Spawning Dynamics and Associated Management Implications for Atlantic Cod

AbstractMany stocks of Atlantic Cod Gadus morhua have been depleted due to interactions between overfishing and environmental variation. Stock declines were often accompanied by reductions in spawning diversity and collapses of population structure. Studying Atlantic Cod spawning activity can provide insights into the mechanisms involved in rebuilding. This paper reviews the existing literature on Atlantic Cod spawning dynamics, including habitat, timing, behavior, gamete production, larval survivorship, and fishery impacts. The associated implications for fisheries management are discussed, and critical information gaps are identified for inclusion in future research. Of primary importance for consideration by fisheries managers are the spatial and temporal extent of spawning, the behavior of spawners, and the reproductive contributions of older age-classes. The application of spawning closures as part of a multidisciplinary approach to fisheries management is advocated to prevent the disruption of spawn...

[1]  K. G. Waiwood,et al.  Maternal and seasonal differences in egg sizes and spawning characteristics of captive Atlantic cod, Gadus morhua , 1996 .

[2]  Jason S. Link,et al.  The Trophic Ecology of Atlantic Cod: Insights from Tri-monthly, Localized Scales of Sampling , 2007 .

[3]  Y. Sadovy,et al.  Are aggregation-fisheries sustainable? Reef fish fisheries as a case study , 2005, Coral Reefs.

[4]  J. J. Hunt Rates of Sexual Maturation of Atlantic Cod in NAFO Division 5Ze and Commercial Fishery Implications , 1996 .

[5]  Steven X. Cadrin,et al.  Accounting for Spatial Population Structure in Stock Assessment: Past, Present, and Future , 2009 .

[6]  R. Muñoz,et al.  Preliminary evidence of increased spawning aggregations of mutton snapper (Lutjanus analis) at Riley's Hump two years after establishment of the Tortugas South Ecological Reserve , 2005 .

[7]  M. McCormick BEHAVIORALLY INDUCED MATERNAL STRESS IN A FISH INFLUENCES PROGENY QUALITY BY A HORMONAL MECHANISM , 1998 .

[8]  Christopher L. Brown,et al.  Photoperiod regulates the timing of sexual maturation, spawning, sex steroid and thyroid hormone profiles in the Atlantic cod (Gadus morhua) , 2004 .

[9]  Nils Chr. Stenseth,et al.  Home range and elevated egg densities within an inshore spawning ground of coastal cod , 2007 .

[10]  Assessing evacuation rates and spawning abundance of marine fishes using coupled telemetric and acoustic surveys , 2002 .

[11]  J. Hutchings,et al.  Effect of Age on the Seasonality of Maturation and Spawning of Atlantic Cod, Gadus morhua, in the Northwest Atlantic , 1993 .

[12]  P. Dayton,et al.  The importance in fishery management of leaving the big ones. , 2005, Trends in ecology & evolution.

[13]  B. Rothschild Coherence of Atlantic Cod Stock Dynamics in the Northwest Atlantic Ocean , 2007 .

[14]  K. S. Chan,et al.  Cod and climate: effect of the North Atlantic Oscillation on recruitment in the North Atlantic , 2006 .

[15]  Michael P. Armstrong,et al.  Fine-scale diel and gender-based patterns in behaviour of Atlantic cod (Gadus morhua) on a spawning ground in the Western Gulf of Maine , 2014 .

[16]  R. Nash,et al.  Potential Variability in the Paternal Contribution to Stock Reproductive Potential of Northeast Arctic Cod (Gadus morhua) , 2008 .

[17]  B. Planque,et al.  Calanus and environment in the eastern North Atlantic. 2. Role of the North Atlantic Oscillation on Calanus finmarchicus and C. helgolandicus , 1996 .

[18]  Aaron N. Rice,et al.  Acoustic monitoring of Atlantic cod (Gadus morhua) in Massachusetts Bay: implications for management and conservation , 2013 .

[19]  D. Ruzzante,et al.  Stability in the historical pattern of genetic structure of Newfoundland cod (Gadus morhua) despite the catastrophic decline in population size from 1964 to 1994 , 2001, Conservation Genetics.

[20]  D. M. Ware,et al.  Reproductive Strategies of Demersal and Pelagic Spawning Fish , 1984 .

[21]  E. Trippel Estimation of Male Reproductive Success of Marine Fisheries , 2003 .

[22]  E. Knut,et al.  Paris Meeting of the International Council for the Exploration of the Sea , 1923, Nature.

