Toward responsible stock enhancement: broadcast spawning dynamics and adaptive genetic management in white seabass aquaculture

Abstract

The evolutionary effects captive-bred individuals that can have on wild conspecifics are necessary considerations for stock enhancement programs, but breeding protocols are often developed without the knowledge of realized reproductive behavior. To help fill that gap, parentage was assigned to offspring produced by a freely mating group of 50 white seabass (Atractoscion nobilis), a representative broadcast spawning marine finfish cultured for conservation. Similar to the well-known and closely related red drum (Sciaenops ocellatus), A. nobilis exhibited large variation in reproductive success. More males contributed and contributed more equally than females within and among spawns in a mating system best described as lottery polygyny. Two females produced 27% of the seasonal offspring pool and female breeding effective size averaged 1.85 per spawn and 12.38 seasonally, whereas male breeding effective size was higher (6.42 and 20.87, respectively), with every male contributing 1–7% of offspring. Further, females batch spawned every 1–5 weeks, while males displayed continuous reproductive readiness. Sex-specific mating strategies resulted in multiple successful mate pairings and a breeding effective to census size ratio of ≥0.62. Understanding a depleted species’ mating system allowed management to more effectively utilize parental genetic variability for culture, but the fitness consequences of long-term stocking can be difficult to address.

Literature cited Aalbers, S. A., and M. A. Drawbridge. 2008. White seabass spawning behavior and sound production. Transaction of the American Fisheries Society137:542–550. Akey, J. M., K. Zhang, M. Xiong, P. Doris, and L. Jin. 2001. The effect that genotyping errors have on the robustness of common linkage disequilibrium measures. American Journal of Human Genetics68:1447–1456. Allen, L. G., D. J. Pondella II, and M. A. Shane. 2007. Fisheries independent assessment of a returning fishery: abundance of juvenile while seabass (Atractoscion nobilis) in the shallow nearshore waters of the Southern California Bight, 1995-2005. Fisheries Research88:24–32. Allendorf, F. W., and N. Ryman. 1987. Genetic management of hatchery stocks. In N. Ryman, and F. Utter, eds. Population Genetics and Fishery Management, pp. 141–159. University of Washington Press, Seattle. Araki, H., and C. Schmid. 2010. Is hatchery stocking a help or harm? Evidence, limitations and future direction in ecological and genetic surveysAquaculture308:S2–S11. Araki, H., B. Cooper, and M. S. Blouin. 2007. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science318:100–103. Bartley, D. M., D. B. Kent, and M. A. Drawbridge. 1995. Conservation of genetic diversity of white seabass enhancement program in southern California. American Fisheries Society Symposium15:249–258. von Bertalanffy, L.1938. A quantitative theory of organic growth. Human Biology10:181–213. Birkhead, T. R., and A. P. Møller. 1992. Sperm Competition in Birds. Evolutionary Causes and Consequences. Academic Press, San Diego. Bishop, J. D. D.1998. Fertilization in the sea: are the hazards of broadcast spawning avoided when free-spawned sperm fertilize retained eggs?Proceedings of the Royal Society B265:721–735. Blankenship, H. L., and K. M. Leber. 1995. A responsible approach to marine stock enhancement. American Fisheries Society Symposium15:167–175. Botstein, D., R. L. White, M. Skolnick, and R. W. Davis. 1980. Construction of a genetic linkage map in the man using restriction fragment length polymorphisms. American Journal of Human Genetics32:314–331. California Department of Fish and Game (CDFG), Marine Region. 2002. White Seabass Fishery Management Plan. The Resources Agency, Sacramento, CA. Coykendall, D. K.2005. Population structure and dynamics of white seabass (Atractoscion nobilis) and the genetic effect of hatchery supplementation on the wild population. Ph.D. dissertation, University of California Davis, Davis, CA. Dean, M. D., K. G. Ardlie, and M. W. Nachman. 2006. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Molecular Ecology15:4141–4151. Donohoe, C. J. 1997. Age, growth, distribution, and food habits of recently settled white seabass, Atractoscion nobilis, off San Diego County, California. Fisheries Bulletin95:709–721. Duchesne, P., and L. Bernatchez. 