Breeding and feeding management models aimed at optimising animal performance (milk yield and composition), behaviour and welfare become particularly important when uncontrollable changes in climatic conditions come into play (Erduran and Dag, Reference Erduran and Dag2021). Goats have an important socioeconomic role in many countries around the world due to their ability to survive and be prolific in rural areas (Dubeuf et al., Reference Dubeuf, Morales and Guerrero2018). Understanding the goat–environment relationship is critical for efficient breeding programmes, agro-ecological integration and the implementation of sustainable methodological goat production systems (Dubeuf et al., Reference Dubeuf, Morales and Guerrero2018; Erduran and Dag, Reference Erduran and Dag2021). As examples, short daylength and extreme ambient temperatures are potential barriers to achieving high productivity and lactation persistency in goats (Saipin et al., Reference Saipin, Semsirmboon, Rungsiwiwut and Thammacharoen2020; Zamuner et al., Reference Zamuner, DiGiacomo, Cameron and Leury2020).
Correct management during the peripartum period including parturition itself is critical for health and productivity of dairy animals. Goats mostly give birth during daylight hours (Erduran, Reference Erduran2021). In general, information on the temporal and behavioural characteristics of parturition in animals is rather limited, and in particular, there is no available information on the relationship between parturition time and milk yield characteristics in dairy animals.
In mammals, the circadian rhythm is generated endogenously by molecular clock genes in the suprachiasmatic nucleus, following the approximately 24-h photoperiod cycle (Patke et al., Reference Patke, Young and Axelrod2020). The biological clock regulates daily changes during pregnancy, parturition, and lactation by coordinating the metabolic, endocrine, physiological and behavioural systems to produce circadian rhythms (Hernández-Castellano et al., Reference Hernández-Castellano, Moreno-Indias, Sánchez-Macías, Morales-delaNuez, Torres, Argüello and Castro2019; Teng et al., Reference Teng, Yang, Wang, Fu, Lian, Sun, Han, Zhang and Gao2021). Additionally, environmental stressors such as climate, farm routines and anthropogenic noise sources can have important consequences, affecting the immune status, welfare, and performance of ruminants (Cipolla-Neto and Amaral, Reference Cipolla-Neto and Amaral2018; Moralia et al., Reference Moralia, Quignon, Simonneaux and Simonneaux2022). Somatic cell count (SCC), lactose, electrical conductivity, pH, and milk freezing point are indirect indicators used in dairy farming to determine the state of udder health and the quality of milk and milk products (Lôbo et al., Reference Lôbo, Lôbo, Facó, Souza, Alves, Costa and Albuquerque2017; Erduran, Reference Erduran2021; Teng et al., Reference Teng, Yang, Wang, Fu, Lian, Sun, Han, Zhang and Gao2021). Furthermore, the structure and characteristics of the udder are important determinants of milk yield (Mavrogenis et al., Reference Mavrogenis, Papachristoforou, Lysandrides and Roushias1988; Erduran, Reference Erduran2021).
To the best of my knowledge, there is no evidence that a mammal's parturition time influences milk production. Knowing the parturition time of goats may be an important factor both in increasing the profitability of the enterprises and in the selection, productivity, permanence and durability of the goats. Therefore, to test this hypothesis, this is the first report to investigate the relationships between time of parturition of goats and milk production, quality and physicochemical properties of milk, and udder traits considering climatic conditions.
Materials and methods
All procedures were approved by the Bahri Dağdaş International Agricultural Research Institute Animal Ethics Committee prior to the commencement of the experiment (licence number 2669).
