Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T08:04:59.990Z Has data issue: false hasContentIssue false
  • English
  • Français

Effective freezing rate for semen cryopreservation in endangered Mediterranean brown trout (Salmo trutta macrostigma) inhabiting the Biferno river (South Italy)

Published online by Cambridge University Press:  28 December 2015

Nicolaia Iaffaldano ,
Michele Di Iorio ,
Angelo Manchisi ,
Stefano Esposito  and
Pier Paolo Gibertoni
Nicolaia Iaffaldano*
Affiliation:
Department of Agricultural, Environmental and Food Sciences, University of Molise, via De Sanctis snc, 86100 Campobasso, Italy. Department of Agricultural, Environmental and Food Sciences, University of Molise, 86100 Italy.
Michele Di Iorio
Affiliation:
Department of Agricultural, Environmental and Food Sciences, University of Molise, 86100 Italy.
Angelo Manchisi
Affiliation:
Department of Agricultural, Environmental and Food Sciences, University of Molise, 86100 Italy.
Stefano Esposito
Affiliation:
Mediterranean Trout Research Group–Centro di ricerche ‘I Giardini dell’Acqua’, 42037 Collagna (RE), Italy.
Pier Paolo Gibertoni*
Affiliation:
Department of Agricultural, Environmental and Food Sciences, University of Molise, via De Sanctis snc, 86100 Campobasso, Italy. Mediterranean Trout Research Group–Centro di ricerche ‘I Giardini dell’Acqua’, 42037 Collagna (RE), Italy.
*
All correspondence to: Nicolaia Iaffaldano, Department of Agricultural, Environmental and Food Sciences, University of Molise, via De Sanctis snc, 86100 Campobasso, Italy. Tel. +39 0874 404697. Fax +39 0874 404855. E-mail: [email protected]
Pier Paolo Gibertoni, Mediterranean Trout Research Group–Centro di ricerche ‘I Giardini dell’Acqua’ – 42037 Collagna (RE), Italy. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study was designed to determine: (i) the in vitro effects of different freezing rates on post-thaw semen quality of Mediterranean brown trout (Salmo trutta macrostigma) from the Biferno river; and (ii) the in vivo fertilization and hatching percentage of freezing rate giving rise to the best post-thaw semen quality.

Pooled semen samples were diluted 1:3 (v:v) in a freezing extender composed of 300 mM glucose, 10% egg yolk and 10% dimethyl sulfoxide (DMSO). The extended semen was packaged in 0.25 ml plastic straws and frozen at different heights above the liquid nitrogen surface (1, 5 or 10 cm) for 10 min to give three different freezing rates. Semen samples were thawed at 30°C for 10 s. The variables assessed after thawing were sperm motility, duration of motility and viability.

Our results clearly indicate a significant effect of freezing rate on post-thaw semen quality. Semen frozen 5 cm above the liquid nitrogen surface showed the best quality after freezing/thawing. Based on these in vitro data, 2 groups of 200 eggs were fertilized with fresh semen or semen frozen 5 cm above the liquid nitrogen surface. Fertilization and hatching rates recorded for eggs fertilized with frozen semen were significantly lower (25.4% and 22.5%, respectively) than the ones obtained using fresh semen (87.8% and 75.5%, respectively). An effective freezing protocol will allow for the creation of a sperm cryobank to recover the original population of Mediterranean brown trout in the Biferno river.