[23]  K. Wieland,et al.  Spawning and life history information for North Atlantic cod stocks , 2005 .

[24]  George Sugihara,et al.  Why fishing magnifies fluctuations in fish abundance , 2008, Nature.

[25]  E. DeBlois,et al.  Effect of foraging activity on the shoal structure of cod (Gadus morhua) , 1995 .

[26]  S. V. Goddard,et al.  Distribution shifts and overfishing the northern cod (Gadus morhua): a view from the ocean , 2000 .

[27]  E. Trippel,et al.  Male reproductive success and body size in Atlantic cod Gadus morhua L. , 2001 .

[28]  R. Myers,et al.  Match/mismatch predictions of spawning duration versus recruitment variability , 1994 .

[29]  M. Sinclair Marine Populations: An Essay on Population Regulation and Speciation , 1988 .

[30]  K. Brander Comparison of Spawning Characteristics of Cod (Gadus morhua) Stocks in the North Atlantic , 1993 .

[31]  O. S. Kjesbu,et al.  Timing and determination of potential fecundity in Atlantic cod (Gadus morhua) , 2006 .

[32]  E. Trippel,et al.  Fertility and Sperm Quality of Virgin and Repeat-Spawning Atlantic Cod (Gadus morhua) and Associated Hatching Success , 1992 .

[33]  J. Hutchings,et al.  Extreme spawning-site fidelity in Atlantic cod , 2011 .

[34]  L. Kaufman,et al.  Estimating the importance of maternal age, size, and spawning experience to recruitment of Atlantic cod (Gadus morhua) , 2009 .

[35]  P. C. Reid,et al.  Plankton effect on cod recruitment in the North Sea , 2003, Nature.

[36]  G. Lawson,et al.  Small-scale spatial and temporal patterns in spawning of Atlantic cod (Gadus morhua) in coastal Newfoundland waters , 2000 .

[37]  U. Dieckmann,et al.  The logic of skipped spawning in fish , 2006 .

[38]  D. Hamoutene,et al.  Sperm Metabolism and Biochemical Characteristics in First‐Time and Second‐Time Spawners of Farmed Atlantic Cod , 2011 .

[39]  U. Dieckmann,et al.  Propensity of marine reserves to reduce the evolutionary effects of fishing in a migratory species , 2009, Evolutionary applications.

[40]  W. Howell,et al.  Fine-scale temporal and spatial distributions of Atlantic cod (Gadus morhua) on a western Gulf of Maine spawning ground , 2013 .

[41]  Keith Brander,et al.  Cod recruitment is strongly affected by climate when stock biomass is low , 2005 .

[42]  O. Godø,et al.  Migratory behaviour of north-east Arctic cod, studied by use of data storage tags , 2000 .

[43]  K. Drinkwater,et al.  Recruitment Variability in North Atlantic Cod and Match-Mismatch Dynamics , 2011, PloS one.

[44]  G. Rose,et al.  Sex differences in cod residency on a spawning ground , 2003 .

[45]  J. Hutchings,et al.  Nonrandom mating in a broadcast spawner: mate size influences reproductive success in Atlantic cod (Gadus morhua) , 2007 .

[46]  E. Trippel,et al.  Feeding behaviour of cod (Gadus morhua) in relation to spawning , 1999 .

[47]  K. Drinkwater,et al.  The response of Atlantic cod (Gadus morhua) to future climate change , 2005 .

[48]  I. Folstad,et al.  Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua) , 2005, Journal of evolutionary biology.

[49]  Michael P. Armstrong,et al.  The application of small scale fishery closures to protect Atlantic cod spawning aggregations in the inshore Gulf of Maine , 2013 .

[50]  A. Nissling,et al.  Maternal effects on egg size and egg buoyancy of Baltic cod, Gadus morhua: Implications for stock structure effects on recruitment , 2000 .

[51]  C. T. Marshall,et al.  The evaluation of reference points and stock productivity in the context of alternative indices of stock reproductive potential , 2009 .

[52]  J. Tomkiewicz,et al.  Egg production of Baltic cod (Gadus morhua) in relation to variable sex ratio, maturity, and fecundity , 2002 .

[53]  A. Kovach,et al.  Fine-scale spatial and temporal genetic structure of Atlantic cod off the Atlantic coast of the USA , 2010 .

[54]  G. Marteinsdóttir,et al.  Maternal influence on the size and viability of Iceland cod Gadus morhua eggs and larvae , 1998 .

