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Spawning of bluefin tuna in the Black Sea: historical evidence, environmental constraints and population plasticity.

MacKenzie BR, Mariani P - PLoS ONE (2012)

Bottom Line: Here we identify the main genetic and phenotypic adaptations that the population must have (had) in order to reproduce successfully in the specific hydrographic (estuarine) conditions of the Black Sea.We conclude that these adaptations would have been necessary for successful local reproduction by bluefin tuna in the Black Sea, and that a locally-adapted reproducing population may have disappeared.Recovery of bluefin tuna in the Black Sea, either for spawning or foraging, will occur fastest if any remaining locally adapted individuals are allowed to survive, and by conservation and recovery of depleted Mediterranean populations which could through time re-establish local Black Sea spawning and foraging.

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Affiliation: Center for Macroecology, Evolution and Climate, National Institute for Aquatic Resources (DTU Aqua), Technical University of Denmark, Charlottenlund, Denmark. brm@aqua.dtu.dk

ABSTRACT
The lucrative and highly migratory Atlantic bluefin tuna, Thunnus thynnus (Linnaeus 1758; Scombridae), used to be distributed widely throughout the north Atlantic Ocean, Mediterranean Sea and Black Sea. Its migrations have supported sustainable fisheries and impacted local cultures since antiquity, but its biogeographic range has contracted since the 1950s. Most recently, the species disappeared from the Black Sea in the late 1980s and has not yet recovered. Reasons for the Black Sea disappearance, and the species-wide range contraction, are unclear. However bluefin tuna formerly foraged and possibly spawned in the Black Sea. Loss of a locally-reproducing population would represent a decline in population richness, and an increase in species vulnerability to perturbations such as exploitation and environmental change. Here we identify the main genetic and phenotypic adaptations that the population must have (had) in order to reproduce successfully in the specific hydrographic (estuarine) conditions of the Black Sea. By comparing hydrographic conditions in spawning areas of the three species of bluefin tunas, and applying a mechanistic model of egg buoyancy and sinking rate, we show that reproduction in the Black Sea must have required specific adaptations of egg buoyancy, fertilisation and development for reproductive success. Such adaptations by local populations of marine fish species spawning in estuarine areas are common as is evident from a meta-analysis of egg buoyancy data from 16 species of fish. We conclude that these adaptations would have been necessary for successful local reproduction by bluefin tuna in the Black Sea, and that a locally-adapted reproducing population may have disappeared. Recovery of bluefin tuna in the Black Sea, either for spawning or foraging, will occur fastest if any remaining locally adapted individuals are allowed to survive, and by conservation and recovery of depleted Mediterranean populations which could through time re-establish local Black Sea spawning and foraging.

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Seawater density of neutral buoyancy for populations of 16 marine fish species inhabiting habitats with different salinities, compared with the natural local salinity at fertilisation or capture.Fish eggs for most populations and species were obtained by stripping eggs and fertilisation in the laboratory or onboard research vessels (denoted as lab-fertilised below) or were captured at sea in ichthyoplankton surveys (denoted as field-captured below). One study [44] involved capture of live eggs and transfer to different salinities for buoyancy measurements; numerical codes for these data are shown with a “T” in panels. Symbols represent different populations within following species: Cynoscion nebulosus, spotted seatrout (lab-fertilised) [69]: 1– Matagorda Bay, Texas; 2– Upper Laguna Madre, Texas; Enchelyopus cimbrius, fourbeard rockling (all eggs captured at sea): 1 =  Baltic Sea, Gotland Basin [104], 2 =  Baltic Sea, Kiel Bay (field-captured and transfered) [44], 3 =  Conception Bay, Newfoundland, Canada [105], 4 =  Placentia Bay, Newfoundland, Canada [106] with hydrographic data from [107], 5 =  Tracadie Bay offshore, Gulf of St. Lawrence, Canada [108]; Engraulis encrasicolus, anchovy, (all