Cryopreservation in fish: current status and pathways to quality assurance and quality control in repository development
Leticia Torres A , E. Hu B and Terrence R. Tiersch A C
+ Author Affiliations
- Author Affiliations
A Aquatic Germplasm and Genetic Resources Center, School of Renewable Natural Resources, Louisiana State University Agricultural Center, 2288 Gourrier Avenue, Baton Rouge, LA 70820, USA.
B Center for Aquaculture Technologies, Inc., 8395 Camino Santa Fe. Suite E, San Diego, CA 92126, USA.
C Corresponding author. Email: ttiersch@agcenter.lsu.edu
Reproduction, Fertility and Development 28(8) 1105-1115 https://doi.org/10.1071/RD15388
Submitted: 2 October 2015 Accepted: 21 November 2015 Published: 7 January 2016
Abstract
Cryopreservation in aquatic species in general has been constrained to research activities for more than 60 years. Although the need for application and commercialisation pathways has become clear, the lack of comprehensive quality assurance and quality control programs has impeded the progress of the field, delaying the establishment of germplasm repositories and commercial-scale applications. In this review we focus on the opportunities for standardisation in the practices involved in the four main stages of the cryopreservation process: (1) source, housing and conditioning of fish; (2) sample collection and preparation; (3) freezing and cryogenic storage of samples; and (4) egg collection and use of thawed sperm samples. In addition, we introduce some key factors that would assist the transition to commercial-scale, high-throughput application.
Additional keywords: commercial scale, quality, spermatozoa.
References
Åberg Andersson, M., Silva, P. I. M., Steffensen, J. F., and Höglund, E. (2011). Effects of maternal stress coping style on offspring characteristics in rainbow trout (Oncorhynchus mykiss). Horm. Behav. 60, 699–705.| Effects of maternal stress coping style on offspring characteristics in rainbow trout (Oncorhynchus mykiss).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVagsrbK&md5=0d94dd4ec4cf969bc9bb0a91f30629ceCAS | 21983227PubMed |
Alavi, S. M. H., and Cosson, J. (2006). Sperm motility in fishes. II. Effects of ions and osmolality: a review. Cell Biol. Int. 30, 1–14.
| Sperm motility in fishes. II. Effects of ions and osmolality: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsF2ntr8%3D&md5=a72db912a85ae47d208092432d630211CAS |
Aliniya, M., Khara, H., Noveiri, S. B., and Dadras, H. (2013). Influence of age of common carp (Cyprinus carpio) broodstock on reproductive traits and fertilization. Turk. J. Fish. Aquat. Sci. 13, 19–25.
| Influence of age of common carp (Cyprinus carpio) broodstock on reproductive traits and fertilization.Crossref | GoogleScholarGoogle Scholar |
Amann, R. P., and Waberski, D. (2014). Computer-assisted sperm analysis (CASA): capabilities and potential developments. Theriogenology 81, 5–17.e3.
| Computer-assisted sperm analysis (CASA): capabilities and potential developments.Crossref | GoogleScholarGoogle Scholar | 24274405PubMed |
Asturiano, J. F., Sorbera, L. A., Carrillo, M., Zanuy, S., Ramos, J., Navarro, J. C., and Bromage, N. (2001). Reproductive performance in male European sea bass (Dicentrarchus labrax, L.) fed two PUFA-enriched experimental diets: a comparison with males fed a wet diet. Aquaculture 194, 173–190.
| Reproductive performance in male European sea bass (Dicentrarchus labrax, L.) fed two PUFA-enriched experimental diets: a comparison with males fed a wet diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFajtr4%3D&md5=987363c88afb9cf8e75da544076525e0CAS |
Babiak, I., Glogowski, J., Luczynski, M. J., and Luczynski, M. (1997). Effect of individual male variability on cryopreservation of northern pike, Esox lucius L., sperm. Aquacult. Res. 28, 191–197.
| Effect of individual male variability on cryopreservation of northern pike, Esox lucius L., sperm.Crossref | GoogleScholarGoogle Scholar |
Babiak, I., Marschháuser, V., Ottesen, O., Rudolfsen, G., Eggen, B., and Babiak, J. (2012). Effects of extender, storage and sperm-to-egg ratio on cryopreservation success of Atlantic cod (Gadus morhua L.) sperm. J. Appl. Ichthyol. 28, 941–947.
| Effects of extender, storage and sperm-to-egg ratio on cryopreservation success of Atlantic cod (Gadus morhua L.) sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Gqsr3F&md5=1fe16e9ea616f799fd9c0c4b97908bceCAS |
Blaxter, J. H. S. (2011). Seminal studies in the cryopreservation of fish sperm. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green.) pp. 886–889. (World Aquaculture Society: Baton Rouge, LA.)