Animal and management conditions
The effects of time of parturition and parity on milk yield, physicochemical composition and SCC characteristics of Saanen goats were evaluated. Data included 2050 records (morning and evening milkings) collected on 106 Saanen goats raised in a Konya research farm. Parities varied from one to four (16, 32, 37 and 15%, respectively) and weights from 33 to 58 kg. The kidding season was from the middle of February until the middle of March. During this period the goats were observed hourly during the day and every 2 h at night. The new-born kid's date of birth, time of birth, type of birth, gender, and maternal tag number were all recorded. After birth, the kids were allowed to suckle their mother's milk (colostrum) for the first 3 d, then separated from their mothers and fed with a bottle until weaning at approximately 2 months. Goats were kept at pasture from February to November with a daily grazing duration ranging from 4 to 6 h. In addition to pasture, the goats were fed approximately 800 g d−1 concentrate daily (17.1% CP, 2600 kcal ME kg−1 DM: given in equal portions at milking times) and 400 g d−1 of dry alfalfa hay during the lactation period. In winter, animals were kept indoors if grazing was not possible, they were fed with hay (mixed 800 g alfalfa and 400 g wheat) and 1000 g concentrated feed (2450 kcal/kg ME, 15% crude protein) for about 3 months. A more detailed account of animal management is given in the online Supplementary materials and methods.
The averages for ambient temperature, precipitation, and relative humidity were provided by the meteorological station in Konya, detailed in the online Supplementary materials and methods.
Milking, milk samples, SCC and udder measurements
All goats on the farm were milked twice a day, at 06 : 00 and 18 : 00 h, throughout the lactation period. By using in-line milk meters (Tru-Test, Auckland, New Zealand) once every 28 d, both the milk yield of individual goats was recorded and a milk sample of each goat was collected. Milk production was measured until daily production level dropped below 100 g d−1. Only 18 goats were dried off or removed from the study before completion of a 36-week (ninth recorded milking) lactation period, either when they decreased milk production or developed health problems. Lactation milk productions were calculated using the Fleischmann method (ICAR, 2009).
Milk samples were collected from each goat and fat, protein, lactose, solids-non-fat, total solids, density, conductivity and freezing point were immediately analysed in the field by an ultrasonic milk analyser (MILKANA EP 45 sec Milk Analyser, Mayasan Ltd, Türkiye). The milk pH was measured by a pH meter (WTW, InoLab, pH 720, Weilheim, Germany). SCC in the milk samples was determined by direct microscopic SCC method (Erduran, Reference Erduran2021).
Udder measurements were taken only once after the morning milking from each animal, at approximately 84 d (peak period) of lactation following the methods of Mavrogenis et al. (Reference Mavrogenis, Papachristoforou, Lysandrides and Roushias1988) and, for udder volume (UV), Emediato et al. (Reference Emediato, Siquera, Stradiotto, Maesta and Fernandes2008).
Statistical analysis
The data were analysed using the Jump 11 computer-based program. Time of parturition, parity, and the interaction of parity and time of parturition were evaluated using a general linear model. Relationships between milk SCC and daily milk yield, lactation stage, parity and time of parturition as well as the relationship between time of parturition and udder measurements were analysed using one-way ANOVA. When needed the differences among the factor levels were ascertained using the Tukey multiple comparisons test (Kesici and Kocabas, Reference Kesici and Kocabas2007). Pearson's correlation was used to examine the relationship between daily milk yield and meteorological data. Statistical significance was accepted when P < 0.05.
Results
As shown in Table 1, time of parturition had an effect on Saanen goat milk productivity (P < 0.05), while there were no differences in milk composition (P > 0.05). Parity and parturition time × parity interaction had a significant effect on lactation milk yield, lactation length, total solids, fat, protein, and lactose content and electrical conductivity (P < 0.01 or P < 0.05). However, parity and parturition time × parity interaction had no effect on daily milk yield, density, pH, and freezing point.
Table 1. Effect of time of parturition, parity and their interaction on milk production and composition in Saanen goats
sem, Standard error of the mean.
a,b Means with different letters within the same column differ significantly at small letters – (P < 0.01), capital letters – (P < 0.05).
