Figure 1.
Map showing spawning areas for bluefin tuna species throughout the world, as estimated from ichthyoplankton surveys and gondal development of adults.
Atlantic bluefin tuna T. thynnus: 1) Black Sea, 2) Levantin Sea, 3) Sicily Channel, 4) Tyrrhenian Sea, 5) Balearic sea, 6) Gulf of Mexico; southern bluefin tuna T. maccoyii: 7) northern Australia - Indonesia; Pacific bluefin tuna T. orientalis: 8) Japan Sea. Latitude and longitude coordinates for each area are available in Table 1.
Table 1.
Spawning times and areas for bluefin tuna species, T. thynnus, T. orientalis and T. macoyii, compiled from literature.
Table 2.
Summary of ichthyoplankton studies which have sampled bluefin tuna eggs in the Black Sea (no egg concentrations were given in the studies).
Figure 2.
Long-term averaged vertical profiles of density, salinity, temperature and oxygen concentration in bluefin tuna spawning habitats (Black Sea, Levantine Sea, south of Sicily, southern Tyrrhenian Sea, south of Balearic Islands, Gulf of Mexico, Japan, northern Australia - Indonesia) during peak spawning periods (Table 1) in different regions.
Data source [31]. Each line is a statistical fit to 100s of data points using General Additive Models (Table S2). See all observed data with GAM fits and 95% confidence intervals in site-specific vertical profiles for each variable in Supporting Information (Figures S3, S4, S5, S6).
Figure 3.
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 and lab-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].
Figure 4.
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.
Figure 5.
Analytical solution of the distribution of sinking bluefin tuna eggs in the Black Sea over time (0–48h).
Particles have been released at time t0 and depth z0 = 5 m with an initial concentration C0 and terminal velocity W = 1 mm s−1, corresponding to egg density = 1019 kg m−3.
Figure 6.
Simulated vertical distribution of bluefin tuna eggs at different times and specific gravities under modest wind-induced mixing.
Panels from top to bottom represent simulations for egg densities ρS = 1019, 1017 and 1015.7 kg m−3. Particle concentration calculated from the average number of particles passing the numerical box of 1 m side between two time steps (dt = 60 seconds).
Figure 7.
Time after which no bluefin tuna eggs remain in the upper 10 m of the numerical domain vs. egg density.
For densities ρS ≤1012 kg m−3 some eggs can remain within the upper 10 m during 48 h, even under modest wind-induced mixing. The proportion of eggs remaining is linearly scaled to symbol size for the black circles; white circles indicate 0% of eggs remaining in upper 10 m. Solid and dashed lines represent simulations assuming long-term mean and mean +1 SD of density profile as estimated by GAM of World Ocean Atlas data. The solid and dashed lines for densities ρS ≤1012 kg m−3 are shown plotted at 48−2 and 48+2 hours for clarity. Horizontal bars below figure indicate ranges of measured buoyancies of fish eggs in the Black Sea [20] and for bluefin tuna eggs in the Mediterranean Sea and near Japan.