ANNA WYSOKIŃSKA, STANISŁAW KONDRACKI, DARIUSZ KOWALEWSKI, AGNIESZKA ADAMIAK, AND ELWIRA MUCZYŃSKA
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1 Bull Vet Inst Pulawy 53, , 2009 EFFECT OF SEASONAL FACTORS ON THE EJACULATE PROPERTIES OF CROSSBRED DUROC X PIETRAIN AND PIETRAIN X DUROC BOARS AS WELL AS PUREBRED DUROC AND PIETRAIN BOARS ANNA WYSOKIŃSKA, STANISŁAW KONDRACKI, DARIUSZ KOWALEWSKI, AGNIESZKA ADAMIAK, AND ELWIRA MUCZYŃSKA Department of Animal Reproduction and Hygiene, University of Podlasie, Siedlce, Poland sk@ap.siedlce.pl Received for publication June 24, 2009 Abstract The experimental material consisted of 12,285 ejaculates obtained from 93 boars, including 18 boars, 30 boars, 24 x crossbreds and 21 x crossbreds. The boars were utilised for at least 6 s and qualified for insemination from January 1, 1992 to December 31, Each ejaculate was assessed using standard methods for the following physical traits: volume, sperm concentration, spermatozoon motility, total number of spermatozoa, and number of insemination doses per ejaculate. The data obtained were classified into 12 sub-groups consisting of ejaculates collected in successive s. Ejaculates collected in the summer s had less spermatozoa than in the autumn and winter period. Ejaculates collected in the summer (mainly in July) yielded the least amount of insemination doses. Ejaculates of both types of crossbreds were characterised by greater spermatozoon motility compared with purebred boars, irrespective of the of ejaculate collection. Key words: boar, breeds, ejaculate, spermatozoa, season. The level of reproduction traits has a pronounced effect on livestock production effectiveness. Fertility and number of offspring are determined by a set of genetic, physiological, and environmental factors. The non-genetic factors determining boar reproduction include raising conditions while animals grow, feeding, and rearing conditions, care during breeding utilisation, manner of semen collection, and others. Genetic factors include genetic breed- or strain-related effects and crossing options. The breed structure of boars utilised in insemination depends mainly on demand in a given region for breeding boars characterised by certain genotypes. Two-breed boars are often used in reproduction because they show marked libido and easily ejaculate semen, which is particularly important as far as utilisation for insemination purposes is concerned. Not all crossbreeding options produce the same benefits in terms of ejaculate qualitative characteristics (8). Crossing effects depend to a large extent on the appropriate selection of breeds used to produce crossbred boars. In general, crossbred boars are characterised by good quality of ejaculates, which is displayed in heterosis effects indicating that crossbreds showed an advantage over purebred boars (24, 25, 30). There are also crossbreds whose ejaculates are characterised by less beneficial properties compared with purebred boars (33). The environmental factors influencing reproduction include seasonal factors like ambient temperature, day length and light intensity. Domestic pigs are polyoestrous animals but the effectiveness of the reproductive utilisation of both sows and boars displays seasonal variation. Over the summer s, semen quality deteriorates and, as a result, there is observed poorer fertilisation effectiveness. Seasonal fluctuations of reproduction effectiveness are to a large extent determined by variation in quantitative and qualitative properties of an ejaculate, as well as the mating activity of boars. Sensitivity of different breeds or crossbreds to seasonal factors may vary, however. The aim of the present work was to determine the effect of seasonal factors on ejaculate properties of crossbred x and boars as well as purebred boars of and breeds. Material and Methods The experimental material consisted of 12,285 ejaculates obtained from 93 boars, including 18 boars, 30 boars, 24 x crossbreds, and 21 x crossbreds kept at the Artificial Insemination Station in Zielkowice