[55]  J. Taggart,et al.  Analysis of the parental contribution to a group of fry from a single day of spawning from a commercial Atlantic cod (Gadus morhua) breeding tank , 2008 .

[56]  Peter J. Wright,et al.  Evidence for metapopulation structuring in cod from the west of Scotland and North Sea , 2006 .

[57]  Diana Perdiguero-Alonso,et al.  Multi-disciplinary fingerprints reveal the harvest location of cod Gadus morhua in the northeast Atlantic , 2010 .

[58]  A. Govender,et al.  Are closed fishing seasons an effective means of increasing reproductive output?: A per-recruit simulation using the limpet Cymbula granatina as a case history , 2007 .

[59]  Ø. Fiksen,et al.  Parental migration, climate and thermal exposure of larvae: spawning in southern regions gives Northeast Arctic cod a warm start , 2011 .

[60]  G. Rose,et al.  Atlantic cod (Gadus morhua) feed during spawning off Newfoundland and Labrador , 2012 .

[61]  G. Rose,et al.  Passive- and active-acoustic properties of a spawning Atlantic cod (Gadus morhua) aggregation , 2009 .

[62]  O. S. Kjesbu Time of start of spawning in Atlantic cod (Gadus morhua) females in relation to vitellogenic oocyte diameter, temperature, fish length and condition , 1994 .

[63]  G. Rose,et al.  Cod spawning on a migration highway in the north-west Atlantic , 1993, Nature.

[64]  O. S. Kjesbu,et al.  Ovulatory Rhythm and a Method to Determine the Stage of Spawning in Atlantic Cod (Gadus morhua) , 1990 .

[65]  H. Svedäng,et al.  Consequences of Subpopulation Structure on Fisheries Management: Cod (Gadus morhua) in the Kattegat and Öresund (North Sea) , 2010 .

[66]  Ransom A. Myers,et al.  What can be learned from the collapse of a renewable resource? Atlantic cod, Gadus morhua, of Newfoundland and Labrador , 1994 .

[67]  Michael P. Armstrong,et al.  Disruption of an Atlantic Cod Spawning Aggregation Resulting from the Opening of a Directed Gill‐Net Fishery , 2012 .

[68]  F. Jones,et al.  THE STRUCTURE AND FUNCTIONS OF THE THELEOSTEAN SWEMBLADDER , 1953 .

[69]  Tom G. Pottinger,et al.  Preliminary evidence that chronic confinement stress reduces the quality of gametes produced by brown and rainbow trout , 1994 .

[70]  J. Hutchings,et al.  Sexual dimorphism in pelvic fin length of Atlantic cod , 2006 .

[71]  S. Tilseth,et al.  Growth, Development, and Feeding Success of Atlantic Cod Larvae Gadus morhua Related to Egg Size , 1985 .

[72]  C. T. Marshall,et al.  Systematic bias in estimates of reproductive potential of an Atlantic cod (Gadus morhua) stock: implications for stock–recruit theory and management , 2006 .

[73]  A. K. Daníelsdóttir,et al.  The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments , 2006 .

[74]  P. Pepin,et al.  Time to hatch and larval size in relation to temperature and egg size in Atlantic cod (Gadus morhua) , 1997 .

[75]  M. Ryan Sexual selection, sensory systems and sensory exploitation. , 1990 .

[76]  A. Svardal,et al.  Seasonal trends in adenylate nucleotide content in eggs of recruit and repeat spawning Atlantic cod (Gadus morhua L.) and implications for egg quality and buoyancy , 2012 .

[77]  G. Rosenlund,et al.  The effect of dietary lipid content and stress on egg quality in farmed Atlantic cod Gadus morhua. , 2012, Journal of fish biology.

[78]  Ray Hilborn,et al.  Causes of Decline and Potential for Recovery of Atlantic Cod Populations , 2009 .

[79]  Vilhjalmur Thorsteinsson,et al.  Consistency in the behaviour types of the Atlantic cod: repeatability, timing of migration and geo-location , 2012 .

[80]  M. Morgan,et al.  Effect of changes in reproductive potential on perceived productivity of three Northwest Atlantic cod (Gadus morhua) stocks , 2005 .

[81]  M. Morgan,et al.  The effect of stress on reproduction in Atlantic cod , 1999 .

[82]  Svein Sundby,et al.  Effects of temperature, wind and spawning stock biomass on recruitment of Arcto-Norwegian cod , 1995 .

[83]  Ransom A. Myers,et al.  Hypotheses for the decline of cod in the North Atlantic , 1996 .

