J. Appl. Poult. Res.
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J APPL POULT RES 2008. 17:101-108. doi:10.3382/japr.2007-00048
© 2008 Poultry Science Association
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Research Reports

Effect of Semen Extenders and Storage Time on Sperm Morphology of Four Chicken Breeds

A. Siudzinska and E. Lukaszewicz1

Wroclaw University of Environmental and Life Sciences, Department of Poultry Breeding, Chelmonskiego 38c, 51-630 Wroclaw, Poland

Correspondence: 1 Corresponding author: ewa{at}gen.ar.wroc.pl


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
A wide range of extenders are available for storing fowl semen. Three of them (the Lake extender, the EK extender described by lukaszewicz, and an extender described by Tselutin et al.) were tested for their suitability to store semen of 4 fowl breeds: Green-Legged Partridge, Black Minorca, White Crested Black Polish, and Italian Partridge. Changes in spermatozoa viability and morphology were evaluated in fresh neat semen and in semen diluted 1:4 and stored for 3, 6, and 24 h at 4°C. During the time of semen storage, a decrease in the number of live, morphologically normal spermatozoa and an increase in dead spermatozoa and spermatozoa with bent necks were observed. The EK extender was found to be the most suitable regardless of the fowl breed because the number of live spermatozoa did not decrease as much as in semen diluted with the other extenders. The Lake extender had the least beneficial effect on stored sperm morphology in every breed.

Key Words: sperm quality • in vitro storage • semen extender • sperm morphology


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The increasing importance of artificial insemination in poultry reproduction has caused investigators to become interested in developing the proper conditions for liquid (short-term) and frozen (long-term) semen storage [1–5]. The possibility of dilution and storage of avian sperm would make the work of poultry breeders much easier, enabling them to transport semen even to distant farms, to inseminate large groups of females, and to improve the utilization of sperm from superior males.

The most common procedure for short-term fowl semen storage (hours to days at refrigerator temperature) requires suspending sperm in an extender to retain their viability in vitro. Comparison of diluted and undiluted stored semen showed that applying extenders is necessary to sustain good-quality sperm [6, 7]. It was demonstrated that diluted fowl semen could be stored up to 24 h without impairing its viability and fertilizing ability [8–11].

An appropriate semen extender has to provide an energy source for spermatozoa and maintain pH and osmolarity levels identical to those of seminal plasma, the natural medium for sperm. Beginning with the first synthetic extender [1], experiments on the optimal extender composition for avian semen storage are still in progress. Since the biochemical composition of seminal plasma was first described [12, 13], extenders have been based on this composition. Glutamic acid, the most important constituent of avian seminal plasma, has become a standard component of extenders [14]. Many special buffered salt solutions are available that can be used as extenders of chicken semen [15], both commercial products and extenders developed by individual investigators. These extenders have different compositions, sometimes with special additives such as skimmed milk, egg albumin, gentamicin sulfate [2, 16], caproic acid [3], or even antibiotics [17].

Ensuring proper pH and osmotic pressure of the suspension is of great significance in sustaining the viability of spermatozoa. Several experiments have indicated that chicken sperm can tolerate a pH range of 6.0 to 8.0 [2, 18]. Lake and Ravie [11] obtained the most satisfying fertilization results when using sperm held at pH 6.8 and 7.1. Chicken sperm can maintain its fertilizing ability in extenders with osmolarities from 250 to 460 mOsmol/kg, but the ideal recommended osmotic pressure is 325 to 350 mOsmol/kg [16].

Domestic fowl comprise a wide range of breeds and strains. The history of fowl domestication dates back to approximately 2000 BCE. Breeders worked to generate lines with features useful in production and beautiful, colorful, fancy amateur breeds within one species. Significant morphological and physiological differences among males originating from different breeds are known to exist. Sperm quality depends on many variable factors, including species and breed of the bird [4, 19–21]. Just as there are many different poultry breeds, there are also breed differences in the storability of fowl semen [22]. Thus, sperm collected from roosters of different breeds requires different storage conditions to retain their viability [23]. Therefore, a need exists to adjust extenders to individual breeds.