eggs captured at sea): 1– Bay of Biscay [109], [110]; 2– Black Sea [20], [111] with hydrographic data from [112], 3 - Gulf of Lyons [54]; 4– NW Africa-Morocco [113], 5– Po River plume, northern Adriatic Sea [114]; Gadus morhua, cod: 1– Arcto-Norwegian cod: Lofoten (lab-fertilised) [25]; 2 - eastern Baltic (lab-fertilised) [24], [26]; 3– Baltic Sea, Gotland Basin (lab-fertilised) [25], [26]); 4 and 4-T –Baltic Sea, Kiel Bay (field-captured and transferred) [44], 5– Baltic Sea, ICES SD 23 (lab-fertilised) [26], 6– Baltic Sea, ICES SD 24 (lab-fertilised) [26], 7– Baltic Sea ICES SD 25 (lab-fertilised) [26], 9– Baltic Sea, ICES SD 26 (field-captured) [104], 10– Conception Bay, Newfoundland, Canada (field-captured) [105], 11– Gulf of St. Lawrence, Canada (field-captured) [115], 12– Grand Banks, Newfoundland, Canada (field-fertilised) [116], 13– Gullmarenfjord, Kattegat, western Sweden (lab-fertilised) [26], 14 - inshore Newfoundland, Canada (lab-fertilised) [116], 15– Norwegian coastal cod (lab-fertilised) [23]; 16– Norwegian coastal cod, Helgeland, Norway (field-captured) [117], 17- Norwegian coastal cod, Øygården, Norway (field-captured) [117], 18 - Norwegian coastal cod, Porsanger, Norway (field-captured) [117]; 19– Norwegian coastal cod, Tysfjord, Norway (field-captured) [117], 20– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108]; Hippoglossoides platessoides, American plaice: 1– Conception Bay, Newfoundland, Canada (field-captured) [105], 2 - Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108], 3– Trinity Bay, Newfoundland, Canada (field-captured) [118]; Limanda limanda, dab: 1– Baltic Sea, Kiel Bay (field-captured and transferred) [44] and (lab-fertilised) [40], 2– Baltic Sea, ICES SD 23 (lab-fertilised) [43], 3 Baltic Sea, ICES SD 24 (lab-fertilised) [43]; 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5– Bergen, Norway (lab-fertilised) [40]; Platichthys flesus, flounder (all are lab-fertilised except eggs captured at sea at site 7): 1– Baltic Sea, ICES SD 23 [43], 2 - Baltic Sea, ICES SD 24 [22], [40], [43], 3 - Baltic Sea, ICES SD 25 [43], 4 - Baltic Sea, ICES SD 28 [43], 5– Baltic Sea, Tvärminne, Finland [22], [40], [45]; 6 -Bergen,Norway [22], [45]; 7 - Black Sea [20] with temperature data from [6]; Pleuronectes platessa, European plaice: 1–Baltic Sea, Kiel Bay (field-captured and transferred) [44], 2- Baltic Sea, ICES SD 24 (lab-fertilised) [22], [43]; 3 - Baltic Sea, ICES SD 24–25 (lab-fertilised) [43], 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5- Bergen, Norway (lab-fertilised) [22]; 6– North Sea, southern (field-captured) [119]; Pomatus saltatrix, bluefish (all are field-captured): 1– Black Sea [20], [66] with temperature data from [112], 2 =  NW Africa, Morocco [120]; Sarda sarda, bonito: 1– Black Sea (field-captured) [20], [121], 2 =  NW Africa-Morocco (field-captured) [113], 3 =  NW Mediterranean-Spain (lab-fertilised in land-based tanks) [38]; Sardina pilchardus, sardine (all are field-captured): 1– Bay of Biscay [109]; 2– NW Africa, Morocco [113]; 3 - Plymouth, UK [68]; Scomber scombrus, Atlantic mackerel: 1– Celtic Plateau (field captured andlab-fertilized) [53], 2– Conception Bay, Newfoundland, Canada (field captured) [105], 3 - St. George’s Bay, so. Gulf of St. Lawrence, Canada (field captured) [122], 4– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field captured) [108]; Sprattus sprattus, sprat: 1– Baltic Sea, Gotland Basin (field captured) [104], 2 - Baltic Sea, SD 25 (lab fertilised) [84], [92], 3 - Baltic Sea, ICES SD 25–28 [92], 4– Baltic Sea, SD 26 (field captured and lab fertilised) [92], [104], 5– Black Sea (field captured) [20], [67] with temperature data from [112], 6– Plymouth, UK (field captured) [68]; Thunnus thynnus, Atlantic bluefin tuna and Thunnus orientalis, Pacific bluefin tuna: 1 - unknown developmental stages of T. thynnus from the Black Sea caught in the upper 1 m of the water column [19], 2– northern Ionian Sea and Strait of Messina, Mediterranean Sea [63] (field-captured) 3 - unknown developmental stages of T. thynnus from the northwest Mediterranean (lab-fertilized) [38]; 1-ES and 1-LS – early and late-stages of T. orientalis eggs collected in in situ rearing cages in Japan [39]; Xiphias gladius, swordfish (all field captured): 1 - Black Sea [89], 2– Ionian Sea and Strait of Messina, Mediterranean Sea ([63], 2– Mediterranean Sea, 3 - so. Tyrrhenian Sea [123], 4– Mediterranean Sea, NW Aegean Sea [124], with hydrography data from [125].