[84]  P. Sale,et al.  Metapopulation ecology in the sea: from Levins' model to marine ecology and fisheries science , 2004 .

[85]  B. K. Stensholt Cod migration patterns in relation to temperature: analysis of storage tag data , 2001 .

[86]  D. Kulka,et al.  Recent changes in the winter distribution and movements of northern Atlantic cod (Gadus morhua Linnaeus, 1758) on the Newfoundland-Labrador Shelf , 1995 .

[87]  R. Gardner,et al.  Modeling Disaster: The Failure of the Management of the New England Groundfish Industry , 2011 .

[88]  J. Hutchings Life history consequences of overexploitation to population recovery in Northwest Atlantic cod (Gadus morhua) , 2005 .

[89]  D. Methven,et al.  Protracted spawning of Atlantic cod (Gadus morhua) in Newfoundland waters: evidence from otolith microstructure , 1997 .

[90]  A. O. Bui,et al.  Searching for Atlantic cod (Gadus morhua) spawning sites in the northwest Gulf of St Lawrence (Canada) using molecular techniques , 2011 .

[91]  Ivar Folstad,et al.  Cod courtship song: a song at the expense of dance? , 1999 .

[92]  Ø. Karlsen,et al.  The expression of secondary sexual characteristics in recruit- and repeat-spawning farmed and wild Atlantic cod (Gadus morhua) , 2008 .

[93]  P. Rago,et al.  Incorporating Early-Life History Parameters in the Estimation of the Stock-Recruit Relationship of Georges Bank Atlantic Cod (Gadus morhua) , 2003 .

[94]  Nordeide,et al.  Is cod lekking or a promiscuous group spawner , 2000 .

[95]  E. Trippel Egg Size and Viability and Seasonal Offspring Production of Young Atlantic Cod , 1998 .

[96]  H. Browman Application of evolutionary theory to fisheries science and stock assessment- management , 2000 .

[97]  Douglas R. Zemeckis,et al.  Stock identification of Atlantic cod (Gadus morhua) in US waters: an interdisciplinary approach , 2014 .

[98]  T. Reusch,et al.  Severe tissue damage in Atlantic cod larvae under increasing ocean acidification , 2012 .

[99]  D. Dewsbury,et al.  Ejaculate Cost and Male Choice , 1982, The American Naturalist.

[100]  G. Begg,et al.  Discrimination between Icelandic cod (Gadus morhua L.) populations from adjacent spawning areas based on otolith growth and shape , 2006 .

[101]  D. H. Cushing,et al.  Plankton Production and Year-class Strength in Fish Populations: an Update of the Match/Mismatch Hypothesis , 1990 .

[102]  Vivien M. Brawn,et al.  Sound Production By the Cod (Gadus Callarias L.) , 1961 .

[103]  N. Stenseth,et al.  Fine‐scaled geographical population structuring in a highly mobile marine species: the Atlantic cod , 2003, Molecular ecology.

[104]  K. Wieland,et al.  Changes in the timing of spawning of Baltic cod: possible causes and implications for recruitment , 2000 .

[105]  Vivien M. Brawn,et al.  Aggressive Behaviour in the Cod (Gadus Callarias L.) , 1961 .

[106]  E. Durbin,et al.  Seasonal and inter-annual trends in the zooplankton prey and growth rate of Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) larvae on Georges Bank , 2006 .

[107]  G A Rose,et al.  An observation on the reaction of Atlantic cod (Gadus morhua) in a spawning shoal to bottom trawling , 1997 .

[108]  G. Rose,et al.  Multiyear homing of Atlantic cod to a spawning ground , 2001 .

[109]  Y. Lambert,et al.  Energetic consequences of reproduction in Atlantic cod (Gadus morhua) in relation to spawning level of somatic energy reserves. , 2000 .

[110]  S. Fevolden,et al.  The scnDNA locus Pan I reveals concurrent presence of different populations of Atlantic cod (Gadus morhua L.) within a single fjord , 2005 .

[111]  J. Hutchings,et al.  Sound production by Atlantic Cod during spawning , 2006 .

[112]  C. T. Marshall,et al.  Is spawner biomass a sensitive measure of the reproductive and recruitment potential of Northeast Arctic cod , 1998 .

[113]  Geir Huse,et al.  Modelling buoyancy regulation in fishes with swimbladders: bioenergetics and behaviour , 2005 .

