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.
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
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
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
Alder J, Campbell B, Karpouzi V, Kaschner K, Pauly D (2008) Forage fish: from ecosystems to markets. Annu Rev Environ Resour 33:153–166
Allendorf FW, Luikart G (2007) Conservation and the Genetics of Populations. Blackwell Publishing, Australia
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
*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
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
Avise JC (1998) Conservation in the marine realm. J Hered 89:377–382
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
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
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
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
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
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
Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43:35–44
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
Beverton R (1998) Fish, fact and fantasy: a long view. Rev Fish Biol Fisher 8:229–249
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
Bruford MW, Wayne RK (1993) Microsatellites and their application to population genetic studies. Curr Opin Genet Dev 31:939–943
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
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
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
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
*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
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
Checkley DM, Barth JA (2009) Patterns and processes in the California current system. Prog Oceanogr 83:49–64
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
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
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
Collie JS, Gislason H (2001) Biological reference points in a multispecies context. Can J Fish Aquat Sci 58:2167–2176
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
Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evol 58:198–202
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
Criscione CD, Cooper B, Blouin MS (2006) Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecol 87:823–828
Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257
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
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
Dahlgren EH (1936) Further developments in the tagging of the Pacific herring, (Clupea pallasii). J Conseil 11:229–247
DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473
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
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
Felin FE (1954) Population heterogeneity in the Pacific pilchard. Fish Bull US 54:201–225
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
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
Fitch JE (1969) Fossil records of certain schooling fishes of the California current system. Calif Mar Res Comm CalCOFI Rep 13:71–80
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
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
Graham M (1935) Modern theory of exploiting a fishery, and application to North Sea trawling. J Cons Int Explor Mer 10:264–274
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
Grant WS, Utter FM (1984) Biochemical population genetics of Pacific herring (Clupea pallasi). Can J Fish Aquat Sci 41:856–864
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
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
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
Hansen MM, Kenchington E, Nielsen EE (2001) Assigning individual fish to populations using microsatellite DNA markers. Fish Fish 2:93–112
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
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
Harris H (1966) Enzyme polymorphism in man. Proc R Soc Ser B 164:298–310
Harrt AC (1963) Problems in tagging salmon at sea. ICNAF Spec Publ 4:144–155
Hart JL (1943) Tagging experiments on British Columbia pilchards. J Fish Res Bd Can 6:164–182
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
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
Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evol 53:313–318
*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
Hewitt GM (2004) The structure of biodiversity—insights from molecular phylogeography. Front Zool 1:4
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
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
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
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
Jakobsson J (1970) On fish tags and tagging. Oceanogr Mar Bio 8:457–499
Janssen JF Jr (1938) Second report of sardine tagging in California. Fish Bull Calif Dept Fish Game 24:376–389
Janssen JF Jr, Alpen JF (1945) The effect of internal tags upon sardines. Fish Bull 61:43–62
Jones CM (2006) Estuarine and diadromous fish metapopulations. In: Kritzer JP, Sale PF (eds) Marine metapopulations. Elsevier Academic Press, San Francisco, pp 119–154
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
King RC, Stansfield WD (1985) A dictionary of genetics, 3rd edn. Oxford University Press, New York
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
*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
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
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
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
Lester RJG (1990) Reappraisal of the use of parasites for fish stock identification. Aust J Mar Freshwater Res 41:855–864
*Lester RJG, Barnes A, Habib G (1985) Parasites of skipjack tuna, Katsuwonus pelamis: fishery implications. Fish Bull 83:343–356
*Lester RJG, Sewell KB, Barnes A, Evans K (1988) Stock discrimination of orange roughy Hoplostethus atlanticus, by parasite analysis. Mar Biol 99:137–144
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
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
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
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
Longhurst A (2006) The sustainability myth. Fish Res 81:107–112
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
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
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
MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitol 124:S153–S163
*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
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
*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
Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142
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
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
Marcogliese DJ (1995) The role of zooplankton in the transmission of helminth parasites to fish. Rev Fish Biol Fish 5:336–371
Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitol 124:S83–S99
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
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
*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
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
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
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
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
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
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
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
McFarlane GA, Wydoski RS, Prince ED (1990) Historical review of the development of external tags and marks. Am Fish Soc Symp 7:9–29
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
Moles A (2007) Parasites of the fishes of Alaska and surrounding waters. Alaska Fish Res Bull 12:197–226
Montgomery WR (1957) Studies on digenetic trematodes from marine fishes of La Jolla, California. Trans Amer Micro Soc 76:13–35
Morin PA, Luikart G, Wayne RK, The SNP workshop group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216
*Moser M, Hsieh J (1992) Biological tags for stock separation in Pacific herring Clupea harengus pallasi in California. J Parasitol 78:54–60
Nadler, SA (1995) Microevolution and the genetic structure of parasite populations. J Parasitol 81:395–403
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
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
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
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
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
*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
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
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
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
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
Peterson WT, Schwing FB (2003) A new climate regime in northeast pacific ecosystems. Geophys Res Lett 30:6,1–6,4
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
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
Pratt I, McCauley JE (1961) Trematodes of the Pacific Northwest. An annotated catalog. Oregon University Press, Corvallis Oregon
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
Quinn TJ II, Collie JS (2005) Sustainability in single-species population models. Phil Trans R Soc B 360:147–162
Quinn TJ II, Deriso RB, Neal PR (1990) Migratory catch age analysis. Can J Fish Aquat Sci 47:2315–2327
Quinn TJ II, Deriso RB (1999) Quantitative fish dynamics. Oxford University Press, New York
Radovich J (1962) Effects of sardine spawning stock size and environment on year-class production. Calif Fish Game 48:123–140
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
Ramon MM, Castro JA (1997) Genetic variation in natural stocks of Sardina pilchardus (sardines) from the western Mediterranean Sea. Heredity 78:520–528
*Reimer LW (1993) Parasites of Merluccius capensis, and M. paradoxus from the coast of Namibia. Appl Parasitol 34:143–150
Ricker WE (1954) Stock and recruitment. J Fish Res Board Can 11:559–623
Rohde K (1984) Ecology of marine parasites. Helgoländer Meeresunters 37:5–33
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
Rose GA (1997) The trouble with fisheries science!. Rev Fish Biol Fisher 7:365–370
Rounsefell GA, Dahlgren EH (1933) Tagging experiments on the Pacific herring, Clupeapallasii. J Conseil 8:371–384
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
Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5:417–446
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
Schnute JT, Richards LJ (2001) Use and abuse of fishery models. Can J Fish Aquat Sci 58:10–17
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
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
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
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
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
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
*Speare P (1995) Parasites as biological tags for sailfish Istiophorus platypterus, from east coast Australian waters. Mar Ecol Prog Ser 118:43–50
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
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
Stephensen RL (1999) Stock complexity in fisheries management: a perspective of emerging issues related to population sub-units. Fish Res 43:247–249
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
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
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
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
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
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
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
von Bertalanffy L (1938) A quantitative theory of organic growth. Human Biol 10:181–213
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
Waples RS (1998) Separating the wheat form the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450
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
Welch DW, Boehlert GW, Ward BR (2003) POST-the Pacific Ocean salmon tracking project. Oceanol Acta 25:243–253
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
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
Wolf P (1992) Recovery of the Pacific sardine and the California sardine fishery. CalCOFI Rep 33:76–86
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)
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-011-9227-5