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Correlation between estrus onset and ovarian parameters in dairy goats

Abstract

This study assessed the effects of social dominance on the behavioral estrus and ovarian parameters of dairy goats subjected to synchronous estrus induction during the non-breeding season. Synchronous estrus was induced in 23 dairy goats allocated to collective pens. Ovarian ultrasonography was performed at 12 h intervals from device removal to ovulation. Upon estrus onset (EO) detection, the goats were immediately removed from the pens. Dominance was scored according to EO in relation to device removal in each pen, with HD - high dominants (<36 h; n = 8), MD - medium dominants (36 to 48 h; n = 10) and LD - low dominants (>48 h; n = 5). Goats in estrus underwent flexible time artificial insemination (FxTAI) according to EO. The estrus response was 100.0%. The interval to estrus was longer (P<0.05) in LD (53.7 ± 6.5 h) than in MD (37.9 ± 5.5 h) and HD goats (32.3 ± 6.6 h), while the interval from device removal to ovulation was similar (P>0.05) among all groups. The interval from EO to FxTAI was longer in HD goats compared to the other groups (P<0.05). In conclusion, although social hierarchy influenced the time of EO, the ovarian parameters, including ovulation, were not affected.

Keywords:
goats; estrus behavior; follicular dynamics; social hierarchy; ovulation

Resumo

Este estudo avaliou os efeitos da dominância social sobre o comportamento do estro e os parâmetros ovarianos de cabras leiteiras submetidas à indução sincronizada do estro durante a estação não reprodutiva. A sincronização foi induzida em 23 cabras leiteira alocadas em baias coletivas. A ultrassonografia foi realizada em intervalos de 12 horas desde a remoção do dispositivo até a ovulação. Após a detecção do início do estro (EO), as cabras foram imediatamente removidas dos currais. A dominância foi pontuada de acordo com EO em relação à remoção do dispositivo, sendo: HD - alto dominante (<36 h; n = 8), MD - médio dominante (36 a 48 h; n = 10) e LD - baixo dominante (>478 h; n = 5). As cabras em estro foram inseminadas artificialmente em tempo flexível (FxTAI). O intervalo de estro foi maior (P<0,05) em LD (53,7 ± 6,5 h) do que em MD (37,9 ± 5,5 h) e cabras HD (32,3 ± 6,6 h), por sua vez, o intervalo entre a remoção do dispositivo e a ovulação foi semelhante (P> 0,05) em todos os grupos. O intervalo de EO a FxTAI foi maior em cabras HD quando comparado aos outros grupos (P<0,05). Em conclusão, embora a hierarquia social tenha influenciado o tempo de início do estro, os parâmetros ovarianos incluindo a ovulação não foram afetados.

Palavras-chave:
caprino; dinâmica folicular; hierarquia social; manifestação de estro; ovulação

Introduction

In tropical weather conditions, Saanen goats show reproductive seasonality as they are in the anestrus condition in spring(11 Balaro MFA, Mello SGV, Santos AS, Cavalcanti LM, Almosny NRP, Fonseca JF, Brandão FZ. Reproductive seasonality in Saanen goats kept under tropical conditions. Tropical Animal Health and Production. 2018; 51 (2):345-353. Available from: https://doi.org/10.1007/s11250-018-1696-2
https://doi.org/10.1007/s11250-018-1696-...
). Specialized breeds, including Saanen, require reproductive management to ensure sufficient milk production throughout the year. The implementation of a flexible time artificial insemination (FxTAI) program is key to overcoming this challenge(22 Fonseca JF, Souza-Fabjan JMG, Oliveira MEF, Cruz RC, Esteves L, Paiva MPSLM, Brandão FZ, Mancio AB. Evaluation of cervical mucus and reproductive efficiency of seasonally anovular dairy goats after short-term progestagen-based estrus induction protocols with different gonadotropins. Reproductive Biology. 2017; 17(4): 363-369. Available from: https://doi.org/10.1016/j.repbio.2017.10.002
https://doi.org/10.1016/j.repbio.2017.10...
). The use of reproductive biotechniques, such as the application of exogenous hormones, is hereby essential to achieving higher rates of estrus response and synchrony to guarantee the efficiency of a FxTAI program(22 Fonseca JF, Souza-Fabjan JMG, Oliveira MEF, Cruz RC, Esteves L, Paiva MPSLM, Brandão FZ, Mancio AB. Evaluation of cervical mucus and reproductive efficiency of seasonally anovular dairy goats after short-term progestagen-based estrus induction protocols with different gonadotropins. Reproductive Biology. 2017; 17(4): 363-369. Available from: https://doi.org/10.1016/j.repbio.2017.10.002
https://doi.org/10.1016/j.repbio.2017.10...
). However, even with the use of hormonal protocols, small ruminants present a high degree of estrus onset dispersion(33 Gómez JD, Balasch S, Gómez LD, Martino A, Fernández N. A Comparison between intravaginal progestogen and melatonin implant treatments on the reproductive efficiency of ewes. Small Ruminants Research. 2006; 66:156-163. Avaiable from: https://doi.org/10.1016/j.smallrumres.2005.08.020
https://doi.org/10.1016/j.smallrumres.20...
).

