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Animal and environmental factors associated with gestation length in the endangered Old Kladruber horse
Theriogenology 129 (2019) 116e120
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Theriogenology journal homepage: www.theriojournal.com
Animal and environmental factors associated with gestation length in the endangered Old Kladruber horse M. Malinska, Z. Havlicek, E. Koru, P. Rezac* Mendel University, Zemedelska 1, 61300, Brno, Czech Republic
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 September 2018 Received in revised form 14 February 2019 Accepted 19 February 2019 Available online 20 February 2019
Little is known about factors influencing gestation length in heavier types of horses. The objective was to assess the effects of the weight and age of mares, weight and sex of foals, lactation, month and year of conception, month of foaling, stallion and mare on gestation length in the endangered Old Kladruber breed that once served as a heavy coach horse for ceremonies of the Imperial Court in Vienna. The study was performed at the stud farm Slatinany, Czech Republic and reports data from foaling seasons between 2001 and 2018. A total of 649 gestations were included in the study. Gestation in mares weighing 680 kg and more was 1.9 days shorter than in those weighing up to 639 kg (P < 0.0001). Gestation in lactating mares was 3.9 days shorter than in non-lactating mares (P < 0.0001). Gestation was longest in mares conceiving in March (343.9 ± 0.60 days); thereafter it gradually shortened, with the shortest (P < 0.0001) in mares conceiving in July (334.9 ± 0.90 days). Gestation length in mares increased (P < 0.0001) from February foaling (340.4 ± 0.73 days) to March foaling (343.6 ± 0.55 days), and then decreased (P < 0.0001) up to the end of the breeding season in June (336.7 ± 0.92 days). Year of conception had an effect on GL (P < 0.02). Gestation in mares carrying male foals was 2.0 days longer than in those carrying female foals (P < 0.01). Gestation in mares delivering foals weighing 70 kg and more was 1.0 days longer than in those delivering foals weighing up to 60 kg (P < 0.01). Mare’s age had no effect on gestation length. In conclusion, gestation length was associated with the weight of mares and foals, lactation, month and year of conception, month of foaling, and sex of foals. © 2019 Elsevier Inc. All rights reserved.
Keywords: Mare Gestation length The sex of the foal Weight Season Lactation
1. Introduction Old Kladruber is one of the world’s oldest horse breeds, bred especially for ceremonial purposes for more than 400 years. This endangered breed is an important genetic resource with unique characteristics and high cultural and historical value. The baroque character of the breed has been preserved up to the present [1]. The breed was based on imported Old Spanish and Italian horses. The Old Kladruber was bred to be a heavy type of carriage horse used for pulling the coach at ceremonies, usually four- or six-in-hand. Currently, 5e10 stallions and around 60e80 breeding mares, producing 35e40 foals, are kept on the stud farm Slatinany [2]. Accurate prediction of parturition is an important aspect of managing equine pregnancy and parturition, especially during high-risk phases of mares’ lives. Preparations for impending foaling would be more efficient with improved information on the
* Corresponding author. E-mail address: [email protected] (P. Rezac). https://doi.org/10.1016/j.theriogenology.2019.02.013 0093-691X/© 2019 Elsevier Inc. All rights reserved.
expected date of birth, because gestation length (GL) in mares is highly variable; ranging between 322 and 366 days with viable foals having been delivered [3]. However, little information exists about GL in heavier horse types [4]. Several factors influence prenatal development from conception to birth. The sex of foals is associated with GL: male foals are carried longer than females [5e8]. On the other hand, El-Wishy et al. [9] did not find any difference between colts and fillies. The month of conception also has an effect on GL: mares that conceived early in the year have longer gestation than those that conceived at the end of the breeding season [7,10,11]. The month of foaling has an effect on GL as well, but different than the month of conceiving. Mares that foaled in April had longer gestation than those that foaled in January [7,12]. The effect of milk production on GL was assessed in Holstein cattle. Cows with higher milk yield tend to have a longer GL [13,14]. Based on this we hypothesize that lactation may also influence GL in mares. The effect of the weight diversity of mares on GL has not been investigated yet. Similarly to Czech Warmblood mares [7], we assume that the month of conception and month of foaling may
M. Malinska et al. / Theriogenology 129 (2019) 116e120
have a different effect on GL early in the year in Old Kladruber horses. It is not known whether the age of mares, sex of foals and year of conception in this old horse breed have a similar effect on GL compared to other breeds. Therefore, the objective of the present study was to examine the effects of the weight and age of mares, weight and sex of foals, lactation, month and year of conception, month of foaling, stallion and mare on GL in Old Kladruber horses. 2. Materials and methods 2.1. Animals The study did not include experiments on horses and the ethics committee of the Mendel University in Brno determined that it did not require approval. The study was performed on the stud farm Slatinany (Czech Republic) at a latitude of 50 north. All mares (n ¼ 153) and stallions (n ¼ 32) were Old Kladrubers. The average inbreeding coefficient was 0.13 [1]. Inclusion factors for breeding the mare were successful completion of performance tests, character and health. Exclusion factors for breeding the mare were reproductive problems, health problems, age and unsuitable offspring. The age of the mare at the first breeding was 5 years. The lactation period was at least 6 months. The mean number of births (±SEM) was 4.2 ± 0.2. The mean interval between foalings (±SEM) was 549 ± 12 days. The present and last gestation lengths were positively correlated (r ¼ 0.35, P < 0.01). The pregnancies selected were those that produced a single live foal in the period from 2001 to 2018 which did not die within 3 days of birth. Veterinary records were used to determine mating, ovulation and foaling dates for each pregnancy. In each case the ovulation date was determined, to within 24 h, using sequential ultrasonic scanning during estrus until ovulation was detected. Mating was then carried out on the basis of ultrasonic scanning evidence regarding the imminence of ovulation. Information on mare age and foal gender for each pregnancy was obtained from the stud records. A total of 649 foals and gestations (Gs) were included in the study. Mares were classified into three groups based on their age: (1) 4e6 years, (2) 7e12 years and (3) 13e23 years old. Mares were divided into three groups based on their weight 2 days after foaling: (1) 430e639 kg, (2) 640e679 kg and (3) 680e810 kg. Foals were classified into three groups based on their weight 2 days after birth: (1) 40e60 kg, (2) 61e69 kg and (3) 70e90 kg. Lactating mares were those lactating at the time of conception. All mares were kept in pasture under field conditions and natural photoperiod from spring to fall; they grazed native grass. In winter, pregnant mares were housed together in a spacious stable; they were given 12 kg hay/day. In the last trimester of gestation, mares were additionally fed 1.5 kg oats/day and 0.5 kg barley/day. Mares had full access to water and trace mineralized salt throughout the year. 2.2. Statistical analyses Statistical analyses were performed using SAS (SAS Institute Inc., Cary, NC, USA). The normality of the GL and foals’ birth weight distributions was established using the Kolmogorov-Smirnov test. The effects on GL and on the foals’ birth weight were analyzed using the mixed model procedure [15]. All models were analyzed in two steps: (1) fixed effects and their two-way interactions were examined; (2) only fixed effects were assessed, because all two-way interactions were not an important source of variation and were excluded from the final models. The fixed effect of the age of the mare on GL was also excluded from the final models, because of statistical insignificance.
