What Are Jellyfishes and Thaliaceans and Why Do They Bloom

The jellyfishes and thaliaceans comprise primarily planktonic species of cnidarians, ctenophores (jellyfishes) and chordates (thaliaceans or pelagic tunicates). Grouped together because of their gelatinous bodies, these diverse species nonetheless differ in their evolutionary histories and may have distinct morphologies, life histories, ecologies and other traits. Subsets of these species occur at some times and places in highly elevated concentrations, i.e. they accumulate, aggregate, bloom or swarm. Why jellyfishes and thaliaceans occur in such masses is, however, somewhat unclear; the reasons obscured in part by a tendency to treat many gelatinous zooplankton, including jellyfishes and thaliaceans, as a single functional group. Here we summarize the evolutionary relationships among gelatinous zooplankton and review the characteristics of blooms, before focusing on comparing and contrasting medusae, ctenophores and thaliaceans. We highlight some substantial knowledge gaps, emphasize biological factors that likely contribute to blooms and outline a population genetic framework for investigating the ecological causes of boom and bust population dynamics in the plankton.

[1]  M. Dawson,et al.  Jellyfish blooms: Crambionella orsini (Scyphozoa: Rhizostomeae) in the Gulf of Oman, Iran, 2002–2003 , 2008, Journal of the Marine Biological Association of the United Kingdom.

[2]  J. Giske,et al.  Habitat profitability in pelagic environments , 1990 .

[3]  M. Arai,et al.  A Functional Biology of Scyphozoa , 1996, Springer Netherlands.

[4]  D. Angel,et al.  Blooms of the invasive ctenophore, Mnemiopsis leidyi, span the Mediterranean Sea in 2009 , 2010, Hydrobiologia.

[5]  Claudia E. Mills,et al.  Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? , 2001, Hydrobiologia.

[6]  W. Hamner,et al.  Growth, Degrowth, and Irreversible Cell Differentiation in Aurelia aurita , 1974 .

[7]  D. Deibel,et al.  A review of the life cycles and life-history adaptations of pelagic tunicates to environmental conditions , 2012 .

[8]  U. Båmstedt Trophodynamics of the scyphomedusae Aurelia aurita . Predation rate in relation to abundance, size and type of prey organism , 1990 .

[9]  A. Tsuda,et al.  Distribution and growth of salps in a Kuroshio warm-core ring during summer 1987 , 1992 .

[10]  C. H. Lucas,et al.  Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment , 2001, Hydrobiologia.

[11]  N. Bond,et al.  Rise and fall of jellyfish in the eastern Bering Sea in relation to climate regime shifts , 2008 .

[12]  W. Graham,et al.  Biological Invasions by Marine Jellyfish , 2008 .

[13]  A. C. Giese,et al.  Reproduction of marine invertebrates , 1974 .

[14]  J. Titelman,et al.  Feeding rates of the jellyfish Aurelia aurita on fish larvae , 2006 .

[15]  Some implications of molecular phylogenetics for understanding biodiversity in jellyfishes, with emphasis on Scyphozoa , 2004 .

[16]  M. Hadfield,et al.  Variability, flexibility and plasticity in life histories of marine invertebrates , 1996 .

[17]  E. V. Thuesen,et al.  The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi , 2005, Journal of the Marine Biological Association of the United Kingdom.

[18]  J. Purcell Extension of methods for jellyfish and ctenophore trophic ecology to large-scale research , 2008, Hydrobiologia.

[19]  R. Shine The Evolution of Large Body Size in Females: A Critique of Darwin's "Fecundity Advantage" Model , 1988, The American Naturalist.

[20]  A. Collins Phylogeny of Medusozoa and the evolution of cnidarian life cycles , 2002 .

[21]  S. Holst Effects of climate warming on strobilation and ephyra production of North Sea scyphozoan jellyfish , 2012, Hydrobiologia.

[22]  R. Peters,et al.  Relationships between body size and some life history parameters , 2004, Oecologia.

