Skip to main content

Advertisement

Log in

Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax)

  • Reviews
  • Published:
Reviews in Fish Biology and Fisheries Aims and scope Submit manuscript

Abstract

There is an urgent need to clarify how different stocks, or subpopulations of fish species, are vulnerable to fishing pressure and unfavorable ocean conditions because of the increasing demand on fisheries for human consumption. For marine fishes, the potential for high gene flow increases the difficulty in determining the number of subpopulations managed in a specific fishery. Although the use of molecular data has become a common method in the past 15 years to identify fish subpopulations, no single technique or suite of techniques has been established for fish stock structure studies. We review the use of fish morphometrics, artificial tags, fish genetics, parasite genetics, and parasites as biological tags to identify subpopulations of marine fishes with a focus on the Pacific sardine (Sardinops sagax) fishery off the west coast of North America. We suggest an integration of fish- and parasite-based techniques for future stock structure studies, particularly for pelagic fish species whose stock structure can be elusive. An integration of techniques may also resolve fish stock structure over small geographic areas by increasing the number of spatial and temporal scales studied simultaneously leading to methods for successful management of marine fish species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

Reference indicated by an asterisk (*) are noted in Table 1

  • Abaunza P, Murta AG, Campbell N, Cimmaruta R, Comesaña AS, Dahle G, Gallo E, García Santamaría MT, Gordo LS, Iversen SA, MacKenzie K, Magoulas A, Mattiucci S, Molloy J, Nascetti G, Pinto AL, Quinta R, Ramos P, Ruggi A, Sanjuan A, Santos AT, Stransky C, Zimmerman C (2008a) Considerations on sampling strategies for an holistic approach to stock identification: the example of the HOMSIR project. Fish Res 89:104–113

    Article  Google Scholar 

  • Abaunza P, Murta AG, Campbell N, Cimmaruta R, Comesaña AS, Dahle G, García Santamaría MT, Gordo LS, Iversen SA, MacKenzie K, Magoulas A, Mattiucci S, Molloy J, Nascetti G, Pinto AL, Quinta R, Ramos P, Sanjuan A, Santos AT, Stransky C, Zimmerman C (2008b) Stock identity of horse mackerel (Trachurus Trachurus) in the Northeast Atlantic and Mediterranean Sea: integrating the results from different stock identification approaches. Fish Res 89:196–209

    Article  Google Scholar 

  • Ahlstrom EH (1957) A review of recent studies of subpopulations of Pacific fishes. In: Marr JC (ed) Contributions to the study of subpopulations of fishes. Special Scientific Report, Fisheries No. 208. Washington DC, pp 44–73

  • Aiken HM, Bott NJ, Mladineo I, Montero FE, Nowak BF, Hayward CJ (2007) Molecular evidence for cosmopolitan distribution of platyhelminth parasites of tunas (Thunnus spp.). Fish Fish 8:167–180

    Google Scholar 

  • Alder J, Campbell B, Karpouzi V, Kaschner K, Pauly D (2008) Forage fish: from ecosystems to markets. Annu Rev Environ Resour 33:153–166

    Article  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the Genetics of Populations. Blackwell Publishing, Australia

    Google Scholar 

  • Armannsson H, Jonsson ST, Neilson JD, Marteinsdottir G (2007) Distribution and migration of saithe (Pollachius virens) around Iceland inferred from mark-recapture studies. ICES J Mar Sci 64:1006–1016

    Article  Google Scholar 

  • *Arthur JR, Albert E (1993) Use of parasites for separating stocks of Greenland halibut (Reinhardtius hippoglossoides) in the Canadian Northwest Atlantic. Can J Fish Aquat Sci 50:2175–2181

    Article  Google Scholar 

  • Atarhouch T, Rüber L, Gonzalez EG, Albert EM, Rami M, Dakkak A, Zardoya R (2006) Signature of an early genetic bottleneck in a population of Moroccan sardines (Sardina pilchardus). Mol Phylogenet Evol 39:373–383

    Article  PubMed  CAS  Google Scholar 

  • Avise JC (1998) Conservation in the marine realm. J Hered 89:377–382

    Article  Google Scholar 

  • Baldwin REB (2010) Using parasite community data and population genetics for assessing Pacific sardine (Sardinops sagax) population structure along the west coast of North America. Doctor of Philosophy dissertation, Oregon State University, Corvallis, Oregon, 207 pp

  • *Baker TG, Morand S, Wenner CA, Roumillat WA, de Buron I (2007) Stock identification of the sciaenid fish Micropogonias undulatus in the western north Atlantic Ocean using parasites as biological tags. J Helminthol 81:155–167

    Article  PubMed  Google Scholar 

  • Bakun A (1996) Patterns in the ocean. Ocean processes and marine population dynamics. California Sea grant college system, National Oceanic and Atmospheric Administration in cooperation with Centro de Investigaciones Biológicas del Noroeste, La Paz, BCS México

  • Baranov FI (1918) On the question of the biological basis of fisheries. Nauchn Issled Iktiol Inst Izv 1:81–128

    Google Scholar 

  • Baumgartner TR, Soutar A, Ferriera-Bartrina V (1992) Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Rep 33:24–40