[114]  P. Snelgrove,et al.  Rebuilding Atlantic Cod: Lessons from a Spawning Ground in Coastal Newfoundland , 2008 .

[115]  A. Friedlander,et al.  Evaluation of a conservation strategy: a spawning aggregation closure for red hind, Epinephelus guttatus, in the U.S. Virgin Islands , 1999, Environmental Biology of Fishes.

[116]  D. Shapiro,et al.  Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[117]  E. Trippel,et al.  Skewed sex ratios in spawning shoals of Atlantic cod (Gadus morhua) , 1996 .

[118]  J. Wroblewski,et al.  Metapopulation theory and northern cod population structure: interdependency of subpopulations in recovery of a groundfish population , 2002 .

[119]  Mark J. Kurlansky,et al.  Cod: A Biography of the Fish that Changed the World , 1997 .

[120]  Shane Abeare,et al.  Fishing effort redistribution in response to area closures , 2009 .

[121]  G. Huse,et al.  Stock collapses and their recovery: mechanisms that establish and maintain life-cycle closure in space and time , 2010 .

[122]  K. Frank,et al.  Contemporary management issues confronting fisheries science , 2001 .

[123]  G. Begg,et al.  Spawning origins of pelagic juvenile cod Gadus morhua inferred from spatially explicit age distributions : potential influences on year-class strength and recruitment , 2000 .

[124]  Christian Möllmann,et al.  A model-based evaluation of Marine Protected Areas: the example of eastern Baltic cod (Gadus morhua callarias L.) , 2009 .

[125]  O. S. Kjesbu,et al.  Mechanisms regulating oocyte recruitment and skipped spawning in Northeast Arctic cod (Gadus morhua) , 2009 .

[126]  A. K. Daníelsdóttir,et al.  Neutral and Nonneutral Genetic Markers Revealed the Presence of Inshore and Offshore Stock Components of Atlantic Cod in Greenland Waters , 2011 .

[127]  M. Sinclair,et al.  Seal-cod interactions on the Eastern Scotian Shelf: Reconsideration of modelling assumptions , 2012 .

[128]  Svein Løkkeborg,et al.  Reproductive interactions between fugitive farmed and wild Atlantic cod (Gadus morhua) in the field , 2010 .

[129]  G. Stefansson,et al.  Spatial variation in abundance, size composition and viable egg production of spawning cod (Gadus morhua L.) in Icelandic waters , 2000 .

[130]  S. Sundby,et al.  Modelling dispersal of eggs and quantifying connectivity among Norwegian coastal cod subpopulations , 2014 .

[131]  Y. Lambert,et al.  Environmental and fishing limitations to the rebuilding of the northern Gulf of St. Lawrence cod stock (Gadus morhua) , 2011 .

[132]  Robert L. Stephenson,et al.  The importance of managing within-species diversity in cod and herring fisheries of the north-western Atlantic , 2001 .

[133]  R. Beverton Small marine pelagic fish and the threat of fishing; are they endangered? , 1990 .

[134]  D. Duplisea,et al.  Fishing under low productivity conditions is further delaying recovery of Northwest Atlantic cod (Gadus morhua) , 2006 .

[135]  J. Link,et al.  Trophic role of Atlantic cod in the ecosystem , 2009 .

[136]  G. Rose,et al.  Isolation or metapopulation: whence and whither the Smith Sound cod? , 2011 .

[137]  James E. Byers,et al.  Going against the flow: retention, range limits and invasions in advective environments , 2006 .

[138]  W. Gurney,et al.  Modelling the spatial demography of Atlantic cod (Gadus morhua) on the European continental shelf , 2006 .

[139]  P. Snelgrove,et al.  Discrete spatial dynamics in a marine broadcast spawner: Re-evaluating scales of connectivity and habitat associations in Atlantic cod (Gadus morhua L.) in coastal Newfoundland , 2008 .

[140]  B. Neis,et al.  Inshore Stocks of Atlantic Cod Are Important for Rebuilding the East Coast Fishery , 2005 .

[141]  N. Stenseth,et al.  Small-scale genetic structure in a marine population in relation to water circulation and egg characteristics. , 2010, Ecology.

[142]  T. Grabowski,et al.  Evidence of Segregated Spawning in a Single Marine Fish Stock: Sympatric Divergence of Ecotypes in Icelandic Cod? , 2011, PloS one.

[143]  R. G. Halliday,et al.  The roles of fishing and environmental change in the decline of Northwest Atlantic groundfish populations in the early 1990s , 2009 .

