https://orcid.org/0000-0002-4555-6382
Figures
Abstract
Despite their broad distribution across the North Pacific Ocean, the only known spawning grounds for Pacific Bluefin Tuna (Thunnus orientalis) are around coastal Japan and the East China Sea. However, an increase in the prevalence of large bluefin tuna up to 10 years old in the California Current System during exceptionally warm ocean conditions has led to speculation that they may be spawning in this region. To investigate this possibility, we collected samples from 36 females (estimated 3–8 years old) between 2015 and 2019. Histological analyses revealed no signs of imminent, active, or recent spawning. Further examination of historical ichthyoplankton collections showed no records of larval bluefin tuna, but confirmed the presence of the larvae of other tuna species in waters > 24°C. Fishery-dependent records showed that bluefin tuna are rarely recorded in purse seine catches where surface temperatures exceed 23°C. Our study, therefore, provided no evidence of bluefin tuna reproduction in the CCS. However, more comprehensive sampling, in particular off southern Baja California, may be required to confirm the absence of spawning.
Citation: Dewar H, Snodgrass OE, Muhling BA, Schaefer KM (2022) Recent and historical data show no evidence of Pacific bluefin tuna reproduction in the southern California Current system. PLoS ONE 17(5): e0269069. https://doi.org/10.1371/journal.pone.0269069
Editor: Aldo Corriero, Universita degli Studi di Bari Aldo Moro, ITALY
Received: March 4, 2022; Accepted: May 13, 2022; Published: May 26, 2022
This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Data Availability: Non-confidential aggregated purse seine fishery data are freely available through the Inter-American Tropical Tuna Commission at https://www.iattc.org/CatchReportsDataENG.htm. CalCOFI larval survey data are freely available through ERDDAP at https://coastwatch.pfeg.noaa.gov/erddap/index.html. All histological classification data are available in the Supporting Information.
Funding: Funding for sample collection was provided by the NOAA Cooperative Research Program.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Bluefin tunas (family Scombridae) are broadly distributed in tropical and temperate waters with three species occurring globally: Atlantic bluefin (Thunnus thynnus), Southern bluefin (T. maccoyii) and Pacific bluefin (PBF, T. orientalis). Unlike the tropical tunas, bluefin tunas spawn in restricted geographic areas within defined spawning seasons [1, 2]. PBF are known to spawn only in the Sea of Japan, the East China Sea, and off the Pacific coast of Japan [3, 4], with most larvae are collected where sea surface temperatures (SST) are 24–28°C [5]. PBF spawning in the Sea of Japan are younger (3–8 years old), while spawners in the East China Sea are typically 8 years of age or older [6, 7]. The current stock assessment [8] considers that 100% of PBF are mature at age five.
A portion of juvenile PBF migrate to the California Current System (CCS) to forage in their first or second year, and typically remain for 2–3 years before returning to the western Pacific [9]. Consequently, PBF landed by CCS fisheries have historically been relatively young (1–3 years old). However, in the late 1970s many 4–6 year old PBF were caught using purse seines [10], and fish approximately 4–8 years old were landed by recreational fishers in 1994 [11]. Since 2014, larger PBF have again been reported in CCS fisheries, with some potentially as old as 10 [12].
Spawning of PBF has never been reported in the CCS. However, large PBF caught in recent years are similar sizes to western Pacific spawners [6, 7], leading to speculation that PBF may be maturing and spawning in the CCS. Other lines of evidence support the plausibility of this hypothesis. Firstly, new spawning grounds have recently been discovered for other bluefin tunas. Atlantic bluefin tuna spawning was thought to be restricted to the Gulf of Mexico and Mediterranean Sea, but larvae were recently collected in the northern Caribbean, Mid-Atlantic Bight, and Bay of Biscay [2, 13, 14]. In the North Pacific, PBF larvae were recently reported for the first time in the Kuroshio Current off eastern Japan [4]. Secondly, the CCS was anomalously warm during a marine heatwave in 2014–2016 [15] and SSTs stayed above average through 2019. This may have increased the thermal habitat suitable for PBF spawning and larval development. Lastly, fishers and spotter plane pilots reported behavior they considered consistent with spawning (e.g., large schools aggregating at the surface and unwilling to take bait) off southern California and northern Baja California. Previous studies have shown the high potential for at-sea observations from industry professionals and interested citizens to inform science and conservation (e.g. [16, 17]). PBF are intensively managed and currently overfished [8]. The discovery of additional spawning areas would have important implications for stock assessment, conservation, and management (e.g., [13]).
