 12 non-pregnant isolated females and another five maintained in the presence of a male. Two complete cycles were evaluated in the first group, with an average cycle length of 15.8 ± 1.4 days, ranging from 14 to 19 days(2323 Santos AC, Viana DC, Bertassoli BM, Oliveira GB, Oliveira DM, Bezerra FVF, Oliveira MF, Assis-Neto AC. Characterization of the estrous cycle in Galea spixii (Wagler, 1831). Pesquisa Veterinária Brasileira. 2015; 35(1):89-94. https://doi.org/10.1590/S0100-736X2015000100017.
https://doi.org/10.1590/S0100-736X201500...
). Females maintained in the presence of the male could not be evaluated, as most became fertilized. This was not an issue in the present study, as the male was maintained in a separate cage and was thus unable to fertilize the females.

In another study, the reproductive cycle of redrumped agoutis (Dasyprocta leporina) raised in captivity in the Brazilian semi-arid region was assessed by vaginal cytology associated with transabdominal ultrasounds for eight complete cycles averaging 28.2 ± 0.7 days, ranging from 24 to 31 days(2424 Campos LB, Peixoto GCX, Lima GL, Castelo TS, Souza ALP, Oliveira MF, Silva AR Monitoramento do ciclo estral de cutias (Dasyprocta leporina Lichtenstein, 1823) através de citologia esfoliativa vaginal e ultrassonografia. Pesquisa Veterinária Brasileira. 2015; 35(2):188-192. https://dx.doi.org/10.1590/S0100-736X2015000200016
https://dx.doi.org/10.1590/S0100-736X201...
). These results are similar to those reported for black-rumped agoutis (Dasyprocta prymnlopha), reported as 30.69 ± 4.65 days, ranging from 19 to 40 days(2525 Guimarães DA, Moreira D, Vale WG. Determinação do ciclo reprodutivo da cutia (Dasyprocta prymnolopha) através do diagnóstico colpocitológico. Acta Amazônica. 1997. 27(1):55-64. https://doi.org/10.1590/1809-43921997271064.
https://doi.org/10.1590/1809-43921997271...
), and 29.94 ± 6.77 days, ranging from 18 to 41 days(2626 Carreiro AN, Diniz JARA, Souza JG, Araújo DVF, Dias RFF, Azerêdo LMS, Rocha EF, Salles AYF, Peña-Alfaro CE, Carvalho MAM, Illera MJ, Menezes DJA. Ovary and vaginal epithelium dynamics during the estrous cycle in Dasyprocta prymnolopha Wagler, 1831: ultrasound and cytological examinations. Journal of veterinary science. 2018; 31(3):446-451. https://doi.org/10.4142/jvs.2018.19.3.446.
https://doi.org/10.4142/jvs.2018.19.3.44...
). Another assessment concerning black-rumped agoutis reported an average estrous cycle of 32.05 ± 4.17 days ranging from 25 to 40 days for 20 total cycles, which were non-statistically different in relation to a male effect in the experimental groups during cycles. However, most experimental groups contained adult and young females maintained alongside vasectomized males. Hormonal measurements carried out by the radioimmunoassay method indicated two concentration 17β-estradiol peaks, the first in the metestrus phase and the second in the proestrus phase, suggesting two follicular development phases. Concerning progesterone, a statistically significant difference (p˂0.05) was noted between phases, which was low in the estrus phase, increasing after 24 h and reaching the highest average in the diestrus phase(2727 Guimarães DA, Ramos RL, Ohashi OM, Garcia GW, Vale WG. Plasma concentration of progesterone and 17β-estradiol of black-rumped agouti (Dasyprocta prymnolopha) during the estrous cycle. Revista de Biologia Tropical. 2011; 59(1):29-35. https://doi.org/10.15517/rbt.v59i1.3176.
https://doi.org/10.15517/rbt.v59i1.3176...
).

In this sense, the presence of a male significantly influenced the diestrus phase in our study, which was longer (4.0 ± 0.63 days) when compared to the group of five females maintained in the absence of a male (2.4 ± 0.24 days) as determined by vaginal cytology. These findings suggest that males can influence progesterone concentrations after ovulation, subsequently acting on corpus luteum activity.

In terms of cytological findings, the criteria applied to determine each cavy reproductive cycle phase and assess cellular morphological aspects included the presence of superficial cells and anucleate scales in the estrus phase, with a minimum requirement of at least 70% representation of these squamous cell types. These cells exhibited eosinophilic cytoplasms, polygonal morphology, low nucleus/cytoplasm ratios, finely granular chromatin or a pyknotic nucleus in the case of superficial and nucleus-free cells. Furthermore, leukocytes and bacteria were detected at low concentrations or were absent.