    Google Scholar 

  • Beacham TD, Schweigert JF, MacConnachie C, Le KD, Flostrand L (2008) Use of microsatellites to determine population structure and migration of Pacific herring in British Columbia and adjacent Regions. Trans Am Fish Soc 137:1795–1811

    Article  Google Scholar 

  • Beamish RJ, Benson AJ, Sweeting RM, Neville CM (2004) Regimes and the history of the major fisheries off Canada’s west coast. Prog Oceanogr 60:355–385

    Article  Google Scholar 

  • Beamish RJ, McFarlane GA, King JR (2000) Fisheries climatology: understanding decadal scale processes that naturally regulate British Columbia fish populations. In: Harrison PJ, Parsons TR (eds) Fisheries oceanography. An integrative approach to fisheries ecology and management, 1st edn. Blackwell Science, Maldan, pp 94–139

    Google Scholar 

  • Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43:35–44

    Google Scholar 

  • Bentley PJ, Emmett RL, Lo NCH, Moser HG (1996) Egg production of the Pacific sardine (Sardinops sagax) off Oregon in 1994. Calif Coop Oceanic Fish Invest Rep 7:193–200

    Google Scholar 

  • Beverton R (1998) Fish, fact and fantasy: a long view. Rev Fish Biol Fisher 8:229–249

    Article  Google Scholar 

  • Beverton RJH (2002) Reflections on 100 years of fisheries research. In: The Raymond JH (ed) Beverton lectures at woods hole, Massachusetts. Three lectures on fisheries science given May 2–3, 1994, U.S. Dep. Commer., NOAA Tech. Memo. NMFS-F/SPO-54, pp 107–158

  • Beverton RJH, Holt SJ (1957) On the dynamics of exploited fish populations. Fish investigations, Ser 2, No. 19, Ministry of Agriculture, Fisheries and Food, London

  • Brown WM (1983) Evolution of animal mitochondrial DNA. In: Kerry KR, Hempel G (eds) Evolution of Genes and Proteins. Sinauer, Sunderland, pp 271–277

    Google Scholar 

  • Bruford MW, Wayne RK (1993) Microsatellites and their application to population genetic studies. Curr Opin Genet Dev 31:939–943

    Google Scholar 

  • Buonaccorsi VP, McDowell JR, Graves JE (2001) Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Mol Ecol 10:1179–1196

    Article  PubMed  CAS  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms. Margolis et al. revisited. J Parasitol 83:575–583

    Article  PubMed  CAS  Google Scholar 

  • Caddy JF, Seijo JC (2005) This is more difficult than we thought! The responsibility of scientists, managers and stakeholders to mitigate the unsustainability of marine fisheres. Phil Trans R Soc B 360:59–75

    Article  PubMed  CAS  Google Scholar 

  • Cadrin SX, Friedland KD, Waldman JR (2005) Stock identification methods. In: Cadrin SX, Friedland KD, Waldman JR (eds) Applications in fishery science. Elsevier Academic Press, San Francisco, pp 3–6

    Google Scholar 

  • *Campbell N, MacKenzie K, Zuur AF, Ieno EN, Smith GM (2007) Fish stock identification through neural network analysis of parasite fauna. In: Zuur AF, Ieno EN, Smith GM (eds) Analysing ecological data. Springer, New York, pp 449–462

    Chapter  Google Scholar 

  • Casini M, Hjelm J, Molinero J-C, Lövgren J, Cardinale M, Bartolino V, Belgrano A, Kornilovs G (2009) Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. P Natl Acad Sci USA 106:197–202

    Article  CAS  Google Scholar 

  • Checkley DM, Barth JA (2009) Patterns and processes in the California current system. Prog Oceanogr 83:49–64

    Article  Google Scholar 

  • Checkley DM, Ayon P, Baumgartner TR, Bernal M, Coetzee JC, Emmett R, Guevara-Carrasco R, Hutchings L, Ibaibarriaga L, Nakata H, Oozeki Y, Planque B, Schweigert J, Stratoudakis Y, van der Lingen CD (2009) Habitats In: Checkley DM, Alheit J, Oozeki Y, Roy C (eds) Climate change and small pelagic fish, 1st edn. Cambridge University Press, New York, NY, pp 13–44

  • Chlaida M, Kifani S, Lenfant P, Ouragh L (2006) First approach for the identification of sardine populations Sardina pilchardus (Walbaum 1792) in the Moroccan Atlantic by allozymes. Mar Biol 149:169–175

    Article  CAS  Google Scholar 

  • Clark FN (1935) A summary of the life-history of the California sardine and its influence on the fishery. Calif Fish Game 21:1–9

    Google Scholar 

  • Clark FN (1947) Analysis of populations of the Pacific sardine on the basis of vertebral counts. Calif Dep Fish Game Fish Bull 65

  • Clark FN, Janssen JF (1945) Movements and abundance of the sardine as measured by tag returns. California Fish and Game 61:1–42

    Google Scholar 

  • Collie JS, Gislason H (2001) Biological reference points in a multispecies context. Can J Fish Aquat Sci 58:2167–2176

    Article  Google Scholar 

  • Cope JM (2004) Population genetics and phylogeography of the blue rockfish (Sebastes mystinus) from Washington to California. Can J Fish Aquat Sci 61:332–342