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pone-0039998-g003: Seawater density of neutral buoyancy for populations of 16 marine fish species inhabiting habitats with different salinities, compared with the natural local salinity at fertilisation or capture.Fish eggs for most populations and species were obtained by stripping eggs and fertilisation in the laboratory or onboard research vessels (denoted as lab-fertilised below) or were captured at sea in ichthyoplankton surveys (denoted as field-captured below). One study [44] involved capture of live eggs and transfer to different salinities for buoyancy measurements; numerical codes for these data are shown with a “T” in panels. Symbols represent different populations within following species: Cynoscion nebulosus, spotted seatrout (lab-fertilised) [69]: 1– Matagorda Bay, Texas; 2– Upper Laguna Madre, Texas; Enchelyopus cimbrius, fourbeard rockling (all eggs captured at sea): 1 =  Baltic Sea, Gotland Basin [104], 2 =  Baltic Sea, Kiel Bay (field-captured and transfered) [44], 3 =  Conception Bay, Newfoundland, Canada [105], 4 =  Placentia Bay, Newfoundland, Canada [106] with hydrographic data from [107], 5 =  Tracadie Bay offshore, Gulf of St. Lawrence, Canada [108]; Engraulis encrasicolus, anchovy, (all eggs captured at sea): 1– Bay of Biscay [109], [110]; 2– Black Sea [20], [111] with hydrographic data from [112], 3 - Gulf of Lyons [54]; 4– NW Africa-Morocco [113], 5– Po River plume, northern Adriatic Sea [114]; Gadus morhua, cod: 1– Arcto-Norwegian cod: Lofoten (lab-fertilised) [25]; 2 - eastern Baltic (lab-fertilised) [24], [26]; 3– Baltic Sea, Gotland Basin (lab-fertilised) [25], [26]); 4 and 4-T –Baltic Sea, Kiel Bay (field-captured and transferred) [44], 5– Baltic Sea, ICES SD 23 (lab-fertilised) [26], 6– Baltic Sea, ICES SD 24 (lab-fertilised) [26], 7– Baltic Sea ICES SD 25 (lab-fertilised) [26], 9– Baltic Sea, ICES SD 26 (field-captured) [104], 10– Conception Bay, Newfoundland, Canada (field-captured) [105], 11– Gulf of St. Lawrence, Canada (field-captured) [115], 12– Grand Banks, Newfoundland, Canada (field-fertilised) [116], 13– Gullmarenfjord, Kattegat, western Sweden (lab-fertilised) [26], 14 - inshore Newfoundland, Canada (lab-fertilised) [116], 15– Norwegian coastal cod (lab-fertilised) [23]; 16– Norwegian coastal cod, Helgeland, Norway (field-captured) [117], 17- Norwegian coastal cod, Øygården, Norway (field-captured) [117], 18 - Norwegian coastal cod, Porsanger, Norway (field-captured) [117]; 19– Norwegian coastal cod, Tysfjord, Norway (field-captured) [117], 20– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108]; Hippoglossoides platessoides, American plaice: 1– Conception Bay, Newfoundland, Canada (field-captured) [105], 2 - Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108], 3– Trinity Bay, Newfoundland, Canada (field-captured) [118]; Limanda limanda, dab: 1– Baltic Sea, Kiel Bay (field-captured and transferred) [44] and (lab-fertilised) [40], 2– Baltic Sea, ICES SD 23 (lab-fertilised) [43], 3 Baltic Sea, ICES SD 24 (lab-fertilised) [43]; 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5– Bergen, Norway (lab-fertilised) [40]; Platichthys flesus, flounder (all are lab-fertilised except eggs captured at sea at site 7): 1– Baltic Sea, ICES SD 23 [43], 2 - Baltic Sea, ICES SD 24 [22], [40], [43], 3 - Baltic Sea, ICES SD 25 [43], 4 - Baltic