117
The effects on GL were tested using two models. The use of two different models was based on the finding that the month of foaling had a different effect on GL than the month of conceiving early in the year in the Old Kladruber horse. The final version of the first model of the effects on GL included the fixed effects of the month of conception (5 categories: months of the breeding season from March to July), year of conception (18 categories: from 2000 to 2017), lactation (2 categories: lactating vs non-lactating mares), sex of the foal (2 categories: males vs females), weight of the mare (3 categories: up to 639 kg, 640e679 kg, 680 kg and more), and weight of the foal (3 categories: up to 60 kg, 61e69 kg, 70 kg and more). The first model included the random mare and stallion effects and random residual effect. The final version of the second model of the effects on GL included the fixed effects of the month of foaling (5 categories: months of foaling from February to June), year of conception (18 categories: from 2000 to 2017), lactation (2 categories: lactating vs non-lactating mares), sex of the foal (2 categories: males vs females), weight of the mare (3 categories: up to 639 kg, 640e679 kg, 680 kg and more), and weight of the foal (3 categories: up to 60 kg, 61e69 kg, 70 kg and more). The second model included the random mare and stallion effects and random residual effect. The final model of the effects on the birth weight of foals included the fixed effects of the sex of the foal (2 categories: males vs females), age of the mare (3 categories: up to 6 years, 7e12 years, 13 years and more), and weight of the mare (3 categories: up to 639 kg, 640e679 kg, 680 kg and more). The model included the random mare and stallion effects and random residual effect. 3. Results 3.1. Factors affecting gestation length The mean GL (±SEM) in 649 gestations with spontaneous foaling of mature and viable foal was 341.6 ± 0.3 days (range: 311e388 days). The mean age of mares (±SEM) was 10.0 ± 0.2 years (range: 4e23 years). The mean weight of mares (±SEM) was 659.8 ± 1.7 kg. The proportion of male and female foals was 49.8% (323 of 649) and 50.2% (326 of 649), respectively. No two-way interactions nor mare’s age had significant effect on GL. In the first model, GL was associated with the month of conception (P < 0.0001), year of conception (P < 0.02), weight of mares (P < 0.0001), lactation (P < 0.0001), weight of foals (P < 0.01), and sex of foals (P < 0.01). In the second model, GL was associated with the month of foaling (P < 0.0001), year of conception (P < 0.02), weight of mares (P < 0.0001), lactation (P < 0.0001), weight of foals (P < 0.01), and sex of foals (P < 0.01). No two-way interactions nor mare’s age had significant effect on GL. Gestation in mares weighing 680 kg and more (340.4 ± 0.48 days, n ¼ 226 Gs) was shorter (P < 0.0001) than in those weighing up to 639 kg (342.3 ± 0.59 days, n ¼ 191 Gs) and 640e679 kg (342.1 ± 0.54 days, n ¼ 232 Gs). Gestation in lactating mares (339.5 ± 0.44 days, n ¼ 302 Gs) was shorter (P < 0.0001) than in non-lactating mares (343.4 ± 0.41 days, n ¼ 347 Gs). The number of mares that conceived in different months of the year is shown in Fig. 1. Distribution of GL for mares that conceived in different months of the year is shown in Fig. 2. Gestation was longest in mares conceiving in March (343.9 ± 0.60 days, n ¼ 144 Gs); thereafter GL gradually shortened, and the shortest GL (P < 0.0001) was in mares conceiving in July (334.9 ± 0.90 days, n ¼ 49 Gs). The number of mares that foaled in different months of the year is shown in Fig. 3. Distribution of GL for mares that foaled in different months of the year is shown in Fig. 4. Gestation lasted 340.4 ± 0.73 days (n ¼ 87 Gs) in mares foaling in February, the longest gestation (343.6 ± 0.55 days, n ¼ 170 Gs) was in mares foaling in March
M. Malinska et al. / Theriogenology 129 (2019) 116e120
170
346
150
344 Gestation length (days)
Number of mares
118
130 110 90 70 50
April
May
June
July
Fig. 1. The number of mares that conceived in different months of the year.
a1,b1
a1,b1
344 Gestation length (days)
b1
342 340
b2 338 336 334
330 March
b1
342
a2,c1
340 338 b2,c2 336
February
March
April
May
June
Fig. 4. Gestation length (mean ± SEM) in mares that foaled in different months of the year. Differences between months of the year are indicated by the same letter with different numbers (P < 0.0001).
based on the year of conception was 5.5 days between 2000 and 2002 (Fig. 5). Gestation in mares carrying male foals (342.6 ± 0.43 days, n ¼ 323 Gs) was longer (P < 0.001) than in those carrying female foals (340.6 ± 0.44 days, n ¼ 326 Gs). Gestation in mares delivering foals weighing 70 kg and more (342.3 ± 0.52 days, n ¼ 189 Gs) was longer (P < 0.01) than in those delivering foals weighing up to 60 kg (341.3 ± 0.56 days, n ¼ 225 Gs) and 61e69 kg (341.2 ± 0.53 days, n ¼ 228 Gs).