Sequential transrectal ultrasound examinations have been used to identify ovarian follicular dynamics in dairy goats, using the associated ovulation parameters to conduct comparisons of how each animal responds to synchronous estrus induction protocols(44 Fonseca JF, Alvim GP, Souza-Fabjan JMG, Oliveira MEF, Brair VL, Brandão FZ, Facó O. Reproductive features and use of an anti-inflammatory drug in estrus-induced dairy goats artificially inseminated in a standing position with cervix immobilization. Reproductive Biology 2017; 17(3):268-273. Available from: https://doi.org/10.1016/j.repbio.2017.07.002
https://doi.org/10.1016/j.repbio.2017.07...
, 55 Bonato GC, Maia ALRS, Côrtes LR, Oliveira TA, Arrais AM, Figueira LM, Oliveira MEF, Souza-Fabjan JMG, Fonseca JF. Effects of d-cloprostenol administrations with 7.5 and 11.5-day intervals between administrations on pregnancy rates after artificial insemination in estrus cyclic dairy goats. Animal Reproduction Science. 2019; 209:106172. Available from: https://doi.org/10.1016/j.anireprosci.2019.106172
https://doi.org/10.1016/j.anireprosci.20...
, 66 Andrade ABP, Morais MCC, Rangel PSC, Oliveira MEF, Souza-Fabjan JMG, Fonseca JF. Effect of eCG in a short-term synchronization treatment on ovarian status, estrus synchrony, and ovulation in dairy goats managed under tropical conditions. Tropical Animal Health and Production. 2021; 53(2):246. Available from: https://doi.org/10.1007/s11250-021-02699-y
https://doi.org/10.1007/s11250-021-02699...
). The combination of ovarian parameters with estrus behavioral characteristics has been used to define the most appropriate time to apply artificial insemination and achieve high pregnancy rates(77 Maia ALRS, Brandão FZ, Souza-Fabjan JMG, Balaro MFA, Oliveira MEF, Facó O, Fonseca JF. Reproductive parameters of dairy goats after receiving two doses of d-cloprostenol at different intervals. Animal Reproduction Science. 2017; 181:16-23. Available from: https://doi.org/10.1016/j.anireprosci.2017.02.013
https://doi.org/10.1016/j.anireprosci.20...
, 55 Bonato GC, Maia ALRS, Côrtes LR, Oliveira TA, Arrais AM, Figueira LM, Oliveira MEF, Souza-Fabjan JMG, Fonseca JF. Effects of d-cloprostenol administrations with 7.5 and 11.5-day intervals between administrations on pregnancy rates after artificial insemination in estrus cyclic dairy goats. Animal Reproduction Science. 2019; 209:106172. Available from: https://doi.org/10.1016/j.anireprosci.2019.106172
https://doi.org/10.1016/j.anireprosci.20...
, 88 Carvalho-de-Paula CJ, Souza-Fabjan JMG, Gonçalves JD, Dias JH, Souza GN, Oliveira MEF, Fonseca JF. Effect of a 12-h increment in the short-term treatment regimen on ovarian status, estrus synchrony, and pregnancy rate in artificially inseminated dairy goats. Animal Reproduction Science. 2020; 221. Available from: https://doi.org/10.1016/j.anireprosci.2020.106571
https://doi.org/10.1016/j.anireprosci.20...
). The final benchmark of a synchronous estrus induction protocol is the time of device withdrawal. This parameter was taken into account in the development of the FxTAI strategy in dairy goats(99 Fonseca, J. F. Inseminação Artificial Transcervical em Tempo Flexível (IATFx) em cabras leiteiras. Sobral: Embrapa Caprinos e Ovinos, 2020. 13 p. il. color. (Embrapa Caprinos e Ovinos. Circular Técnica, 49). Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/221325/1/CNPC-2020-Art.53.pdf
http://ainfo.cnptia.embrapa.br/digital/b...
). It is known that the onset of estrus after device removal can be susceptible to the effect of social hierarchy, which determines the efficiency and fertility of goats(88 Carvalho-de-Paula CJ, Souza-Fabjan JMG, Gonçalves JD, Dias JH, Souza GN, Oliveira MEF, Fonseca JF. Effect of a 12-h increment in the short-term treatment regimen on ovarian status, estrus synchrony, and pregnancy rate in artificially inseminated dairy goats. Animal Reproduction Science. 2020; 221. Available from: https://doi.org/10.1016/j.anireprosci.2020.106571
https://doi.org/10.1016/j.anireprosci.20...
). However, no information on ovulatory parameters in relation to social hierarchy has been recorded for synchronous estrus-induced dairy goats.