2 678 owned by the Mazovian Centre of Animal Breeding and Reproduction Ltd in Łowicz. The ejaculates were collected using the gloved-hand technique (7) every 4-5 d. The studies included ejaculates obtained from boars utilised for least 6 s and qualified for insemination from January 1, 1992 to December 31, Each ejaculate was assessed using standard methods for the following physical traits: volume, sperm concentration, spermatozoon motility, total number of spermatozoa, and number of insemination doses per ejaculate. Ejaculate volume was determined after isolating the gelatinous fraction on the basis of ejaculate weight established on electronic balance. Sperm concentration per ejaculate was determined by the colorimetric method, while spermatozoa motility by means of the microscope under 200x magnification, setting the percentage of spermatozoa with proper motility in the total number of spermatozoa seen in the view field. The total number of spermatozoa and the number of insemination doses per ejaculate were determined by the computer programme SYSTEM SUL. The data obtained were classified into 12 sub-groups consisting of ejaculates collected in successive s (Table 1). The analysis of the variation of semen traits was carried out using a procedure according to the following model: Y ijk = µ + a i + b j + ab ij + e ijk where: Y ij trait value, µ - population mean, a i effect of boar breed, b j effect of the season of the year, ab ij effect of cooperation of controlled factors, e ij error. Differences between means were evaluated based upon Tukey s test. Results Table 2 presents data on the physical characteristics of ejaculates collected from and boars, as well as x and x crossbreds, over successive s of the year. The analysis of the data demonstrated that there was a clear and statistically-significant effect of season of the year on individual physical characteristics of the ejaculate. The ejaculates of the poorest quality, characterised by the smallest number of spermatozoa, were collected in July. The number of spermatozoa in ejaculates collected in late autumn and winter (November, December, January) was greater compared with ejaculates collected in the remaining s. Additionally, the ejaculates collected in this period yielded the greatest number of insemination doses. The ejaculates collected in December produced about 27 insemination doses, that is by almost three doses more compared with the ejaculates collected in July (P 0.01). Ejaculates of two-breed sires of both crossing variants were characterised by a considerably higher motility of spermatozoa than ejaculates of purebred boars irrespective of the ejaculate collection (Fig. 1). Ejaculates with the greatest motility of spermatozoa were produced by crossbreds, whereas the least motile were spermatozoa of purebred boars. Differences in the motility of spermatozoa from boars and crossbreds were substantial and reached 10% (P 0.01). Kondracki et al. (10) showed that variation in motility of spermatozoa is strongly boar breed-dependent. Moreover, it was found that spermatozoa of crossbred boars are more motile than purebred boars. in particular boars, which were found to have the lowest motility of spermatozoa. Month Table 1 Number of ejaculates in the particular s Breed x Total I ,046 II III ,083 IV ,054 V ,043 VI ,086 VII ,052 VIII ,019 IX X ,022 XI XII ,021 Total 1,748 4,819 3,065 2,653 12,285
3 x % LSD 0.05 =1.28 LSD 0.01 = Fig. 1. Percentage of spermatozoa with progressive motility depending on the season of the year. mld x LSD 0.05 =6.15 LSD 0.01 = Fig. 2. Total number of spermatozoa in ejaculate depending on the season of the year.
4 x number of doses LSD 0.05 =1.68 LSD 0.01 = Fig. 3. The number of insemination doses from one ejaculate depending on the season of the year. 300 x 280 ml LSD 0.05 =16.76 LSD 0.01 = Fig. 4. Volume of ejaculate depending on the season of the year.
5 x 650 thous./mm LSD 0.05 =36.82 LSD 0.01 = Fig. 5. Sperm concentration in the ejaculate depending on the season of the year. Table 3 Physical traits of boar ejaculates depending on the breed Breed Specification x Number of ejaculates 1,748 4,819 3,065 2,653 x A B C C Ejaculate volume (ml) sd Sperm concentration (thousand/mm 3 ) x A B C D sd x A B C D Spermatozoon motility (%) sd Total number of sperm in ejaculate (mld) Number of insemination doses per ejaculate x A B C D sd x A B B B sd Means followed by different letters within the rows are significantly different (A, B, C, D - P 0.01).