Boryshpolets, S., Kowalski, R. K., Dietrich, G. J., Dzyuba, B., and Ciereszko, A. (2013). Different computer-assisted sperm analysis (CASA) systems highly influence sperm motility parameters. Theriogenology 80, 758–765.
| Different computer-assisted sperm analysis (CASA) systems highly influence sperm motility parameters.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sfotlCjtw%3D%3D&md5=ae12d90f259ebbefe8d58ec3bcc578b1CAS | 23932168PubMed |
Brooks, S., Tyler, C. R., and Sumpter, J. P. (1997). Egg quality in fish: what makes a good egg? Rev. Fish Biol. Fish. 7, 387–416.
| Egg quality in fish: what makes a good egg?Crossref | GoogleScholarGoogle Scholar |
Butts, I. A. E., Trippel, E. A., and Litvak, M. K. (2009). The effect of sperm to egg ratio and gamete contact time on fertilization success in Atlantic cod Gadus morhua L. Aquaculture 286, 89–94.
| The effect of sperm to egg ratio and gamete contact time on fertilization success in Atlantic cod Gadus morhua L.Crossref | GoogleScholarGoogle Scholar |
Butts, I. A. E., Sørensen, S. R., Politis, S. N., Pitcher, T. E., and Tomkiewicz, J. (2014). Standardization of fertilization protocols for the European eel, Anguilla anguilla. Aquaculture 426–427, 9–13.
| Standardization of fertilization protocols for the European eel, Anguilla anguilla.Crossref | GoogleScholarGoogle Scholar |
Caffey, R. H., and Tiersch, T. R. (2000). Cost analysis for integrating cryopreservation into an existing fish hatchery. J. World Aquac. Soc. 31, 51–58.
| Cost analysis for integrating cryopreservation into an existing fish hatchery.Crossref | GoogleScholarGoogle Scholar |
Carter, A. B., Carton, A. G., McCormick, M. I., Tobin, A. J., and Williams, A. J. (2015). Maternal size, not age, influences egg quality of a wild, protogynous coral reef fish Plectropomus leopardus. Mar. Ecol. Prog. Ser. 529, 249–263.
| Maternal size, not age, influences egg quality of a wild, protogynous coral reef fish Plectropomus leopardus.Crossref | GoogleScholarGoogle Scholar |
Chalah, T., and Brillard, J. P. (1998). Comparisson of assessment of fowl sperm viability by eosin–nigrosin and dual fluorescence (SYBR-14/PI). Theriogenology 50, 487–493.
| Comparisson of assessment of fowl sperm viability by eosin–nigrosin and dual fluorescence (SYBR-14/PI).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1Kqsg%3D%3D&md5=2b314c6a6b0c36ec444e4411496e3ba6CAS | 10732141PubMed |
Chatakondi, N. G., and Davis, K. B. (2013). Maturity stage and plasma testosterone levels are related to sperm production in blue catfish, Ictalurus furcatus. Aquacult. Res. 44, 161–166.
| Maturity stage and plasma testosterone levels are related to sperm production in blue catfish, Ictalurus furcatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFWlt78%3D&md5=92044f39b1e4902932ef580dc7be33b9CAS |
Ciereszko, A., and Dabrowski, K. (1993). Estimation of sperm concentration of rainbow trout, whitefish and yellow perch using a spectrophotometric technique. Aquaculture 109, 367–373.
| Estimation of sperm concentration of rainbow trout, whitefish and yellow perch using a spectrophotometric technique.Crossref | GoogleScholarGoogle Scholar |
Cosson, J. (2004). The ionic and osmotic factors controlling motility of fish spermatozoa. Aquac. Int. 12, 69–85.
| The ionic and osmotic factors controlling motility of fish spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFSjsro%3D&md5=c0d2394fb792398e51b5bacc74118fe8CAS |
Cuevas-Uribe, R., and Tiersch, T. R. (2011). Estimation of fish sperm concentration by use of spectrophotometry. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green.) pp. 162–200. (World Aquaculture Society: Baton Rouge, LA.)