The social hierarchy effect on productivity can be substantial, depending on the species and the production system(1010 Barroso FG, Alados CL, Boza J. Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science. 2000; 69 (1):35-53. Available from: https://doi.org/10.1016/S0168-1591(00)00113-1
https://doi.org/10.1016/S0168-1591(00)00...
). Dominance is determined by a variety of features(1111 Miranda-de la Lama, GC, Mattiello S. The importance of social behaviour for goat welfare in livestock farming. Small Ruminant Research. 2010; 90 1-10. Available from: https://doi.org/10.1016/j.smallrumres.2010.01.006
https://doi.org/10.1016/j.smallrumres.20...
) and has been defined as the relationship between individuals in situations of dispute, wherein one is dominant and the other is subordinate(1212 Kaufmann, J. H. On the definition and functions of dominance and territoriality. Biological Reviews. 1983; 58 (1):1-20. Available from: https://doi.org/10.1111/j.1469-185X.1983.tb00379.x
https://doi.org/10.1111/j.1469-185X.1983...
). This hierarchy can be observed in access to resources such as food, resting places, shade, and mates(1010 Barroso FG, Alados CL, Boza J. Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science. 2000; 69 (1):35-53. Available from: https://doi.org/10.1016/S0168-1591(00)00113-1
https://doi.org/10.1016/S0168-1591(00)00...
). In a natural environment, the dominant females are normally the most actively reproductive(1313 Côté, SD, Festa-Bianchet M. Reproductive Success in Female Mountain Goats: The Influence of Age and Social Rank. Animal Behaviour. 2001; 62 (1):173-181. Available from: http://dx.doi.org/10.1006/anbe.2001.1719
http://dx.doi.org/10.1006/anbe.2001.1719...
) and partially or completely suppress the reproductive behavior and breeding of their subordinate counterparts. In studies on domestic animals, although dominance is recognized,(1010 Barroso FG, Alados CL, Boza J. Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science. 2000; 69 (1):35-53. Available from: https://doi.org/10.1016/S0168-1591(00)00113-1
https://doi.org/10.1016/S0168-1591(00)00...
, 1313 Côté, SD, Festa-Bianchet M. Reproductive Success in Female Mountain Goats: The Influence of Age and Social Rank. Animal Behaviour. 2001; 62 (1):173-181. Available from: http://dx.doi.org/10.1006/anbe.2001.1719
http://dx.doi.org/10.1006/anbe.2001.1719...
) its influence on reproduction remains unclear. Nonetheless, it is well known that small ruminants express social hierarchy behavior in the herd(1010 Barroso FG, Alados CL, Boza J. Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science. 2000; 69 (1):35-53. Available from: https://doi.org/10.1016/S0168-1591(00)00113-1
https://doi.org/10.1016/S0168-1591(00)00...
), and social dominance may play an essential role in reproductive management(1414 Zuñiga-Garcia S, Meza-Herrera CA, Mendoza-Cortina A, Otal-Salaverri J, Perez-Marin C, Lopez-Flores NM, Carrillo E, Calderon-Leyva G, Gutierrez-Guzman UN, Veliz-Deras FG. Effect of Social Rank upon Estrus Induction and Some Reproductive Outcomes in Anestrus Goats Treated With Progesterone + ECG. Animals. 2020; 10 (7):1125. Available from: https://doi.org/10.3390/ani10071125
https://doi.org/10.3390/ani10071125...
).

We hypothesize that in synchronous estrus-induced dairy goats, the hierarchical order influences the onset of estrus, but not the ovarian follicular dynamics and ovulation parameters. Specifically, this study aims to compare the reproductive parameters of dairy goats submitted to synchronous estrus induction and classified in order of dominance according to the onset of estrus.

Material and Methods

This study was conducted under the principles of the Brazilian Society of Laboratory Animal Science and was approved by the Ethics Committee for the Use of Animals of Universidade Federal Fluminense under protocol #6405230719. It was carried out at Embrapa, in Coronel Pacheco (21º 35’S and 43º 15’ W), Minas Gerais state, Brazil, in the non-breeding season. All goats were equally kept in collective pens and managed in an intensive system under natural photoperiod at room temperature. The animals were fed with corn silage and received a balanced concentrated supplement. Mineralized salt (Caprinofós® Tortuga, São Paulo, Brazil) and water were available ad libitum.