334
3.2. Factors affecting the birth weight of foals
332
The birth weight of foals was associated with the weight of mares (P < 0.0001), age of mares (P < 0.0001) and sex of foals (P < 0.0001). Foals delivered by mares weighing 680 kg and more (67.3 ± 0.53 kg, n ¼ 226) were heavier (P < 0.0001) than those delivered by mares weighing up to 639 kg (61.5 ± 0.44 kg, n ¼ 191) and 640e679 kg (64.1 ± 0.47 kg, n ¼ 232). Foals delivered by mares 7e12 years (65.8 ± 0.42 kg, n ¼ 323) and 13e23 years old (64.5 ± 0.58 kg, n ¼ 166) were heavier (P < 0.0001) than those delivered by mares up to 6 years old (61.6 ± 0.54 kg, n ¼ 160). Foals delivered by mares 7e12 years old were about 1.2 kg heavier than those delivered by mares 13e23 years old (P < 0.0001). Male foals (65.5 ± 0.43 kg, n ¼ 323) were heavier (P < 0.0001) than female foals (63.4 ± 0.40 kg, n ¼ 326). The birth weight of foals in lactating mares (64.8 ± 0.41 kg, n ¼ 302) was almost significantly heavier (P < 0.08) than in non-lactating mares (64.1 ± 0.42 kg, n ¼ 347). No two-way interactions had significant effect on the birth weight of foals.
330 March
April
May
June
July
Fig. 2. Gestation length (mean ± SEM) in mares that conceived in different months of the year. Differences between months of the year are indicated by the same letter with different numbers (P < 0.001).
190 170 Number of mares
b1 a1
332
30
346
a2,b1
150 130 110
4. Discussion
90
4.1. Animal factors affecting gestation length
70 50 February
March
April
May
June
Fig. 3. The number of mares that foaled in different months of the year.
(P < 0.0001), and in the subsequent periods GL gradually decreased (P < 0.0001) up to the end of the breeding season in June (336.7 ± 0.92 days, n ¼ 63 Gs). The largest difference in GL (P < 0.01)
The sex of foals had an effect on GL in Old Kladruber horses. The development of colts from conception to delivery was significantly longer than the development of fillies. Other studies [5e8] similarly found that male foals are usually carried 2e3 days longer than females. The reason why the variation of GL is associated with the sex of the foal has not been satisfactorily explained yet. It has been postulated that the difference in foal gender is due to different endocrine functions of the fetus, interacting differently with the control of parturition [16]. This variability has been shown in human pregnancies to be related to differences in androgen action
M. Malinska et al. / Theriogenology 129 (2019) 116e120
a2,b1
348 Gestation length (days)
119
c2
346
c2
344 342
a1,c1
b2,c1
b2,c1 b2,c1
340 338 336 334 332 330 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017
Fig. 5. Gestation length (mean ± SEM) in mares that conceived in different years (2000, n ¼ 33; 2001, n ¼ 49; 2002, n ¼ 17; 2003, n ¼ 44; 2004, n ¼ 42; 2005, n ¼ 41; 2006, n ¼ 43; 2007, n ¼ 40; 2008, n ¼ 37; 2009, n ¼ 44; 2010, n ¼ 35; 2011, n ¼ 31; 2012, n ¼ 22; 2013, n ¼ 31; 2014, n ¼ 47; 2015, n ¼ 36; 2016, n ¼ 34; 2017, n ¼ 23). Differences between years are indicated by the same letter with different numbers (P < 0.05).
[17]. Our results showed that GL was associated with the birth weight of foals: colts were significantly heavier than fillies. This suggests that the sex of the foal can influence GL by means of the weight diversity between colts and fillies. Similarly, Wilsher and Allen [18] found that male foals were heavier than females. On the other hand, Elliott et al. [19] report that GL was not associated with the birth weight of foals. Gestation length was associated with the mare’s weight in the Old Kladruber breed. The development of foals from conception to delivery was significantly shorter in heavier mares than in lighter ones. It is difficult to compare these results with other studies, because only the effect of mares’ body height on GL has been thus far investigated [20], where no correlation between the height at the wither and GL was found. Our results also showed that the body weight of Old Kladruber mares was associated with the body weight of their foals. Heavier mares had significantly heavier foals than lighter mares. Thus, the birth weight of foals was not only influenced by the sex of foals, but also by the weight of mares. However, the body weight of mares is likely associated with GL in a different way than the sex of foals, because heavier mares had heavier foals at birth and shorter gestation, whereas male foals were heavier at birth and had longer gestation. The association between the weight of mares and birth weight of foals may be connected with uterine blood flow. Klewitz et al. [21] observed that mares with heavier foals at birth had a higher blood flow volume in the last 60 days of gestation. Similarly, blood flow volume was higher in cows giving birth to heavier calves compared with those that produced lighter calves [22]. Results showed that the age of Old Kladruber mares was associated with the birth weight of foals. Mares aged from 7 to 12 years and from 13 to 23 years delivered significantly heavier foals compared with those up to 6 years old. Moreover, mares aged from 7 to 12 years delivered significantly heavier foals compared with those from 13 to 23 years. Similarly, Klewitz et al. [21] observed that mares aged between 8 and 11 years delivered significantly heavier foals compared with younger and older mares. The explanation of these findings may be endometrial degeneration in older mares, whereas lower fetomaternal contact could be due to fewer previous pregnancies in younger mares [18]. Contrary to the mare’s weight, our results showed that the age of mares was not associated with GL. Similarly, several other studies failed to detect the association between mare’s age and GL [12,23,24]. This suggests that not all factors affecting the birth weight of foals necessarily influence GL. The length of gestation was significantly associated with lactation in Old Kladruber horses. The interval from conception to
foaling was shorter in lactating mares than in non-lactating ones. There is no study, to our knowledge, investigating the relationship between lactation and GL in horses. The influence of lactation on GL has been examined mainly in dairy cattle [13,14]. Further research will be necessary to explain the association between lactation and GL in mares. 4.2. Environmental factors affecting gestation length The month of conception had an effect on GL in Old Kladruber horses. Mares that conceived early in the year tended to have a longer gestation than those that conceived later in the breeding season. The average gestation was 9 days longer in mares that conceived in March, at the beginning of the breeding season, than at the end of the season, in July. That represents a decrease of about 2.3 days per month. Similar variability of GL was also described in other studies [7e11,23,25]. Based on these findings, a longer gestation resulting from earlier breeding was most likely related to environmental factors associated with the timing of breeding in the temperate zone. Mares are seasonal long-day breeders and in the northern hemisphere their natural breeding season lasts from April to October [26], triggered mainly by an increase in daylight [27]. Regulations in many breeding associations have established January 1 in the northern hemisphere as the official birth date of foals [28]. This can be achieved by breeding mares before the natural breeding season. The application of supplemental lighting treatments during the winter anestrus stimulates ovarian follicular activity and the long daylight photoperiod advances the date of the first ovulation [29]. The longer gestation in mares conceiving during the natural photoperiod early in the year observed in the present and other studies [5,30] may be an attempt to shift the foaling back to the natural season, when climate and food supplies are favorable for the survival and growth of foals [5]. A similar tendency was observed in dairy cattle [14]. The month of foaling also affected GL in Old Kladruber horses. A shorter gestation was found when foals were born in February. The longest gestation was seen when foals were born in March, decreasing in later months. Davies Morel et al. [12] report a significant increase of GL in Thoroughbred mares that foaled between January and April. A similar trend in GL was observed in Czech Warmblood mares [7]. Thus, the effects of the month of conception and month of foaling on GL are reversed early in the year not only in lighter breeds like Thoroughbreds or Warmbloods, but also in heavier horses such as the Old Kladruber.