[23]  K. Pitt,et al.  What's in a jellyfish? Proximate and elemental composition and biometric relationships for use in biogeochemical studies , 2011 .

[24]  R. Stocker,et al.  Filtration of submicrometer particles by pelagic tunicates , 2010, Proceedings of the National Academy of Sciences.

[25]  U. Båmstedt,et al.  Development and biology of Periphyllaperiphylla (Scyphozoa: Coronatae) in a Norwegian fjord , 2002 .

[26]  H. U. Riisgård,et al.  Feeding, bioenergetics and growth in the common jellyfish Aurelia aurita and two hydromedusae, Sarsia tubulosa and Aequorea vitrina , 2007 .

[27]  Hiroshi Miyake,et al.  On the Polyps of the Common Jellyfish Aurelia aurita in Kagoshima Bay , 2002 .

[28]  J. Ruiz,et al.  Environmental Control of Phase Transition and Polyp Survival of a Massive-Outbreaker Jellyfish , 2010, PloS one.

[29]  E. R. Llodra Fecundity and life-history strategies in marine invertebrates. , 2002 .

[30]  Anthony J Richardson,et al.  The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. , 2009, Trends in ecology & evolution.

[31]  S. Colin,et al.  Faking Giants: The Evolution of High Prey Clearance Rates in Jellyfishes , 2011, Science.

[32]  R. R. Strathmann Why Life Histories Evolve Differently in the Sea , 1990 .

[33]  Peter Delves,et al.  Encyclopedia of life sciences , 2009 .

[34]  M. Dawson,et al.  Evolutionary relationships among scyphozoan jellyfish families based on complete taxon sampling and phylogenetic analyses of 18S and 28S ribosomal DNA. , 2010, Integrative and comparative biology.

[35]  D. Breitburg,et al.  Effects of low dissolved oxygen on zooplankton predation by the ctenophore Mnemiopsis leidyi , 2004 .

[36]  M. Frischer,et al.  Seasonal patterns in size and abundance of Phyllorhiza punctata: an invasive scyphomedusa in coastal Georgia (USA) , 2011 .

[37]  Q. Bone Gelatinous animals and physiology , 2005, Journal of the Marine Biological Association of the United Kingdom.

[38]  J. Jackson,et al.  Ecological extinction and evolution in the brave new ocean , 2008, Proceedings of the National Academy of Sciences.

[39]  M. Dawson,et al.  Molecular Evidence for Cryptic Species of Aurelia aurita (Cnidaria, Scyphozoa) , 2001, The Biological Bulletin.

[40]  W. Hamner,et al.  Collection and Culture Techniques for Gelatinous Zooplankton , 2003, The Biological Bulletin.

[41]  L. Madin,et al.  Elemental and biochemical composition of salps (Tunicata: Thaliacea) , 1981 .

[42]  L. P. Schultz,et al.  Further Observations on the Biology of the Sea Nettle and Jellyfishes in Chesapeake Bay , 1967 .

[43]  A. Collins,et al.  A New Deepwater Species of Stauromedusae, Lucernaria janetae (Cnidaria, Staurozoa, Lucernariidae), and a Preliminary Investigation of Stauromedusan Phylogeny Based on Nuclear and Mitochondrial rDNA Data , 2005, The Biological Bulletin.

[44]  M. Byrne,et al.  A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms , 2009 .

[45]  M. Dawson,et al.  Five new subspecies of Mastigias (Scyphozoa: Rhizostomeae: Mastigiidae) from marine lakes, Palau, Micronesia , 2005, Journal of the Marine Biological Association of the United Kingdom.

[46]  G. Paffenhöfer,et al.  SHORT COMMUNICATION Determination of generation time and asexual fecundity of doliolids (Tunicata, Thaliacea) , 1999 .

[47]  J. Purcell,et al.  Diel patterns of migration, feeding, and spawning by salps in the subarctic Pacific , 1991 .