Keywords

Freezing rateMediterranean brown trout (Salmo trutta macrostigma)Post-thaw semen qualityReproductive performancesSperm cryopreservation
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 668 - 675
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akçay, E., Bozkurt, Y., Seçer, S. & Tekin, N. (2004). Cryopreservation of mirror carp semen. Turk. J. Vet. Anim. Sci. 28, 837–43.Google Scholar
Bailey, J.L., Bilodeau, J.F. & Cormier, N. (2000). Semen cryopreservation in domestics animals: a damaging and capaciting phenomenon. J. Androl. 21, 1–7.CrossRefGoogle Scholar
Bianco, P.G., Caputo, V., Ferrito, V., Lorenzoni, M., Nonnis Marzano, F., Stefani, F., Sabatini, A. & Tancioni, L. (2013). Pesci d’acqua dolce. In Lista Rossa IUCN dei Vertebrati Italiani (eds Rondinini, C., Battistoni, A., Peronace, V., & Teofili, C.), 54 pp. Roma: Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare.Google Scholar
Billard, R. (1977). A new technique of artificial insemination for salmonids using a sperm diluent. Fisheries 1, 24–5.Google Scholar
Billard, R. & Zhang, T. (2001). Techniques of genetic resource banking in fish. In Cryobanking the Genetic Resources: Wildlife Conservation for the Future? (eds Watson, P.F. & Holt, W.V.), pp. 145–70. UK, Taylor & Francis.Google Scholar
Bozkurt, Y., Akçay, E., Tekin, N. & Seçer, S. (2005). Effect of freezing techniques, extenders and cryoprotectants on the fertilization rate of frozen rainbow trout (Oncorhynchus mykiss) sperm. Isr. J. Aquacult-Bamid. 57, 125–30.Google Scholar
Bozkurt, Y., Yavas, I. & Karaca, F. (2012). Cryopreservation of brown trout (Salmo trutta macrostigma) and ornamental Koi carp (Cyprinus carpio) sperm. In Current Frontiers in Cryopreservation (ed. Katkov, I.), 15, 29–304. Croatia: In Tech.Google Scholar
Cabrita, E., Alvarez, R., Anel, L., Rana, K.J. & Herraez, M.P. (1998). Sublethal damage during cryopreservation of rainbow trout sperm. Cryobiology 37, 245–53.Google Scholar
Cabrita, E., Sarasquete, C., Martínez-Páramo, S., Robles, V., Beirão, J., Pérez-Cerezales, S. & Herráez, M.P. (2010). Cryopreservation of fish sperm: applications and perspectives. J. Appl. Ichthyol. 26, 623–35.CrossRefGoogle Scholar
Cabrita, E., Martínez-Páramo, S., Gavaia, P.J., Riesco, M.F., Valcarce, D.G., Sarasquete, C., Herráez, M.P. & Robles, V. (2014). Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture 432, 389–401.Google Scholar
Chao, N.H. & Liao, I.C. (2001). Cryopreservation on finfish and shellfish gametes and embryos. Aquaculture 197, 161–89.Google Scholar
Conget, P., Fernandez, M., Herrera, G. & Minguell, J.J. (1996). Cryopreservation of rainbow trout (Oncorhynchus mykiss) spermatozoa using programmable freezing. Aquaculture 143, 319–29.Google Scholar
Drokin, S., Stein, H. & Bartseherer, H. (1998). Effect of cryopreservation on the fine structure of spermatozoa of rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta F. fario). Cryobiology 37, 263–70.Google Scholar
Dziewulska, K. & Domagała, J. (2013). Effect of pH and cation concentrations on spermatozoan motility of sea trout (Salmo trutta m. trutta L.). Theriogenology 79, 48–58.Google Scholar
Fujikawa, S. & Miura, K. (1986). Plasma membrane ultrastructural changes caused by mechanical stress in the formation of extracellular ice as a primary cause of slow freezing injury in fruit-bodies of basidiomycetes (Lyophyllum ulmarium). Cryobiology 23, 371–82.Google Scholar
Gausen, D. (1993). The Norwegian gene bank programme for Atlantic salmon (Salmo salar). In Genetic conservation of salmonid fishes. (eds Cloud, J.C. & Thorgaard, G.H.), pp. 181–7. New York, Plenum Press.Google Scholar
Gibertoni, P.P., Jelli, F. & Bracchi, P. (1998). Allevamento, riproduzione e reintroduzione in ambiente naturale di trote fario di ‘ceppo mediterraneo’, Salmo (trutta) trutta, L. Annali della Facoltà di Medicina Veterinaria, XVIII, 1–20. Università di Parma.Google Scholar
Gopalakrishnan, A., Thakur, K.L., Ponniah, A.G., Kumar, K. & Dayal, R. (1999). Cryopreservation of brown trout (Salmo trutta fario) sperm: the influence of extender composition and fertilization procedure. Fish. Technol. 36, 104–109.Google Scholar
Gwo, J.C. & Arnold, C.R. (1992). Cryopreservation of Atlantic croaker spermatozoa: evaluation of morphological changes. J. Exp. Zool. 264, 444–453.CrossRefGoogle ScholarPubMed
Henry, M.A., Noiles, E.E., Gao, D., Mazur, P. & Critser, J.K. (1993). Cryopreservation of human spermatozoa. IV. The effects of cooling rate and warming rate on the maintenance of motility, plasma membrane integrity, and mitochondrial function. Fertil. Steril. 60, 911–8.Google Scholar
Holt, W.V. (2000). Basic aspects of frozen storage of semen. Anim. Reprod. Sci. 62, 3–22.Google Scholar
Iaffaldano, N., Romagnoli, L., Manchisi, A. & Rosato, M.P. (2011). Cryopreservation of turkey semen by the pellet method: effects of variables such as the extender, cryoprotectant concentration, cooling time and warming temperature on sperm quality determined through principal components analysis. Theriogenology 76, 794–801.CrossRefGoogle ScholarPubMed