In this study, we combined historical data, fishery-dependent observations, and biological sampling to evaluate the potential for PBF spawning in the CCS. Our primary objective was to examine the gonads of large PBF for evidence of maturity and active spawning. In addition, we used multi-decadal ichthyoplankton collections to determine whether larval PBF may have been collected in the CCS previously. Lastly, we used satellite SST and fishery-dependent datasets to define overlap between PBF caught in purse seines and potentially suitable spawning habitat.
Materials and methods
We used biological knowledge of PBF and the two other bluefin tuna species (T. thynnus, T. orientalis) to define our study area. While most bluefin tuna larvae have been collected where SSTs exceed 24°C, [6] reported female PBF in spawning condition in the Sea of Japan where temperatures were as cool as 19.3°C, and [18] collected Atlantic bluefin tuna larvae in the Mediterranean Sea down to 20.5°C. We thus considered areas with SSTs > 20°C in the eastern North Pacific to be potential spawning habitat. Bluefin tuna spawning grounds are also distinct from those of other tunas in that they are concentrated in semi-enclosed seas and offshore continental shelf environments, rather than the open ocean [2]. Decades of ichthyoplankton surveys (e.g. [19–21]) have not recorded any bluefin tuna larvae more than 1,000 km from a major landmass, and so we restricted our study area to waters within approximately 1,000 km of the North American coast. Lastly, more than 60 years of purse seine and pelagic longline fisheries data collected by the Inter-American Tropical Tuna Commission (see below) have not recorded PBF of any size south of approximately 20°N within 1,000 km of land. The spatiotemporal coverage of sampling for gonads and for ichthyoplankton in relation to these constraints is shown in S1 Fig., and each aspect of sampling within the study area is described in more detail below.
Gonad sampling
We collaborated with local fishers and fish processors to collect heads and gonads from 36 female PBF caught during the recreational fishing season (May—November) from 2015 to 2019. Precise fish catch locations were not available, but we defined the spatial extent of the fleet using logbook data from the California Department of Fish and Wildlife (Fig 1). Fish fork length (FL) was estimated from operculum length using a published regression for the southern CCS [22], and estimated ages were generated based on the length-at-age equation provided in [7]. An approximately 1 cm section from the central portion of one of the gonads was sampled from each fish and preserved in 10% neutral buffered formalin. A small section of preserved ovarian tissue from each gonad sample was embedded in paraffin, sectioned at approximately 4μm, and stained with hematoxylin followed by eosin counterstain (Reveal Biosciences, San Diego, CA, USA).
(A) Collection area for Pacific bluefin tuna obtained from the Commercial Passenger Fishing Vessel fleet in 2015–2019 (blue), with U.S. and Mexico Exclusive Economic Zone boundaries also shown, (B) Length distribution of sampled fish, (C) ichthyoplankton sampling stations aggregated to 1 degree resolution from the CalCOFI and IMECOCAL sampling programs (1951–2020), (D) locations where presence of tuna larvae was recorded in either CalCOFI or IMECOCAL samples across all sampled years. “skj” = Katsuwonus pelamis, “thu” = Thunnus spp. larvae not identified further, “yft” = Thunnus albacares, “aux” = Auxis spp. larvae, “eut” = Euthynnus lineatus larvae.