    Article  Google Scholar 

  • Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evol 58:198–202

    Google Scholar 

  • Criscione CD, Blouin MS (2006) Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evol 60:553–562

    CAS  Google Scholar 

  • Criscione CD, Cooper B, Blouin MS (2006) Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecol 87:823–828

    Article  Google Scholar 

  • Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257

    Article  PubMed  CAS  Google Scholar 

  • Cross MA, Collins C, Campbell N, Watts PC, Chubb JC, Cunningham CO, Hatfield EMC, MacKenzie K (2007) Levels of intra-host and temporal sequence variation in a large CO1 sub-units from Anisakis simplex sensu stricto (Rudolphi 1809) (Nematoda: Anisakidae): implications for fisheries management. Mar Biol 151:695–702

    Article  Google Scholar 

  • Crowder LB, Hazen EL, Avissar N, Bjorkland R, Latanich C, Ogburn MB (2008) The impacts of fisheries on marine ecosystems and the transition to ecosystem-based management. Ann Rev Ecol Evol Syst 39:259–278

    Article  Google Scholar 

  • Dahlgren EH (1936) Further developments in the tagging of the Pacific herring, (Clupea pallasii). J Conseil 11:229–247

    Article  Google Scholar 

  • DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473

    Article  CAS  Google Scholar 

  • Dick TA, Belosevic M (1981) Parasites of arctic charr Salvelinus alpinus (Linnaeus) and their use in separating sea-run and non-migrating charr. J Fish Biol 18:339–347

    Google Scholar 

  • Emmett RL, Brodeur RD, Miller TW, Pool SS, Bentley PJ, Krutzikowsky GK, McCrae J (2005) Pacific sardine (Sardinops sagax) abundance, distribution and ecological relationships in the Pacific Northwest. CalCOFI Rep 46:122–143

    Google Scholar 

  • Felin FE (1954) Population heterogeneity in the Pacific pilchard. Fish Bull US 54:201–225

    Google Scholar 

  • Félix-Uraga R, Quiñónez-Velázquea C, Hill KT, Gómez-Muñoz VM, Melo-Barrera FN, García-Franco W (2005) Pacific sardine (Sardinops sagax) stock discrimination off the west coast of Baja California and southern California using otolith morphometry. CalCOFI Rep 46:113–121

    Google Scholar 

  • Félix-Uraga R, Gómez-Muñoz VM, Quiñónez-Velázquez C, Melo-Barrera FN, García-Franco W (2004) On the existence of Pacific sardine groups off the west coast of Baja California and southern California. CalCOFI Rep 46:146–151

    Google Scholar 

  • Fitch JE (1969) Fossil records of certain schooling fishes of the California current system. Calif Mar Res Comm CalCOFI Rep 13:71–80

    Google Scholar 

  • Gascuel D, Tremblay-Boyer L, Pauly D (2009) EcoTroph (ET): A trophic level based software for assessing the impacts of fishing on aquatic ecosystems. Fish Centre Res Rep 17:87

    Google Scholar 

  • Gonzalez EG, Zardoya R (2007) Relative role of life-history traits and historical factors in shaping genetic population structure of sardines (Sardina pilchardus). BMC Evol Biol 7:197

    Article  PubMed  CAS  Google Scholar 

  • Graham M (1935) Modern theory of exploiting a fishery, and application to North Sea trawling. J Cons Int Explor Mer 10:264–274

    Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Grant WS, Utter FM (1984) Biochemical population genetics of Pacific herring (Clupea pallasi). Can J Fish Aquat Sci 41:856–864

    Article  Google Scholar 

  • Grantham BA, Chan F, Nielsen KJ, Fox DS, Barth JA, Huyer A, Lubchenco J, Menge BA (2004) Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429:749–754

    Article  PubMed  CAS  Google Scholar 

  • Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA (1994) Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265:1087–1090

    Article  PubMed  CAS  Google Scholar 

  • Hansen LP, Jacobsen JA (2003) Origin, migration and growth of wild and escaped farmed Atlantic salmon, Salmo salar L., in oceanic areas north of the Faroe Islands. ICES J Mar Sci 60:110–119

    Article  Google Scholar 

  • Hansen MM, Kenchington E, Nielsen EE (2001) Assigning individual fish to populations using microsatellite DNA markers. Fish Fish 2:93–112

    Google Scholar 

  • Hargreaves NB, Ware DM, McFarlane GM (1994) Return of Pacific sardine (Sardinops sagax)to the British Columbia coast in 1992. Can J Fish Aquat Sci 51:460–463

    Article  Google Scholar 

  • Harley CDG, Rogers-Bennett L (2004) The potential synergistic effects of climate change and fishing pressure on exploited invertebrates on rocky intertidal shores. CalCOFI Rep 45:98–110

    Google Scholar 

  • Harris H (1966) Enzyme polymorphism in man. Proc R Soc Ser B 164:298–310

    Article  CAS  Google Scholar 

  • Harrt AC (1963) Problems in tagging salmon at sea. ICNAF Spec Publ 4:144–155

    Google Scholar 

  • Hart JL (1943) Tagging experiments on British Columbia pilchards. J Fish Res Bd Can 6:164–182