[48]  Jellyfish swarms, tourists, and the Christ-child , 2001 .

[49]  Gonzalo Giribet,et al.  Higher-level metazoan relationships: recent progress and remaining questions , 2011, Organisms Diversity & Evolution.

[50]  R. Hopcroft,et al.  Zooplankton growth rates : extraordinary production by the larvacean Oikopleura dioica in tropical waters , 1995 .

[51]  K. Bailey,et al.  Laboratory study of predation by Aurelia aurita on larvae of cod, flounder, plaice and herring: development and vulnerability to capture , 1984 .

[52]  P. Kremer,et al.  Growth dynamics of a ctenophore ( Mnemiopsis ) in relation to variable food supply. I. Carbon biomass, feeding, egg production, growth and assimilation efficiency , 1989 .

[53]  Q. Bone,et al.  Tunicate feeding filters , 2003, Journal of the Marine Biological Association of the United Kingdom.

[54]  S. Strand,et al.  Sun-compass migration by Aurelia aurita (Scyphozoa): population retention and reproduction in Saanich Inlet, British Columbia , 1994 .

[55]  Q. Bone The biology of pelagic Tunicates , 1998 .

[56]  M. Dawson,et al.  A character-based analysis of the evolution of jellyfish blooms: adaptation and exaptation , 2008, Hydrobiologia.

[57]  M. Vellend,et al.  Connections between species diversity and genetic diversity , 2005 .

[58]  Y. Loya,et al.  Life cycle ofRhopilema nomadica: a new immigrant scyphomedusan in the Mediterranean , 1992 .

[59]  L. P. Schultz,et al.  Notes on the biology of the sea nettle, Chrysaora quinquecirrha , in Chesapeake Bay , 1966 .

[60]  J. Purcell,et al.  Interactions of pelagic cnidarians and ctenophores with fish: a review , 2001 .

[61]  W. Gardner,et al.  Lipid and lipid class content of the pelagic tunicate Oikopleura vanhoeffeni , 1992 .

[62]  I. Stöger,et al.  On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia , 2010, BMC Evolutionary Biology.

[63]  M. Dawson,et al.  New Family of Allomorphic Jellyfishes, Drymonematidae (Scyphozoa, Discomedusae), Emphasizes Evolution in the Functional Morphology and Trophic Ecology of Gelatinous Zooplankton , 2010, The Biological Bulletin.

[64]  E. V. Thuesen,et al.  Metabolic performance and survival of medusae in estuarine hypoxia , 2005 .

[65]  R. Miller,et al.  Not all ctenophores are hermaphrodites. Studies on the systematics, distribution, sexuality and development of two species of Ocyropsis , 1986 .

[66]  C. Hubbs,et al.  The elementary chemical composition of marine organisms , 1955 .

[67]  Claudia E. Mills,et al.  Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change , 1999 .

[68]  M. Dawson,et al.  Questioning the Rise of Gelatinous Zooplankton in the World's Oceans , 2012 .

[69]  L. Madin,et al.  A molecular phylogeny of the Thaliacea , 2011 .

[70]  C. Duarte,et al.  Jellyfish Body Plans Provide Allometric Advantages beyond Low Carbon Content , 2013, PloS one.

[71]  Daniel Pauly,et al.  Increasing jellyfish populations: trends in Large Marine Ecosystems , 2012, Hydrobiologia.

[72]  W. Ponder,et al.  Molecular phylogenetics of Caenogastropoda (Gastropoda: Mollusca). , 2007, Molecular phylogenetics and evolution.

[73]  J. Gerritsen,et al.  Encounter Probabilities and Community Structure in Zooplankton: a Mathematical Model , 1977 .

[74]  S. Uye,et al.  Unusual population explosion of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) in East Asian waters , 2006 .

[75]  T. Dobzhansky Nothing in Biology Makes Sense Except in the Light of Evolution , 1973 .

[76]  Claudia E. Mills,et al.  Medusae, siphonophores, and ctenophores as planktivorous predators in changing global ecosystems , 1995 .