A total of 23 clinically healthy multiparous dairy goats were used, with body condition scores of 3.0 ± 0.4 (on a scale from 1 to 5, where 1 = very thin and 5 = very fat) and a body weight of 58.2 ±13.2 kg. Goats were subjected to short-term progestogen synchronous estrus induction(88 Carvalho-de-Paula CJ, Souza-Fabjan JMG, Gonçalves JD, Dias JH, Souza GN, Oliveira MEF, Fonseca JF. Effect of a 12-h increment in the short-term treatment regimen on ovarian status, estrus synchrony, and pregnancy rate in artificially inseminated dairy goats. Animal Reproduction Science. 2020; 221. Available from: https://doi.org/10.1016/j.anireprosci.2020.106571
https://doi.org/10.1016/j.anireprosci.20...
). After device removal, estrus detection was performed twice daily over 120 min (30 min per pen) for three days. According to the estrus onset recorded in each pen, the animals were categorized into three groups: HD (high dominants; <36 h; n = 8), MD (medium dominants; 36 to 48 h; n = 10) and LD (low dominants; >48 h; n = 5)(1515 Ungerfeld R, González-Pensado S, Dago AL, Vilariño M, Menchaca A. Social Dominance of Female Dairy Goats and Response to Oestrus Synchronisation and Superovulatory Treatments. Applied Animal Behaviour Science. 2007; 105:115 - 121. 10. Available from: https://doi.org/10.1016/j.applanim.2006.06.008
https://doi.org/10.1016/j.applanim.2006....
). Females in estrus were removed from their pens at estrus onset and underwent FxTAI(88 Carvalho-de-Paula CJ, Souza-Fabjan JMG, Gonçalves JD, Dias JH, Souza GN, Oliveira MEF, Fonseca JF. Effect of a 12-h increment in the short-term treatment regimen on ovarian status, estrus synchrony, and pregnancy rate in artificially inseminated dairy goats. Animal Reproduction Science. 2020; 221. Available from: https://doi.org/10.1016/j.anireprosci.2020.106571
https://doi.org/10.1016/j.anireprosci.20...
).

Ovarian follicular dynamics were assessed every 24 h from the day of device insertion to the day of removal and every 12 h from device removal to ovulation. All ultrasound exams were done by the same experienced operator using ultrasound equipment (Mindray® M5Vet, Shenzhen, China) coupled with a 7.5 MHz linear transducer. The following ovarian parameters were calculated: follicular wave emergence time after device insertion or removal (the day a follicle reached 3 mm in diameter followed by an increase to 4 mm the next day) (h); estrus response (%); interval from device insertion and removal to estrus onset (h); interval from device insertion and removal to ovulation (h); interval from estrus onset to ovulation (h); animals ovulating (%); interval from follicular wave emergence to ovulation (h); diameter of the largest and second-largest ovulatory follicle (mm); average diameter of ovulatory follicle (mm); number of ovulations (total number of ovulations/animals that ovulated × 100); number of corpora lutea (CL) on Day 7 after estrus onset; interval from device removal to FxTAI (h); and interval from estrus onset to FxTAI (h); and pregnancy (%).

Statistical analysis was performed, whereby P < 0.05 considered as significant. Parametric variables were subjected to one-way ANOVA, followed by a Tukey test, and non-parametric variables were subjected to a Kruskal-Wallis test, using a Dunn test to determine differences. The results are described as mean ± S.E.M.