Sea, ICES SD 28 [43], 5– Baltic Sea, Tvärminne, Finland [22], [40], [45]; 6 -Bergen,Norway [22], [45]; 7 - Black Sea [20] with temperature data from [6]; Pleuronectes platessa, European plaice: 1–Baltic Sea, Kiel Bay (field-captured and transferred) [44], 2- Baltic Sea, ICES SD 24 (lab-fertilised) [22], [43]; 3 - Baltic Sea, ICES SD 24–25 (lab-fertilised) [43], 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5- Bergen, Norway (lab-fertilised) [22]; 6– North Sea, southern (field-captured) [119]; Pomatus saltatrix, bluefish (all are field-captured): 1– Black Sea [20], [66] with temperature data from [112], 2 =  NW Africa, Morocco [120]; Sarda sarda, bonito: 1– Black Sea (field-captured) [20], [121], 2 =  NW Africa-Morocco (field-captured) [113], 3 =  NW Mediterranean-Spain (lab-fertilised in land-based tanks) [38]; Sardina pilchardus, sardine (all are field-captured): 1– Bay of Biscay [109]; 2– NW Africa, Morocco [113]; 3 - Plymouth, UK [68]; Scomber scombrus, Atlantic mackerel: 1– Celtic Plateau (field captured andlab-fertilized) [53], 2– Conception Bay, Newfoundland, Canada (field captured) [105], 3 - St. George’s Bay, so. Gulf of St. Lawrence, Canada (field captured) [122], 4– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field captured) [108]; Sprattus sprattus, sprat: 1– Baltic Sea, Gotland Basin (field captured) [104], 2 - Baltic Sea, SD 25 (lab fertilised) [84], [92], 3 - Baltic Sea, ICES SD 25–28 [92], 4– Baltic Sea, SD 26 (field captured and lab fertilised) [92], [104], 5– Black Sea (field captured) [20], [67] with temperature data from [112], 6– Plymouth, UK (field captured) [68]; Thunnus thynnus, Atlantic bluefin tuna and Thunnus orientalis, Pacific bluefin tuna: 1 - unknown developmental stages of T. thynnus from the Black Sea caught in the upper 1 m of the water column [19], 2– northern Ionian Sea and Strait of Messina, Mediterranean Sea [63] (field-captured) 3 - unknown developmental stages of T. thynnus from the northwest Mediterranean (lab-fertilized) [38]; 1-ES and 1-LS – early and late-stages of T. orientalis eggs collected in in situ rearing cages in Japan [39]; Xiphias gladius, swordfish (all field captured): 1 - Black Sea [89], 2– Ionian Sea and Strait of Messina, Mediterranean Sea ([63], 2– Mediterranean Sea, 3 - so. Tyrrhenian Sea [123], 4– Mediterranean Sea, NW Aegean Sea [124], with hydrography data from [125].

Mentions: The density of Atlantic bluefin tuna T. thunnus eggs (Figure 3, 4) spawned in captivity by adults from the northwest Mediterranean Sea is 1017 kg m−3[38]. The variability or range of the reported density was not reported, and no information about ontogenetic changes in egg density was presented, nor was the stage of development of the eggs used for density measurements stated. The reported density is at the lower limit of the range of density (1018–1020 kg m−3) measured for eggs of Pacific bluefin tuna T. orientalis in early stages of development [39], and produced by adult Mediterranean bluefin tuna fed artificial diets in a sea-ranching operation; as eggs approached hatching, density increased to 1020–1028 kg m−3. Densities of bluefin tuna eggs captured in the upper 25 m of the Ionian Sea, Mediterranean Sea [63] can be estimated to be 1026–1027 kg m−3 (Figure 3, 4).


Spawning of bluefin tuna in the Black Sea: historical evidence, environmental constraints and population plasticity.