[77]  H. Ishii,et al.  Seasonal and vertical distribution of Aurelia aurita polyps on a pylon in the innermost part of Tokyo Bay , 2010 .

[78]  G. Paffenhöfer,et al.  Predictability of patches of neritic salps and doliolids (Tunicata, Thaliacea) , 2009 .

[79]  M. Ghiselin The Evolution of Hermaphroditism Among Animals , 1969, The Quarterly Review of Biology.

[80]  B. Schierwater,et al.  Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. , 2006, Systematic biology.

[81]  W. Graham,et al.  Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. , 2012, Advances in marine biology.

[82]  W. Hamner,et al.  The importance of ethology for investigations of marine zooplankton , 1985 .

[83]  D. Justić,et al.  Enigmatic changes in the hydromedusan fauna of the northern Adriatic Sea , 1987, Nature.

[84]  C. Lucas,et al.  Sexual reproduction of the scyphomedusa Aurelia aurita in relation to temperature and variable food supply , 1998 .

[85]  D. Breitburg,et al.  VARYING EFFECTS OF LOW DISSOLVED OXYGEN ON TROPHIC INTERACTIONS IN AN ESTUARINE FOOD WEB , 1997 .

[86]  J. Purcell Climate effects on formation of jellyfish and ctenophore blooms: a review , 2005, Journal of the Marine Biological Association of the United Kingdom.

[87]  M. Martindale Larval reproduction in the ctenophore Mnemiopsis mccradyi (order Lobata) , 1987 .

[88]  William M. Hamner,et al.  A physical context for gelatinous zooplankton aggregations: a review , 2001 .

[89]  T. Kiørboe,et al.  Effects of large gut volume in gelatinous zooplankton: ingestion rate, bolus production and food patch utilization by the jellyfish Sarsia tubulosa , 2006 .

[90]  A. Dinapoli,et al.  From sea to land and beyond – New insights into the evolution of euthyneuran Gastropoda (Mollusca) , 2008, BMC Evolutionary Biology.

[91]  L. Madin,et al.  Zooplankton feeding ecology: clearance and ingestion rates of the salps Thalia democratica, Cyclosalpa affinis and Salpa cylindrica on naturally occurring particles in the Mid-Atlantic Bight , 2004 .

[92]  B. Monger,et al.  Foraging Behavior and Prey Selection by the Ambush Entangling Predator Pleurobrachia Bachei , 1986 .

[93]  S. Uye,et al.  Bloom or non-bloom in the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae): roles of dormant podocysts , 2013 .

[94]  J. Pechenik On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles , 1999 .

[95]  A. C. Marques,et al.  Do Staurozoa bloom? A review of stauromedusan population biology , 2012, Hydrobiologia.

[96]  J. Hagadorn,et al.  The fossil record of cnidarian medusae , 2010 .

[97]  L. C. Cole The Population Consequences of Life History Phenomena , 1954, The Quarterly Review of Biology.

[98]  Daniel A. Brazeau,et al.  Self-fertilization in brooding hermaphroditic Caribbean corals: Evidence from molecular markers , 1998 .

[99]  J. Santora,et al.  Population dynamics of Salpa thompsoni near the Antarctic Peninsula: Growth rates and interannual variations in reproductive activity (1993–2009) , 2012 .

[100]  Temperature effects on asexual reproduction rates of scyphozoan species from the northwest Mediterranean Sea , 2012, Hydrobiologia.

[101]  S. Holst,et al.  Life cycle of the rhizostome jellyfish Rhizostoma octopus (L.) (Scyphozoa, Rhizostomeae), with studies on cnidocysts and statoliths , 2007 .

[102]  J. Purcell Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata and Aequorea aequorea, in Prince William Sound, Alaska , 2003 .

[103]  J. Purcell Environmental effects on asexual reproduction rates of the scyphozoan Aurelia labiata , 2007 .