    Article  Google Scholar 

  • Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? B Mar Sci 39:550–564

    Google Scholar 

  • Hedgecock D, Hutchingson ES, Li G, Sly FL, Nelson K (1989) Genetic and morphometric variation in the Pacific sardine, Sardinops caerulea: comparisons and contrasts with historical data and with variability in the northern anchovy, Engraulis mordax. Fish Bull 87:63–671

    Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evol 53:313–318

    Article  Google Scholar 

  • *Herrington WC, Bearsem HM, Firth FE (1939) Observations on the life history, occurrence and distribution of the redfish parasite Sphyrion lumpi. US Bur Fish Spec Rep 5:1–18

    Google Scholar 

  • Hewitt GM (2004) The structure of biodiversity—insights from molecular phylogeography. Front Zool 1:4

    Article  PubMed  Google Scholar 

  • Hill KT, Lo NCH, Macewicz BJ, Crone PR, Félix-Uraga R (2010) Assessment of the Pacific sardine resource in 2010 for U.S. management in 2011. NOAA-TM-NMFS-SWFSC-469

  • Hoenig JM, Latour RJ, Olney JE (2008) Estimating stock composition of anadromous fishes from mark-recovery data: possible application to American shad. N Am J Fish Manage 58:507–515

    Article  Google Scholar 

  • Hollowed AB, Bax N, Beamish R, Collie JS, Fogarty M, Livingston PA, Pope J, Rice JC (2000) Are multi- species models an improvement on single-species models for measuring fishing impacts on marine ecosystems? ICES J Mar Sci 57:707–719

    Article  Google Scholar 

  • Hubby JL, Lewontin RC (1966) A molecular approach to the study of genetic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics 54:577–594

    PubMed  CAS  Google Scholar 

  • Jacobsen JA, Hansen LP (2005) Internal and external tags. In: Cadrin SX, Friedland KD, Waldman JR (eds) Stock identification methods. Applications in fishery science, 1st edn. Elsevier Academic Press, San Francisco, pp 415–433

    Chapter  Google Scholar 

  • Jakobsson J (1970) On fish tags and tagging. Oceanogr Mar Bio 8:457–499

    Google Scholar 

  • Janssen JF Jr (1938) Second report of sardine tagging in California. Fish Bull Calif Dept Fish Game 24:376–389

    Google Scholar 

  • Janssen JF Jr, Alpen JF (1945) The effect of internal tags upon sardines. Fish Bull 61:43–62

    Google Scholar 

  • Jones CM (2006) Estuarine and diadromous fish metapopulations. In: Kritzer JP, Sale PF (eds) Marine metapopulations. Elsevier Academic Press, San Francisco, pp 119–154

    Google Scholar 

  • Jousson O, Bartoli P, Pawlowski J (2000) Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). J Evol Biol 13:778–785

    Article  Google Scholar 

  • King RC, Stansfield WD (1985) A dictionary of genetics, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Koljonen M-L, Wilmot R (2005) Genetic analysis: allozymes. In: Cadrin SX, Friedland KD, Waldman JR (eds) Stock identification methods. Applications in fisheries science. Elsevier Academic Press, San Francisco, pp 295–309

    Google Scholar 

  • *Larsen G, Hemmingsen W, MacKenzie K, Lysne DA (1997) A population study of cod, Gadus morhua L. in northern Norway using otolith structure and parasite tags. Fish Res 32:13–20

    Article  Google Scholar 

  • Laurent V, Caneco B, Magoulas A, Planes S (2007) Isolation by distance and selection effects on genetic structure of sardine Sardina pilchardus Walbaum. J Fish Biol 71s:1–17

    Article  Google Scholar 

  • Lecomte F, Grant WS, Dodson JJ, Rodriguez-Sanchez R, Bowen BW (2004) Living withuncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax). Mol Ecol 13:2169–2182

    Article  PubMed  CAS  Google Scholar 

  • Lessios HA, Kessing BD, Robertson DR (1998) Massive gene flow across the world’s most potent marine biogeographic barrier. Proc R Soc B 265:583–588

    Article  Google Scholar 

  • Lester RJG (1990) Reappraisal of the use of parasites for fish stock identification. Aust J Mar Freshwater Res 41:855–864

    Article  Google Scholar 

  • *Lester RJG, Barnes A, Habib G (1985) Parasites of skipjack tuna, Katsuwonus pelamis: fishery implications. Fish Bull 83:343–356

    Google Scholar 

  • *Lester RJG, Sewell KB, Barnes A, Evans K (1988) Stock discrimination of orange roughy Hoplostethus atlanticus, by parasite analysis. Mar Biol 99:137–144

    Article  Google Scholar 

  • Lewontin RC, Hubby JL (1966) A molecular approach to the study of genetic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54:595–609

    PubMed  CAS  Google Scholar 

  • Lluch-Belda D, Lluch-Cota DB, Lluch-Cota SE (2003) Baja California’s biological transition zones: refuges for the California sardine. J Oceanogr 59:503–513