MacKenzie BR, Mariani P - PLoS ONE (2012)

Seawater density of neutral buoyancy for populations of 16 marine fish species inhabiting habitats with different salinities, compared with the natural local salinity at fertilisation or capture.Fish eggs for most populations and species were obtained by stripping eggs and fertilisation in the laboratory or onboard research vessels (denoted as lab-fertilised below) or were captured at sea in ichthyoplankton surveys (denoted as field-captured below). One study [44] involved capture of live eggs and transfer to different salinities for buoyancy measurements; numerical codes for these data are shown with a “T” in panels. Symbols represent different populations within following species: Cynoscion nebulosus, spotted seatrout (lab-fertilised) [69]: 1– Matagorda Bay, Texas; 2– Upper Laguna Madre, Texas; Enchelyopus cimbrius, fourbeard rockling (all eggs captured at sea): 1 =  Baltic Sea, Gotland Basin [104], 2 =  Baltic Sea, Kiel Bay (field-captured and transfered) [44], 3 =  Conception Bay, Newfoundland, Canada [105], 4 =  Placentia Bay, Newfoundland, Canada [106] with hydrographic data from [107], 5 =  Tracadie Bay offshore, Gulf of St. Lawrence, Canada [108]; Engraulis encrasicolus, anchovy, (all eggs captured at sea): 1– Bay of Biscay [109], [110]; 2– Black Sea [20], [111] with hydrographic data from [112], 3 - Gulf of Lyons [54]; 4– NW Africa-Morocco [113], 5– Po River plume, northern Adriatic Sea [114]; Gadus morhua, cod: 1– Arcto-Norwegian cod: Lofoten (lab-fertilised) [25]; 2 - eastern Baltic (lab-fertilised) [24], [26]; 3– Baltic Sea, Gotland Basin (lab-fertilised) [25], [26]); 4 and 4-T –Baltic Sea, Kiel Bay (field-captured and transferred) [44], 5– Baltic Sea, ICES SD 23 (lab-fertilised) [26], 6– Baltic Sea, ICES SD 24 (lab-fertilised) [26], 7– Baltic Sea ICES SD 25 (lab-fertilised) [26], 9– Baltic Sea, ICES SD 26 (field-captured) [104], 10– Conception Bay, Newfoundland, Canada (field-captured) [105], 11– Gulf of St. Lawrence, Canada (field-captured) [115], 12– Grand Banks, Newfoundland, Canada (field-fertilised) [116], 13– Gullmarenfjord, Kattegat, western Sweden (lab-fertilised) [26], 14 - inshore Newfoundland, Canada (lab-fertilised) [116], 15– Norwegian coastal cod (lab-fertilised) [23]; 16– Norwegian coastal cod, Helgeland, Norway (field-captured) [117], 17- Norwegian coastal cod, Øygården, Norway (field-captured) [117], 18 - Norwegian coastal cod, Porsanger, Norway (field-captured) [117]; 19– Norwegian coastal cod, Tysfjord, Norway (field-captured) [117], 20– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108]; Hippoglossoides platessoides, American plaice: 1– Conception Bay, Newfoundland, Canada (field-captured) [105], 2 - Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108], 3– Trinity Bay, Newfoundland, Canada (field-captured) [118]; Limanda limanda, dab: 1– Baltic Sea, Kiel Bay (field-captured and transferred) [44] and (lab-fertilised) [40], 2– Baltic Sea, ICES SD 23 (lab-fertilised) [43], 3 Baltic Sea, ICES SD 24 (lab-fertilised) [43]; 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5– Bergen, Norway (lab-fertilised) [40]; Platichthys flesus, flounder (all are lab-fertilised except eggs captured at sea at site 7): 1– Baltic Sea, ICES SD 23 [43], 2 - Baltic Sea, ICES SD 24 [22], [40], [43], 3 - Baltic Sea, ICES SD 25 [43], 4 - Baltic Sea, ICES SD 28 [43], 5– Baltic Sea, Tvärminne, Finland [22], [40], [45]; 6 -Bergen,Norway [22], [45]; 7 - Black Sea [20] with temperature data from [6]; Pleuronectes platessa, European plaice: 1–Baltic Sea, Kiel Bay (field-captured and transferred) [44], 2- Baltic Sea, ICES SD 24 (lab-fertilised) [22], [43]; 3 - Baltic Sea, ICES SD 24–25 (lab-fertilised) [43], 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5- Bergen, Norway (lab-fertilised) [22]; 6– North Sea, southern (field-captured) [119]; Pomatus saltatrix, bluefish (all are field-captured): 1– Black Sea [20], [66] with temperature data from [112], 2 =  NW Africa, Morocco [120]; Sarda sarda, bonito: 1– Black Sea (field-captured) [20], [121], 2 =  NW Africa-Morocco (field-captured) [113], 3 =  NW Mediterranean-Spain (lab-fertilised in land-based tanks) [38]; Sardina pilchardus, sardine (all are field-captured): 1– Bay of Biscay [109]; 2– NW Africa, Morocco [113]; 3 - Plymouth, UK [68]; Scomber scombrus, Atlantic mackerel: 1– Celtic Plateau (field captured andlab-fertilized) [53], 2– Conception Bay, Newfoundland, Canada (field captured) [105], 3 - St. George’s Bay, so. Gulf of St. Lawrence, Canada (field captured) [122], 4– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field captured) [108]; Sprattus sprattus, sprat: 1– Baltic Sea, Gotland Basin (field captured) [104], 2 - Baltic Sea, SD 25 (lab fertilised) [84], [92], 3 - Baltic Sea, ICES SD 25–28 [92], 4– Baltic Sea, SD 26 (field captured and lab fertilised) [92], [104], 5– Black Sea (field captured) [20], [67] with temperature data from [112], 6– Plymouth, UK (field captured) [68]; Thunnus thynnus, Atlantic bluefin tuna and Thunnus orientalis, Pacific bluefin tuna: 1 - unknown developmental stages of T. thynnus from the Black Sea caught in the upper 1 m of the water column [19], 2– northern Ionian Sea and Strait of Messina, Mediterranean Sea [63] (field-captured) 3 - unknown developmental stages of T. thynnus from the northwest Mediterranean (lab-fertilized) [38]; 1-ES and 1-LS – early and late-stages of T. orientalis eggs collected in in situ rearing cages in Japan [39]; Xiphias gladius, swordfish (all field captured): 1 - Black Sea [89], 2– Ionian Sea and Strait of Messina, Mediterranean Sea ([63], 2– Mediterranean Sea, 3 - so. Tyrrhenian Sea [123], 4– Mediterranean Sea, NW Aegean Sea [124], with hydrography data from [125].
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3404090&req=5

pone-0039998-g003: Seawater density of neutral buoyancy for populations of 16 marine fish species inhabiting habitats with different salinities, compared with the natural local salinity at fertilisation or capture.Fish eggs for most populations and species were obtained by stripping eggs and fertilisation in the laboratory or onboard research vessels (denoted as lab-fertilised below) or were captured at sea in ichthyoplankton surveys (denoted as field-captured below). One study [44] involved capture of live eggs and transfer to different salinities for buoyancy measurements; numerical codes for these data are shown with a “T” in panels. Symbols represent different populations within following species: Cynoscion nebulosus, spotted seatrout (lab-fertilised) [69]: 1– Matagorda Bay, Texas; 2– Upper Laguna Madre, Texas; Enchelyopus cimbrius, fourbeard rockling (all eggs captured at sea): 1 =  Baltic Sea, Gotland Basin [104], 2 =  Baltic Sea, Kiel Bay (field-captured and transfered) [44], 3 =  Conception Bay, Newfoundland, Canada [105], 4 =  Placentia Bay, Newfoundland, Canada [106] with hydrographic data from [107], 5 =  Tracadie Bay offshore, Gulf of St. Lawrence, Canada [108]; Engraulis encrasicolus, anchovy, (all eggs captured at sea): 1– Bay of Biscay [109], [110]; 2– Black Sea [20], [111] with hydrographic data from [112], 3 - Gulf of Lyons [54]; 4– NW Africa-Morocco [113], 5– Po River plume, northern Adriatic Sea [114]; Gadus morhua, cod: 1– Arcto-Norwegian cod: Lofoten (lab-fertilised) [25]; 2 - eastern Baltic (lab-fertilised) [24], [26]; 3– Baltic Sea, Gotland Basin (lab-fertilised) [25], [26]); 4 and 4-T –Baltic Sea, Kiel Bay (field-captured and transferred) [44], 5– Baltic Sea, ICES SD 23 (lab-fertilised) [26], 6– Baltic Sea, ICES SD 24 (lab-fertilised) [26], 7– Baltic Sea ICES SD 25 (lab-fertilised) [26], 9– Baltic Sea, ICES SD 26 (field-captured) [104], 