Iaffaldano, N., Di Iorio, M. & Rosato, M.P. (2012). The cryoprotectant used, its concentration and the equilibrium time are critical for the successful cryopreservation of rabbit sperm: dimethylacetamide versus dimethylsulfoxide. Theriogenology 78, 1381–9.Google Scholar
Jelli, F. & Gibertoni, P.P. (1999). Recupero e reintroduzione di ceppi autoctoni di trota fario, Salmo (trutta) trutta L., nel bacino del fiume Secchia. Atti del Convegno: Recupero e reintroduzione dei ceppi autoctoni di trota fario, Salmo (trutta) trutta L., di ‘ceppo mediterraneo’ in ambienti appenninici tipici. Esperienze a confronto; 1999; Reggio Emilia.Google Scholar
Johnson, L.A., Weitze, K.F., Fiser, P. & Maxwell, W.M.C. (2000). Storage of boar semen. Anim. Reprod. Sci. 62, 142–72.Google Scholar
Labbé, C. & Maisse, G. (2001). Characteristics and freezing tolerance of brown trout spermatozoa according to rearing water salinity. Aquaculture 201, 287–99.Google Scholar
Lahnsteiner, F., Weismann, T. & Patzner, R.A. (1992). Fine structural changes in spermatozoa of the grayling, Thymallus thymallus (Pisces: Teleostei), during routine cryopreservation. Aquaculture 103, 73–84.Google Scholar
Lahnsteiner, F., Berger, B., Weismann, T. & Patzner, R. (1996b). Fine structure and motility of spermatozoa and composition of the seminal plasma in the perch. J. Fish. Biol. 47, 492–508.Google Scholar
Lahnsteiner, F., Weismann, T. & Patzner, R.A. (1997). Methanol as cryoprotectant and the suitability of 1.2 ml and 5 ml straws for cryopreservation of semen from salmonid fishes. Aquacult. Res. 28, 471–9.CrossRefGoogle Scholar
Lahnsteiner, F. (2000). Semen cryopreservation in the salmonidae and in the northern pike. Aquacult. Res. 31, 245–58.Google Scholar
Maldjian, A., Pizzi, F., Gliozzi, T., Cerolini, S., Penny, P. & Noble, R. (2005). Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology 63, 411–21.Google Scholar
Mansour, N., Richardson, G.F. & McNiven, M.A. (2006). Effect of extender composition and freezing rate on post-thaw motility and fertility of Arctic char, Salvelinus alpinus (L.), spermatozoa. Aquacult. Res. 37, 862–8.Google Scholar
Martínez-Páramo, S., Pérez-Cerezales, S., Gómez-Romano, F., Blanco, G., Sánchez, J.A. & Herráez, M.P. (2009). Cryobanking as tool for conservation of biodiversity: effect of brown trout sperm cryopreservation on the male genetic potential. Theriogenology 71, 594–604.Google Scholar
Mazur, P. (1984). Freezing of living cells: mechanisms and applications. Am. J. Physiol. 247, 125–42.CrossRefGoogle Scholar
Müller, K., Müller, P., Pincemy, G., Kurz, A. & Labbé, C. (2008). Characterization of sperm plasma membrane properties after cholesterol modification: consequences for cryopreservation of rainbow trout spermatozoa. Biol. Reprod. 78, 390–9.Google Scholar
Penserini, M., Nonnis Marzano, F., Gandolfi, G., Maldini, M., Marconato, E. & Gibertoni, P.P (2006). Fenotipi della trota mediterranea: metodologia di indagine molecolare combinata e selezione morfologica per l’identificazione degli esemplari autoctoni. J. Freshwater Biol. 34, 69– 75.Google Scholar
Rana, K.J. (1995). Preservation of gametes. In Broodstock Management and Eggs and Larval Quality (eds Bromage, N.R., & Roberts, R.J.), pp. 53–76. UK: Cambridge University Press.Google Scholar
Roldan, E. & Garde, J. (2004). Biotecnologìa de la reproducciòn y conservaciòn de especies en peligro de extinciòn. In Los Retos Medioambientales del siglo XXI. La Conservacioòn de la Biodiversidad en Espana (ed. Gomendio, M.), pp. 283–307. Bilbao: Fundaciòn BBVA.Google Scholar
Sarvi, K., Niksirat, H., Amiri, B.M., Mirtorabi, S.M., Rafiee, G.R. & Bakhtiyari, M. (2006). Cryopreservation of semen from the endangered Caspian brown trout (Salmo trutta caspius). Aquaculture 256, 564–9.Google Scholar
Suquet, M.D., Dreanno, C., Petton, B., Normant, Y., Omnes, M.H. & Billard, R. (1998). Longterm effects of the cryopreservation of turbot (Psetta maxima) spermatozoa. Aquat. Living. Resour. 11, 45–8.Google Scholar
Tekin, N., Seçer, S., Akçay, E. & Bozkurt, Y. (2003). Cryopreservation of rainbow trout (Oncorhynchus mykiss) semen. Isr. J. Aquacult-Bamid. 55, 208–12.Google Scholar
Tiersch, T.R., Yang, H., Jenkins, J.A. & Dong, Q. (2007). Sperm cryopreservation in fish and shellfish. Soc. Reprod. Fertil. Suppl. 65, 493–508.Google Scholar
Yavas, I., Bozkurt, Y. & Yıldız, C. (2014). Cryopreservation of scaly carp (Cyprinus carpio) sperm: effect of different cryoprotectant concentrations on post thaw motility, fertilization and hatching success of embryos. Aquacult. Int. 22, 141–148.Google Scholar
Zhang, X.Z., Liu, Y., Xu, Y., Wang, C.L., Sawant, M.S., Li, J. & Chen, S.L. (2003). Cryopreservation of flounder (Paralichthys olivaceus) sperm with a practical methodology. Theriogenology 60, 989–96.Google Scholar