The relationship between daily milk yield and daylight length and temperature in Saanen goats was significant and moderately positive, while the relationship between daily milk yield and relative humidity was insignificant and moderately negative (Fig. 1), although it needs to be borne in mind that these relationships relate in large part to stage of lactation. The primiparous goats had the lowest lactation yield, milk fat and total solids contents compared to those with higher parities, but they had the highest milk protein and lactose contents. The changing effects of parity number on daily milk yield, fat, protein, and lactose contents during lactation period are presented in online Supplementary Fig. S1.
Fig. 1. Mean daylight length, temperature and relative humidity data by lactation days.
The relationships between lactation stage, daily milk yield, parity and time of parturition on SCC, pH, total solids, electrical conductivity and freezing point of milk are presented in Table 2. SCC in milk decreased (P < 0.01) as the daily milk yield of the goats increased and increased rapidly with progressing lactation stage (P < 0.01) and increasing parity (P < 0.05). However, goats giving birth in the evening had lower SCC in milk than those giving birth in daylight or at night (P < 0.05). Table 3 shows that goats giving birth during darkness had greater rear udder depth, udder circumference and udder volume traits than those giving birth during the day (P < 0.01).
Table 2. Effects of time of parturition, daily milk yield, lactation stage and parity on milk somatic cell count (SCC) in Saanen goats
a. b Means with different letters within the same block differ significantly at small letters (P < 0.01), capital letters (P < 0.05).
Table 3. Effect of the time of parturition on udder traits in Saanen goats
DBUT, distance between udder teats.
a.b Means with different letters within the same row differ significantly at small letters (P < 0.01), capital letters (P < 0.05).
Discussion
Relationships between time of parturition and milk production
In mammals, the time of parturition occurs mainly just before or during the sleep/rest phase, depending on the day and night activity, physiology, and behaviour of the maternal and foetus during pregnancy, as influenced by photoperiod, endocrine patterns and management routine (Takayama et al., Reference Takayama, Nakamura, Tamura, Yamagata, Harada, Nakata, Sugino and Kato2003; Mabjeesh et al., Reference Mabjeesh, Sabastian, Gal-Garber and Shamay2013; Hernández-Castellano et al., Reference Hernández-Castellano, Moreno-Indias, Sánchez-Macías, Morales-delaNuez, Torres, Argüello and Castro2019; Pan et al., Reference Pan, Taylor, Cohen, Hanna and Mota2020). Animals that are active during the day tend to give birth at night, while those that are active at night tend to give birth during the day (Takayama et al., Reference Takayama, Nakamura, Tamura, Yamagata, Harada, Nakata, Sugino and Kato2003; Hopper et al., Reference Hopper, Fernandez-Duque and Williams2019; McCarthy et al., Reference McCarthy, Jungheim, Fay, Bates, Herzog and England2019). In this study of Saanen goats, a diurnal parturition pattern was observed, with up to 73% of parturition occurring during daylight hours and 44% of all parturitions occurring between midday and 18 : 00. However, the fact that the majority of parturitions in this study occur around noon in daytime-active goats suggests that the circadian rhythm has evolved under the influence of environmental factors that alter the parturition process and time (Hopper et al., Reference Hopper, Fernandez-Duque and Williams2019; Nagy and Juhász, Reference Nagy and Juhász2019). Disruption of clock genes can negatively affect endocrine and metabolic systems, including physiological and behavioural activities (Pan and Hussain, Reference Pan and Hussain2009; Moralia et al., Reference Moralia, Quignon, Simonneaux and Simonneaux2022). Therefore, the difference in milk production between day and dark-parturition goats may be related to adaptation to their living environment (Dulude-de Broin et al., Reference Dulude-de Broin, Hamel, Mastromonaco and Côté2020).