10– Conception Bay, Newfoundland, Canada (field-captured) [105], 11– Gulf of St. Lawrence, Canada (field-captured) [115], 12– Grand Banks, Newfoundland, Canada (field-fertilised) [116], 13– Gullmarenfjord, Kattegat, western Sweden (lab-fertilised) [26], 14 - inshore Newfoundland, Canada (lab-fertilised) [116], 15– Norwegian coastal cod (lab-fertilised) [23]; 16– Norwegian coastal cod, Helgeland, Norway (field-captured) [117], 17- Norwegian coastal cod, Øygården, Norway (field-captured) [117], 18 - Norwegian coastal cod, Porsanger, Norway (field-captured) [117]; 19– Norwegian coastal cod, Tysfjord, Norway (field-captured) [117], 20– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108]; Hippoglossoides platessoides, American plaice: 1– Conception Bay, Newfoundland, Canada (field-captured) [105], 2 - Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field-captured) [108], 3– Trinity Bay, Newfoundland, Canada (field-captured) [118]; Limanda limanda, dab: 1– Baltic Sea, Kiel Bay (field-captured and transferred) [44] and (lab-fertilised) [40], 2– Baltic Sea, ICES SD 23 (lab-fertilised) [43], 3 Baltic Sea, ICES SD 24 (lab-fertilised) [43]; 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5– Bergen, Norway (lab-fertilised) [40]; Platichthys flesus, flounder (all are lab-fertilised except eggs captured at sea at site 7): 1– Baltic Sea, ICES SD 23 [43], 2 - Baltic Sea, ICES SD 24 [22], [40], [43], 3 - Baltic Sea, ICES SD 25 [43], 4 - Baltic Sea, ICES SD 28 [43], 5– Baltic Sea, Tvärminne, Finland [22], [40], [45]; 6 -Bergen,Norway [22], [45]; 7 - Black Sea [20] with temperature data from [6]; Pleuronectes platessa, European plaice: 1–Baltic Sea, Kiel Bay (field-captured and transferred) [44], 2- Baltic Sea, ICES SD 24 (lab-fertilised) [22], [43]; 3 - Baltic Sea, ICES SD 24–25 (lab-fertilised) [43], 4 - Baltic Sea, ICES SD 25 (lab-fertilised) [43]; 5- Bergen, Norway (lab-fertilised) [22]; 6– North Sea, southern (field-captured) [119]; Pomatus saltatrix, bluefish (all are field-captured): 1– Black Sea [20], [66] with temperature data from [112], 2 =  NW Africa, Morocco [120]; Sarda sarda, bonito: 1– Black Sea (field-captured) [20], [121], 2 =  NW Africa-Morocco (field-captured) [113], 3 =  NW Mediterranean-Spain (lab-fertilised in land-based tanks) [38]; Sardina pilchardus, sardine (all are field-captured): 1– Bay of Biscay [109]; 2– NW Africa, Morocco [113]; 3 - Plymouth, UK [68]; Scomber scombrus, Atlantic mackerel: 1– Celtic Plateau (field captured andlab-fertilized) [53], 2– Conception Bay, Newfoundland, Canada (field captured) [105], 3 - St. George’s Bay, so. Gulf of St. Lawrence, Canada (field captured) [122], 4– Tracadie Bay offshore, Gulf of St. Lawrence, Canada (field captured) [108]; Sprattus sprattus, sprat: 1– Baltic Sea, Gotland Basin (field captured) [104], 2 - Baltic Sea, SD 25 (lab fertilised) [84], [92], 3 - Baltic Sea, ICES SD 25–28 [92], 4– Baltic Sea, SD 26 (field captured and lab fertilised) [92], [104], 5– Black Sea (field captured) [20], [67] with temperature data from [112], 6– Plymouth, UK (field captured) [68]; Thunnus thynnus, Atlantic bluefin tuna and Thunnus orientalis, Pacific bluefin tuna: 1 - unknown developmental stages of T. thynnus from the Black Sea caught in the upper 1 m of the water column [19], 2– northern Ionian Sea and Strait of Messina, Mediterranean Sea [63] (field-captured) 3 - unknown developmental stages of T. thynnus from the northwest Mediterranean (lab-fertilized) [38]; 1-ES and 1-LS – early and late-stages of T. orientalis eggs collected in in situ rearing cages in Japan [39]; Xiphias gladius, swordfish (all field captured): 1 - Black Sea [89], 2– Ionian Sea and Strait of Messina, Mediterranean Sea ([63], 2– Mediterranean Sea, 3 - so. Tyrrhenian Sea [123], 4– Mediterranean Sea, NW Aegean Sea [124], with hydrography data from [125].