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The year of conception was also associated with GL. Similar results were described in other studies [5,6]. Valera et al. [5] report that mares in dry years with high average temperatures have longer GL than in other years. The main reason could be that during hot, dry years foodstuffs may have lower nutritional quality. On the other hand, favorable weather conditions boost the nutritional value of grasslands, mares will have a better nutritional intake and foals will need less time to reach the proper weight for birth [12]. 5. Conclusion Awareness of several animal and environmental factors can help improve the prediction of foaling date. The length of gestation is not significantly affected by the mare’s age. On the other hand, mares that are lighter, carrying males, non-lactating, and those conceiving earlier in the year tend to have a longer gestation. Foals with a longer gestation are likely heavier at birth because of the longer time in the uterus. The month of foaling has a different effect on GL early in the year than the month of conception. The year of conception has an influence on GL. A more precise prediction of GL can help horse breeders in the management of mares during late pregnancy and parturition. Acknowledgements This study was supported by a grant IP 2018/045 from IGA AF MENDELU, Czech Republic. References B, Krupa E, Zavadilova L. Pedigree [1] Vostr a-Vydrov a H, Vostrý L, Hofmanova analysis of the endangered Old Kladruber horse population. Livest Sci 2016;185:17e23. [2] Janova E, Futas J, Klumplerova M, Putnova L, Vrtkova I, Vyskocil M, Frolkova P, Horin P. Genetic diversity and conservation in a small endangered horse population. J Appl Genet 2013;54:285e92. [3] Duggan VE, Holyoak GR, MacAllister CG, Cooper SR, Confer AW. Amyloid A in equine colostrum and early milk. Vet Immunol Immunopathol 2008;121: 150e5. [4] Aoki T, Yamakawa K, Ishii M. Factors affecting gestation length in heavy draft mares. J Equine Vet Sci 2013;33:437e40. [5] Valera M, Blesa F, Dos Santos R, Molina A. Genetic study of gestation length in Andalusian and Arabian mares. Anim Reprod Sci 2006;95:75e96. [6] Cilek S. The survey of reproductive success in Arabian horse breeding from 1976e2007 at Anadolu State farm in Turkey. J Anim Vet Adv 2009;8:389e96. [7] Rezac P, Pospisilova D, Slama P, Havlicek Z. Different effects of month of conception and birth on gestation length in mares. J Anim Vet Adv 2013;12: 731e5. [8] Marteniuk JV, Carleton CL, Lloyd JW, Shea ME. Association of sex of fetus, sire, month of conception, or year of foaling with duration of gestation in standardbred mares. J Am Vet Med Assoc 1998;212:1743e5.
[9] El-Wishy AB, El-Sayed MAI, Seida AA, Ghoneim IM, Serur BH. Some aspects of reproductive performance in Arabian mares in Egypt. Reprod Domest Anim 1990;25:227e34. rez CC, Rodríguez I, Mota J, Dorado J, Hidalgo M, Felipe M, Sanz J. Gestation [10] Pe length in carthusian spanishbred mares. Livest Prod Sci 2003;82:181e7. [11] Meliani S, Benallou B, Abdelhadi SA, Halbouche M, Naceri A. Environmental factors affecting gestation duration and time of foaling of pure bred Arabian mares in Algeria. Asian J Anim Vet Adv 2011;6:599e608. [12] Davies Morel MCG, Newcombe JR, Holland SJ. Factors affecting gestation length in the Thoroughbred mare. Anim Reprod Sci 2002;74:175e85. [13] Norman HD, Wright JR, Kuhn MT, Hubbard SM, Cole JB, VanRaden PM. Genetic and environmental factors that affect gestation length in dairy cattle. J Dairy Sci 2009;92:2259e69. [14] Tomasek R, Rezac P, Havlicek Z. Environmental and animal factors associated with gestation length in Holstein cows and heifers in two herds in the Czech Republic. Theriogenology 2017;87:100e7. [15] Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O. SAS for mixed models. second ed. Cary: SAS Institute Inc.; 2006. [16] Jainudeen MR, Hafez ESE. Gestation, prenatal physiology and parturition. In: Hafez ESE, Hafez B, editors. Reproduction in farm animals. seventh ed. Baltimore: Lippincott Williams and Wilkins; 2000. p. 140e55. [17] De Zegher F, Devlieger H, Eeckels R. Fetal growth: boys before girls. Horm Res 1999;51:258e9. [18] Wilsher S, Allen WR. The effects of maternal age and parity on placental and fetal development in the mare. Equine Vet J 2003;35:476e83. [19] Elliott C, Morton J, Chopin J. Factors affecting foal birth weight in Thoroughbred horses. Theriogenology 2009;71:683e9. [20] Heck L, Clauss M, S anchez-Villagra MR. Gestation length variation in domesticated horses and its relation to breed and body size diversity. Mamm Biol 2017;84:44e51. [21] Klewitz J, Struebing C, Rohn K, Goergens A, Martinsson G, Orgies F, Probst J, Hollinshead F, Bollwein H, Sieme H. Effects of age, parity, and pregnancy abnormalities on foal birth weight and uterine blood flow in the mare. Theriogenology 2015;83:721e9. [22] Herzog K, Koerte