[144]  O. S. Kjesbu,et al.  Effects of adult age and size structure on reproductive output in marine fishes , 1997 .

[145]  G. Carvalho,et al.  Marked genetic structuring in localised spawning populations of cod Gadus morhua in the North Sea and adjoining waters, as revealed by microsatellites , 2001 .

[146]  O. Fiksen,et al.  The evolution of spawning migrations: state dependence and fishing-induced changes. , 2008, Ecology.

[147]  Ransom A. Myers,et al.  Geographic Variation in the Spawning of Atlantic Cod, Gadus morhua, in the Northwest Atlantic , 1993 .

[148]  T. Sterner Unobserved diversity, depletion and irreversibility The importance of subpopulations for management of cod stocks , 2007 .

[149]  J. Hutchings,et al.  Correlates of recovery for Canadian Atlantic cod (Gadus morhua) , 2011 .

[150]  J. Hutchings,et al.  Morphological and behavioural correlates of reproductive success in Atlantic cod Gadus morhua , 2008 .

[151]  O. S. Kjesbu,et al.  Is spawning time of marine fish imprinted in the genes? A two-generation experiment on local Atlantic cod (Gadus morhua L.) populations from different geographical regions , 2012 .

[152]  S. Biddiscombe,et al.  Time course of gametogenesis in Northwest Atlantic cod (Gadus morhua) , 1997 .

[153]  L. Crowder,et al.  Larval Size and Recruitment Mechanisms in Fishes: Toward a Conceptual Framework , 1988 .

[154]  S. Sundby Recruitment of Atlantic cod stocks in relation to temperature and advectlon of copepod populations , 2000 .

[155]  N. Stenseth,et al.  Changes in spawning stock structure strengthen the link between climate and recruitment in a heavily fished cod (Gadus morhua) stock , 2006 .

[156]  V. M. Brawn Reproductive Behaviour of the Cod (Gad Us Callarias L.) , 1961 .

[157]  M. Heino,et al.  Secondary sexual characteristics in codfishes (Gadidae) in relation to sound production, habitat use and social behaviour , 2012 .

[158]  M. Cardinale,et al.  Modelling recruitment and abundance of Atlantic cod, Gadus morhua, in the eastern Skagerrak-Kattegat (North Sea): evidence of severe depletion due to a prolonged period of high fishing pressure , 2004 .

[159]  E. Ames Atlantic Cod Stock Structure in the Gulf of Maine , 2004 .

[160]  K. Frank,et al.  Allee effects and compensatory population dynamics within a stock complex , 2000 .

[161]  O. S. Kjesbu,et al.  Temporal variations in the fecundity of Arcto-Norwegian cod (Gadus morhua) in response to natural changes in food and temperature , 1998 .

[162]  R. Nemeth Population characteristics of a recovering US Virgin Islands red hind spawning aggregation following protection. , 2005, Marine ecology progress series.

[163]  J. Hare,et al.  Does the fall phytoplankton bloom control recruitment of Georges Bank haddock, Melanogrammus aeglefinus, through parental condition? , 2008 .

[164]  Olav Sigurd Kjesbu,et al.  The spawning activity of cod, Gadus morhua L. , 1989 .

[165]  L. J. Bolle,et al.  Mapping the spawning grounds of North Sea cod (Gadus morhua) by direct and indirect means , 2008, Proceedings of the Royal Society B: Biological Sciences.

[166]  R. Billard A quantitative analysis of spermatogenesis in the trout, Salmo trutta fario , 2004, Cell and Tissue Research.

[167]  George C. Williams,et al.  Sex and evolution. , 1975, Monographs in population biology.

[168]  G. Rose,et al.  Do cod form spawning leks? Evidence from a Newfoundland spawning ground , 2006 .

[169]  R. Hilborn,et al.  Biocomplexity and fisheries sustainability , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[170]  D. Ruzzante,et al.  A nuclear DNA basis for shelf‐ and bank‐scale population structure in northwest Atlantic cod (Gadus morhua): Labrador to Georges Bank , 1998 .

[171]  B. Bogstad,et al.  Feeding of mature cod (Gadus morhua) on the spawning grounds in Lofoten , 2008 .

[172]  Michael J. Fogarty,et al.  Potential climate change impacts on Atlantic cod (Gadus morhua) off the northeastern USA , 2008 .

[173]  Walter H. F. Smith,et al.  Spawning strategies of fishes in relation to circulation, phytoplankton production, and pulses in zooplankton off the north-eastern United States , 1984 .