[104]  H. Mianzan,et al.  Life cycle of the jellyfish Lychnorhiza lucerna (Scyphozoa: Rhizostomeae) , 2008 .

[105]  T. Smayda,et al.  Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea , 1997 .

[106]  M. Dawson,et al.  A review and synthesis on the systematics and evolution of jellyfish blooms: advantageous aggregations and adaptive assemblages , 2008, Hydrobiologia.

[107]  D. L. Aksnes,et al.  Predation efficiency in visual and tactile zooplanktivores , 2004 .

[108]  L. Baker,et al.  Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity , 1974 .

[109]  J. Roughgarden Is there a general theory of community ecology? , 2009 .

[110]  Effects of low dissolved oxygen on survival and asexual reproduction of scyphozoan polyps (Chrysaora quinquecirrha) , 2001 .

[111]  J. Purcell Pelagic cnidarians and ctenophores as predators: Selective predation, feeding rates, and effects on prey populations , 1997 .

[112]  Kung-Sik Chan,et al.  Ecological Effects of Climate Fluctuations , 2002, Science.

[113]  P. Kremer,et al.  Growth dynamics of a ctenophore ( Mnemiopsis ) in relation to variable food supply. II. Carbon budgets and growth model , 1989 .

[114]  Geir Ottersen,et al.  Covariability in early growth and year-class strength of Barents Sea cod, haddock, and herring: the environmental link , 2000 .

[115]  E. V. Thuesen,et al.  Intragel oxygen promotes hypoxia tolerance of scyphomedusae , 2005, Journal of Experimental Biology.

[116]  L. Madin,et al.  A comparison of filtration rates among pelagic tunicates using kinematic measurements , 2010 .

[117]  M. Sogin,et al.  A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. , 2001, Molecular phylogenetics and evolution.

[118]  G. Hays,et al.  Identification of genetically and oceanographically distinct blooms of jellyfish , 2013, Journal of The Royal Society Interface.

[119]  H. González,et al.  Gelatinous zooplankton assemblages associated with water masses in the Humboldt Current System, and potential predatory impact by Bassia bassensis (Siphonophora: Calycophorae) , 2001 .

[120]  S. Uye,et al.  Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. , 2010 .

[121]  J. Miller,et al.  Swimming sea cucumbers (Echinodermata, Holothuroidea) : a survey, with analysis of swimming behavior in four bathyal species , 1990 .

[122]  J. Costello,et al.  Flow and feeding by swimming scyphomedusae , 1995 .

[123]  K. Myrberg,et al.  Spreading and physico-biological reproduction limitations of the invasive American comb jelly Mnemiopsis leidyi in the Baltic Sea , 2011, Biological Invasions.

[124]  C. Cunningham,et al.  Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria) , 2005 .

[125]  Steven D. Gaines,et al.  Marine community ecology , 2001 .

[126]  Claudia E. Mills,et al.  Pacific Coast Pelagic Invertebrates: A Guide to the Common Gelatinous Animals , 1998 .

[127]  R. Pamplona,et al.  Life and death: metabolic rate, membrane composition, and life span of animals. , 2007, Physiological reviews.

[128]  Mark Vellend,et al.  Conceptual Synthesis in Community Ecology , 2010, The Quarterly Review of Biology.

[129]  K. Pitt,et al.  Temporal and spatial variation in recruitment and growth of medusae of the jellyfish, Catostylus mosaicus (Scyphozoa : Rhizostomeae) , 2003 .

[130]  Simon P. Wilson,et al.  The Magnitude of Global Marine Species Diversity , 2012, Current Biology.

[131]  L. Madin,et al.  Pelagic Tunicates: Unique Herbivores in the Marine Plankton , 1982 .

[132]  P. Tiselius,et al.  Bioenergetics and growth in the ctenophore Pleurobrachia pileus , 2010, Hydrobiologia.

[133]  Richard L. Miller,et al.  Evidence of dioecy in the mesopelagic ctenophore Bathocyroe fosteri (Lobata Ctenophora) , 2000 .