J, Flachowsky G, Bollwein H. Variability of uterine blood flow in lactating cows during the second half of gestation. Theriogenology 2011;75:1688e94. [23] Hintz HF, Williams J, Hillman R, Houssay H, Reyer RF. Effect of month of breeding on duration of gestation period of Thoroughbreds in Argentina. Equine Pract 1992;14:16e20. [24] Winter GHZ, Rubin MIB, De La Corte FD, Silva CAM. Gestational length and first postpartum ovulation of Criollo mares on a stud farm in Southern Brazil. J Equine Vet Sci 2007;27:531e4. € ro €cz J, Uphaus H, Distl O, Sieme H. Determinants of [25] Ewert M, Lüders I, Bo gestation length in Thoroughbred mares on German stud farms. Anim Reprod Sci 2018;191:22e33. [26] Williams GL, Thorson JF, Prezotto LD, Velez IC, Cardoso RC, Amstalden M. Reproductive seasonality in the mare: neuroendocrine basis and pharmacologic control. Domest Anim Endocrinol 2012;43:103e15. [27] Palmer E, Guillaume D. Some mechanisms involved in the response of mares to photoperiodic stimulation of reproductive activity. Reprod Domest Anim 1998;33:205e8. [28] Ginther OJ. Reproductive biology of the mare: basic and applied aspects. second ed. 1992. Cross Plains: Equiservices. [29] Nagy P, Guillaume D, Daels P. Seasonality in mares. Anim Reprod Sci 2000;60e61:245e62. [30] Nolan MB, Walsh CM, Duff N, McCrarren C, Prendergast RL, Murphy BA. Artificially extended photoperiod administered to pre-partum mares via blue light to a single eye: observations on gestation length, foal birth weight and foal hair coat at birth. Theriogenology 2017;100:126e33.
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Animal and environmental factors associated with gestation length in the endangered Old Kladruber horse M. Malinska, Z. Havlicek, E. Koru, P. Rezac* Mendel University, Zemedelska 1, 61300, Brno, Czech Republic
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 September 2018 Received in revised form 14 February 2019 Accepted 19 February 2019 Available online 20 February 2019
Little is known about factors influencing gestation length in heavier types of horses. The objective was to assess the effects of the weight and age of mares, weight and sex of foals, lactation, month and year of conception, month of foaling, stallion and mare on gestation length in the endangered Old Kladruber breed that once served as a heavy coach horse for ceremonies of the Imperial Court in Vienna. The study was performed at the stud farm Slatinany, Czech Republic and reports data from foaling seasons between 2001 and 2018. A total of 649 gestations were included in the study. Gestation in mares weighing 680 kg and more was 1.9 days shorter than in those weighing up to 639 kg (P < 0.0001). Gestation in lactating mares was 3.9 days shorter than in non-lactating mares (P < 0.0001). Gestation was longest in mares conceiving in March (343.9 ± 0.60 days); thereafter it gradually shortened, with the shortest (P < 0.0001) in mares conceiving in July (334.9 ± 0.90 days). Gestation length in mares increased (P < 0.0001) from February foaling (340.4 ± 0.73 days) to March foaling (343.6 ± 0.55 days), and then decreased (P < 0.0001) up to the end of the breeding season in June (336.7 ± 0.92 days). Year of conception had an effect on GL (P < 0.02). Gestation in mares carrying male foals was 2.0 days longer than in those carrying female foals (P < 0.01). Gestation in mares delivering foals weighing 70 kg and more was 1.0 days longer than in those delivering foals weighing up to 60 kg (P < 0.01). Mare’s age had no effect on gestation length. In conclusion, gestation length was associated with the weight of mares and foals, lactation, month and year of conception, month of foaling, and sex of foals. © 2019 Elsevier Inc. All rights reserved.
Keywords: Mare Gestation length The sex of the foal Weight Season Lactation
1. Introduction Old Kladruber is one of the world’s oldest horse breeds, bred especially for ceremonial purposes for more than 400 years. This endangered breed is an important genetic resource with unique characteristics and high cultural and historical value. The baroque character of the breed has been preserved up to the present [1]. The breed was based on imported Old Spanish and Italian horses. The Old Kladruber was bred to be a heavy type of carriage horse used for pulling the coach at ceremonies, usually four- or six-in-hand. Currently, 5e10 stallions and around 60e80 breeding mares, producing 35e40 foals, are kept on the stud farm Slatinany [2]. Accurate prediction of parturition is an important aspect of managing equine pregnancy and parturition, especially during high-risk phases of mares’ lives. Preparations for impending foaling would be more efficient with improved information on the
* Corresponding author. E-mail address: [email protected] (P. Rezac). https://doi.org/10.1016/j.theriogenology.2019.02.013 0093-691X/© 2019 Elsevier Inc. All rights reserved.