The histological classification of the ovaries was based on [3, 23] and simplified to focus on distinguishing between spawning (e.g., spawning capable, actively spawning) and non-spawning females. Each ovary was assessed for the most advanced stage of oocytes: (1) unyolked (i.e., previtellogenic), (2) early yolked, (3) advanced yolked, (4) migratory-nucleus stage, or (5) hydrated. Ovaries were also examined for signs of atresia. Assignment of imminent, active, or prior spawning requires the presence of advanced yolked oocytes or atresia in yolked oocytes [3]. Females with ovaries containing only unyolked or early-yolked oocytes and with no signs of atresia were classified as inactive.
Ichthyoplankton
Ichthyoplankton data were sourced from the CalCOFI (1951–2020 via https://coastwatch.pfeg.noaa.gov/erddap/tabledap) and IMECOCAL (1997–2017) sampling programs [24, 25]: Fig 1. Occurrences of scombrid larvae from the Thunnini tribe (genera Auxis, Euthynnus, Katsuwonus, Thunnus) were considered to represent potentially suitable tuna spawning habitat. SSTs at sampling stations with and without tuna larvae were compared. Where no in situ surface or near-surface (shallower than 5m) temperature was available, we extracted SST from the 0.25 degree NOAA high-resolution blended daily analysis [26]. This resulted in 43,753 separate ichthyoplankton sampling stations with SST data available.
Fishery-dependent data
The distribution of PBF in the southern CCS was approximated using 1 degree aggregated purse-seine catch data collected by the Inter-American Tropical Tuna Commission. We used data from sets not associated with dolphins or floating objects, reported between 1982 and 2020. SST data were extracted at each 1x1 degree location for each year and month using the NOAA Optimum Interpolation monthly analysis. The presence of PBF in purse seine sets was then quantified with respect to both geography and SST.
Results
Sampled females ranged in length from 125 to 188 cm FL, and from 3–8 years old (Table 1, S1 Table). Histological analyses of the ovarian tissues revealed no evidence of imminent, active, or prior spawning. The ovaries of all 36 females contained only previtellogenic oocytes (e.g., oogonia, perinucleolar, cortical alveoli). Ovaries from two females (148 and 157 cm FL, both 5 years old) collected in July of 2015 contained a few cortical alveolar oocytes (Fig 2, S1 Table). No atresia was observed.
Note the two cortical alveolar oocytes indicated by the arrows. The black scale bar represents 100 μm.
Note that all data are included in S1 Table.
Ichthyoplankton sampling was most concentrated off southern California and Baja California but included stations throughout the CCS (Fig 1). Among the 43,753 stations sampled since 1951, 261 contained tuna larvae. Auxis spp. were the most abundant, and distributed the furthest north, with 2936 larvae collected from 233 stations. Of 86 Thunnus spp. larvae recorded, 26 were Yellowfin Tuna (T. albacares), and 60 were not identified past genus. Larval taxonomist notes from the times of collection show that these 60 larvae were either too small or in too poor a condition to identify to species. However, none resembled PBF larvae (which can usually be separated visually from other Thunnus spp. larvae using pigment patterns: [27]). All Thunnus larvae were collected south of 26°N (Fig 1). Twenty-one Black Skipjack (Euthynnus lineatus) larvae and 1 Skipjack tuna (Katsuwonus pelamis) larvae were collected south of 27°N.
Only 4 tuna larvae were recorded where SSTs were <20°C (Fig 3). Of 69 larvae collected at 20–24°C, 67 were Auxis spp. Thunnus spp. larvae were restricted to SSTs > 23.7°C. Conversely, PBF were mostly caught by purse seines when monthly SSTs at fishing locations were < 23°C (Fig 3). During 2015–2019, waters >24°C were located to the south of Baja California during winter and spring, with some warmer waters reaching the southern peninsula in summer and fall (Fig 4). Calculation of the maximum SST recorded in each pixel during 2015–2019 showed that some southern Baja waters were > 24°C during summer and fall. Despite recent heatwave conditions, the position of the 24°C isotherm was not markedly different in the southern CCS in 2015–2019 than in prior years (1982–2012) (Fig 4). Catches of PBF in purse seines were low off southern Baja California during these warmer seasons, consistent with their association with cooler SSTs (Fig 3). The overlap between PBF and Thunnus spp. larvae was thus minimal in both geographic and thermal space.