2002. An analytical investigation of the dynamics of inbreeding in multi-generation supportive breeding. Conservation Genetics3:47–60. Frankham, R. 1995. Effective population size/adult population size ratios in wildlife: a review. Genetical Research66:95–107. Franklin, M. P.1997. An investigation into the population structure of white seabass (Atractoscion nobilis) in California and Mexican waters using microsatellite DNA analysis. Ph.D. dissertation, University of California Santa Barbara, Santa Barbara, CA. Gold, J. R.2004. Stock structure and effective size of red drum (Sciaenops ocellatus) in the northern Gulf of Mexico and implications relative to stock enhancement and recruitment. In K. M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching: Developments, Pitfalls and Opportunities, 2nd edn. pp. 353–370. Blackwell Publishing Ltd, Oxford. Gold, J. R., L. Ma, E. Saillant, P. S. Silva, and R. R. Vega. 2008. Genetic effective size in populations of hatchery-raised red drum released for stock enhancement. Transactions of the American Fisheries Society137:1327–1344. Gold, J. R., M. A. Renshaw, E. Saillant, and R. R. Vega. 2010. Spawning frequency of dams and sires in a marine fish stock-enhancement hatchery. Journal of Fish Biology77:1030–1040. Hedgecock, D.1994. Does variance in reproductive success limit effective population sizes of marine organisms? In A. Beaumont, ed. Genetics and Evolution of Aquatic Organisms. pp. 1222–1344. Chapman and Hall, London. Hervas, S., K. Lorenzen, M. A. Shane, and M. A. Drawbridge. 2010. Quantitative assessment of a white seabass (Atractoscion nobilis) stock enhancement program in California: post-release dispersal, growth and survival. Fisheries Research105:237–243. Jørstad, K. E.2004. Genetic studies in marine stock enhancement in Norway. In K. M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching: Developments, Pitfalls and Opportunities, 2nd edn. pp. 339–352. Blackwell Publishing Ltd., Oxford. Kalinowski, S. T., A. P. Wagner, and M. L. Taper. 2006. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes6:576–579. Kalinowski, S. T., M. L. Taper, and T. C. Marshall. 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology16:1099–1106. Leber, K. M.2004. Marine stock enhancement in the USA: status, trends, and needs. In K. M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching: Developments, Pitfalls and Opportunities, 2nd edn. pp. 11–24. Blackwell Publishing Ltd, Oxford. Leet, W. S., C. M. Dewees, R. Klingbeil, and E. J. Larson2001. California’s Living Marine Resources: A Status Report. CDFG. The Resources Agency, Sacramento, CA. Pub SG01–11. Letcher, B. H., and T. L. King. 1999. Targeted stock identification using multilocus genotype ‘familyprinting’. Fisheries Research43:99–111. Levitan, D. R.2005. The distribution of male and female reproductive success in a broadcast spawning marine invertebrate. Integrative and Comparative Biology45:848–855. Lorenzen, K., K. M. Leber, and H. L. Blankenship. 2010. Responsible approach to stock enhancement: an update. Reviews in Fisheries Science18:189–210. McEachron, L. W., C. W. McCarty, and R. R. Vega1993. Successful enhancement of Texas red drum (Sciaenops ocellatus) population. In Interactions between Cultured Species and Naturally Occurring Species in the Environment: Proceedings of the 22nd U.S.-Japan Aquaculture Panel Symposium, Homer. pp. 53–56. Michalczyk, Ł., A. L. Millard, O. Y. Martin, A. J. Lumley, B. C. Emerson, T. Chapman, and M. J. G. Gage. 2011. Inbreeding promotes female promiscuity. Science333:1739–1742. Moser, H. G., D. A. Ambrose, M. S. Busby, J. L. Butler, E. M. Sandknop, B. Y. Sumida, and E. G. Stevens. 1983. Description of early stages of white seabass, Atractoscion nobilis, with notes on distribution. CalCOFI Report24:182–193. Nunney, L.1993. The influence of mating system and overlapping generations on effective population size. Evolution47:1329–1341. Oliver, J., and R. Babcock. 1992. Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution and measurements of fertilization. Biological Bulletin183:409–417. Pearse, D. E., R. J. Janzen, and J. C. Avise. 2001. Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behavioral Ecology and Sociobiology51:164–171. Pella, J. J., and G. B. Milner1987. Use of genetic marks in stock composition analysis. In N. Ryman, and F. Utter, eds. Population Genetic and Fisheries Management. pp. 247–276. University of Washington Press, Seattle. Pennington, J. T.1985. The ecology of fertilization of echinoid eggs – the consequences of sperm dilution, adult aggregation and synchronous spawning. Biological Bulletin169:417–430. Reisenbichler, R., S. Rubin, L. Wetzel, and S. Phelps. 2004. Natural selection after release from a hatchery leads to domestication in steelhead, Oncorhynchus mykiss. In K. M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching: Developments, Pitfalls and Opportunities, 2nd edn, pp. 371–383. Blackwell Publishing Ltd, Oxford. Rousset, F.2008. GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources8:103–106. Rowe, S., and J. A. Hutchings. 2003. Mating systems and the conservation of commercially exploited marine fish. Trends in Ecology and Evolution18:567–572. Rowe, S., and J. A. Hutchings. 2008. A link between sound producing musculature and mating success in Atlantic cod. Journal of Fish Biology72:500–511. Rowe, S., J. A. Hutchings, and J. E. Skjæraasen. 2007. Nonrandom mating in a broadcast spawner: mate size influences reproductive success in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences64:219–226. Ryman, N., and L. Laikre. 1991. Effects of supportive breeding on the genetically effective population size. Conservation Biology5:325–329. Ryman, N., F. Utter, and L. Laikre. 1995. Protection of intraspecific biodiversity of exploited fishes. Reviews in Fish Biology and Fisheries5:417–446. Schmeller, D. S., and J. Merilä. 2007. Demographic and genetic estimates of effective population and breeding size in the amphibian Rana temporaria. Conservation Biology21:142–151. Smith, T. I. J., W. E. Jenkins, M. R. Denson, and M. R. Collins. 2003. Stock enhancement research with anadromous and marine fishes in South Carolina. UJNR Technical Report30:175–189. Stockley, P., M. J. G. Gage, G. A. Parker, and A. P. Møller. 1997. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. The American Naturalist149:933–954. Taborsky, M.1998. Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. Trends in Ecology and Evolution13:222–227. Taniguchi, N.2003. Genetic factors in broodstock management for seed production. Reviews in Fish Biology and Fisheries13:177–185. Taniguchi, N.2004. Broodstock management for stock enhancement programs of marine fish with assistance of DNA marker (a review). In K. M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching: Developments, Pitfalls and Opportunities, 2nd edn. pp. 329–338. Blackwell Publishing Ltd, Oxford. Thrower, F. P., and J. E. Joyce. 2004. Effects of 70 years of freshwater residency on survival, growth, early maturation, and smolting in a stock of anadromous rainbow trout from southeast Alaska. American Fisheries Society Symposium44:485–496. Tringali, M. D., and T. M. Bert. 1998. Risk to genetic effective population size should be an important consideration in fish stock-enhancement programs. Bulletin of Marine Science62:641–659. Tringali, M. D., T. M. Bert, F. Cross, J. W. Dodrill, L. M. Gregg, W. G. Halstead, R. A. Krause et al.2007. Genetic Policy for the Release of Finfishes in Florida. Florida Fish and Wildlife Conservation Commission. Florida Fish and Wildlife Research Institute, Publication No. IHR-2007-1, St. Petersburg. Tringali, M. D., K. M. Leber, W. G. Halstead, R. McMichael, J. O’Hop, B. Winner, R. Cody et al.2008. Marine stock enhancement in Florida: a multi-disciplinary, stakeholder-supported, accountability-based approach. Reviews in Fisheries Science16:51–57. Turner, J. F., J. P. Wares, and J. R. Gold. 2002. Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-depended marine fish (Sciaenops ocellatus). Genetics162:1329–1339. Waples, R. S.1990. Conservation genetics of Pacific salmon. II. Effective population size and the rate of loss of genetic variability. Journal of Heredity81:267–276. Waples, R. S.1994. Genetic considerations in recovery efforts for Pacific salmon. Conservation Biology8:884–886. Waples, R. S.. 2006. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci*. Conservation Genetics7:167–184. Waples, R. S., and C. Do. 2008. LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources8:753–756. Waples, R. S., and K. A. Naish2009. Genetic and evolutionary considerations in fishery management: research needs for the future. In J. Beamish, and B. J. Rothschild, eds. The Future of Fisheries Science in North America. pp. 427–451. Springer, Dordrecht.