expected date of birth, because gestation length (GL) in mares is highly variable; ranging between 322 and 366 days with viable foals having been delivered [3]. However, little information exists about GL in heavier horse types [4]. Several factors influence prenatal development from conception to birth. The sex of foals is associated with GL: male foals are carried longer than females [5e8]. On the other hand, El-Wishy et al. [9] did not find any difference between colts and fillies. The month of conception also has an effect on GL: mares that conceived early in the year have longer gestation than those that conceived at the end of the breeding season [7,10,11]. The month of foaling has an effect on GL as well, but different than the month of conceiving. Mares that foaled in April had longer gestation than those that foaled in January [7,12]. The effect of milk production on GL was assessed in Holstein cattle. Cows with higher milk yield tend to have a longer GL [13,14]. Based on this we hypothesize that lactation may also influence GL in mares. The effect of the weight diversity of mares on GL has not been investigated yet. Similarly to Czech Warmblood mares [7], we assume that the month of conception and month of foaling may
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have a different effect on GL early in the year in Old Kladruber horses. It is not known whether the age of mares, sex of foals and year of conception in this old horse breed have a similar effect on GL compared to other breeds. Therefore, the objective of the present study was to examine the effects of the weight and age of mares, weight and sex of foals, lactation, month and year of conception, month of foaling, stallion and mare on GL in Old Kladruber horses. 2. Materials and methods 2.1. Animals The study did not include experiments on horses and the ethics committee of the Mendel University in Brno determined that it did not require approval. The study was performed on the stud farm Slatinany (Czech Republic) at a latitude of 50 north. All mares (n ¼ 153) and stallions (n ¼ 32) were Old Kladrubers. The average inbreeding coefficient was 0.13 [1]. Inclusion factors for breeding the mare were successful completion of performance tests, character and health. Exclusion factors for breeding the mare were reproductive problems, health problems, age and unsuitable offspring. The age of the mare at the first breeding was 5 years. The lactation period was at least 6 months. The mean number of births (±SEM) was 4.2 ± 0.2. The mean interval between foalings (±SEM) was 549 ± 12 days. The present and last gestation lengths were positively correlated (r ¼ 0.35, P < 0.01). The pregnancies selected were those that produced a single live foal in the period from 2001 to 2018 which did not die within 3 days of birth. Veterinary records were used to determine mating, ovulation and foaling dates for each pregnancy. In each case the ovulation date was determined, to within 24 h, using sequential ultrasonic scanning during estrus until ovulation was detected. Mating was then carried out on the basis of ultrasonic scanning evidence regarding the imminence of ovulation. Information on mare age and foal gender for each pregnancy was obtained from the stud records. A total of 649 foals and gestations (Gs) were included in the study. Mares were classified into three groups based on their age: (1) 4e6 years, (2) 7e12 years and (3) 13e23 years old. Mares were divided into three groups based on their weight 2 days after foaling: (1) 430e639 kg, (2) 640e679 kg and (3) 680e810 kg. Foals were classified into three groups based on their weight 2 days after birth: (1) 40e60 kg, (2) 61e69 kg and (3) 70e90 kg. Lactating mares were those lactating at the time of conception. All mares were kept in pasture under field conditions and natural photoperiod from spring to fall; they grazed native grass. In winter, pregnant mares were housed together in a spacious stable; they were given 12 kg hay/day. In the last trimester of gestation, mares were additionally fed 1.5 kg oats/day and 0.5 kg barley/day. Mares had full access to water and trace mineralized salt throughout the year. 2.2. Statistical analyses Statistical analyses were performed using SAS (SAS Institute Inc., Cary, NC, USA). The normality of the GL and foals’ birth weight distributions was established using the Kolmogorov-Smirnov test. The effects on GL and on the foals’ birth weight were analyzed using the mixed model procedure [15]. All models were analyzed in two steps: (1) fixed effects and their two-way interactions were examined; (2) only fixed effects were assessed, because all two-way interactions were not an important source of variation and were excluded from the final models. The fixed effect of the age of the mare on GL was also excluded from the final models, because of statistical insignificance.
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The effects on GL were tested using two models. The use of two different models was based on the finding that the month of foaling had a different effect on GL than the month of conceiving early in the year in the Old Kladruber horse. The final version of the first model of the effects on GL included the fixed effects of the month of conception (5 categories: months of the breeding season from March to July), year of conception (18 categories: from 2000 to 2017), lactation (2 categories: lactating vs non-lactating mares), sex of the foal (2 categories: males vs females), weight of the mare (3 categories: up to 639 kg, 640e679 kg, 680 kg and more), and weight of the foal (3 categories: up to 60 kg, 61e69 kg, 70 kg and more). The first model included the random mare and stallion effects and random residual effect. The final version of the second model of the effects on GL included the fixed effects of the month of foaling (5 categories: months of foaling from February to June), year of conception (18 categories: from 2000 to 2017), lactation (2 categories: lactating vs non-lactating mares), sex of the foal (2 categories: males vs females), weight of the mare (3 categories: up to 639 kg, 640e679 kg, 680 kg and more), and weight of the foal (3 categories: up to 60 kg, 61e69 kg, 70 kg and more). The second model included the random mare and stallion effects and random residual effect. The final model of the effects on the birth weight of foals included the fixed effects of the sex of the foal (2 categories: males vs females), age of the mare (3 categories: up to 6 years, 7e12 years, 13 years and more), and weight of the mare (3 categories: up to 639 kg, 640e679 kg, 680 kg and more). The model included the random mare and stallion effects and random residual effect. 3. Results 3.1. Factors affecting gestation length The mean GL (±SEM) in 649 gestations with spontaneous foaling of mature and viable foal was 341.6 ± 0.3 days (range: 311e388 days). The mean age of mares (±SEM) was 10.0 ± 0.2 years (range: 4e23 years). The mean weight of mares (±SEM) was 659.8 ± 1.7 kg. The proportion of male and female foals was 49.8% (323 of 649) and 50.2% (326 of 649), respectively. No two-way interactions nor mare’s age had significant effect on GL. In the first model, GL was associated with the month of conception (P < 0.0001), year of conception (P < 0.02), weight of mares (P < 0.0001), lactation (P < 0.0001), weight of foals (P < 0.01), and sex of foals (P < 0.01). In the second model, GL was associated with the month of foaling (P < 0.0001), year of conception (P < 0.02), weight of mares (P < 0.0001), lactation (P < 0.0001), weight of foals (P < 0.01), and sex of foals (P < 0.01). No two-way interactions nor mare’s age had significant effect on GL. Gestation in mares weighing 680 kg and more (340.4 ± 0.48 days, n ¼ 226 Gs) was shorter (P < 0.0001) than in those weighing up to 639 kg (342.3 ± 0.59 days, n ¼ 191 Gs) and 640e679 kg (342.1 ± 0.54 days, n ¼ 232 Gs). Gestation in lactating mares (339.5 ± 0.44 days, n ¼ 302 Gs) was shorter (P < 0.0001) than in non-lactating mares (343.4 ± 0.41 days, n ¼ 347 Gs). The number of mares that conceived in different months of the year is shown in Fig. 1. Distribution of GL for mares that conceived in different months of the year is shown in Fig. 2. Gestation was longest in mares conceiving in March (343.9 ± 0.60 days, n ¼ 144 Gs); thereafter GL gradually shortened, and the shortest GL (P < 0.0001) was in mares conceiving in July (334.9 ± 0.90 days, n ¼ 49 Gs). The number of mares that foaled in different months of the year is shown in Fig. 3. Distribution of GL for mares that foaled in different months of the year is shown in Fig. 4. Gestation lasted 340.4 ± 0.73 days (n ¼ 87 Gs) in mares foaling in February, the longest gestation (343.6 ± 0.55 days, n ¼ 170 Gs) was in mares foaling in March
M. Malinska et al. / Theriogenology 129 (2019) 116e120
170
346
150
344 Gestation length (days)
Number of mares
118
130 110 90 70 50
April
May
June
July
Fig. 1. The number of mares that conceived in different months of the year.