(A) Histograms of sea surface temperature at all CalCOFI and IMECOCAL stations without (left) and with (right) tuna larvae recorded. In situ SST was used if available, otherwise the NOAA high-resolution blended daily analysis was used instead. (B) Histograms of sea surface temperature at all 1x1 degree monthly purse seine fishing locations without (left) and with (right) PBF recorded. SST was extracted from the NOAA Optimum Interpolation Sea Surface Temperature monthly analysis.
The dark red line shows the position of the maximum 24°C isotherm for all months and years 2015–2019. The black line shows the position of the maximum 24°C isotherm for all months and years 1982–2012, for comparison. Mean PBF/set at aggregated 1x1 degree resolution for years 1982–2020 is also shown, to approximate the geographical distribution of PBF in the southern CCS. Black crosses indicate zero PBF catch.
Discussion
This study combined new biological collections with historical data to examine the potential for PBF spawning in the southern CCS. Based on histological evaluations of ovarian tissues, there was no evidence that female PBF sampled were actively spawning, or had previously spawned, in this region of the eastern Pacific. Two females had very few cortical alveolar oocytes present, suggesting they may have been in a very early “developing” phase towards sexual maturity [28]. However, it is unknown whether these animals may actually mature and spawn in the CCS or will resorb those oocytes and forego maturation until they migrate to the western Pacific. While we found no definitive evidence of recent or imminent spawning among sampled females, atresia and resorption of yolked oocytes and post-ovulatory follicles in tunas can occur over a period of a few days [29, 30]. Therefore, we cannot completely eliminate the possibility that some of the sampled females may have previously spawned.
Gonad sampling was spatially restricted due to our reliance on U.S. fisheries for samples. However, ichthyoplankton and fishery-dependent data covered both U.S. and Mexican waters across multiple decades. These data showed minimal geographic and thermal overlap between larval tuna habitat and PBF fishing habitat. Although purse seine data may be biased by seasonal fishing closures, they are consistent with previous tagging studies. Tagged PBF rarely moved south of Baja California, and did not occupy waters > 24°C in the CCS [9, 31]. Based on lengths reported at release and recapture, these tagged PBF were likely a mix of juvenile and adult fish (based on [6]). A more recent study during the 2014–2016 marine heatwave [32] recorded PBF where SSTs were as high as 24.5°C, but the majority of occurrences were still at < 23°C.
In contrast, Thunnus larvae were primarily associated with SSTs > 23–24°C, as has been reported for other regions [2]. In the CCS, these temperatures are largely restricted to southern Baja California during summer and fall. The 60 Thunnus spp. larvae not identified to species in ichthyoplankton collections are thus very unlikely to be PBF. In addition, conditions in the CCS are not typical of those on bluefin tuna spawning grounds. Spawning areas in the western North Pacific, Atlantic, and Indian Oceans are oligotrophic with warm SSTs [2, 5]. In addition, most spawning grounds are linked to juvenile foraging habitats via poleward boundary currents, which transport small juveniles to cooler, more productive waters at higher latitudes. For example, the Kuroshio Current transports juvenile PBF from the Nansei Islands towards coastal Japan, the Gulf Stream takes juveniles north to the Mid-Atlantic Bight [2], and the Leeuwin Current transports juveniles to southern Australia [1]. In contrast, the CCS is a productive upwelling boundary current, which flows equatorwards towards the subtropics.