    Article  Google Scholar 

  • Lo NCH, Macewicz BJ, Griffith DA (2010) Biomass and reproduction of Pacific sardine (Sardinops sagax) off the Pacific northwestern United States, 2003–2005. Fish Bull 108:174–192

    Google Scholar 

  • Locke SA, McLaughlin JD, Dayanandan S, Marcogliese DJ (2010) Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcriber spacer sequences. Int J Parasitol 40:333–343

    Article  PubMed  CAS  Google Scholar 

  • Longhurst A (2006) The sustainability myth. Fish Res 81:107–112

    Article  Google Scholar 

  • Love MS, Moser M (1983) A checklist of parasites of California, Oregon, and Washington marine and estuarine fishes. NOAA Technical Report NMFS SSRF-777. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Services

  • Lynn RJ (2003) Variability in the spawning habitat of Pacific sardine (Sardinops sagax) off southern and central California. Fish Oceanogr 12:541–553

    Google Scholar 

  • Mace PM (2001) A new role for MSY in single-species and ecosystem approaches to fisheries stock assessment and management. Fish Fish 2:2–32

    Google Scholar 

  • MacKenzie K (1985) The use of parasites as biological tags in population studies of herring (Clupea harengus L.) in the North Sea and to the north and west of Scotland. J Cons Int Explor Mer 42:33–64

    Google Scholar 

  • MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitol 124:S153–S163

    Google Scholar 

  • *MacKenzie K (unpublished) Parasites as biological tags for pacific sardines, Sardinops sagax (Jenyns) in coastal waters of Ecuador and Peru. Aberdeen, Scotland, DAFS Marine Laboratory

  • MacKenzie K, Abaunza P (1998) Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish Res 38:45–56

    Article  Google Scholar 

  • MacKenzie K, Campbell N, Mattiucci S, Ramos P, Pinto AL, Abaunza P (2008) Parasites as biological tags for stock identification of Atlantic horse mackerel Trachurus Trachurus L. Fish Res 89:136–145

    Article  Google Scholar 

  • *MacKenzie K, Longshaw M (1995) Parasites of the hakes Merluccius australis and M. hubbsi in the waters around the Falkland Islands, southern Chile, and Argentina, with an assessment of their potential value as biological tags. Can J Fish Aquat Sci 52S:213–224

    Article  Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142

    Article  PubMed  Google Scholar 

  • Mann K (2000) Commentary: environmental effects on fish stocks. In: Harrison PJ, Parsons TR (eds) Fisheries oceanography. An integrative approach to fisheries ecology and management. Blackwell Science, Maldan, MA, pp 140–145

    Google Scholar 

  • Mantua NJ, Hare SR, Zhang Y, Wallace JM, Francis RC (1997) A Pacific interdecadal climate oscillation with impacts on salmon production. BAMS 78:1069–1079

    Article  Google Scholar 

  • Marcogliese DJ (1995) The role of zooplankton in the transmission of helminth parasites to fish. Rev Fish Biol Fish 5:336–371

    Article  Google Scholar 

  • Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitol 124:S83–S99

    Google Scholar 

  • Marcogliese DJ, Albert E, Gagnon P, Sevigny J-M (2003) Use of parasites in stock identification of the deepwater redfish (Sebastes mentella) in the Northwest Atlantic. Fish Bull 101:183–188

    Google Scholar 

  • Margolis L (1963) Parasites as indicators of the geographical origins of sockeye salmon, Oncorhynchus nerka (Walbaum), occurring in the north Pacific Ocean and adjacent seas. Bull Int North Pac Fish Comm 11:101–156

    Google Scholar 

  • *Margolis L (1984) Preliminary report on identification of continent of origin of ocean-caught steelhead trout, Salmo gairdneri, using naturally occurring parasite “tags”. Nanaimo, British Columbia, Department of Fisheries and Oceans, Fisheries Research Branch, Pacific Biological Station

  • Marr JC (1957) The subpopulation problem in the Pacific sardine, Sardinops caerulea. In: Marr JC (ed) Contributions to the study of subpopulations of fishes. Special scientific report, Fisheries No. 208. Washington, pp 108–125

  • Marr JC (1960) The causes of major variations in the catch of the Pacific sardine, Sardinops caerulea (Girard). In: Rosa H, Murphy GI (eds) Proceedings of the world scientific meeting on the biology of sardines and related species. Food and Agriculture Organization of the United Nations III, pp 667–791

  • Mattiucci S (2006) Parasites as biological tags in population studies of demersal and pelagic fish species. Parassitologia 48:23–25

    PubMed  CAS  Google Scholar 

  • Mattiucci S, Abaunza P, Ramadori L, Nascetti G (2004) Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock identification. J Fish Biol 65:495–510

    Article  Google Scholar 

  • Mattiucci S, Farina V, Campbell N, MacKenzie K, Ramos P, Pinto AL, Abaunza P, Nascetti G (2008) Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: their genetic differentiation and use as biological tags for host stock characterization. Fish Res 89:146–151

    Article  Google Scholar 

  • Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasitol 66:47–148

    Article  PubMed  Google Scholar 

  • Mattiucci S, Paoletti M, Webb SC (2009) Anisakis nascettii n. sp. (Nematoda: Anisakidae) from beaked whales of the southern Hemisphere: morphological description, genetic relationships between congeners and ecological data. Syst Parasitol 74:199–217