The primary objective of this experiment was to determine whether semen originating from different chicken breeds would differ appreciably in semen characteristics and to evaluate the effect of extenders of different composition on the quality of sperm from the breeds concerned. For the purpose of devising methods for the storage of fowl spermatozoa in vitro for long periods of time, assessment of the basic quality of the sperm during the time of storage is indispensable. The quality of semen can be determined from the viability and morphology of the sperm. In this study, we investigated aspects of adverse morphological changes after storage of semen samples in selected extenders at 4°C for 24 h.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Semen was collected from males originating from 4 breeds of domestic fowl (Gallus gallus L.): Green-Legged Partridge, Black Minorca, White Crested Black Polish, and Italian Partridge. Green-Legged Partridge is kept in small households or agrotourist farms because of its easy adaptation to extensive environmental conditions and utilization of natural nutrients from green forages. They produce taste-quality meat and eggs with a lower cholesterol content. As an endangered breed, as demonstrated by the Food and Agriculture Organization of the United Nations, it was included in the Red Book of Animals. The Italian Partridge and Black Minorca belong to laying breeds kept by amateurs for egg laying as well as for decorative purposes, whereas the White Crested Black Polish is very famous in Poland as a typical fancy amateur breed. Every breed was represented by five 6-mo-old sexually mature males. Birds were kept in large individual cages and provided with appropriate management conditions (commercial feed for reproductive chickens and water ad libitum, temperature of approximately 15 to 18°C, and 14L:10D).

Semen was collected 2 times a week by dorso-abdominal massage [24]. Ejaculates obtained from males of the same breed were pooled and evaluated as one sample. Semen was collected 12 times from every male. To minimize stress and maximize the quality of semen, semen collection was always done by the same persons, at the same time, and under the same conditions. Special care was taken to avoid contamination of semen with feces, urates, and transparent fluid, which lower semen quality.

In freshly collected semen, the following parameters were examined: volume of pooled ejaculates (with automatic pipette), pH (P 731 pH meter [25]), osmolarity (Semi-Micro Osmometr) [26], concentration, and sperm morphology. On the basis of the total volume of pooled ejaculates, the mean volume of a single ejaculate was calculated within each breed. The concentration of spermatozoa was calculated by using a hemocytometer. Sperm morphology was evaluated in nigrosin-eosin smears [27] under a light microscope (1,250x) [28]. With a nigrosin-eosin staining technique, it is possible not only to demonstrate the viability of spermatozoa, but also to identify within a live sperm population the fraction of spermatozoa with abnormalities in morphology that may limit fertilization. This method is well tested and has been widely used to assess semen quality [7, 29, 30]. In every slide, 300 cells were counted and classified as live (unstained cells) and dead (every cell stained by eosin). Spermatozoa within the fraction of live cells were classified as morphologically normal (spindle-shaped head with well-marked acrosome and visible tail) or with a swollen head, bent neck, defective mid-piece, or other deformity (coiled tail, lack of tail, spermatides, etc.). The results of morphological evaluation were expressed as the percentage of particular categories of spermatozoa (300 cells = 100%).

Within 20 min of semen collection, samples were divided into 3 parts and diluted in a 1:4 ratio (0.25 mL of semen:1 mL of extender) at room temperature with 3 different extenders: the extender described by Lake [1], extender EK developed by lukaszewicz [4], and the extender elaborated by Tselutin et al. [31]. Composition, pH, and osmolarity of the extenders are shown in Table 1Go. Diluted semen was placed into 10-mL open glass tubes and stored at 4°C in a refrigerator. To determine the effect of semen extender on the viability of fowl semen, sperm morphology was evaluated after 3, 6, and 24 h of storage by using the nigrosineosin staining technique. The differences between measured parameters were analyzed with ANOVA and Duncan’s multiple range test (Statistica, version 7.1) [32].