Results and Discussion

This study characterized for the first time the ovarian follicular parameters preceding and after device removal in synchronous estrus-induced dairy goats in relation to their social hierarchy. The ovarian follicular wave pattern was associated before and after device removal with ovulation. For the first time, this association was compared in goats presenting estrus early or late in relation to sponge removal in each pen. Some studies applying estrus synchronization(33 Gómez JD, Balasch S, Gómez LD, Martino A, Fernández N. A Comparison between intravaginal progestogen and melatonin implant treatments on the reproductive efficiency of ewes. Small Ruminants Research. 2006; 66:156-163. Avaiable from: https://doi.org/10.1016/j.smallrumres.2005.08.020
https://doi.org/10.1016/j.smallrumres.20...
) and synchronous estrus induction(1616 Pietroski ACCA, Brandão FZ, Souza JMG, Fonseca JF. Short, Medium or Long-Term Hormonal Treatments for Induction of Synchronized Estrus and Ovulation in Saanen Goats during the Nonbreeding Season. Revista Brasileira de Zootecnia. 2013; 42 (3):168-173. Available from: https://doi.org/10.1590/S1516-35982013000300004
https://doi.org/10.1590/S1516-3598201300...
) have reported that the interval to estrus in relation to the end of the protocol (i.e., second prostaglandin administration or progestogen device removal) was negatively associated with estrus duration(1414 Zuñiga-Garcia S, Meza-Herrera CA, Mendoza-Cortina A, Otal-Salaverri J, Perez-Marin C, Lopez-Flores NM, Carrillo E, Calderon-Leyva G, Gutierrez-Guzman UN, Veliz-Deras FG. Effect of Social Rank upon Estrus Induction and Some Reproductive Outcomes in Anestrus Goats Treated With Progesterone + ECG. Animals. 2020; 10 (7):1125. Available from: https://doi.org/10.3390/ani10071125
https://doi.org/10.3390/ani10071125...
). Conversely, the interval to ovulation appears to not be significantly affected by estrus onset in goats presenting either earlier or later(1616 Pietroski ACCA, Brandão FZ, Souza JMG, Fonseca JF. Short, Medium or Long-Term Hormonal Treatments for Induction of Synchronized Estrus and Ovulation in Saanen Goats during the Nonbreeding Season. Revista Brasileira de Zootecnia. 2013; 42 (3):168-173. Available from: https://doi.org/10.1590/S1516-35982013000300004
https://doi.org/10.1590/S1516-3598201300...
). The reproductive parameters are shown in Tab. 1.

Table 1
Reproductive parameters of different hierarchical categories of dairy goats after short-term progestogen synchronous estrus induction during the non-breeding season.

The present study showed that all females started estrus between 24 and 60 h after device removal; the consideration of the time of estrus onset facilitated their categorization. As hypothesized, the goats displaying estrus earlier in the HD group did not necessarily have the different ovarian follicular profiles able to affect the ovulation time in relation to device removal when compared to the low hierarchical position (LD). The ovarian follicular wave emergence before and after device removal was similar among the categories studied. In fact, shorter intervals for the onset of estrus are mainly associated with longer intervals from the onset of estrus to ovulation, as the duration of estrus is therefore longer(1414 Zuñiga-Garcia S, Meza-Herrera CA, Mendoza-Cortina A, Otal-Salaverri J, Perez-Marin C, Lopez-Flores NM, Carrillo E, Calderon-Leyva G, Gutierrez-Guzman UN, Veliz-Deras FG. Effect of Social Rank upon Estrus Induction and Some Reproductive Outcomes in Anestrus Goats Treated With Progesterone + ECG. Animals. 2020; 10 (7):1125. Available from: https://doi.org/10.3390/ani10071125
https://doi.org/10.3390/ani10071125...
).

Because of the negative correlation between the interval to estrus and estrus duration(1717 Romano JE. Effects of different stimuli of service on estrus duration in dairy goats. Theriogenology. 1994; 42 (5):875 - 879. Available from: https://doi.org/10.1016/0093-691X(94)90455-R
https://doi.org/10.1016/0093-691X(94)904...
) and ovulation occurring near the end of estrus(1818 Fonseca JF, Maffili VV, Santos ADF, Fürst R, Prosperi CP, Rovay H, J.M.G. Souza, Torres CAA. Effects of prostaglandin administration 10 days apart on reproductive parameters of cyclic dairy nulliparous goats. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2012; 64 (2). Available from: https://doi.org/10.1590/S0102-09352012000200014
https://doi.org/10.1590/S0102-0935201200...
), a longer estrus duration was expected for HD goats. Consequently, dominant goats in a given herd are likely to engage in more natural matings (shorter estrous interval and longer estrous duration), while subordinate goats are likely to engage in fewer or no matings. This occurrence can be circumvented with the use of preferential natural improvement(99 Fonseca, J. F. Inseminação Artificial Transcervical em Tempo Flexível (IATFx) em cabras leiteiras. Sobral: Embrapa Caprinos e Ovinos, 2020. 13 p. il. color. (Embrapa Caprinos e Ovinos. Circular Técnica, 49). Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/221325/1/CNPC-2020-Art.53.pdf
http://ainfo.cnptia.embrapa.br/digital/b...
). On the other hand, adjusting the FxTAI(88 Carvalho-de-Paula CJ, Souza-Fabjan JMG, Gonçalves JD, Dias JH, Souza GN, Oliveira MEF, Fonseca JF. Effect of a 12-h increment in the short-term treatment regimen on ovarian status, estrus synchrony, and pregnancy rate in artificially inseminated dairy goats. Animal Reproduction Science. 2020; 221. Available from: https://doi.org/10.1016/j.anireprosci.2020.106571
https://doi.org/10.1016/j.anireprosci.20...
) may allow the FxTAI-like strategy of goats being inseminated at a fixed time in a short period of time and before the expected mean time of ovulation (Figure 1).