    Article  PubMed  Google Scholar 

  • McClelland G, Melendy J, Osborne J, Reid D, Douglas S (2005) Use of parasite and genetic markers in delineating populations of winter flounder from the central south-west Scotian Shelf and north-east Gulf of Maine. J Fish Biol 66:1082–1100

    Article  Google Scholar 

  • McDonald TE, Margolis L (1995) Synopsis of the parasites of fishes of Canada: supplement (1978–1993). Canadian Special Publication of Fisheries and Aquatic Sciences 122:265 pp

  • McEvoy AF, Scheiber HN (1984) Scientists, entrepreneurs, and the policy process: a study of the post-1945 California sardine depletion. J Eco Hist 44:393–406

    Article  Google Scholar 

  • McFarlane GA, Schweigert J, MacDougall L, Hrabok C (2005) Distribution and biology of Pacific sardines (Sardinops sagax) off British Columbia, Canada. CalCOFI Rep 46:144–160

    Google Scholar 

  • McFarlane GA, Wydoski RS, Prince ED (1990) Historical review of the development of external tags and marks. Am Fish Soc Symp 7:9–29

    Google Scholar 

  • McGladdery SE, Burt MDB (1985) Potential of parasites for use as biological indicators of migration, feeding, and spawning behavior of Northwestern Atlantic herring (Clupea harengus). Can J Fish Aquat Sci 42:1957–1968

    Article  Google Scholar 

  • Moles A (2007) Parasites of the fishes of Alaska and surrounding waters. Alaska Fish Res Bull 12:197–226

    Google Scholar 

  • Montgomery WR (1957) Studies on digenetic trematodes from marine fishes of La Jolla, California. Trans Amer Micro Soc 76:13–35

    Google Scholar 

  • Morin PA, Luikart G, Wayne RK, The SNP workshop group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216

    Article  Google Scholar 

  • *Moser M, Hsieh J (1992) Biological tags for stock separation in Pacific herring Clupea harengus pallasi in California. J Parasitol 78:54–60

    Article  PubMed  CAS  Google Scholar 

  • Nadler, SA (1995) Microevolution and the genetic structure of parasite populations. J Parasitol 81:395–403

    Google Scholar 

  • Narum SR, Banks M, Beacham TD, Bellinger MR, Campbell MR, Dekoning J, Elz A, Gutherie CM III, Kozfkay C, Miller KM, Moran P, Phillips R, Seeb LW, Smith CT, Warheit K, Young SF, Garza JC (2008) Differentiating salmon populations at broad and fine geographical scales with microsatellites and single nucleotide polymorphisms. Mol Ecol 17:3464–3477

    PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Neilson JD, Stobo WT, Perley P (2006) Pollock (Pollachius virens) stock structure in theCanadian Maritimes inferred from mark-recapture studies. ICES J Mar Sci 63:749–765

    Article  Google Scholar 

  • Nielsen EE, Hemmer-Hansen J, Poulsen NA, Loeschcke V, Moen T, Johansen T, Mittelholzer C, Taranger G-L, Ogden R, Carvalho GR (2009a) Genomic signatures of local directional selection in a high gene flow marine organism: the Atlantic cod (Gadus morhua). BMC Evol Biol 9:276

    Article  PubMed  CAS  Google Scholar 

  • Nielsen EE, Wright PJ, Hemmer-Hansen J, Poulsen NA, Gibb IM, Meldrup D (2009b) Microgeograhical population structure of cod Gadus morhua in the North Sea and west of Scotland: the role of sampling loci and individuals. Mar Ecol Pro Ser 376:213–225

    Article  Google Scholar 

  • *Oliva ME, Ballón I (2002) Metazoan parasites of the Chilean hake Merluccius gayi gayi as a tool for stock discrimination. Fish Res 56:313–320

    Article  Google Scholar 

  • Olson DB, Cosner C, Cantrell S, Hastings A (2005) Persistence of fish populations in time and space as a key to sustainable fisheries. Bull Mar Sci 76:213–231

    Google Scholar 

  • Orbesen ES, Hoolihan JP, Serafy JE, Snodgrass D, Peel EM, Prince ED (2008) Transboundary movement of Atlantic istiophoris billfishes among international and U.S. domestic management areas inferred from mark-recapture studies. Mar Fish Rev 70:14–23

    Google Scholar 

  • Pauly D, Christensen V, Froese R, Palomares ML (2000) Fishing down aquatic food webs. Industrial fishing over the past half-century has noticeably depleted the topmost links in aquatic food chains. Am Sci 88:46–51

    Google Scholar 

  • Pereyra RT, Saillant E, Pruett L, Rexroad CE III, Rocha-Olivares A, Gold JR (2004) Characterization of polymorphic microsatellites in the Pacific sardine Sardinops sagax sagax (Clupeidae). Mol Ecol Notes 4:739–741

    Article  CAS  Google Scholar 

  • Peterson WT, Schwing FB (2003) A new climate regime in northeast pacific ecosystems. Geophys Res Lett 30:6,1–6,4