a1,b1
a1,b1
344 Gestation length (days)
b1
342 340
b2 338 336 334
330 March
b1
342
a2,c1
340 338 b2,c2 336
February
March
April
May
June
Fig. 4. Gestation length (mean ± SEM) in mares that foaled in different months of the year. Differences between months of the year are indicated by the same letter with different numbers (P < 0.0001).
based on the year of conception was 5.5 days between 2000 and 2002 (Fig. 5). Gestation in mares carrying male foals (342.6 ± 0.43 days, n ¼ 323 Gs) was longer (P < 0.001) than in those carrying female foals (340.6 ± 0.44 days, n ¼ 326 Gs). Gestation in mares delivering foals weighing 70 kg and more (342.3 ± 0.52 days, n ¼ 189 Gs) was longer (P < 0.01) than in those delivering foals weighing up to 60 kg (341.3 ± 0.56 days, n ¼ 225 Gs) and 61e69 kg (341.2 ± 0.53 days, n ¼ 228 Gs).
334
3.2. Factors affecting the birth weight of foals
332
The birth weight of foals was associated with the weight of mares (P < 0.0001), age of mares (P < 0.0001) and sex of foals (P < 0.0001). Foals delivered by mares weighing 680 kg and more (67.3 ± 0.53 kg, n ¼ 226) were heavier (P < 0.0001) than those delivered by mares weighing up to 639 kg (61.5 ± 0.44 kg, n ¼ 191) and 640e679 kg (64.1 ± 0.47 kg, n ¼ 232). Foals delivered by mares 7e12 years (65.8 ± 0.42 kg, n ¼ 323) and 13e23 years old (64.5 ± 0.58 kg, n ¼ 166) were heavier (P < 0.0001) than those delivered by mares up to 6 years old (61.6 ± 0.54 kg, n ¼ 160). Foals delivered by mares 7e12 years old were about 1.2 kg heavier than those delivered by mares 13e23 years old (P < 0.0001). Male foals (65.5 ± 0.43 kg, n ¼ 323) were heavier (P < 0.0001) than female foals (63.4 ± 0.40 kg, n ¼ 326). The birth weight of foals in lactating mares (64.8 ± 0.41 kg, n ¼ 302) was almost significantly heavier (P < 0.08) than in non-lactating mares (64.1 ± 0.42 kg, n ¼ 347). No two-way interactions had significant effect on the birth weight of foals.
330 March
April
May
June
July
Fig. 2. Gestation length (mean ± SEM) in mares that conceived in different months of the year. Differences between months of the year are indicated by the same letter with different numbers (P < 0.001).
190 170 Number of mares
b1 a1
332
30
346
a2,b1
150 130 110
4. Discussion
90
4.1. Animal factors affecting gestation length
70 50 February
March
April
May
June
Fig. 3. The number of mares that foaled in different months of the year.
(P < 0.0001), and in the subsequent periods GL gradually decreased (P < 0.0001) up to the end of the breeding season in June (336.7 ± 0.92 days, n ¼ 63 Gs). The largest difference in GL (P < 0.01)
The sex of foals had an effect on GL in Old Kladruber horses. The development of colts from conception to delivery was significantly longer than the development of fillies. Other studies [5e8] similarly found that male foals are usually carried 2e3 days longer than females. The reason why the variation of GL is associated with the sex of the foal has not been satisfactorily explained yet. It has been postulated that the difference in foal gender is due to different endocrine functions of the fetus, interacting differently with the control of parturition [16]. This variability has been shown in human pregnancies to be related to differences in androgen action
M. Malinska et al. / Theriogenology 129 (2019) 116e120
a2,b1
348 Gestation length (days)
119
c2
346
c2
344 342
a1,c1
b2,c1
b2,c1 b2,c1
340 338 336 334 332 330 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017
Fig. 5. Gestation length (mean ± SEM) in mares that conceived in different years (2000, n ¼ 33; 2001, n ¼ 49; 2002, n ¼ 17; 2003, n ¼ 44; 2004, n ¼ 42; 2005, n ¼ 41; 2006, n ¼ 43; 2007, n ¼ 40; 2008, n ¼ 37; 2009, n ¼ 44; 2010, n ¼ 35; 2011, n ¼ 31; 2012, n ¼ 22; 2013, n ¼ 31; 2014, n ¼ 47; 2015, n ¼ 36; 2016, n ¼ 34; 2017, n ¼ 23). Differences between years are indicated by the same letter with different numbers (P < 0.05).