Daly, J., and Tiersch, T. R. (2011). Flow cytometry for the assessment of sperm quality in aquatic species. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green) pp. 201–207. (World Aquaculture Society, Baton Rouge, LA.)
Donaldson, E., Solar, I. I., and Harvey, B. (2011). Induced ovulation and spermiation, and factors influencing gamete quality of fishes. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green) pp. 37–45. (World Aquaculture Society, Baton Rouge, LA.)
Dong, Q., Eudeline, B., Huang, C., and Tiersch, T. R. (2005). Standardization of photometric measurement of sperm concentration from diploid and tetraploid Pacific oysters, Crassostrea gigas (Thunberg). Aquacult. Res. 36, 86–93.
| Standardization of photometric measurement of sperm concentration from diploid and tetraploid Pacific oysters, Crassostrea gigas (Thunberg).Crossref | GoogleScholarGoogle Scholar |
Food and Agriculture Organization of the United Nations (FAO) (2011). ‘Draft Guidelines for the Cryoconservation of Animal Genetic Resources.’ Available at http://www.fao.org/docrep/meeting/022/mb553e.pdf. [verified 28 September 2015].
Galo, J. M., Ribeiro, R. P. B., Streit, D. P., Albuquerque, D. M., Fornari, D. C., Roma, C. F. C., and Guerreiro, L. R. J. (2015). Oocyte quality of Tambaqui (Colossoma macropomum) during the reproductive season. Braz. J. Biol. 75, 279–284.
| Oocyte quality of Tambaqui (Colossoma macropomum) during the reproductive season.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2Mbps1amtA%3D%3D&md5=b4853bd4ac903ad1425dd5cc3698a949CAS | 26132008PubMed |
Garner, D. L., Johnson, L. A., Yue, S. T., Roth, B. L., and Haugland, R. P. (1994). Dual DNA staining assessment of bovine sperm viability using SYBR-14 and propidium iodide. J. Androl. 15, 620–629.
| 1:STN:280:DyaK2M3jvVansw%3D%3D&md5=2a2fa8f4fd97ae1ed49c1ecb7f134479CAS | 7721666PubMed |
Geffen, A. J. (1999). Variations in sperm motility of the Atlantic herring Clupea harengus. Mar. Biol. 134, 637–643.
| Variations in sperm motility of the Atlantic herring Clupea harengus.Crossref | GoogleScholarGoogle Scholar |
Giesing, E. R., Suski, C. D., Warner, R. E., and Bell, A. M. (2011). Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proc. Biol. Sci. 278, 1753–1759.
| Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring.Crossref | GoogleScholarGoogle Scholar | 21068041PubMed |
Glenn, D. W., III, Lang, R. P., and Tiersch, T. R. (2011). Evaluation of extenders for refrigerated storage of koi carp and goldfish sperm. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green.) pp. 107–124. (World Aquaculture Society: Baton Rouge, LA.)
Hadfield, C. A., and Clayton, L. A. (2011). Fish quarantine: current practices in public zoos and aquaria. J. Zoo Wildl. Med. 42, 641–650.
| Fish quarantine: current practices in public zoos and aquaria.Crossref | GoogleScholarGoogle Scholar | 22204059PubMed |
Hauville, M. R., Rhody, N. R., Resley, M. J., Bell, J. G., Main, K. L., and Migaud, H. (2015). Comparative study of lipids and fatty acids in the liver, muscle, and eggs of wild and captive common snook broodstock. Aquaculture 446, 227–235.
| Comparative study of lipids and fatty acids in the liver, muscle, and eggs of wild and captive common snook broodstock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXns1Gqsb8%3D&md5=3c4a0543aad86268878e77382fc8b575CAS |
He, S., and Woods, L. C. (2004). Effects of dimethyl sulfoxide and glycine on cryopreservation induced damage of plasma membranes and mitochondria to striped bass (Morone saxatilis) sperm. Cryobiology 48, 254–262.
| Effects of dimethyl sulfoxide and glycine on cryopreservation induced damage of plasma membranes and mitochondria to striped bass (Morone saxatilis) sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1CntLY%3D&md5=cf432b4c13c432ea67bf0f4333a09516CAS | 15157774PubMed |
Hu, E. (2012). High-throughput sperm cryopreservation of aquatic species. Ph.D. Thesis, Louisiana State University, Baton Rouge, LA, USA.