6 Table 2 Physical traits of boar ejaculates in the particular s of the year (means for and and x and breeds) Specification Month LSD0.05 LSD0.01 Number of ejaculates 1, ,083 1,054 1,043 1,086 1,052 1, , ,021 Ejaculate volume (ml) x sd Sperm concentration (thousand/mm 3 ) x sd Spermatozoon motility (%) x sd Total number of sperm in ejaculate (mld) x sd Number of insemination doses per ejaculate x sd
7 683 Fig. 2 displays data describing the total number of spermatozoa in the ejaculates of boars of individual breeds according to the season of the year. The analysis of the data revealed that, in terms of the number of spermatozoa per ejaculate, both purebred and boars, as well as x and x crossbreds were equally sensitive to seasonal factors. The ejaculates collected in December and January from boars representing all the sub-groups had the greatest number of spermatozoa, whereas the ejaculates with the lowest number of spermatozoa were collected in July from two-breed boars, and in June to September from purebred boars. As shown in Table 3, ejaculates of x crossbreds were characterised by the greatest number of spermatozoa, which was by over 14 and 4 mld higher compared with purebred and boars, respectively (P 0.01). boars produced ejaculates with an intermediate number of spermatozoa compared with ejaculates of purebred and boars. Furthermore, the data in Table 3 demonstrate that one ejaculate of crossbred boars and boars yielded a much greater number of insemination doses than ejaculates of boars. The differences were appreciable (about six doses from an ejaculate) and statistically significant (P 0.01). One ejaculate of boars yielded most insemination doses when collected over the autumnwinter s (September to February). For x boars, the greatest was the number of insemination doses from ejaculates collected in November, December, and February (Fig. 3). and purebred boars produced ejaculates, which yielded most insemination doses in autumn-winter s (November to January). Ejaculates of the greatest volume were collected over the autumn-winter s (Table 2). Ejaculates collected in November and December had by 20 ml greater volume than ejaculates collected in the spring (March, April, May) (P 0.01). Seasonal variation in ejaculate volume of both purebred and crossbred boars varied (Fig. 4). Ejaculates of x boars and boars, as well as boars had the smallest volume in spring (March, April, May) and summer s (July, August, September) whereas boars produced such ejaculates from February to April. Ejaculate volume increased in successive s. Purebred boars produced ejaculates whose volume was by over 40 ml greater compared with crossbred boars, and by almost 90 ml greater compared with boars (P 0.01) (Table 3). x as well as crossbreds produced ejaculates characterised by intermediate ejaculate volume compared with purebred animals. Discussion On the basis of data presented it can be inferred that ejaculate physical properties of purebred boars, as well as x and crossbredsm vary according to the season of the year. The most favourable ejaculate characteristics were observed in autumn and winter (November to January). These ejaculates had the greatest volume and contained most progressively motile spermatozoa. The number of insemination doses, which can be made from one ejaculate is an important characteristic from the standpoint of the economic effectiveness of boar utilisation. Most insemination doses were produced in late autumn and winter. Similar tendencies of changes in ejaculate characteristics were observed in wild pig x domestic pig crosses (12). Seasonal changes in the sexual activity of pigs may result from the close kinship of the domestic pig and European wild pig (9). Pigs are polyoestrous animals, which means that sows have multiple oestrous cycles and boars display sexual activity all year round. The wild pig (Sus scrofa ferus) is believed to be one of progenitors of present-day domestic pigs. Additionally, in terms of biological properties, pigs and wild pigs represent the same species, because the domestic pig can be successfully mated to the wild pig and their progeny are fertile. According to Kondracki et al. (9), the seasonal variability of boar semen properties results from domestic pigs atavistic tendency toward increased sexual activity during the natural period of being in oestrus, and decreased sexual activity during the period which does not favour reproduction in wild pigs. The fact that pigs are polyoestrous is not a natural condition but is an effect of domestication. Changes in sexual behaviour as well as sperm production by testicles are associated with the influence of gonadotropin hormones produced by the pituitary gland on the excretory function of the gonads. The testicles enlarge and the testosterone level increases in blood in autumn (5, 19). Mechanisms behind seasonal reproduction in wild pigs may be stimulated by changes in the day length over the year, which influences the secretion by the pineal gland and the amount of melatonin hormone excreted (13). Secretion of melatonin increases in darkness in all animals so the melatonin level is controlled by the daily pattern of light and darkness. In mammals melatonin regulates seasonality of reproductive processes (11). Seasonal reproduction in wild animals is a physiological adaptation of the animals to living under