In the current study, goats giving birth during darkness had higher milk production than goats having parturition during the day. Daily milk yield appeared to be associated more strongly with day length than with ambient temperature and relative humidity (Fig. 1). Thus, since day length does not fluctuate randomly on the scale exhibited by other seasonal factors, it may be an ideal signal for inducing annual changes in biological systems (Sen and Hoffmann, Reference Sen and Hoffmann2020). There is strong evidence that melatonin, an important circadian transition signal depending on photoperiod intensity, directly plays a role in the timing of parturition by participating in the rest/activity cycle in mammals (Takayama et al., Reference Takayama, Nakamura, Tamura, Yamagata, Harada, Nakata, Sugino and Kato2003; McCarthy et al., Reference McCarthy, Jungheim, Fay, Bates, Herzog and England2019). More importantly, darkness exposure of goats at parturition may create variations in the circadian rhythm to commence or activate the biological clock sooner for wakefulness depending on the light intensity of the lunar phase, especially the full moon phase (Hopper et al., Reference Hopper, Fernandez-Duque and Williams2019). One could speculate that changes in the profile of daily secreted melatonin may not only affect the timing of parturition in goats giving birth in the dark but may also lead to more efficient use of cellular resources for mammary gland development and milk production.
Within the first few hours or days after parturition, postnatal up-regulation of genes that promote mammary gland secretory cell development and proliferation and inhibit apoptosis, is likely essential for long-term milk production (Svennersten-Sjaunja and Olsson, Reference Svennersten-Sjaunja and Olsson2005; Hernández-Castellano et al., Reference Hernández-Castellano, Moreno-Indias, Sánchez-Macías, Morales-delaNuez, Torres, Argüello and Castro2019; Parker et al., Reference Parker, Sullivan, Kruger and Mueller2020). Lactation is a complex phenomenon, and lactogenesis is the period when abundant milk secretion begins after parturition (Knight, Reference Knight2001; Lérias et al., Reference Lérias, Hernández-Castellano, Suárez-Trujillo, Castro, Pourlis and Almeida2014). Time of parturition may cause a delayed onset of lactogenesis by affecting maternal circadian rhythm, altering daily signal duration with an initial phase of different metabolism and hormones (İlhan et al., Reference İlhan, Atmaca, Çümen, Zebitay, Güngör and Karasu2018). Melatonin is likely to play a larger role in milk production in darkness-parturition goats by contributing to clock gene regulation and mitochondrial integrity protection in the body against oxidative stress (McCarthy et al., Reference McCarthy, Jungheim, Fay, Bates, Herzog and England2019). Accordingly, once could again speculate that melatonin level and release time may directly contribute to the milk synthesis of darkness-parturition goats by affecting prolactin secretion, regulating metabolic flow and enhancing oxytocin release, quite possibly through synergistic interactions with other hormones such as adrenaline, cortisol, oestrogen, leptin, insulin, oxytocin, progesterone, prolactin, somatotropin and thyroxine, all of which affect mammary function (Svennersten-Sjaunja and Olsson, Reference Svennersten-Sjaunja and Olsson2005; Mabjeesh et al., Reference Mabjeesh, Sabastian, Gal-Garber and Shamay2013).
Behavioural and physiological responses can be altered by repeated exposure to a variety of stressors, and these changes can also be passed on to offspring through epigenetic mechanisms (Harding et al., Reference Harding, Gordon, Eastcott, Simpson and Radford2019). Thus, the goats in daytime parturition are likely to be exposed to high cortisol and adrenaline levels for a long time due to stress factors such as more activity, anthropogenic noise sources and the instinct to protect their offspring from external factors (Dulude-de Broin et al., Reference Dulude-de Broin, Hamel, Mastromonaco and Côté2020; Pan et al., Reference Pan, Taylor, Cohen, Hanna and Mota2020). These external factors may lead to chronic overstimulation of the endocrine system, physiological down-regulation of cortisol and adrenaline-responsive systems, and functional insufficiency of the capillary network and metabolic activity required for milk synthesis (Cipolla-Neto and Amaral, Reference Cipolla-Neto and Amaral2018). Goats exposed to the complications of environmental factors during daytime parturition might be expected to have delayed mammary gland secretory activation, reduced milk ejection reflex and shortened lactation duration (Parker et al., Reference Parker, Sullivan, Kruger and Mueller2020). In support of this, goats kidding during darkness hours had higher rear udder depth, udder circumference and udder volume when measured at around peak lactation. In addition, it is possible that gene expression and secretory activation begin earlier in goats giving parturition in calm, quiet, dark conditions, when maternal–offspring orientation and bonding is most secure, as occurs in primates (Hopper et al., Reference Hopper, Fernandez-Duque and Williams2019).