Hu, E., and Tiersch, T. R. (2011). Development of high-throughput cryopreservation for aquatic species. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green.) pp. 995–1003. (World Aquaculture Society: Baton Rouge, LA.)
Hu, E., Liao, T. W., and Tiersch, T. R. (2013). A quality assurance initiative for commercial-scale production in high-throughput cryopreservation of blue catfish sperm. Cryobiology 67, 214–224.
| A quality assurance initiative for commercial-scale production in high-throughput cryopreservation of blue catfish sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sfitlKlsA%3D%3D&md5=c608091c6dddc2ccd30e7ddde18672b9CAS | 23872356PubMed |
Hu, E., Bosworth, B., Baxter, J., and Tiersch, T. R. (2014). On-site evaluation of commercial-scale hybrid catfish production using cryopreserved blue catfish sperm. Aquaculture 426–427, 88–95.
| On-site evaluation of commercial-scale hybrid catfish production using cryopreserved blue catfish sperm.Crossref | GoogleScholarGoogle Scholar |
Iigo, M., and Aida, K. (1995). Effects of season, temperature, and photoperiod on plasma melatonin rhythms in the goldfish, Carassius auratus. J. Pineal Res. 18, 62–68.
| Effects of season, temperature, and photoperiod on plasma melatonin rhythms in the goldfish, Carassius auratus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2Mzls1Snsw%3D%3D&md5=c390531e410b95db4c222a132ca9b682CAS | 7629692PubMed |
Izquierdo, M. S., Fernández-Palacios, H., and Tacon, A. G. J. (2001). Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197, 25–42.
| Effect of broodstock nutrition on reproductive performance of fish.Crossref | GoogleScholarGoogle Scholar |
Jenkins, J. A. (2011). Minimizing microbial contamination of sperm samples. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green.) pp. 684–687. (World Aquaculture Society: Baton Rouge, LA.)
Kjesbu, O. S., Kryvi, H., Sundby, S., and Solemdal, P. (1992). Buoyancy variations in eggs of Atlantic cod (Gadus morhua L.) in relation to chorion thickness and egg size: theory and observations. J. Fish Biol. 41, 581–599.
| Buoyancy variations in eggs of Atlantic cod (Gadus morhua L.) in relation to chorion thickness and egg size: theory and observations.Crossref | GoogleScholarGoogle Scholar |
Li, M. L., Manning, B. B., Robinson, E. H., Bosworth, B. G., and Wolters, W. R. (2001). Comparison of growth, processing yield, and body composition of USDA103 and Mississippi ‘normal’ strains of channel catfish fed diets containing three concentrations of protein. J. World Aquac. Soc. 32, 402–408.
| Comparison of growth, processing yield, and body composition of USDA103 and Mississippi ‘normal’ strains of channel catfish fed diets containing three concentrations of protein.Crossref | GoogleScholarGoogle Scholar |
Li, M. L., Robinson, E. H., Manning, B. B., Yant, D. R., Chatakondi, N. G., Bosworth, B. G., and Wolters, W. R. (2004). Comparison of the channel catfish, Ictalurus punctatus (NWAC103 Strain) and the channel × blue catfish, I. punctatus × I. furcatus, F1 hybrid for growth, feed efficiency, processing yield, and body composition. J. Appl. Aquaculture 15, 63–71.
| Comparison of the channel catfish, Ictalurus punctatus (NWAC103 Strain) and the channel × blue catfish, I. punctatus × I. furcatus, F1 hybrid for growth, feed efficiency, processing yield, and body composition.Crossref | GoogleScholarGoogle Scholar |
Liu, B., Liu, Y., and Wang, X. (2015). The effect of stocking density on growth and seven physiological parameters with assessment of their potential as stress response indicators for the Atlantic Salmon (Salmo salar). Mar. Freshwater Behav. Physiol. 48, 177–192.