[134]  H. Ishii,et al.  Development time of planula larvae on the oral arms of the scyphomedusa Aurelia aurita , 2003 .

[135]  M. Walter,et al.  Nutritional Ecology of Ctenophores—A Review of Recent Research , 1979 .

[136]  G. Paffenhöfer,et al.  Asexual reproduction of the doliolid, Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea) , 2002 .

[137]  Geographic variation and ecological adaptation in Aurelia (Scyphozoa, Semaeostomeae): some implications from molecular phylogenetics , 2001 .

[138]  G. Paffenhöfer,et al.  From one to many: on the life cycle of Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea) , 2011 .

[139]  E. Houde,et al.  The ctenophore Mnemiopsis in native and exotic habitats: U.S. estuaries versus the Black Sea basin , 2001, Hydrobiologia.

[140]  J. Tomlinson,et al.  The advantages of hermaphroditism and parthenogenesis. , 1966, Journal of theoretical biology.

[141]  J. Hauxwell,et al.  Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences , 1997 .

[142]  R. Larson Water content, organic content, and carbon and nitrogen composition of medusae from the northeast Pacific☆ , 1986 .

[143]  G. Schneider A comparison of carbon-specific respiration rates in gelatinous and non-gelatinous zooplankton: A search for general rules in zooplankton metabolism , 1992, Helgoländer Meeresuntersuchungen.

[144]  D. Deibel Laboratory determined mortality, fecundity and growth rates of Thalia democratica Forskal and Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea) , 1982 .

[145]  M. Arai The potential importance of podocysts to the formation of scyphozoan blooms: a review , 2008, Hydrobiologia.

[146]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[147]  T DOBZHANSKY,et al.  BIOLOGY, MOLECULAR AND ORGANISMIC. , 1964, American zoologist.

[148]  A. Heron Population ecology of a colonizing species: The pelagic tunicate Thalia democratica , 1972, Oecologia.

[149]  W. M. Hammer Underwater observations of blue‐water plankton: Logistics, techniques, and safety procedures for divers at sea1 , 1975 .

[150]  J. Acuña Pelagic Tunicates: Why Gelatinous? , 2001, The American Naturalist.

[151]  Andrew C. Heron,et al.  Life history parameters as indicators of growth rate in three salp populations , 1985 .

[152]  R. W. Gilmer,et al.  Underwater observations of gelatinous zooplankton : Sampling problems, feeding biology, and behavior1 , 1975 .

[153]  A. Zavolokin Distribution and abundance dynamics of jellyfish in the Sea of Okhotsk , 2010, Russian Journal of Marine Biology.

[154]  Takeshi Kobayashi,et al.  Effects of low dissolved oxygen on planula settlement, polyp growth and asexual reproduction of Aurelia aurita , 2008 .

[155]  J. Hagadorn,et al.  Stranded on a Late Cambrian shoreline: Medusae from central Wisconsin , 2002 .

[156]  A golden age of gelata: past and future research on planktonic ctenophores and cnidarians , 2004 .

[157]  K. Pitt,et al.  Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production , 2008, Hydrobiologia.

[158]  Angela Dinapoli,et al.  Systematic position of the pelagic Thecosomata and Gymnosomata within Opisthobranchia (Mollusca, Gastropoda) – revival of the Pteropoda , 2006 .

[159]  G. Paffenhöfer,et al.  Feeding and growth rates of the doliolid, Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea) , 2000 .

[160]  M. Machain-Castillo,et al.  Benthic foraminifera in oxygen-poor habitats , 1993 .

[161]  S. Stearns Life history evolution: successes, limitations, and prospects , 2000, Naturwissenschaften.

[162]  D. L. Aksnes,et al.  Resource allocation between somatic growth and reproductive output in the pelagic chordate Oikopleura dioica allows opportunistic response to nutritional variation , 2002 .

[163]  D. Cushing The gadoid outburst in the North Sea , 1984 .