In the metestrus phase, the predominant cell type comprised intermediate cells, followed by considerable amounts of bacteria and leukocytes. Intermediate cells varied from oval to polygonal, with a centered nucleus and dispersed and granular chromatin, in addition to a basophilic cytoplasm. In the diestrus phase, the sum of deep cells (parabasal and basal) is expected to exceed 40% and present intermediate cells as the second most prevalent cell type. Furthermore, numerous leukocyte, bacterial, and mucus infiltrates were also evident. Cavy parabasal and basal cells are both round, with a large and central nucleus, granular chromatin, and a high nucleus/ cytoplasm ratio. In the present study, however, the latter were smaller and with an intensely basophilic cytoplasm.

The onset of the proestrus phase was marked by the prevalence of intermediate cells and bacteria and mucus. The transition to estrus began when superficial cells once again reached or exceeded 70%. The morphological cellular aspects of each phase were similar to those described in agoutis(2424 Campos LB, Peixoto GCX, Lima GL, Castelo TS, Souza ALP, Oliveira MF, Silva AR Monitoramento do ciclo estral de cutias (Dasyprocta leporina Lichtenstein, 1823) através de citologia esfoliativa vaginal e ultrassonografia. Pesquisa Veterinária Brasileira. 2015; 35(2):188-192. https://dx.doi.org/10.1590/S0100-736X2015000200016
https://dx.doi.org/10.1590/S0100-736X201...
, 2525 Guimarães DA, Moreira D, Vale WG. Determinação do ciclo reprodutivo da cutia (Dasyprocta prymnolopha) através do diagnóstico colpocitológico. Acta Amazônica. 1997. 27(1):55-64. https://doi.org/10.1590/1809-43921997271064.
https://doi.org/10.1590/1809-43921997271...
, 2727 Guimarães DA, Ramos RL, Ohashi OM, Garcia GW, Vale WG. Plasma concentration of progesterone and 17β-estradiol of black-rumped agouti (Dasyprocta prymnolopha) during the estrous cycle. Revista de Biologia Tropical. 2011; 59(1):29-35. https://doi.org/10.15517/rbt.v59i1.3176.
https://doi.org/10.15517/rbt.v59i1.3176...
), capybaras(1010 Barbosa LP, Rodrigues MV, Neves MM, Morais DB, Melo BED, Balarini MK, Coelho CDP, Cínthia M. Caracterização da colpocitologia em capivaras (Hydrochoerus hydrochaeris). Revista Brasileira de Saúde e Produção Animal, 2007; 8(4):258-266. https://repositorio.ufba.br/bitstream/ri/1928/1/762-2976-2-PB.pdf
https://repositorio.ufba.br/bitstream/ri...
), pacas(88 Bastos LV, Guimarães DA, Luz-Ramos RS, Ferreira ACS, Ohashi OM. Aspectos da citologia vaginal durante o ciclo estral de Agouti paca criada em cativeiro. Revista Brasileira de Reprodução. 2003; 27(2):294-295.), and cavies(2323 Santos AC, Viana DC, Bertassoli BM, Oliveira GB, Oliveira DM, Bezerra FVF, Oliveira MF, Assis-Neto AC. Characterization of the estrous cycle in Galea spixii (Wagler, 1831). Pesquisa Veterinária Brasileira. 2015; 35(1):89-94. https://doi.org/10.1590/S0100-736X2015000100017.
https://doi.org/10.1590/S0100-736X201500...
). Figurative elements associated with colpocytological smear cells were not included in the results, and their description is limited herein to abundant bacteria, leukocytes, and mucous filaments between the metestrus and diestrus phases.

Our findings concerning the average distributions of different cell types during the estrous phase in cavies resembled those observed during the metestrus phase. Furthermore, the presence of a greater number of nucleated scales compared to nucleated superficial cells across all cycle phases suggests a maturation stage akin to that observed in agoutis(2525 Guimarães DA, Moreira D, Vale WG. Determinação do ciclo reprodutivo da cutia (Dasyprocta prymnolopha) através do diagnóstico colpocitológico. Acta Amazônica. 1997. 27(1):55-64. https://doi.org/10.1590/1809-43921997271064.
https://doi.org/10.1590/1809-43921997271...
) and dissimilar to those of cavies raised in captivity and Rock cavies (Kerodon rupestris)(2323 Santos AC, Viana DC, Bertassoli BM, Oliveira GB, Oliveira DM, Bezerra FVF, Oliveira MF, Assis-Neto AC. Characterization of the estrous cycle in Galea spixii (Wagler, 1831). Pesquisa Veterinária Brasileira. 2015; 35(1):89-94. https://doi.org/10.1590/S0100-736X2015000100017.
https://doi.org/10.1590/S0100-736X201500...
, 2828 Zogno MA. Aspectos reprodutivos da fêmea de mocó (Kerodron rupestris): Análise bioquímica dos líquidos fetais e caracterização colpocitológica do ciclo estral [Internet] [Tese]. [Faculdade de Medicina Veterinária e Zootecnia - Universidade de São Paulo]; 2002. http://www.teses.usp.br/teses/disponiveis/10/10132/tde-04042003-103133/en.php
http://www.teses.usp.br/teses/disponivei...
).