| The effect of stocking density on growth and seven physiological parameters with assessment of their potential as stress response indicators for the Atlantic Salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnsFGgsLo%3D&md5=dc2b574fe1d46674960dc3aef2f729a6CAS |
Lu, J. C., Huang, Y. F., and Lü, N. Q. (2014). Computer-aided sperm analysis: past, present and future. Andrologia 46, 329–338.
| Computer-aided sperm analysis: past, present and future.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3srhslKjsw%3D%3D&md5=7ed2b3d9935b053e322625ce51b8c369CAS | 23550608PubMed |
Meryman, H. T. (1966). Review of biological freezing. In ‘Cryobiology’. (Ed. H. T. Meryman.) pp. 1–114. (Academic Press: New York.)
Montgomery, D. C. (2008). ‘Introduction to Statistical Quality Control.’ (Wiley: New York.)
Newman, A. E. M., Edmunds, N. B., Ferraro, S., Heffell, Q., Merritt, G. M., Pakkala, J. J., Schilling, C. R., and Schorno, S. (2015). Using ecology to inform physiology studies: implications of high population density in the laboratory. Am. J. Physiol. Regul. Integr. Comp. Physiol. 308, R449–R454.
| 1:CAS:528:DC%2BC2MXlsFChsbk%3D&md5=13eaee24bea304b85e01e3c1076e70feCAS |
Oplinger, R. W., and Wagner, E. J. (2015). Use of penicillin and streptomycin to reduce spread of bacterial coldwater disease I: antibiotics in sperm extenders. J. Aquat. Anim. Health 27, 25–31.
| Use of penicillin and streptomycin to reduce spread of bacterial coldwater disease I: antibiotics in sperm extenders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlKqsrc%3D&md5=6d2a487b6c6cd9cfb8175b6e894e9f13CAS | 25581335PubMed |
Ostrach, D. J., Low-Marchelli, J. M., Eder, K. J., Whiteman, S. J., and Zinkl, J. G. (2008). Maternal transfer of xenobiotics and effects on larval striped bass in the San Francisco estuary. Proc. Natl Acad. Sci. USA 105, 19 354–19 359.
| Maternal transfer of xenobiotics and effects on larval striped bass in the San Francisco estuary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFamu7rI&md5=221ea5db3f9a557cac94649fa8667252CAS |
Ottesen, O. H., Babiak, I., and Dahle, G. (2009). Sperm competition and fertilization success of Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 286, 240–245.
| Sperm competition and fertilization success of Atlantic halibut (Hippoglossus hippoglossus L.).Crossref | GoogleScholarGoogle Scholar |
Paterson, B. D., Rimmer, M. A., Meikle, G. M., and Semmens, G. L. (2003). Physiological responses of the Asian sea bass, Lates calcarifer to water quality deterioration during simulated live transport: acidosis, red-cell swelling, and levels of ions and ammonia in the plasma. Aquaculture 218, 717–728.
| Physiological responses of the Asian sea bass, Lates calcarifer to water quality deterioration during simulated live transport: acidosis, red-cell swelling, and levels of ions and ammonia in the plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Ggs74%3D&md5=666f1b65a9597412262b90b032373661CAS |
Perfetto, S. P., Chattopadhyay, P. K., Lamoreaux, L., Nguyen, R., Ambrozak, D., Koup, R. A., and Roederer, M. (2010). Amine-reactive dyes for dead cell discrimination in fixed samples. Curr. Protocol. Cytom. 9.34, 1–20.