Figure 1
Schematic presentation of flexible time artificial insemination (FxTAI) for estrus-induced goats that enter estrus at different intervals after the removal of the device. Note that the goats are inseminated on the same day, at the end of estrus and before ovulation.

The social rank is not related to the conception rate or the number of kids born after estrus synchronization treatment and FxTAI in dairy goats(1515 Ungerfeld R, González-Pensado S, Dago AL, Vilariño M, Menchaca A. Social Dominance of Female Dairy Goats and Response to Oestrus Synchronisation and Superovulatory Treatments. Applied Animal Behaviour Science. 2007; 105:115 - 121. 10. Available from: https://doi.org/10.1016/j.applanim.2006.06.008
https://doi.org/10.1016/j.applanim.2006....
). However, high-dominant goats have a higher level of progesterone than medium- and low-dominant goats(1919 Alvarez L, Arvizu RR, Luna JA, Zarco LA. Social ranking and plasma progesterone levels in goats. Small Ruminant Research. 2010; 90 161-164. Available from: https://doi.org/10.1016/j.smallrumres.2010.02.002
https://doi.org/10.1016/j.smallrumres.20...
). If, like progesterone, the estrogen profile during the follicular phase of the estrous cycle is higher in dominant goats, this category could reach the threshold estrogen level earlier for estrus presentation, which would explain the earlier onset of estrus observed in the present study.

The FxTAI strategy resulted in an acceptable pregnancy rate (43.5%), similar to that reported earlier for goats (47.8%(1515 Ungerfeld R, González-Pensado S, Dago AL, Vilariño M, Menchaca A. Social Dominance of Female Dairy Goats and Response to Oestrus Synchronisation and Superovulatory Treatments. Applied Animal Behaviour Science. 2007; 105:115 - 121. 10. Available from: https://doi.org/10.1016/j.applanim.2006.06.008
https://doi.org/10.1016/j.applanim.2006....
)) subjected to fixed time artificial insemination. However, it should be remembered that the animals in the present study were continuously monitored with various interventions for ultrasound assessments. Animals in similar conditions have been reported to achieve lower pregnancy rates than those simply subjected to the protocol of synchronous estrus induction, estrus monitoring, and artificial insemination(55 Bonato GC, Maia ALRS, Côrtes LR, Oliveira TA, Arrais AM, Figueira LM, Oliveira MEF, Souza-Fabjan JMG, Fonseca JF. Effects of d-cloprostenol administrations with 7.5 and 11.5-day intervals between administrations on pregnancy rates after artificial insemination in estrus cyclic dairy goats. Animal Reproduction Science. 2019; 209:106172. Available from: https://doi.org/10.1016/j.anireprosci.2019.106172
https://doi.org/10.1016/j.anireprosci.20...
, 77 Maia ALRS, Brandão FZ, Souza-Fabjan JMG, Balaro MFA, Oliveira MEF, Facó O, Fonseca JF. Reproductive parameters of dairy goats after receiving two doses of d-cloprostenol at different intervals. Animal Reproduction Science. 2017; 181:16-23. Available from: https://doi.org/10.1016/j.anireprosci.2017.02.013
https://doi.org/10.1016/j.anireprosci.20...
).

Finally, in the present study, at each check, goats that were identified as being in estrus were promptly removed from their pens, allowing the remaining goats to be checked by males in their absence. This could be an interesting strategy to increase the estrus response, allowing subordinate goats to externalize behavioral estrus that could not be observed if the dominant goats had remained in the pens. Moreover, strategic breeding schemes must be employed to prevent dominant goats from receiving successive natural matings, which compromises the amount of matings and semen received by subordinates, as previously proposed(99 Fonseca, J. F. Inseminação Artificial Transcervical em Tempo Flexível (IATFx) em cabras leiteiras. Sobral: Embrapa Caprinos e Ovinos, 2020. 13 p. il. color. (Embrapa Caprinos e Ovinos. Circular Técnica, 49). Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/221325/1/CNPC-2020-Art.53.pdf
http://ainfo.cnptia.embrapa.br/digital/b...
).