    Google Scholar 

  • Podolska M, Horbowy J, Wyszynski M (2006) Discrimination of Baltic herring populations with respect to Anisakis simplex larvae infection. J Fish Biol 68:1241–1256

    Article  Google Scholar 

  • Powles H, Bradford MJ, Bradford RG, Doubleday WG, Innes S, Levings CD (2000) Assessing and protecting marine species. ICES J Mar Sci 57:669–676

    Article  Google Scholar 

  • Pratt I, McCauley JE (1961) Trematodes of the Pacific Northwest. An annotated catalog. Oregon University Press, Corvallis Oregon

    Book  Google Scholar 

  • Prugnolle F, Theron A, Pointer JP, Jabbour-Zahab R, Jarne P, Durand P, De Meeûs T (2005) Dispersal in a parasitic worm and its two hosts and its consequence for local adaptation. Evol 59:296–303

    Google Scholar 

  • Quinn TJ II, Collie JS (2005) Sustainability in single-species population models. Phil Trans R Soc B 360:147–162

    Article  PubMed  Google Scholar 

  • Quinn TJ II, Deriso RB, Neal PR (1990) Migratory catch age analysis. Can J Fish Aquat Sci 47:2315–2327

    Article  Google Scholar 

  • Quinn TJ II, Deriso RB (1999) Quantitative fish dynamics. Oxford University Press, New York

    Google Scholar 

  • Radovich J (1962) Effects of sardine spawning stock size and environment on year-class production. Calif Fish Game 48:123–140

    Google Scholar 

  • Radovich J (1982) The collapse of the California sardine fishery. In: Glantz MH, Thompson JD (eds) Resource management and environmental uncertainty. Lessons from coastal upwelling fisheries. Wiley, New York, pp 107–136

    Google Scholar 

  • Ramon MM, Castro JA (1997) Genetic variation in natural stocks of Sardina pilchardus (sardines) from the western Mediterranean Sea. Heredity 78:520–528

    Article  CAS  Google Scholar 

  • *Reimer LW (1993) Parasites of Merluccius capensis, and M. paradoxus from the coast of Namibia. Appl Parasitol 34:143–150

    PubMed  CAS  Google Scholar 

  • Ricker WE (1954) Stock and recruitment. J Fish Res Board Can 11:559–623

    Article  Google Scholar 

  • Rohde K (1984) Ecology of marine parasites. Helgoländer Meeresunters 37:5–33

    Article  Google Scholar 

  • Roques S, Sevigny J-M, Bérnatchez L (2002) Genetic structure of deep-water redfish, Sebastesmentella, populations across the North Atlantic. Mar Biol 140:297–307

    Article  Google Scholar 

  • Rose GA (1997) The trouble with fisheries science!. Rev Fish Biol Fisher 7:365–370

    Article  Google Scholar 

  • Rounsefell GA, Dahlgren EH (1933) Tagging experiments on the Pacific herring, Clupeapallasii. J Conseil 8:371–384

    Article  Google Scholar 

  • Ruzzante DE, Mariani S, Bekkevold D, André C, Mosegaard H, Clausen LAW, Dahlgren TG, Hutchinson WF, Hatfield EMC, Torstensen E, Brigham J, Simmonds EJ, Laikre L, Larsson LC, Stet RJM, Ryman N, Carvalho GR (2010) Biocomplexity in a highly migratory pelagic marine fish, Atlantic herring. Proc R Soc B 273:1459–1464

    Article  Google Scholar 

  • Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5:417–446

    Article  Google Scholar 

  • Sarmaşik A, Arik Çolakoğlu F, Altun T (2008) Mitochondrial DNA sequence and body size variations in Turkish sardine (Sardina pilchardus) stocks. Turk J Zool 32:229–237

    Google Scholar 

  • Schnute JT, Richards LJ (2001) Use and abuse of fishery models. Can J Fish Aquat Sci 58:10–17

    Article  Google Scholar 

  • Sewell KB, Lester RJG (1995) Stock composition and movement of gemfish, Rexea solandri, as indicated by parasites. Can J Fish Aquat Sci 52S(1):225–232

    Article  Google Scholar 

  • Sinclair M (1988) Marine populations. An essay on population regulation and speciation. Books in recruitment fishery oceanography. Washington Sea Grant Program. Distributed by University of Washington Press, Seattle and London

  • Sinclair M, Solemdal P (1988) The development of “population thinking” in fisheries biology between 1878 and 1930. Aquat Living Resour 1:189–213

    Article  Google Scholar 

  • Smith CT, Seeb LW (2008) Number of alleles as a predictor of the relative assignment accuracy of short tandem repeats (STR) and single-nucleotide-polymorphism (SNP) baselines for chum salmon. Trans Am Fish Soc 137:751–762

    Article  CAS  Google Scholar 

  • Smith PE (2005) A history of proposals for subpopulation structure in the Pacific sardine (Sardinops sagax) population of western North America. CalCOFI Rep 26:75–82

    Google Scholar 

  • Smith TD (1998) “Simultaneous and complementary advances”: mid-century expectations of the interaction of fisheries science and management. Rev Fish Biol Fish 8:335–348

    Article  Google Scholar 

  • Soutar A, Isaacs JD (1969) History of fish populations inferred from fish scales in anaerobic sediments off California. Calif Mar Res Comm CalCOFI Rep 13:63–70