Peterson, B. C., Small, B. C., and Bosworth, B. G. (2004). Effects of bovine growth hormone (Posilac®) on growth performance, body composition, and IGFBPs in two strains of channel catfish. Aquaculture 232, 651–663.
| Effects of bovine growth hormone (Posilac®) on growth performance, body composition, and IGFBPs in two strains of channel catfish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslCitLs%3D&md5=e4d7ac87eae497f23a6e593e7f46fe88CAS |
Renard, P., Strüssmann, C. A., Ling, H., and Takashima, F. (1994). Evaluation of extenders for pejerrey Odontesthes bonariensis sperm. Fish. Sci. 60, 661–666.
| 1:CAS:528:DyaK2MXjvVGjsLs%3D&md5=2401c69fc2cc17b4558b70c8e1f3d851CAS |
Riley, K. L., Chesney, E. J., and Tiersch, T. R. (2008). Field collection, handling, and refrigerated storage of sperm of red snapper and gray snapper. N. Am. J. Aquaculture 70, 356–364.
| Field collection, handling, and refrigerated storage of sperm of red snapper and gray snapper.Crossref | GoogleScholarGoogle Scholar |
Sargent, M. G., and Mohun, T. J. (2005). Cryopreservation of sperm of Xenopus laevis and Xenopus tropicalis. Genesis 41, 41–46.
| Cryopreservation of sperm of Xenopus laevis and Xenopus tropicalis.Crossref | GoogleScholarGoogle Scholar | 15645449PubMed |
Seifi, T., Imanpoor, M. R., and Golpour, A. (2011). The effect of different hormonal treatments on semen quality parameters in cultured and wild carp. Turk. J. Fish. Aquat. Sci. 11, 595–602.
| The effect of different hormonal treatments on semen quality parameters in cultured and wild carp.Crossref | GoogleScholarGoogle Scholar |
Small, B. C., Davis, K. B., and Peterson, B. C. (2008). Elucidating the effects of cortisol and stress on economically important traits in channel catfish. N. Am. J. Aquaculture 70, 223–235.
| Elucidating the effects of cortisol and stress on economically important traits in channel catfish.Crossref | GoogleScholarGoogle Scholar |
Stefansson, E. S., Heyes, A., and Rowe, C. (2014). Tracing maternal transfer of methylmercury in the sheepshead minnow (Cyprinodon variegatus) with an enriched mercury stable isotope. Environ. Sci. Technol. 48, 1957–1963.
| Tracing maternal transfer of methylmercury in the sheepshead minnow (Cyprinodon variegatus) with an enriched mercury stable isotope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltFehsw%3D%3D&md5=d7eb5c45bcf6a88296b70d9a32f832b6CAS | 24404938PubMed |
Strüssmann, C. A., Renard, P., Ling, H., and Takashima, F. (1994). Motility of pejerrey Odontesthes bonariensis spermatozoa. Fish. Sci. 60, 9–13.
Sühring, R., Freese, M., Schneider, M., Schubert, S., Pohlmann, J.-D., Alaee, M., Wolschke, H., Hanel, R., Ebinghaus, R., and Marohn, L. (2015). Maternal transfer of emerging brominated and chlorinated flame retardants in European eels. Sci. Total Environ. 530–531, 209–218.
| Maternal transfer of emerging brominated and chlorinated flame retardants in European eels.Crossref | GoogleScholarGoogle Scholar | 26042896PubMed |
Suquet, M., Omnes, M. H., Normant, Y., and Fauvel, C. (1992). Assessment of sperm concentration and motility in turbot (Scophthalmus maximus). Aquaculture 101, 177–185.
| Assessment of sperm concentration and motility in turbot (Scophthalmus maximus).Crossref | GoogleScholarGoogle Scholar |
Suquet, M., Billard, R., Cosson, J., Normant, Y., and Fauvel, C. (1995). Artificial insemination in turbot (Scophthalmus maximus): determination of the optimal sperm to egg ratio and time of gamete contact. Aquaculture 133, 83–90.
| Artificial insemination in turbot (Scophthalmus maximus): determination of the optimal sperm to egg ratio and time of gamete contact.Crossref | GoogleScholarGoogle Scholar |
Tan, E., Yang, H., and Tiersch, T. R. (2010). Determination of sperm concentration for small-bodied biomedical model fishes by use of microspectrophotometry. Zebrafish 7, 233–240.
| Determination of sperm concentration for small-bodied biomedical model fishes by use of microspectrophotometry.Crossref | GoogleScholarGoogle Scholar | 20515322PubMed |
Tavolga, W. N. (1949). Embryonic development of the platyfish (Platypoecilus), the swordtail (Xiphophorus) and their hybrids. Bull. Am. Mus. Nat. Hist. 94, 161–230.