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  		Table 1. Composition of extenders used for storing chicken semen for 24 h at 4°C1
 

   RESULTS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The smallest volume of semen was obtained from White Crested Black Polish males, with statistically significant differences (P ≤ 0.01) between this breed and the others (Table 2Go). Concentration of spermatozoa was highest in semen of the Black Minorca and White Crested Black Polish and lowest in Green-Legged Partridge semen (P ≤ 0.05). Semen acidity showed nearly neutral pH in each breed, with pH being lower in the Green-Legged Partridge than in the White Crested Black Polish and Italian Partridge. The average osmotic pressure varied from 311 to 327 mOsmol/kg among the breeds (Table 2Go).


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  		Table 2. Comparison of fresh semen collected from roosters of different breeds (n = 12; x ± SD)
 
There were no differences in the proportion of classes of spermatozoa in fresh semen collected from the Green-Legged Partridge, Black Minorca, and White Crested Black Polish. Italian Partridge semen had a lower percentage of normal live spermatozoa, a higher percentage of spermatozoa with bent necks, and a higher percentage of dead spermatozoa (P ≤ 0.01) than semen from the other 3 assessed breeds (Table 2Go).

Evaluation of the effect of storage time on sperm morphology showed that as semen storage increased, the quality of semen decreased. Regardless of extender and breed, from the beginning to the end of the storage period, the quantity of live, normal sperm declined and the number of sperm with bent necks and dead spermatozoa increased (Tables 3Go, 4Go, 5Go, and 6Go). There were significant differences (P ≤ 0.01 or P ≤ 0.05) in percentages of these spermatozoa forms between fresh semen and semen diluted and stored for 24 h. The least significant decrease in percentage of live, normal spermatozoa and the smallest increase in dead spermatozoa and spermatozoa with bent necks were observed when semen was diluted with EK extender.


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  		Table 3. Effect of semen extenders1 and storage time on Green-Legged Partridge sperm morphology (n = 12; x ± SD)
 

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  		Table 4. Effect of semen extenders1 and storage time on Black Minorca sperm morphology (n = 12 x ± SD)
 

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  		Table 5. Effect of semen extenders1 and storage time on White Crested Black Polish sperm morphology (n = 12; x ± SD)
 

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  		Table 6. Effect of semen extenders1 and storage time on Italian Partridge sperm morphology (n = 12; x ± SD)
 
Evaluation of the extender effect on sperm morphology showed that there were differences (P ≤ 0.01 or P ≤ 0.05) in the percentages of morphologically normal spermatozoa and spermatozoa with bent necks among samples diluted with the extenders elaborated by Lake [1], lukaszewicz [4], and Tselutin et al. [31] for all investigated breeds. In relation to fresh semen, the number of live, morphologically normal spermatozoa was higher in the EK extender than in the extenders described by Lake [4] and Tselutin et al. [31] after 3, 6, and 24 h. The number of spermatozoa with bent necks was lower in semen stored in EK extender than in semen stored in the Lake extender, with statistically significant differences (P ≤ 0.01 or P ≤ 0.05) between these extenders for all the breeds after 3, 6, and 24 h of storage (Tables 3Go, 4Go, 5Go, and 6Go).

There was no extender effect on midpiece defects, and the same was found for spermatozoa with swollen heads (Tables 3Go, 4Go, 5Go, and 6Go). The number of these forms of spermatozoa did not change with an increase in storage time. When spermatozoa with other deformities were considered, the only differences (P ≤ 0.05) observed were between the Lake extender and the rest of the extenders for the Green-Legged Partridge breed after 3 h of storage (Table 3Go). With regard to dead spermatozoa, no marked differences were observed among semen diluted with the investigated extenders (Tables 3Go, 4Go, 5Go, and 6Go).


   DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Evaluation of semen quality is of great importance from the point of view of artificial insemination. It is known that sperm originating from different breeds vary in many respects. The Green-Legged Partridge, Black Minorca, White Crested Black Polish, and Italian Partridge are breeds without great commercial significance. Nevertheless, compared with commercial chicken lines, the volume of ejaculates and sperm concentrations of semen collected from the 4 evaluated breeds were not very different. Podgórny et al. [33] found that White Rock roosters produced, on average, 0.42 mL of semen, whereas the concentration of spermatozoa was 3.45 x 109 cells/mL. The volume of ejaculates and sperm concentrations measured in semen from laying and meat-type chicken lines reached, respectively, 0.2 and 0.35 mL with 5.0 and 5.7 x 109 sperm/mL [29]. Several investigators [34, 35] revealed that the number of live spermatozoa without any deformities varied from 91 to 94%, which is in contrast with the results of our study. lukaszewicz [7] found 60 to 85% live, morphologically normal spermatozoa in White Leghorn semen, which is more consistent with our results compared with the values mentioned above. On the other hand, the number of dead spermatozoa observed in semen collected from the 4 breeds examined was higher than that observed for White Leghorn semen [7, 36].

During the time of storage, a decrease in live, morphologically normal spermatozoa and an increase in dead spermatozoa and spermatozoa with bent necks were observed, which was in agreement with studies performed by other investigators [7, 30].

Our data led us to conclude that the Lake, EK and Tselutin extenders had varied effects on sperm viability. On the basis of the current results, we must underline that the EK extender had the least harmful effect on spermatozoa regardless of the fowl breed. The number of live spermatozoa did not decrease in the EK extender as much as in other extenders despite the breed differences observed in sperm morphology in fresh semen. The EK extender was previously used with good results during attempts to freeze gander semen [4, 5]. Therefore, this extender appears to be useful across species. The Lake extender seemed to have the least beneficial effect on stored semen. This conclusion confirmed the results of an earlier study, which demonstrated that, compared with 2 other media, only in the Lake extender did the number of live spermatozoa in chicken semen stored for 6 h at 41°C decline significantly [37].

The percentage of spermatozoa with bent necks in semen diluted with EK extender was relatively low compared with semen diluted with the 2 other extenders. Hyperosmolarity (390 mOsmol/kg) of the EK extender did not cause adverse morphological changes in sperm morphology in relation to forms with bent necks. Some investigators indicated that Rhode Island Red semen stored for 24 h and diluted with hypertonic extender tended to display a lower number of spermatozoa with bent necks compared with semen diluted with an isotonic extender [38]. Perhaps the EK extender with higher osmolarity was better for storing fowl semen than extenders with osmolarities similar to seminal plasma, such as the Lake and Tselutin extenders. Giesen and Sexton [39] suggested that hypertonic extenders could improve turkey spermatozoa survival in vitro, whereas Bakst [40] concluded that a reduction of osmolarity below 200 mOsmol/kg adversely affected fowl and turkey sperm membranes, causing swelling at the midpiece. The above-mentioned observations might suggest that in slightly hypertonic conditions, sperm membranes are more resistant to different types of damage caused by uptake of water.

The number of dead spermatozoa in semen collected from the examined breeds and stored did not vary with the evaluated extender used, yet there were significant differences in the numbers of sperm with deformities. By using the nigrosin-eosin staining technique and assessment of morphological forms of the sperm, it was possible to disclose that the largest group of spermatozoa with abnormalities (mainly bent necks) occurred when semen was diluted with the Lake extender. Other methods of evaluation of sperm that qualify cells only as live and dead perhaps would not have revealed that extenders had varied effects on sperm morphology.