If larger PBF in the CCS are not functionally mature and not spawning, then the reasons for their remaining in the eastern North Pacific are unclear. They may be exploiting optimal foraging habitat, and delaying their return to natal spawning grounds in the western Pacific. We note that plasticity in age at maturity of bluefin tuna is also seen in the North Atlantic. Some juvenile Atlantic Bluefin Tuna migrate from the Mediterranean Sea to western Atlantic foraging grounds, remaining there until they are up to 9 years old before returning to the Mediterranean to spawn [33]. In contrast, fish that remain in the Mediterranean can start spawning as early as 3 years old [34].
Although a “negative” result, we consider our findings important to report. Several new spawning grounds for Atlantic bluefin tuna were described only after exploration of poorly sampled regions [13, 14]. These studies suggest that spawning was not new to these areas but rather had gone unnoticed due to a lack of sampling. In addition, where limited historical samples did show Atlantic bluefin tuna larvae outside known spawning grounds [35], these were largely dismissed as advection events: a conclusion which now seems highly unlikely based on more recent analysis of drifter tracks [13]. The importance of re-visiting historical data and re-examining accepted paradigms on spawning distributions in species such as bluefin tunas should thus be apparent.
As climate change leads to further ocean warming, it will be essential to distinguish between environmentally-driven shifts in spawning areas, and discovery of existing spawning grounds through additional sampling. Although our sampling coverage was imperfect, and could be improved with additional samples from southern Baja California, a combination of multiple data streams suggest that PBF are not likely to be spawning in the CCS. The drivers and ecological consequences of the presence of larger, older PBF in the CCS in recent years thus require further investigation.
Supporting information
S1 Table. Pacific bluefin tuna metadata and results of the histological analyses of female gonads.
Atresia of yolked oocytes was not present in any female.
https://doi.org/10.1371/journal.pone.0269069.s001
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S1 Fig. Sampling effort within the study area.
Color scale shows mean monthly sea surface temperature for years 2015–2019 from the NOAA Optimum Interpolation monthly analysis. The blue contour represents 20°C (hypothesized lower limit for spawning activity), while the dark red represents 24°C (coolest temperature at which bluefin tuna larvae are usually collected). Black dots show ichthyoplankton sampling effort as total number of stations from the CalCOFI and IMECOCAL programs, 1951–2020. The blue polygon shows the area within which PBF gonads were obtained (sampling covered the months of May through November, 2015–2019). Areas more than 1,000 km from the nearest major landmass are masked in white. The subpanel labels denote month of the year.
https://doi.org/10.1371/journal.pone.0269069.s002
(TIF)
Acknowledgments
We thank K. Franke and the Sportfishing Association of California, S. Sebring from Fisherman’s Processing, and M. Medak and D. Card from Five Star Fish Processors for assistance with sample collections. E. Hellmers and P. Serpa at the California Department of Fish and Wildlife are thanked for provision of recreational fishing records using to define sampling areas. SST data were provided by the NOAA PSL, Boulder, Colorado via https://www.psl.noaa.gov/. We acknowledge the CalCOFI program for the provision of data through https://coastwatch.pfeg.noaa.gov/erddap/tabledap, and S. Jimenez-Rosenberg at the IMECOCAL-CONACyT program for making their data available for this study. We thank B. Erisman for his valuable comments and edits to the paper.
References
- 1.
Hobday AJ, Evans K, Eveson JP, Farley JH, Hartog JR, Basson M et al. Distribution and migration—southern bluefin tuna (Thunnus maccoyii). In Kitagawa T, Kimura S (eds) Biology and ecology of bluefin tuna. CRC Press, Boca Raton; 2015. pp. 189–210.
- 2. Muhling BA, Lamkin JT, Alemany F, García A, Farley J, Ingram GW et al. Reproduction and larval biology in tunas, and the importance of restricted area spawning grounds. Rev Fish Biol Fish 2017; 27: 697–732.
- 3.
Schaefer KM. Reproductive Biology of Tunas. In Block BA & Stevens ED (Eds.), Tuna Physiology, Ecology and Evolution, Academic, San Diego; 2001, pp. 225–270.