[17]. Our results showed that GL was associated with the birth weight of foals: colts were significantly heavier than fillies. This suggests that the sex of the foal can influence GL by means of the weight diversity between colts and fillies. Similarly, Wilsher and Allen [18] found that male foals were heavier than females. On the other hand, Elliott et al. [19] report that GL was not associated with the birth weight of foals. Gestation length was associated with the mare’s weight in the Old Kladruber breed. The development of foals from conception to delivery was significantly shorter in heavier mares than in lighter ones. It is difficult to compare these results with other studies, because only the effect of mares’ body height on GL has been thus far investigated [20], where no correlation between the height at the wither and GL was found. Our results also showed that the body weight of Old Kladruber mares was associated with the body weight of their foals. Heavier mares had significantly heavier foals than lighter mares. Thus, the birth weight of foals was not only influenced by the sex of foals, but also by the weight of mares. However, the body weight of mares is likely associated with GL in a different way than the sex of foals, because heavier mares had heavier foals at birth and shorter gestation, whereas male foals were heavier at birth and had longer gestation. The association between the weight of mares and birth weight of foals may be connected with uterine blood flow. Klewitz et al. [21] observed that mares with heavier foals at birth had a higher blood flow volume in the last 60 days of gestation. Similarly, blood flow volume was higher in cows giving birth to heavier calves compared with those that produced lighter calves [22]. Results showed that the age of Old Kladruber mares was associated with the birth weight of foals. Mares aged from 7 to 12 years and from 13 to 23 years delivered significantly heavier foals compared with those up to 6 years old. Moreover, mares aged from 7 to 12 years delivered significantly heavier foals compared with those from 13 to 23 years. Similarly, Klewitz et al. [21] observed that mares aged between 8 and 11 years delivered significantly heavier foals compared with younger and older mares. The explanation of these findings may be endometrial degeneration in older mares, whereas lower fetomaternal contact could be due to fewer previous pregnancies in younger mares [18]. Contrary to the mare’s weight, our results showed that the age of mares was not associated with GL. Similarly, several other studies failed to detect the association between mare’s age and GL [12,23,24]. This suggests that not all factors affecting the birth weight of foals necessarily influence GL. The length of gestation was significantly associated with lactation in Old Kladruber horses. The interval from conception to
foaling was shorter in lactating mares than in non-lactating ones. There is no study, to our knowledge, investigating the relationship between lactation and GL in horses. The influence of lactation on GL has been examined mainly in dairy cattle [13,14]. Further research will be necessary to explain the association between lactation and GL in mares. 4.2. Environmental factors affecting gestation length The month of conception had an effect on GL in Old Kladruber horses. Mares that conceived early in the year tended to have a longer gestation than those that conceived later in the breeding season. The average gestation was 9 days longer in mares that conceived in March, at the beginning of the breeding season, than at the end of the season, in July. That represents a decrease of about 2.3 days per month. Similar variability of GL was also described in other studies [7e11,23,25]. Based on these findings, a longer gestation resulting from earlier breeding was most likely related to environmental factors associated with the timing of breeding in the temperate zone. Mares are seasonal long-day breeders and in the northern hemisphere their natural breeding season lasts from April to October [26], triggered mainly by an increase in daylight [27]. Regulations in many breeding associations have established January 1 in the northern hemisphere as the official birth date of foals [28]. This can be achieved by breeding mares before the natural breeding season. The application of supplemental lighting treatments during the winter anestrus stimulates ovarian follicular activity and the long daylight photoperiod advances the date of the first ovulation [29]. The longer gestation in mares conceiving during the natural photoperiod early in the year observed in the present and other studies [5,30] may be an attempt to shift the foaling back to the natural season, when climate and food supplies are favorable for the survival and growth of foals [5]. A similar tendency was observed in dairy cattle [14]. The month of foaling also affected GL in Old Kladruber horses. A shorter gestation was found when foals were born in February. The longest gestation was seen when foals were born in March, decreasing in later months. Davies Morel et al. [12] report a significant increase of GL in Thoroughbred mares that foaled between January and April. A similar trend in GL was observed in Czech Warmblood mares [7]. Thus, the effects of the month of conception and month of foaling on GL are reversed early in the year not only in lighter breeds like Thoroughbreds or Warmbloods, but also in heavier horses such as the Old Kladruber.
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The year of conception was also associated with GL. Similar results were described in other studies [5,6]. Valera et al. [5] report that mares in dry years with high average temperatures have longer GL than in other years. The main reason could be that during hot, dry years foodstuffs may have lower nutritional quality. On the other hand, favorable weather conditions boost the nutritional value of grasslands, mares will have a better nutritional intake and foals will need less time to reach the proper weight for birth [12]. 5. Conclusion Awareness of several animal and environmental factors can help improve the prediction of foaling date. The length of gestation is not significantly affected by the mare’s age. On the other hand, mares that are lighter, carrying males, non-lactating, and those conceiving earlier in the year tend to have a longer gestation. Foals with a longer gestation are likely heavier at birth because of the longer time in the uterus. The month of foaling has a different effect on GL early in the year than the month of conception. The year of conception has an influence on GL. A more precise prediction of GL can help horse breeders in the management of mares during late pregnancy and parturition. Acknowledgements This study was supported by a grant IP 2018/045 from IGA AF MENDELU, Czech Republic. References B, Krupa E, Zavadilova L. Pedigree [1] Vostr a-Vydrov a H, Vostrý L, Hofmanova analysis of the endangered Old Kladruber horse population. Livest Sci 2016;185:17e23. [2] Janova E, Futas J, Klumplerova M, Putnova L, Vrtkova I, Vyskocil M, Frolkova P, Horin P. Genetic diversity and conservation in a small endangered horse population. J Appl Genet 2013;54:285e92. [3] Duggan VE, Holyoak GR, MacAllister CG, Cooper SR, Confer AW. Amyloid A in equine colostrum and early milk. Vet Immunol Immunopathol 2008;121: 150e5. [4] Aoki T, Yamakawa K, Ishii M. Factors affecting gestation length in heavy draft mares. J Equine Vet Sci 2013;33:437e40. [5] Valera M, Blesa F, Dos Santos R, Molina A. Genetic study of gestation length in Andalusian and Arabian mares. Anim Reprod Sci 2006;95:75e96. [6] Cilek S. The survey of reproductive success in Arabian horse breeding from 1976e2007 at Anadolu State farm in Turkey. J Anim Vet Adv 2009;8:389e96. [7] Rezac P, Pospisilova D, Slama P, Havlicek Z. Different effects of month of conception and birth on gestation length in mares. J Anim Vet Adv 2013;12: 731e5. [8] Marteniuk JV, Carleton CL, Lloyd JW, Shea ME. Association of sex of fetus, sire, month of conception, or year of foaling with duration of gestation in standardbred mares. J Am Vet Med Assoc 1998;212:1743e5.
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