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. Prior to this study, the EK extender was used as the extender for gander semen. The results presented herein revealed that it can be used satisfactorily for liquid storage of fowl semen.
  2. The Lake extender had fewer beneficial effects on stored semen; therefore, on the basis of the present results, it is not recommended for liquid chicken semen storage.
  3. Perhaps extenders of slightly higher osmolarities are more suitable for storing chicken semen in a liquid stage than those of osmolarities similar to seminal plasma.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

  1. Lake, P. E. 1960. Studies on the dilution and storage of fowl semen. J. Reprod. Fertil. 1:30–35.[Medline]
  2. Van Wambeke, F. 1967. Storage of fowl semen: 1. Preliminary results with new extenders. J. Reprod. Fertil. 13:571–575.[Abstract/Free Full Text]
  3. Lake, P. E., and O. Ravie. 1981. An attempt to improve the fertility of stored fowl semen with certain additives in a basic extender. Reprod. Nutr. Dev. 21:1077–1084.[Medline]
  4. lukaszewicz, E. 2002. Cryopreservation of Anser anser L. gander semen (in Polish). Zeszt. Nauk. AR we Wroclawiu, 440, cxc:1–111.
  5. lukaszewicz, E., M. Chrzanowska, A. Jerysz, and B. Chelmonska. 2004. Attempts on freezing the Greylag (Anser anser L.) gander semen. Anim. Rep. Sci. 80:163–173.[CrossRef]
  6. Bilgili, S. F., K. J. Sexton, and J. A. Renden. 1987. Fluorometry of poultry semen: Influence of dilution and storage on chicken spermatozoa viability and fertility. Poult. Sci. 66:2032–2035.[Medline]
  7. lukaszewicz, E. 1988. Study of extenders for cock’s semen storage in the light of laboratory estimation and fertility rates (in Polish). Zeszt. Nauk. AR we Wroclawiu, 168:43–59.
  8. Van Wambeke, F. 1972. Fertility and hatchability results with fowl spermatozoa stored in fresh and freeze-dried extender. Br. Poult. Sci. 13:179–183.[CrossRef][Medline]
  9. Sexton, T. J. 1977. A new poultry semen extender: 1. Effect of extension on the fertility of chicken semen. Poult. Sci. 56:1443–1444.[Medline]
  10. Sexton, T. J. 1978. A new poultry semen extender: 3. Effect of storage conditions on the fertilizing capacity of chicken semen stored at 5°C. Poult. Sci. 57:285–289.[Medline]
  11. Lake, P. E., and O. Ravie. 1979. The effect on fertility of storing fowl semen for 24 h at 5°C in fluids of different pH. J. Reprod. Fertil. 57:149–155.[Abstract/Free Full Text]
  12. Lake, P. E. 1966. A cytochemical examination of the spermatozoon of the domestic fowl. Res. Vet. Sci. 7:121–127.[Medline]
  13. Cherms, F. L. 1967. Elemental analysis of turkey semen. Poult. Sci. 46:1605–1606.[Medline]
  14. Lake, P. E., and W. M. McIndoe. 1959. The glutamic acid and creatine content of cock seminal plasma. Biochem. J. 71:303–306.[Medline]
  15. Bootwalla, S. M., and R. D. Miles. 1992. Development of extenders for domestic fowl semen. World’s Poult. Sci. J. 48:121–128.[CrossRef]
  16. Sexton, T. J., and T. A. Fewlass. 1978. A new poultry semen extender: 2. Effect of the extender components on the fertilizing capacity of chicken semen stored at 5°C. Poult. Sci. 57:277–284.[Medline]
  17. Harris, G. C., T. D. Hobbs, J. E. Brown, and L. B. Warren. 1963. The storage of turkey spermatozoa in sodium citrate and carbon dioxide extenders. Poult. Sci. 42:536–538.
  18. Bogdonoff, P. D., and C. S. Shaffner. 1954. The effect of pH on in vitro survival, metabolic activity, and fertilizing capacity of chicken semen. Poult. Sci. 33:665–669.[Medline]