We observed that milk from goats that give parturition in the evening exhibits a superior quality due to lower SCC values. Due to the change in steroid hormone concentration during the daytime parturition process and the increase in endorphin release in the postpartum period, the formation of a greater energy balance deficit may occur goats kidding during the day (Teng et al., Reference Teng, Yang, Wang, Fu, Lian, Sun, Han, Zhang and Gao2021). The immune system of goats can be directly affected by negative energy balance (Cipolla-Neto and Amaral, Reference Cipolla-Neto and Amaral2018). Therefore, some important components of natural immunity, such as chitotriosidase, which protects the udder against pathogens in lactating goats (Hernández-Castellano et al., Reference Hernández-Castellano, Moreno-Indias, Sánchez-Macías, Morales-delaNuez, Torres, Argüello and Castro2019) may be transferred from blood to milk at a higher rate in darkness-parturition goats than in daytime-parturition goats.
Direct measurements of physiological and environmental stress markers (especially melatonin, cortisol, oestrogen, progesterone, oxytocin, prolactin levels, management routine or behavioural state) will probably provide more direct information about the relationship between parturition time and milk yield of goats. Specifically, it would be helpful to record whether there are changes in the behaviour and physiological state of the goats during the 24-h cycle and throughout the parturition. More data are needed to reveal the link between fluctuations in environmental stressors of goats and their parturition schedules.
Parity and time of parturition × parity interactions on milk yield and composition
All the milk yield and content traits included in the present study were significantly affected by parity. Overall, the averages of milk yield and fat, protein and lactose content were within the range of milk production and composition values reported for exotic and improved goat breeds (Rupp et al., Reference Rupp, Clement, Piacere, Robert-Granie, Manfredi, Robert-Granie and Manfredi2011; Mabjeesh et al., Reference Mabjeesh, Sabastian, Gal-Garber and Shamay2013; Lérias et al., Reference Lérias, Hernández-Castellano, Suárez-Trujillo, Castro, Pourlis and Almeida2014; Lôbo et al. Reference Lôbo, Lôbo, Facó, Souza, Alves, Costa and Albuquerque2017; Erduran and Dag, Reference Erduran and Dag2022). In this study, a general relationship between the length of lactation in Saanen goats and the amount of milk produced was found. Primiparous goats had the lowest lactation milk yield, daily milk yield and lactation length which can be explained by the fact that primiparous goats must use their nutrients for both lactation and their own growth, as well as the fact that primiparous goats have no experience with milking routines or lactation and are less likely to have correspondingly strong internal rhythms (Lôbo et al., Reference Lôbo, Lôbo, Facó, Souza, Alves, Costa and Albuquerque2017; Erduran and Dag, Reference Erduran and Dag2022). Primiparous goats had higher levels of protein and lactose than multiparous goats. This can be explained by lower milk production and fewer metabolic diseases, such as subclinical ketosis or hypocalcaemia, in primiparous goats (Lérias et al., Reference Lérias, Hernández-Castellano, Suárez-Trujillo, Castro, Pourlis and Almeida2014; Huang et al., Reference Huang, Wen, Kong, Zhao, Liu, Liu, Li, Yang, Zhu and Zhao2021). The goats of parity 4 had the highest lactation milk yield of all the parity groups. However, in the interaction between time of parturition and parity, goat's parity with 3 giving parturition in the dark had the highest values for lactation milk yield, while goat's parity with 1 giving parturition in the light had the lowest values.
