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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.

View Article: PubMed Central - PubMed

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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Top panel: Density of neutral buoyancy of eggs from 16 species of fish in relation to the salinity of water during gonadal maturation, egg fertilisation and egg incubation in local spawning areas. Solid line: linear regression model; dashed lines: 95% prediction limits. Regression statistics: y = 0.0009*x+1.0029; R2adj. = 0.87; P<0.0001; residual mean square error SDest  = 0.0026; N = 336. Species codes: 1 =  Cynoscion nebulosus spotted seatrout, 2 =  Enchelyopus cimbrius fourbeard rockling, 3 =  Engraulis encrasicolus European anchovy, 4 =  Gadus morhua cod, 5 =  Hippoglossoides platessoides American plaice, 6 =  Limanda limanda dab, 7 =  Platichthys flesus flounder, 8 =  Pleuronectes platessa European plaice, 9 =  Pomatus saltatrix bluefish, 10 =  Sarda sarda bonito, 11 =  Sardina pilchardus sardine, 12 =  Scomber scombrus Atlantic mackerel, 13 =  Sprattus sprattus sprat, 14 =  Thunnus orientalis Pacific bluefin tuna, 15 =  Thunnus thynnus Atlantic bluefin tuna, 16 =  Xiphias gladius swordfish. Bottom panel: same as top panel, except that salinities were atypical of those in local spawning areas because adults were transferred to nonlocal salinities for gonadal development, spawning and fertilisation, eggs were fertilised and/or incubated at nonlocal salinities, or eggs were captured at sea and then transferred to nonlocal salinities for buoyancy measurements. The relationship is not statistically significant (P = 0.14; N = 99). Species codes (N = 7) as above. Populations and data sources given in Figure 3 and Supplementary Table 1.
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pone-0039998-g004: Top panel: Density of neutral buoyancy of eggs from 16 species of fish in relation to the salinity of water during gonadal maturation, egg fertilisation and egg incubation in local spawning areas. Solid line: linear regression model; dashed lines: 95% prediction limits. Regression statistics: y = 0.0009*x+1.0029; R2adj. = 0.87; P<0.0001; residual mean square error SDest  = 0.0026; N = 336. Species codes: 1 =  Cynoscion nebulosus spotted seatrout, 2 =  Enchelyopus cimbrius fourbeard rockling, 3 =  Engraulis encrasicolus European anchovy, 4 =  Gadus morhua cod, 5 =  Hippoglossoides platessoides American plaice, 6 =  Limanda limanda dab, 7 =  Platichthys flesus flounder, 8 =  Pleuronectes platessa European plaice, 9 =  Pomatus saltatrix bluefish, 10 =  Sarda sarda bonito, 11 =  Sardina pilchardus sardine, 12 =  Scomber scombrus Atlantic mackerel, 13 =  Sprattus sprattus sprat, 14 =  Thunnus orientalis Pacific bluefin tuna, 15 =  Thunnus thynnus Atlantic bluefin tuna, 16 =  Xiphias gladius swordfish. Bottom panel: same as top panel, except that salinities were atypical of those in local spawning areas because adults were transferred to nonlocal salinities for gonadal development, spawning and fertilisation, eggs were fertilised and/or incubated at nonlocal salinities, or eggs were captured at sea and then transferred to nonlocal salinities for buoyancy measurements. The relationship is not statistically significant (P = 0.14; N = 99). Species codes (N = 7) as above. Populations and data sources given in Figure 3 and Supplementary Table 1.

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)

Top panel: Density of neutral buoyancy of eggs from 16 species of fish in relation to the salinity of water during gonadal maturation, egg fertilisation and egg incubation in local spawning areas. Solid line: linear regression model; dashed lines: 95% prediction limits. Regression statistics: y = 0.0009*x+1.0029; R2adj. = 0.87; P<0.0001; residual mean square error SDest  = 0.0026; N = 336. Species codes: 1 =  Cynoscion nebulosus spotted seatrout, 2 =  Enchelyopus cimbrius fourbeard rockling, 3 =  Engraulis encrasicolus European anchovy, 4 =  Gadus morhua cod, 5 =  Hippoglossoides platessoides American plaice, 6 =  Limanda limanda dab, 7 =  Platichthys flesus flounder, 8 =  Pleuronectes platessa European plaice, 9 =  Pomatus saltatrix bluefish, 10 =  Sarda sarda bonito, 11 =  Sardina pilchardus sardine, 12 =  Scomber scombrus Atlantic mackerel, 13 =  Sprattus sprattus sprat, 14 =  Thunnus orientalis Pacific bluefin tuna, 15 =  Thunnus thynnus Atlantic bluefin tuna, 16 =  Xiphias gladius swordfish. Bottom panel: same as top panel, except that salinities were atypical of those in local spawning areas because adults were transferred to nonlocal salinities for gonadal development, spawning and fertilisation, eggs were fertilised and/or incubated at nonlocal salinities, or eggs were captured at sea and then transferred to nonlocal salinities for buoyancy measurements. The relationship is not statistically significant (P = 0.14; N = 99). Species codes (N = 7) as above. Populations and data sources given in Figure 3 and Supplementary Table 1.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0039998-g004: Top panel: Density of neutral buoyancy of eggs from 16 species of fish in relation to the salinity of water during gonadal maturation, egg fertilisation and egg incubation in local spawning areas. Solid line: linear regression model; dashed lines: 95% prediction limits. Regression statistics: y = 0.0009*x+1.0029; R2adj. = 0.87; P<0.0001; residual mean square error SDest  = 0.0026; N = 336. Species codes: 1 =  Cynoscion nebulosus spotted seatrout, 2 =  Enchelyopus cimbrius fourbeard rockling, 3 =  Engraulis encrasicolus European anchovy, 4 =  Gadus morhua cod, 5 =  Hippoglossoides platessoides American plaice, 6 =  Limanda limanda dab, 7 =  Platichthys flesus flounder, 8 =  Pleuronectes platessa European plaice, 9 =  Pomatus saltatrix bluefish, 10 =  Sarda sarda bonito, 11 =  Sardina pilchardus sardine, 12 =  Scomber scombrus Atlantic mackerel, 13 =  Sprattus sprattus sprat, 14 =  Thunnus orientalis Pacific bluefin tuna, 15 =  Thunnus thynnus Atlantic bluefin tuna, 16 =  Xiphias gladius swordfish. Bottom panel: same as top panel, except that salinities were atypical of those in local spawning areas because adults were transferred to nonlocal salinities for gonadal development, spawning and fertilisation, eggs were fertilised and/or incubated at nonlocal salinities, or eggs were captured at sea and then transferred to nonlocal salinities for buoyancy measurements. The relationship is not statistically significant (P = 0.14; N = 99). Species codes (N = 7) as above. Populations and data sources given in Figure 3 and Supplementary Table 1.
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.

View Article: PubMed Central - PubMed

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.

Show MeSH
Related in: MedlinePlus