  19. Gee, G. F. 1995. Artificial insemination and cryopreservation of semen from nondomestic birds. Pages 262–279 in Proc. First Int. Symp. Artif. Insemin. Poultry. M. R. Bakst and G. J. Whisart, ed. Poult. Sci. Assoc., Savoy, IL.
  20. Fujihara, N. 1990. Comparative physiology of avian semen and spermatozoa. Pages 132–155 in Advances in Reproductive Biology. C. Youngqing and Z. Cheng, ed. Chin. Acad. Sci., Beijing, China.
  21. lukaszewicz, E. 2000. Czestotliwosc pobierania nasienia od gesiorów bialych wloskich a ilosciowe i jakosciowe cechy nasienia pobieranego w ciagu calego sezonu reprodukcyjnego (in Polish). Zeszt. Nauk. Prz. Hod. 49:447–457.
  22. Wilcox, F. H., C. S. Shaffner, and H. R. Wilson. 1961. Breed differences in storing chicken semen. J. Hered. 52:119–121.[Free Full Text]
  23. Lake, P. E. 1983. Factors affecting the fertility level in poultry, with special reference to artificial insemination. World’s Poult. Sci. J. 39:106–117.[CrossRef]
  24. Burrows, W. H., and J. P. Quinn. 1937. The collection of spermatozoa from the domestic fowl and turkey. Poult. Sci. 16:19–24.
  25. Elster Microcomputer, Germany.
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  27. Jaskowski, L. 1966. Attempts to evaluate active spermatozoa with the use of contrast staining. Zesz. Prob. Pod. Nauk. Rol. 61:195.
  28. Jenaval, Carl Zeiss, Jena, Germany.
  29. Lake, P. E., and J. M. Stewart. 1978. Artificial insemination in poultry. Minist. Agric., Fish. Food Bull. 213. Her Majesty’s Stationery Office, London, UK.
  30. Blesbois, E., I. Grasseau, and D. Hermier. 1999. Changes in lipid content of fowl spermatozoa after liquid storage at 2 to 5°C. Theriogenology 52:325–334.[CrossRef][Medline]
  31. Tselutin, K., L. Narubina, T. Mavrodina, and B. Tur. 1995. Cryopreservation of poultry semen. Br. Poult. Sci. 36:805–811.[Web of Science][Medline]
  32. Statistica. 2005. Data Analysis Software System, Version 7.1. StatSoft Inc., Tulsa, OK.
  33. Podgórny, E., S. Weëyk, and A. lada-Gorzowska. 1976. Variations in cock sperm quality throughout the year. Pages 1057–1060 in Proc. VIII Int. Congr. Anim. Reprod. Artif. Insemin., Cracow, Poland. M. Tischner and J. Pilch, ed. Wroclawska Drukarnia Naukowa, Wroclaw, Poland.
  34. Van Voorst, A., and F. R. Leenstra. 1995. Fertility rate of daily collected and cryopreserved fowl semen. Poult. Sci. 74:136–140.[Medline]
  35. Tselutin, K., F. Seigneurin, and E. Blesbois. 1999. Comparison of cryoprotectans and methods of cryopreservation on fowl spermatozoa. Poult. Sci. 78:586–590.[Abstract/Free Full Text]
  36. Al-Daraji, H. J. 2001. Sperm-egg penetration in laying breeder flocks: a technique for the prediction of fertility. Br. Poult. Sci. 42:266–270.[CrossRef][Medline]
  37. Howarth, B., Jr. 1979. Comparison of extenders for holding cock semen six hours at 41°C. J. Reprod. Fertil. 57:149–155.[Abstract/Free Full Text]
  38. Van Wambeke, F. 1977. The effect of tonicity of storage media for fowl semen on the occurrence of spermatozoa with bent necks, fertility and hatchability. Br. Poult. Sci. 18:163–168.[CrossRef][Medline]
  39. Giesen, A. F., and T. J. Sexton. 1983. Beltsville poultry semen extender: 7. Comparison of commercial diluents for holding turkey semen six hours at 15°C. Poult. Sci. 62:379–381.[Medline]
  40. Bakst, M. R. 1980. Fertilizing capacity and morphology of fowl and turkey spermatozoa in hypotonic extender. J. Reprod. Fertil. 60:121–127.[Abstract/Free Full Text]




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