A significant effect (p<0.05) concerning enucleated scales during different estrous cycle phases was noted for both experimental groups, with the highest counts observed in the estrus phase and the lowest in the diestrus phases. This contrasts with findings reported for agoutis, where significant differences in enucleated surface cell counts were only noted in the estrus phase, with higher counts when compared to the other phases, while no difference was observed between phases(2525 Guimarães DA, Moreira D, Vale WG. Determinação do ciclo reprodutivo da cutia (Dasyprocta prymnolopha) através do diagnóstico colpocitológico. Acta Amazônica. 1997. 27(1):55-64. https://doi.org/10.1590/1809-43921997271064.
https://doi.org/10.1590/1809-43921997271...
). Concerning cavy male treatments, statistically higher scale counts were observed in the proestrus phase in the mated female group (35.05 ± 1.97%) compared to the group with no male contact (18.00 ± 2.28%).

The practice of introducing a male into a female group to synchronize the estrous cycle is paramount for various purposes, such as embryo cryopreservation, sanitary colony cleaning, and murine transgenesis(2929 Mattaraia VGM, Silva APR, Sartori DRS, Távora MFCLF, Rodrigues UP, Moreira VB, Moura ASAMT. Efeito macho na indução do estro em ratas Wistar (Rattus norvegicus). Veterinária e Zootecnia. 2009; 16(4):669-677. https://rvz.emnuvens.com.br/rvz/article/view/1266
https://rvz.emnuvens.com.br/rvz/article/...
). In the case of goats and sheep, reproductive performance is directly tied to the profitability of milk and meat production, considering the economic, environmental, and sociological significance of these animals(3030 Rancourt M, Fois N, Lavín MP, Tchakérian E, Vallerand F. Mediterranean sheep and goat production: An uncertain future. Small Ruminant Research. 2006; 62(3):167-179. https://www.sciencedirect.com/science/article/abs/pii/S0921448805003433
https://www.sciencedirect.com/science/ar...
). Therefore, synchronizing estrous cycles offers substantial benefits to livestock producers(3131 Gonzalez-Bulnes A, Veiga-Lopez A, Garcia P, Garcia-Garcia RM, Ariznavarreta C, Sanchez MA, Tresguerres JA, Cocero MJ, Flores JM. Effects of progestogens and prostaglandin analogues on ovarian function and embryo viability in sheep. Theriogenology. 2005; 63(9):2523-2534. https://doi.org/10.1016/j.theriogenology.2004.10.013
https://doi.org/10.1016/j.theriogenology...
).

Although a limited body of research is available on estrus induction in wild rodents, exploring this area could potentially enhance their reproductive control. For instance, the use of prostaglandin alone or associated with the GnRH analogue for estrus induction displays limited efficiency in both agoutis(3232 Peixoto GCX, Maia KM, Almeida LM, Campos LB, Oliveira GB, Oliveira MF, Brito AB, Domingues SFS, Silva AR. Indução do estro em cutias (Dasyprocta leporina) utilizando-se protocolos à base de prostaglandina isolada ou em associação com análogo de GnRH. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2018; 70 (3), 806-814. https://doi.org/10.1590/1678-4162-9907
https://doi.org/10.1590/1678-4162-9907...
) and guinea pigs(3333 Grégoire A, Allard A, Huamán E, León S, Silva RM, Buff S, Berard M, Joly T. Control of the estrous cycle in guinea-pig (Cavia porcellus). Theriogenology. 2012; 78(4), 842-847. https://doi.org/10.1016/j.theriogenology.2012.03.034
https://doi.org/10.1016/j.theriogenology...
). This underscores the need to standardize protocols for better reproductive efficiency in captivity.

Cycle synchronization was not evident for cavies in the present study, although the presence of a male was both directly and indirectly associated with estrogenic stimulation during the proestrus phase. This, in turn, led to an increase in the vaginal epithelium, which tends to stratify from the most differentiated layers, resulting in the desquamation of superficial anucleate cells. In one study in this regard, female rock cavies maintained with a male exhibited statistically different enucleated scale counts in the estrus phase when compared to the other phases according to the Tukey test(2828 Zogno MA. Aspectos reprodutivos da fêmea de mocó (Kerodron rupestris): Análise bioquímica dos líquidos fetais e caracterização colpocitológica do ciclo estral [Internet] [Tese]. [Faculdade de Medicina Veterinária e Zootecnia - Universidade de São Paulo]; 2002. http://www.teses.usp.br/teses/disponiveis/10/10132/tde-04042003-103133/en.php
http://www.teses.usp.br/teses/disponivei...
). This contrasts with our data, as significant enucleated scale differences were observed in all cycle phases in both treatment groups.