Conclusion

Hierarchical order is an important parameter that requires consideration when estrus is induced in dairy goats during the non-breeding season. Females classified as having a higher level of dominance are the first to externalize estrus behavior after the removal of the intravaginal device. Earlier onset of estrus was not significantly accompanied by differences in ovarian follicular parameters or ovulation. Artificial insemination performed in relation to the onset of estrus can circumvent the social hierarchy by allowing dairy goats to receive semen on the same day for different categories, but in all cases before ovulation. The FxTAI strategy is found to be efficient at circumventing the influence of hierarchy on estrus behavior, allowing artificial insemination to be performed for all categories at an almost fixed time.

Acknowledgements

The authors wish to thank EMBRAPA staff for providing and housing the animals employed in this study. This study was supported by the National Council for Scientific and Technological Development (CNPq; Project 403909/2021-0), Fundação de Amparo à Pesquisa de Minas Gerais (Fapemig; Project 00201-17) and EMBRAPA (Project 20.19.01.004.00.03.001). The authors also thank the support by the Carlos Chagas Filho Foundation for Research Support in Rio de Janeiro (FAPERJ). MEFO, JFF and JMGS-F are CNPq fellows and JMGS-F is a fellow of Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

References

  • 1
    Balaro MFA, Mello SGV, Santos AS, Cavalcanti LM, Almosny NRP, Fonseca JF, Brandão FZ. Reproductive seasonality in Saanen goats kept under tropical conditions. Tropical Animal Health and Production. 2018; 51 (2):345-353. Available from: https://doi.org/10.1007/s11250-018-1696-2
    » https://doi.org/10.1007/s11250-018-1696-2
  • 2
    Fonseca JF, Souza-Fabjan JMG, Oliveira MEF, Cruz RC, Esteves L, Paiva MPSLM, Brandão FZ, Mancio AB. Evaluation of cervical mucus and reproductive efficiency of seasonally anovular dairy goats after short-term progestagen-based estrus induction protocols with different gonadotropins. Reproductive Biology. 2017; 17(4): 363-369. Available from: https://doi.org/10.1016/j.repbio.2017.10.002
    » https://doi.org/10.1016/j.repbio.2017.10.002
  • 3
    Gómez JD, Balasch S, Gómez LD, Martino A, Fernández N. A Comparison between intravaginal progestogen and melatonin implant treatments on the reproductive efficiency of ewes. Small Ruminants Research. 2006; 66:156-163. Avaiable from: https://doi.org/10.1016/j.smallrumres.2005.08.020
    » https://doi.org/10.1016/j.smallrumres.2005.08.020
  • 4
    Fonseca JF, Alvim GP, Souza-Fabjan JMG, Oliveira MEF, Brair VL, Brandão FZ, Facó O. Reproductive features and use of an anti-inflammatory drug in estrus-induced dairy goats artificially inseminated in a standing position with cervix immobilization. Reproductive Biology 2017; 17(3):268-273. Available from: https://doi.org/10.1016/j.repbio.2017.07.002
    » https://doi.org/10.1016/j.repbio.2017.07.002
  • 5
    Bonato GC, Maia ALRS, Côrtes LR, Oliveira TA, Arrais AM, Figueira LM, Oliveira MEF, Souza-Fabjan JMG, Fonseca JF. Effects of d-cloprostenol administrations with 7.5 and 11.5-day intervals between administrations on pregnancy rates after artificial insemination in estrus cyclic dairy goats. Animal Reproduction Science. 2019; 209:106172. Available from: https://doi.org/10.1016/j.anireprosci.2019.106172
    » https://doi.org/10.1016/j.anireprosci.2019.106172
  • 6
    Andrade ABP, Morais MCC, Rangel PSC, Oliveira MEF, Souza-Fabjan JMG, Fonseca JF. Effect of eCG in a short-term synchronization treatment on ovarian status, estrus synchrony, and ovulation in dairy goats managed under tropical conditions. Tropical Animal Health and Production. 2021; 53(2):246. Available from: https://doi.org/10.1007/s11250-021-02699-y
    » https://doi.org/10.1007/s11250-021-02699-y
  • 7
    Maia ALRS, Brandão FZ, Souza-Fabjan JMG, Balaro MFA, Oliveira MEF, Facó O, Fonseca JF. Reproductive parameters of dairy goats after receiving two doses of d-cloprostenol at different intervals. Animal Reproduction Science. 2017; 181:16-23. Available from: https://doi.org/10.1016/j.anireprosci.2017.02.013
    » https://doi.org/10.1016/j.anireprosci.2017.02.013