    Google Scholar 

  • *Speare P (1995) Parasites as biological tags for sailfish Istiophorus platypterus, from east coast Australian waters. Mar Ecol Prog Ser 118:43–50

    Article  Google Scholar 

  • Sprague LM, Vrooman AM (1962) A racial analysis of the Pacific sardine Sardinops caeruleus based on studies of erythrocyte antigens. Ann NY Acad Sci 97:131–138

    Article  PubMed  CAS  Google Scholar 

  • Stanley RD, Lee DL, Whitaker DJ (1992) Parasites of yellowtail rockfish, Sebastes flavidus (Ayres, 1862) (Pisces: Teleostei), from the Pacific Coast of North America as potential biological tags for stock identification. Can J Zool 70:1086–1096

    Article  Google Scholar 

  • Stephensen RL (1999) Stock complexity in fisheries management: a perspective of emerging issues related to population sub-units. Fish Res 43:247–249

    Article  Google Scholar 

  • Stepien CA (1995) Population genetic divergence and geographic patterns from DNA sequences: examples from marine and freshwater fishes. Am Fish S S 17:263–287

    Google Scholar 

  • Teel DJ, Van Doornik DM, Kuligowski DR, Grant WS (2003) Genetic analysis of juvenile coho salmon (Oncorhynchus kisutch) off Oregon and Washington reveals few Columbia River wild fish. Fish Bull 101:640–652

    Google Scholar 

  • Thomas F, Verneau O, de Meeûs T, Renaud F (1996) Parasites as to host evolutionary prints: insights into host evolution from parasitological data. Int J Parasitol 26:677–686

    Article  PubMed  CAS  Google Scholar 

  • Timi JT (2003) Parasites of Argentine anchovy in the south-west Atlantic: latitudinal patterns and their use for discrimination of host populations. J Fish Biol 63:90–107

    Article  Google Scholar 

  • Valdivia IM, Chávez RA, Oliva ME (2007) Metazoan parasites of Engraulis ringens as tools for stock discrimination along the Chilean coast. J Fish Biol 70:1504–1511

    Article  Google Scholar 

  • Vignal A, Milan D, SanCristobal M, Eggen A (2001) A review on SNP and other types of molecular markers and their use in animal genetics. Genet Sel Evol 34:272–305

    Google Scholar 

  • Vilas R, Criscione CD, Blouin MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitol 131:839–846

    Article  CAS  Google Scholar 

  • von Bertalanffy L (1938) A quantitative theory of organic growth. Human Biol 10:181–213

    Google Scholar 

  • Waldman JR (2005) Definition of stocks: an evolving concept. In: Cadrin SX, Friedland KD, Waldman JR (eds) Stock identification methods. Applications in fisheries science. Elsevier Academic Press, San Francisco, pp 7–16

    Google Scholar 

  • Waples RS (1998) Separating the wheat form the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Waples RS, Punt AE, Cope JM (2008) Integrating genetic data into management of marine resources: how can we do it better? Fish Fish 9:423–449

    Google Scholar 

  • Welch DW, Boehlert GW, Ward BR (2003) POST-the Pacific Ocean salmon tracking project. Oceanol Acta 25:243–253

    Article  Google Scholar 

  • Whitaker DJ, McFarlane GA (1997) Identification of sablefish, Anoplopoma fimbria (Pallas, 1811), stocks from seamounts off the Canadian Pacific Coast using parasites as biological tags. In: Wilkins MW, Saunders MW (eds). Biology and management of sablefish, Anoplopoma fimbria. NOAA Tech. Rep. NMFS vol 130, pp 131–136

  • Whiteman NK, Parker PG (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Anim Conser 8:175–181

    Article  Google Scholar 

  • Wisner RL (1960) Evidence of a northward movement of stocks of the Pacific sardine based on the number of vertebrae. CalCOFI Rep 8:75–82

    Google Scholar 

  • Wolf P (1992) Recovery of the Pacific sardine and the California sardine fishery. CalCOFI Rep 33:76–86

    Google Scholar 

Electronic Sources

  • FAO (2008) The state of world fisheries and aquaculture (updated 2008). http://fao.org. Accessed: 29 January 2010

  • Johnson JK (2004) Regional overview of coded wire tagging of anadromous salmon and steelhead in Northwest America (updated 2004). http://rmpc.org. Accessed: 20 September 2009

  • WGBH Educational Foundation. 2004. World in the balance (updated 2004)

Download references

Acknowledgments

We would like to thank R. Emmett, M. Blouin, V. Lesser, J. Bolte, E. Casillas, J. Scheurer, and J. Butzen for providing comments on earlier versions of this manuscript. This research was supported through OSU-NOAA Cooperative Institute award #NA17RJ1362, BPA award #1998-014-00 and the Coastal Oregon Marine Experiment Station.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rebecca E. Baldwin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baldwin, R.E., Banks, M.A. & Jacobson, K.C. Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax). Rev Fish Biol Fisheries 22, 137–156 (2012). https://doi.org/10.1007/s11160-011-9227-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11160-011-9227-5

Keywords

Navigation