Tiersch, T. R. (2011). Process pathways for cryopreservation research, application and commercialization. In ‘Cryopreservation in Aquatic Species’. (Eds T. R. Tiersch and C. C. Green.) pp. 646–671. (World Aquaculture Society: Baton Rouge, LA.)
Tiersch, T. R., and Green, C. C. (2011). Cryopreservation in aquatic species. (World Aquaculture Society, Baton Rouge, LA.)
Valdebenito, I. I., Gallegos, P. C., and Effer, B. R. (2015). Gamete quality in fish: evaluation parameters and determining factors. Zygote 23, 177–197.
| Gamete quality in fish: evaluation parameters and determining factors.Crossref | GoogleScholarGoogle Scholar | 24229714PubMed |
Wang, Q., Lai, N. L.-S., Wang, X., Guo, Y., Lam, P. K.-S., Lam, J. C.-W., and Zhou, B. (2015). Bioconcentration and transfer of the organophorous flame retardant 1,3-dichloro-2-propyl phosphate causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish larvae. Environ. Sci. Technol. 49, 5123–5132.
| Bioconcentration and transfer of the organophorous flame retardant 1,3-dichloro-2-propyl phosphate causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsFGgsrs%3D&md5=9abca5a7903fb2ac5a8f514545fe91bcCAS | 25826601PubMed |
Yang, H., and Tiersch, T. R. (2009). Current status of sperm cryopreservation in biomedical research fish models: zebrafish, medaka, and Xiphophorus. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 224–232.
| Current status of sperm cryopreservation in biomedical research fish models: zebrafish, medaka, and Xiphophorus.Crossref | GoogleScholarGoogle Scholar | 18691673PubMed |
Yang, H., Carmichael, C., Varga, Z. M., and Tiersch, T. R. (2007a). Development of a simplified and standardized protocol with potential for high-throughput for sperm cryopreservation in zebrafish Danio rerio. Theriogenology 68, 128–136.
| Development of a simplified and standardized protocol with potential for high-throughput for sperm cryopreservation in zebrafish Danio rerio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFKgs7k%3D&md5=78b9803701724e4db0602dc12567bda5CAS | 17544099PubMed |
Yang, H., Hazlewood, L., Heater, S. J., Guerrero, P. A., Walter, R. B., and Tiersch, T. R. (2007b). Production of F1 interspecies hybrid offspring with cryopreserved sperm from a live-bearing fish, the swordtail Xiphophorus helleri. Biol. Reprod. 76, 401–406.
| Production of F1 interspecies hybrid offspring with cryopreserved sperm from a live-bearing fish, the swordtail Xiphophorus helleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlWhur0%3D&md5=a79647a24767926ecadc8d6016f74ba1CAS | 17108333PubMed |
Yang, H., Hazlewood, L., Walter, R. B., and Tiersch, T. R. (2009). Sperm cryopreservation of a live-bearing fish, Xiphophorus couchianus: male-to-male variation in post-thaw motility and production of F1 hybrid offspring. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 233–239.
| Sperm cryopreservation of a live-bearing fish, Xiphophorus couchianus: male-to-male variation in post-thaw motility and production of F1 hybrid offspring.Crossref | GoogleScholarGoogle Scholar | 19027087PubMed |
Yang, H., Cuevas-Uribe, R., Savage, M. G., Walter, R. B., and Terrence, T. R. (2012). Sperm cryopreservation in live-bearing Xiphophorus fishes: offspring production from Xiphophorus variatus and strategies for establishment of sperm repositories. Zebrafish 9, 126–134.
| Sperm cryopreservation in live-bearing Xiphophorus fishes: offspring production from Xiphophorus variatus and strategies for establishment of sperm repositories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtlyns7rJ&md5=63c0231b0b3a65b7f2bc3a579c305b78CAS | 22924335PubMed |
Yasui, G. S., Arias-Rodriguez, L., Fujimoto, T., and Arai, K. (2008). Simple and inexpensive method for cryopreservation of fish sperm combining straw and powdered dry ice. Cryo Letters 29, 383–390.
| 18946552PubMed |