natural conditions, connected with changes in temperature and feed availability. The domestication of some animals led to partial or complete loss of adaptability to seasonal changes. In the domestic pig, the biologic reproductive rhythm, typical of its wild predecessor, is displayed in sows and boars in the form of the greatest mating activity over the autumn and winter period. It was found in the present work that ejaculates collected in the summer s, in July in particular, were characterised by the lowest number of spermatozoa. In addition, Flowers (4) reported a much lower number of spermatozoa in ejaculates collected in the summer s compared with the remaining s. Studies by other authors showed poorer semen quality, in terms of greater percentage of morphologically-altered spermatozoa in the summer (2, 12, 20, 31). Ejaculates collected in spring and summer
8 684 more frequently have spermatozoa with changes in head morphology as well as defective acrosomes (27). Park and Yi (21) demonstrated that most spermatozoa with the appropriate acrosome were found in the spring. An assessment of the acrosome condition is a very important criterion of semen usefulness for insemination because the enzymes in the acrosome play a very important role in the penetration of an ovum by the spermatozoon as they catalyse the reaction of hydrolytic breakdown of the zona pellucida of the ovum (29). A substantial drop in acrosin activity is observed in September and October (3). Many Polish and foreign researchers have investigated an effect of seasonality on boar reproduction. However, there is no agreement as to direct causes of the occurrence of changes in semen properties in different seasons of the year. Some authors have associated the changes with changing air temperature. High air temperature may negatively impact the process of spermatogenesis in that it may destroy the seminiferous epithelium of the testicles (18). It may lead to reduced production of spermatozoa, which is displayed in reduced spermatozoon concentration in the semen ejaculated (15). A negative influence of high temperatures on semen production was also reported in the works by Kunavongkrit et al. (16), Larsson and Einarsson (17), and Stone (26). Pigs easily adapt to being kept in warm facilities but if the temperature is high during the day and much lower at night it is much more difficult for the animals to adapt to such conditions, particularly if the differences between temperatures during the day and night are over 10 o C and humidity is over 90% (16). Apart from seasonal changes in ambient temperature, the process of spermatogenesis, and as a result the quality and quantity of semen, is impacted by the length of the light period. The influence of these factors may vary by boar breed, geographical situation as well as the extent of an animal s adaptation to changeable climatic conditions. Animals response to the length of the photoperiod varies very much and is to a great extent conditioned by the origin of animals. The more north of the equator a given breed originated, the more sensitive it is to the photoperiod (28). Some between-breed differences in the sensitivity of boars to seasonal factors were also confirmed in this work. Studies of sheep by Aquirre et al. (1) demonstrated that there was an impact of the length of photoperiod on the sexual activity of males. During a short day the testicles of the males were heavier and had greater perimeter compared with a long day. What is more, ejaculates collected in autumn s had the greatest volume and spermatozoon concentration as well as substantial motility (6). Sancho et al. (23) examined the effect of the photoperiod on the semen quality of Landrace boars and found that a short light period was associated with a decline in ejaculate volume, spermatozoa concentration, total number of spermatozoa in an ejaculate, and number of insemination doses per ejaculate. Moreover, the studies showed that the longer the photoperiod, the greater the number of spermatozoa with the appropriate morphology. Rivera et al. (22) believe that variation of day length is an important factor influencing mammal reproduction. They found that in boars this phenomenon did not significantly influence semen quality, although when the light period was shortened, there was observed slightly lower spermatozoon motility and a greater number of spermatozoa with morphological changes compared with the conditions of increasing the day length. According to these authors, air temperature and humidity are more important factors influencing semen quality. In conclusion, the effect of season of the year on ejaculate properties in crossbred boars, as well as purebred males, is clear and statistically confirmed. Ejaculates collected in the summer s had the less number of spermatozoa than in the autumn and winter period. Ejaculates collected in the summer (mainly in July) yielded the least amount of insemination doses. Ejaculates of both types of crossbreds were characterised by greater spermatozoa motility compared with purebred boars, irrespective of the of ejaculate collection. x crossbred boars produced ejaculates with the greatest number of spermatozoa, which was significantly larger compared with ejaculates of purebred boars. In turn, x boars produced ejaculates with an intermediate number of spermatozoa compared