Concerning intermediate cells, significant interaction effects between treatments were also observed in the proestrus phase. However, the male-free group exhibited higher intermediate cell percentages (48.73 ± 2.17%) compared to G3 females (37.85 ± 1.88%). Less shedding of superficial anucleate cells was also noted in the G3 group, probably due to lower circulating estrogens. This, in turn, may lead to more intermediate cells due to higher progesterone levels and, consequently, greater intermediate cell detachment. Furthermore, the G3 proestrus and metestrus phases exhibited the highest intermediate cell counts, with no significant differences. However, significant differences were noted when comparing the diestrus and estrus phases, with the latter exhibiting the lowest intermediate cell counts.

In G2 females, the estrus phase also showed the lowest cell counts, differing significantly from the other phases but not between each other. The metestrus phase exhibited the highest intermediate cell counts, similar to that reported for agoutis(2525 Guimarães DA, Moreira D, Vale WG. Determinação do ciclo reprodutivo da cutia (Dasyprocta prymnolopha) através do diagnóstico colpocitológico. Acta Amazônica. 1997. 27(1):55-64. https://doi.org/10.1590/1809-43921997271064.
https://doi.org/10.1590/1809-43921997271...
) and pacas(2727 Guimarães DA, Ramos RL, Ohashi OM, Garcia GW, Vale WG. Plasma concentration of progesterone and 17β-estradiol of black-rumped agouti (Dasyprocta prymnolopha) during the estrous cycle. Revista de Biologia Tropical. 2011; 59(1):29-35. https://doi.org/10.15517/rbt.v59i1.3176.
https://doi.org/10.15517/rbt.v59i1.3176...
). In these animals, intermediate cell counts differed significantly from the other cycle phases, but not from each other. Furthermore, higher nucleated superficial cell counts were expected in the proestrus and estrus phases in cavies, as greater cell differentiation and proliferation stimulation are noted during these phases due to higher estrogen concentrations. As ovulation takes place during the luteinizing hormone peak in the estrus phase, the highest average percentage of this cell type was detected during this phase, although not statistically different from the preceding phase and differing from the other phases. This corroborates reproductive agouti data except for the proestrus phase findings(2525 Guimarães DA, Moreira D, Vale WG. Determinação do ciclo reprodutivo da cutia (Dasyprocta prymnolopha) através do diagnóstico colpocitológico. Acta Amazônica. 1997. 27(1):55-64. https://doi.org/10.1590/1809-43921997271064.
https://doi.org/10.1590/1809-43921997271...
).

A significant parabasal cell production difference was noted between the diestrus phase and the other cycle phases. However, no difference was observed between the metestrus and proestrus phases, with the lowest production occurring in estrus. Similar results were observed for basal cells, which was higher in the diestrus phase and significantly different (p˃0.05) from the other phases. However, each cycle phase was significantly different, with lower basal cell production in the estrus phase. The observed diestrus phase pattern is consistent with high circulating progesterone concentrations, inducing a thinner vaginal epithelium, which results in a thin germinal layer of deep cells(3434 Westwood FR. The female rat reproductive cycle: a practical histological guide to staging. Toxicologic Pathology. 2008; 36(3):375-384. https://doi.org/10.1177/0192623308315665
https://doi.org/10.1177/0192623308315665...
).

5. Conclusion

Cavy gestation typically lasted 59 days, resulting in the birth of one to two pups at a time. Female cavies exhibit a continuous polyestrous sexual cycle, lasting about 14.8 ± 0.73 days when exposed to a male and 14.6 ± 0.75 days when kept without a male. The presence of a male did not influence cycle length. The reproductive cycle in cavies is similar to that of other cavids, being categorized as the proestrus, estrus, metestrus, and diestrus phases. The absence of a male significantly influenced the number of intermediate and enucleated superficial cells during the proestrus phase. Conversely, the presence of a male extended the diestrus phase duration, which may be associated with high progesterone levels and reduced circulating estrogen levels.

Acknowledgements

The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES, Finance Code 001) for the doctoral fellowship granted to the Graduate Program in Animal Science (PPGCA-UFERSA).

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Publication Dates

  • Publication in this collection
    20 Nov 2023
  • Date of issue
    2023

History

  • Received
    17 July 2023
  • Accepted
    04 Sept 2023
  • Published
    09 Oct 2023
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