[174]  J. Hutchings,et al.  A link between sound producing musculature and mating success in Atlantic cod , 2008 .

[175]  M. Heath,et al.  A model of meta-population dynamics for North Sea and West of Scotland cod - the dynamic consequences of natal fidelity , 2008 .

[176]  Olav Sigurd Kjesbu,et al.  Variation in annual egg production in individual captive Atlantic cod (Gadus morhua) , 1996 .

[177]  V. Tschernij,et al.  Fishermen responses on marine protected areas in the Baltic cod fishery , 2010 .

[178]  J. Holm,et al.  Growth, gonadal development and spawning time of Atlantic cod (Gadus morhua) reared under different photoperiods , 2001 .

[179]  J. Hutchings Spatial and temporal variation in the density of northern cod and a review of hypotheses for the stock's collapse , 1996 .

[180]  J. Hutchings,et al.  Mating systems and the conservation of commercially exploited marine fish , 2003 .

[181]  C. Fauvel,et al.  Changes in Atlantic cod (Gadus morhua L.) sperm quality during the spawning season , 2008 .

[182]  B. Scott,et al.  Potential effects of maternal factors on spawning stock-recruitment relationships under varying fishing pressure , 1999 .

[183]  U. Dieckmann,et al.  Assessing changes in age and size at maturation in collapsing populations of Atlantic cod (Gadus morhua) , 2005 .

[184]  K. Brander,et al.  Distribution of Early-Stage Atlantic Cod (Gadus morhua), Haddock (Melanogrammus aeglefinus), and Witch Flounder (Glyptocephalus cynoglossus) Eggs on the Scotian Shelf: A Reappraisal of Evidence on the Coupling of Cod Spawning and Plankton Production , 1992 .

[185]  G. Rose,et al.  Acoustic markers of Atlantic cod (Gadus morhua) spawning in coastal Newfoundland , 2012 .

[186]  R. Stephenson Stock complexity in fisheries management: a perspective of emerging issues related to population sub-units , 1999 .

[187]  Geir Ottersen Pronounced long-term juvenation in the spawning stock of Arcto-Norwegian cod (Gadus morhua) and possible consequences for recruitment , 2008 .

[188]  P. Jonsson,et al.  Migratory behaviour of Atlantic cod Gadus morhua: natal homing is the prime stock-separating mechanism , 2007 .

[189]  G. Rose,et al.  Migratory behaviour and range in Atlantic cod: inference from a century of tagging , 2004 .

[190]  Ransom A. Myers,et al.  Cod spawning in relation to physical and biological cycles of the northern North–west Atlantic , 1993 .

[191]  J. Link,et al.  The relationship between stomach contents and maturity state for major northwest Atlantic fishes: new paradigms? , 2001 .

[192]  A. HutchingsJeffrey,et al.  Population dynamics of marine fishes at low abundance , 2012 .

[193]  O. Nakken,et al.  Spatial shifts in spawning habitats of Arcto-Norwegian cod related to multidecadal climate oscillations and climate change , 2008 .

[194]  G. Huse,et al.  Vertical migration in adult Atlantic cod (Gadus morhua) , 2007 .

[195]  L. Siceloff Fine-scale activity, distribution and habitat utilization of Atlantic cod (Gadus morhua) on the Ipswich Bay spawning ground , 2009 .

[196]  R. Nash,et al.  Frequent skipped spawning in the world’s largest cod population , 2012, Proceedings of the National Academy of Sciences.

[197]  Andrew A. Rosenberg,et al.  Designing marine protected areas for migrating fish stocks , 2006 .

[198]  J. Tomkiewicz,et al.  Skipped Spawning in Fishes: More Common than You Might Think , 2011 .

[199]  E. Kjørsvik,et al.  Effects of egg quality on normal fertilization and early development of the cod, Gadus morhua L , 1983 .

[200]  T. H. Glutton-Brock,et al.  Sexual selection and the potential reproductive rates of males and females , 1991, Nature.

[201]  M. Love,et al.  Fisheries Sustainability via Protection of Age Structure and Spatial Distribution of Fish Populations , 2004 .

[202]  K. Lindeman,et al.  A Global Baseline for Spawning Aggregations of Reef Fishes , 2008, Conservation biology : the journal of the Society for Conservation Biology.

[203]  Gary R. Carvalho,et al.  Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts , 2008 .

[204]  S. Cadrin,et al.  Simulation modelling as a tool for examining the consequences of spatial structure and connectivity on local and regional population dynamics , 2010 .