Mentions: The density of Atlantic bluefin tuna T. thunnus eggs (Figure 3, 4) spawned in captivity by adults from the northwest Mediterranean Sea is 1017 kg m−3[38]. The variability or range of the reported density was not reported, and no information about ontogenetic changes in egg density was presented, nor was the stage of development of the eggs used for density measurements stated. The reported density is at the lower limit of the range of density (1018–1020 kg m−3) measured for eggs of Pacific bluefin tuna T. orientalis in early stages of development [39], and produced by adult Mediterranean bluefin tuna fed artificial diets in a sea-ranching operation; as eggs approached hatching, density increased to 1020–1028 kg m−3. Densities of bluefin tuna eggs captured in the upper 25 m of the Ionian Sea, Mediterranean Sea [63] can be estimated to be 1026–1027 kg m−3 (Figure 3, 4).

Bottom Line: Here we identify the main genetic and phenotypic adaptations that the population must have (had) in order to reproduce successfully in the specific hydrographic (estuarine) conditions of the Black Sea.We conclude that these adaptations would have been necessary for successful local reproduction by bluefin tuna in the Black Sea, and that a locally-adapted reproducing population may have disappeared.Recovery of bluefin tuna in the Black Sea, either for spawning or foraging, will occur fastest if any remaining locally adapted individuals are allowed to survive, and by conservation and recovery of depleted Mediterranean populations which could through time re-establish local Black Sea spawning and foraging.

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Affiliation: Center for Macroecology, Evolution and Climate, National Institute for Aquatic Resources (DTU Aqua), Technical University of Denmark, Charlottenlund, Denmark. brm@aqua.dtu.dk

ABSTRACT
The lucrative and highly migratory Atlantic bluefin tuna, Thunnus thynnus (Linnaeus 1758; Scombridae), used to be distributed widely throughout the north Atlantic Ocean, Mediterranean Sea and Black Sea. Its migrations have supported sustainable fisheries and impacted local cultures since antiquity, but its biogeographic range has contracted since the 1950s. Most recently, the species disappeared from the Black Sea in the late 1980s and has not yet recovered. Reasons for the Black Sea disappearance, and the species-wide range contraction, are unclear. However bluefin tuna formerly foraged and possibly spawned in the Black Sea. Loss of a locally-reproducing population would represent a decline in population richness, and an increase in species vulnerability to perturbations such as exploitation and environmental change. Here we identify the main genetic and phenotypic adaptations that the population must have (had) in order to reproduce successfully in the specific hydrographic (estuarine) conditions of the Black Sea. By comparing hydrographic conditions in spawning areas of the three species of bluefin tunas, and applying a mechanistic model of egg buoyancy and sinking rate, we show that reproduction in the Black Sea must have required specific adaptations of egg buoyancy, fertilisation and development for reproductive success. Such adaptations by local populations of marine fish species spawning in estuarine areas are common as is evident from a meta-analysis of egg buoyancy data from 16 species of fish. We conclude that these adaptations would have been necessary for successful local reproduction by bluefin tuna in the Black Sea, and that a locally-adapted reproducing population may have disappeared. Recovery of bluefin tuna in the Black Sea, either for spawning or foraging, will occur fastest if any remaining locally adapted individuals are allowed to survive, and by conservation and recovery of depleted Mediterranean populations which could through time re-establish local Black Sea spawning and foraging.

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