As seen in Supplementary Fig. S1, the mean daily milk yield of goats in all parities increased until its peak in the third recorded milking of lactation (84 d). It then displayed a steady decrease until the end of the lactation period. The fat, protein, and lactose contents of parities were higher in the early and late stages of lactation and were their lowest levels in the peak or mid-lactation stage. The lactation curve in Supplementary Fig. S1 showed, however, that the differences between parities generally persisted consistently throughout lactation. Variations in fat content were higher during lactation than that in protein. This can be explained by the fact that the milk fat content of dairy goats is highly affected by environmental factors, whereas the protein content is more affected by the genotype (Costa et al., Reference Costa, Lopez-Villalobos, Sneddon, Shalloo, Franzoi, De Marchi and Penasa2019; Erduran and Dag, Reference Erduran and Dag2022).
The Saanen goats produced more milk in spring and early summer, but milk yield decreased rapidly in summer and autumn as a result of temperature changes and the shortening of days (Lérias et al., Reference Lérias, Hernández-Castellano, Suárez-Trujillo, Castro, Pourlis and Almeida2014). Additionally, the daily milk yield increased within an ambient temperature range of 11°C to 22°C, and peaked around 15 h of photoperiod daylight. This study has shown that the level of milk synthesis is dependent on temperature, and photoperiod. These results are also consistent with that reported by Saipin et al. (Reference Saipin, Semsirmboon, Rungsiwiwut and Thammacharoen2020) for Saanen goats in tropical conditions.
Milk quality and SCC
The average SCC was found to be 3.78 × 105 ml−1 in early lactation, 8.45 × 105 ml−1 in mid lactation and 13.98 × 105 ml−1 in late lactation. The SCC was greatest in fourth-parity goats (10.98 × 105 ml−1) and lowest in primiparous goats (6.30 × 105 ml−1). The onset of various physiological cycles in goats, such as oestrus or pregnancy, and the decrease in milk yield, may have resulted in an increase in SCC in milk towards the end of lactation. These values were also within the range of somatic cell counts previously reported for goat populations of many different countries, suggesting the health situation of the Saanen goats in Türkiye is consistent with other countries (Lôbo et al., Reference Lôbo, Lôbo, Facó, Souza, Alves, Costa and Albuquerque2017; Zamuner et al., Reference Zamuner, DiGiacomo, Cameron and Leury2020).
The increase of SCC in milk with parity and lactation progression seems to be associated with a simultaneous decrease in milk production. This may indicate that the higher SCC level (within the legal limits of goat milk) does not cause changes in goat milk total solids unless affected by a prominent intramammary infection (FDA, 2017). Furthermore, the low amount of SCC in this production system can be said to be effective in protecting udder health, possibly due to the elimination of the risks of intramammary infection and injury in goats that may arise from suckling. These effects are also attributed to changes in several non-pathological variation factors such as genetics, endocrine system, parity, nutrition, physiological and metabolic responses and permeability of the mammary epithelium (Lôbo et al., Reference Lôbo, Lôbo, Facó, Souza, Alves, Costa and Albuquerque2017; Erduran, Reference Erduran2021; Teng et al., Reference Teng, Yang, Wang, Fu, Lian, Sun, Han, Zhang and Gao2021).
In conclusion, this is the first study to show that time of parturition affects milk production, udder health, and udder structure. Data on the effect of parturition time on milk yield traits can be used to improve breeding models to improve milk production and quality. The changing milk composition and related index values in different months and parities generally support previous observations and provide scientific evidence to help improve the feeding management and nutritional supplementation of Saanen goats. Milk production is affected by terrestrial climatic conditions, first by photoperiod and then by temperature, at least under the conditions encountered in this study. It has been demonstrated that dairy goat production can be successfully applied in arid and terrestrial climate conditions.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0022029922000838.
Acknowledgements
The author expresses gratitude to late Bayram Yaman, technician, for his contribution in this study. The study was supported by GDARP (General Directorate of Agricultural Research and Policy, Türkiye Project No: TAGEM/HAYSÜD/10/08/04/01).