  • 8
    Carvalho-de-Paula CJ, Souza-Fabjan JMG, Gonçalves JD, Dias JH, Souza GN, Oliveira MEF, Fonseca JF. Effect of a 12-h increment in the short-term treatment regimen on ovarian status, estrus synchrony, and pregnancy rate in artificially inseminated dairy goats. Animal Reproduction Science. 2020; 221. Available from: https://doi.org/10.1016/j.anireprosci.2020.106571
    » https://doi.org/10.1016/j.anireprosci.2020.106571
  • 9
    Fonseca, J. F. Inseminação Artificial Transcervical em Tempo Flexível (IATFx) em cabras leiteiras. Sobral: Embrapa Caprinos e Ovinos, 2020. 13 p. il. color. (Embrapa Caprinos e Ovinos. Circular Técnica, 49). Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/221325/1/CNPC-2020-Art.53.pdf
    » http://ainfo.cnptia.embrapa.br/digital/bitstream/item/221325/1/CNPC-2020-Art.53.pdf
  • 10
    Barroso FG, Alados CL, Boza J. Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science. 2000; 69 (1):35-53. Available from: https://doi.org/10.1016/S0168-1591(00)00113-1
    » https://doi.org/10.1016/S0168-1591(00)00113-1
  • 11
    Miranda-de la Lama, GC, Mattiello S. The importance of social behaviour for goat welfare in livestock farming. Small Ruminant Research. 2010; 90 1-10. Available from: https://doi.org/10.1016/j.smallrumres.2010.01.006
    » https://doi.org/10.1016/j.smallrumres.2010.01.006
  • 12
    Kaufmann, J. H. On the definition and functions of dominance and territoriality. Biological Reviews. 1983; 58 (1):1-20. Available from: https://doi.org/10.1111/j.1469-185X.1983.tb00379.x
    » https://doi.org/10.1111/j.1469-185X.1983.tb00379.x
  • 13
    Côté, SD, Festa-Bianchet M. Reproductive Success in Female Mountain Goats: The Influence of Age and Social Rank. Animal Behaviour. 2001; 62 (1):173-181. Available from: http://dx.doi.org/10.1006/anbe.2001.1719
    » http://dx.doi.org/10.1006/anbe.2001.1719
  • 14
    Zuñiga-Garcia S, Meza-Herrera CA, Mendoza-Cortina A, Otal-Salaverri J, Perez-Marin C, Lopez-Flores NM, Carrillo E, Calderon-Leyva G, Gutierrez-Guzman UN, Veliz-Deras FG. Effect of Social Rank upon Estrus Induction and Some Reproductive Outcomes in Anestrus Goats Treated With Progesterone + ECG. Animals. 2020; 10 (7):1125. Available from: https://doi.org/10.3390/ani10071125
    » https://doi.org/10.3390/ani10071125
  • 15
    Ungerfeld R, González-Pensado S, Dago AL, Vilariño M, Menchaca A. Social Dominance of Female Dairy Goats and Response to Oestrus Synchronisation and Superovulatory Treatments. Applied Animal Behaviour Science. 2007; 105:115 - 121. 10. Available from: https://doi.org/10.1016/j.applanim.2006.06.008
    » https://doi.org/10.1016/j.applanim.2006.06.008
  • 16
    Pietroski ACCA, Brandão FZ, Souza JMG, Fonseca JF. Short, Medium or Long-Term Hormonal Treatments for Induction of Synchronized Estrus and Ovulation in Saanen Goats during the Nonbreeding Season. Revista Brasileira de Zootecnia. 2013; 42 (3):168-173. Available from: https://doi.org/10.1590/S1516-35982013000300004
    » https://doi.org/10.1590/S1516-35982013000300004
  • 17
    Romano JE. Effects of different stimuli of service on estrus duration in dairy goats. Theriogenology. 1994; 42 (5):875 - 879. Available from: https://doi.org/10.1016/0093-691X(94)90455-R
    » https://doi.org/10.1016/0093-691X(94)90455-R
  • 18
    Fonseca JF, Maffili VV, Santos ADF, Fürst R, Prosperi CP, Rovay H, J.M.G. Souza, Torres CAA. Effects of prostaglandin administration 10 days apart on reproductive parameters of cyclic dairy nulliparous goats. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2012; 64 (2). Available from: https://doi.org/10.1590/S0102-09352012000200014
    » https://doi.org/10.1590/S0102-09352012000200014
  • 19
    Alvarez L, Arvizu RR, Luna JA, Zarco LA. Social ranking and plasma progesterone levels in goats. Small Ruminant Research. 2010; 90 161-164. Available from: https://doi.org/10.1016/j.smallrumres.2010.02.002
    » https://doi.org/10.1016/j.smallrumres.2010.02.002

Publication Dates

  • Publication in this collection
    13 May 2022
  • Date of issue
    2022

History

  • Received
    09 Nov 2021
  • Accepted
    09 Mar 2022
  • Published
    06 Apr 2022
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