with purebred and boars. Ejaculates collected from boars were characterised by small volume and high spermatozoon concentration. The number of insemination doses per ejaculate obtained from one ejaculate of boars was by about six doses less compared with ejaculates of both and crossbred boars. The latter boars produced ejaculates of intermediate volume and concentration of spermatozoa compared with ejaculates of purebred boars. References 1. Aguirre V., Orihuela A., Vazquez R.: Effect of semen collection frequency on seasonal variation in sexual behaviour, testosterone, testicular size and semen characteristics of tropical hair rams. Trop Anim Health Prod 2007, 39, Brito L.F.C., Silva A.E.D.F., Rodrigues L.H., Vieira F.V., Deragon L.A.G., Kastelic J.P.: Effects of environmental factors, age and genotype on sperm production and semen quality in Bos indicus and Bos taurus AI bulls in Brazil. Anim Reprod Sci 2002, 70, Ciereszko A., Ottobre J.S., Glogowski J.: Effects of season and breed on sperm acrosin activity and semen quality of boars. 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9 King G.J., Macpherson J.W.: A comparison of two methods for boar semen collection. J Anim Sci 1973, 36, Kawęcka M.: Relationship between growth rate and meatiness of young boars of sire populations and their reproductive usefulness. Theses, Agricultural University, Szczecin, 2002, 206, Kondracki S., Antolik A., Zwierz B.: Characters of boar semen depending on the season of the year. Rocz Nauk Zoot 1997, 24, Kondracki S., Wysokińska A., Banaszewska D., Zajda J.: Breed-related variation in ejaculate traits of AI boars. Anim Sci Pap Rep 2006, 24, Kowalewska I., Kmieć M., Kulig H.: Melatonin and melatonin receptors. Medycyna Wet 2004, 60, Kozdrowski R., Dubiel A.: The effect of season on the properties of wild boar (Sus scrofa L.) semen. Anim Reprod Sci 2004, 80, Kozdrowski R., Dubiel A.: Reproductive biology of wild boars. Medycyna Wet 2004, 60, Kozdrowski R., Dubiel A.: Properties of semen in the annual cycle of wild boar/domestic pig hybrids. Medycyna Wet 2004, 60, Kunavongkrit A., Prateep P.: Influence of ambient temperature on reproductive efficiency in pigs: (1) boar semen quality. Pig J 1995, 35, Kunavongkrit A., Suriyasomboon A., Lundeheim N., Heard T.W., Einarsson S.: Management and sperm production of boars under differing environmental conditions. Theriogenology 2005, 63, Larsson K., Einarsson S.: Seminal changes in boars after heat stress. Acta Vet Scand 1984, 25, Malmgren L.: Experimentally induced testicular alternations in boars: sperm morphology changes in mature and peripubertal boars. Zbl Vet Med 1989, 36, Mauget R., Boissin J.: Seasonal changes in testis weight and testosterone concentration in the European wild boar (Sus scrofa L.). Anim Reprod Sci 1987, 13, Nichi M., Bols P.E.J., Züge R.M., Barnabe V.H., Goovaerts I.G.F., Barnabe R.C., Cortada C.N.M.: Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions. Theriogenology 2006, 66, Park C.S., Yi Y.J.: Comparison of semen characteristics. sperm freezability and testosterone concentration between and Yorkshire boars during seasons. Anim Reprod Sci 2002, 73, Rivera M.M., Quintero-Moreno A., Barrera X., Palomo M.J., Rigau T., Rodriguez-Gil J.E.: Natural Mediterranean photoperiod does not affect the main parameters of boar-semen quality analysis. Theriogenology 2005, 64, Sancho S., Pinart E., Briz M., Garcia-Gil N., Badia E., Bassols J., Kadar E., Pruneda A., Bussalleu E., Yeste M., Coll M.G., Bonet S.: Semen quality of postpubertal boars during increasing and decreasing natural photoperiods. Theriogenology 2004, 62, Smital J., De Sousa L.L., Mohnsen A.: Differences among breeds and manifestation of heterosis in AI boar sperm output. Anim Reprod Sci 2004, 80, Smital J.: Effects influencing boar semen. Anim Reprod Sci 2009, 110, Stone B.A.: Heat induced infertility of boars: the interrelationship between depressed sperm output and fertility and an estimation of the critical air temperature above which sperm is impaired. Anim Reprod Sci 1982, 4, Soderquist L., Janson L., Haard M., Einarsson S.: Influence of season, age, breed and some other factors on the variation in sperm morphological abnormalities in Swedish dairy A.I. bulls. Anim Reprod Sci 1996, 44, Sonderman J.P., Luebbe J.J.: Semen production and fertility issues related to differences in genetic lines of boars. Theriogenology 2008, 70, Śmigielska J., Strzeżek J.: The activity of acrosin inhibitors in the seminal plasma of bulls as an indicator of the intergrity of acrosome membranes. Zesz Probl Post Nauk Rol 1986, 263, Wysokińska A., Kondracki S.: Heterosis effects on physical traits of ejaculate in x and Hampshire x crossbred boars. Anim Sci Pap Rep 2004, 22, Wysokińska A., Kondracki S.: Frequency of sperm abnormalities in semen of crossbred boars x and Hampshire x and of purebred boars, Hampshire and depending on the season of the year. Zesz Nauk Prz Hod 2004, 72, Wysokińska A., Kondracki S., Banaszewska D.: The influence of the season on the semen quality of, Hampshire and purebred boars and crossbreds of x and Hampshire x. Rocz Nauk PTZ 2005, 1, Wysokińska A., Kondracki S., Banaszewska D.: An assessment of artifical insemination usefulness of the ejaculates gained from crossbred and purebred boars. Post Nauk Rol 2008, 4-5,
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