[205]  D. P. Swain,et al.  Forage fish and the factors governing recovery of Atlantic cod (Gadus morhua) on the eastern Scotian Shelf , 2012 .

[206]  Y. Lambert Long-term changes in life history characteristics and reproductive potential of northern Gulf of St. Lawrence cod (Gadus morhua) and consequences for the stock productivity , 2013 .

[207]  C. Gillet,et al.  Stress, environment and reproduction in teleost fish , 1981 .

[208]  Peter J. Wright,et al.  Effect of age and temperature on spawning time in two gadoid species , 2013 .

[209]  J. Fosseidengen,et al.  CALLS OF THE ATLANTIC COD: DOES CAPTIVITY RESTRICT THEIR VOCAL REPERTOIRE? , 2002 .

[210]  S. Campana Year-class strength and growth rate in young Atlantic cod Gadus morhua , 1996 .

[211]  S. Holmes,et al.  Evidence from survey data for regional variability in cod dynamics in the North Sea and West of Scotland , 2008 .

[212]  T. Beacham,et al.  Multiple stock structure of Atlantic cod (Gadus morhua) off Newfoundland and Labrador determined from genetic variation , 2002 .

[213]  R. Rideout,et al.  Observations on mass atresia and skipped spawning in northern Atlantic cod, from Smith Sound, Newfoundland , 2000 .

[214]  Gudrun Marteinsdottir,et al.  Improving the stock-recruitment relationship in Icelandic cod (Gadus morhua) by including age diversity of spawners , 1998 .

[215]  D. Bekkevold,et al.  Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.) , 2002, Molecular ecology.

[216]  N. Stenseth,et al.  Environmental toxicology: population modeling of cod larvae shows high sensitivity to loss of zooplankton prey. , 2011, Marine pollution bulletin.

[217]  R. Cooper,et al.  Lament for an Ocean: The Collapse of the Atlantic Cod Fishery: A True Crime Story , 1999 .

[218]  G. Rose,et al.  Seasonal spawning and wind-regulated retention-dispersal of early life stage Atlantic cod (Gadus morhua) in a Newfoundland fjord , 2010 .

[219]  E. Trippel,et al.  Spermatocrit and spermatozoa density in Atlantic cod (Gadus morhua): correlation and variation during the spawning season , 1999 .

[220]  A. Bundy,et al.  Seals, cod and forage fish: A comparative exploration of variations in the theme of stock collapse and ecosystem change in four Northwest Atlantic ecosystems , 2009 .

[221]  N. Stenseth,et al.  Spawning stock and recruitment in North Sea cod shaped by food and climate , 2010, Proceedings of the Royal Society B: Biological Sciences.

[222]  Jeffrey A. Hutchings,et al.  Spawning behaviour of Atlantic cod , Gadus morhua : evidence of mate competition and mate choice in a broadcast spawner , 1999 .

[223]  A. F. Opdal Fisheries change spawning ground distribution of northeast Arctic cod , 2010, Biology Letters.

[224]  G. Begg,et al.  Effects of population size/age structure, condition and temporal dynamics of spawning on reproductive output in Atlantic cod (Gadus morhua) , 2006 .

[225]  E. Trippel,et al.  Fishery-induced demographic changes in the timing of spawning: consequences for reproductive success* , 2009 .

[226]  G. Rose Monitoring coastal northern cod: towards an optimal survey of Smith Sound, Newfoundland , 2003 .

[227]  P. Rago,et al.  Impacts of demographic variation in spawning characteristics on reference points for fishery management , 2001 .

[228]  J. Hutchings,et al.  Shifting reproductive success in a shoal of Atlantic Cod, Gadus morhua L. , 2010, Environmental Biology of Fishes.

[229]  Michael J. Fogarty,et al.  Effort distribution and catch patterns adjacent to temperate MPAs , 2005 .

[230]  H. Svedäng,et al.  The spatial distribution of cod (Gadus morhua L.) spawning grounds in the Kattegat, eastern North Sea , 2008 .

[231]  D. Bekkevold,et al.  Depensation, probability of fertilization, and the mating system of Atlantic cod (Gadus morhua L.) , 2004 .

[232]  R. Rideout,et al.  Suppression of reproduction in Atlantic cod Gadus morhua , 2006 .

[233]  W. Holtz,et al.  Sperm output in rainbow trout (Salmo gairdneri) — Effect of age, timing and frequency of stripping and presence of females , 1984 .