- 4. Tanaka Y, Tawa A, Ishihara T, Sawai E, Nakae M, Masujima M et al. Occurrence of Pacific bluefin tuna Thunnus orientalis larvae off the Pacific coast of Tohoku area, northeastern Japan: Possibility of the discovery of the third spawning ground. Fish Oceanogr 2020; 29: 46–51.
- 5. Ohshimo S, Tawa A, Ota T, Nishimoto S, Ishihara T, Watai M et al. Horizontal distribution and habitat of Pacific bluefin tuna, Thunnus orientalis, larvae in the waters around Japan. Bull Mar Sci 2017; 93: 769–787.
- 6. Okochi Y, Abe O, Tanaka S, Ishihara Y, Shimizu A. Reproductive biology of female Pacific bluefin tuna, Thunnus orientalis, in the Sea of Japan. Fish Res 2016; 174: 30–39.
- 7. Shimose T, Tanabe T, Chen KS, Hsu CC Age determination and growth of Pacific bluefin tuna, Thunnus orientalis, off Japan and Taiwan. Fish Res 2009; 100: 134–139.
- 8. ISC. Stock assessment of Pacific Bluefin tuna in the Pacific Ocean in 2020. ISC/20/ANNEX/11, July 2020.
- 9. Fujioka K, Fukuda H, Tei Y, Okamoto S, Kiyofuji H, Furukawa S et al. Spatial and temporal variability in the trans-Pacific migration of Pacific bluefin tuna (Thunnus orientalis) revealed by archival tags. Prog Oceanogr 2018; 162: 52–65.
- 10. Calkins TP. Observations on the purse-seine fishery for northern bluefin tuna (Thunnus thynnus) in the eastern Pacific Ocean. Bull I-ATCC 1982; 18: 121–225.
- 11. Bellquist L. A historical perspective of California recreational fisheries using a new database of "trophy" fish records (1966–2013), combined with fisheries analyses of three species in the genus Paralabrax. PhD Thesis, University of California, San Diego, CA, 2015.
- 12. James KC, Heberer LN, Lee H, Dewar H. Comparison of Length Sampling Programs for recreational fisheries of US Pacific Bluefin Tuna from 2014 to 2020. NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC-652 2021.
- 13. Richardson DE, Marancik KE, Guyon JR, Lutcavage ME, Galuardi B, Lam CH et al. Discovery of a spawning ground reveals diverse migration strategies in Atlantic bluefin tuna (Thunnus thynnus). Proc Natl Acad Sci USA 2016; 113: 3299–3304. pmid:26951668
- 14. Rodriguez JM, Johnstone C, Lozano‐Peral D. Evidence of Atlantic bluefin tuna spawning in the Bay of Biscay, NE Atlantic. J Fish Bio 2021; 99: 964–969.
- 15. Jacox MG, Tommasi D, Alexander MA, Hervieux G, Stock CA. Predicting the evolution of the 2014–2016 California Current System marine heatwave from an ensemble of coupled global climate forecasts. Front Mar Sci 2019; 6, 497.
- 16. Araujo G, Snow S, Lee So C, Labaja J, Murray R, Colucci A, et al. Population structure, residency patterns and movements of whale sharks in Southern Leyte, Philippines: results from dedicated photo‐ID and citizen science. Aquat Conserv 2017; 27: 237–252.
- 17. Mason JG, Alfaro‐Shigueto J, Mangel JC, Brodie S, Bograd SJ, Crowder LB, et al. Convergence of fishers’ knowledge with a species distribution model in a Peruvian shark fishery. Conserv Sci Pract 2019; 1: e13.
- 18. Alemany F, Quintanilla L, Velez-Belchi P, García A, Cortés D, Rodríguez JM, et al. Characterization of the spawning habitat of Atlantic bluefin tuna and related species in the Balearic Sea (western Mediterranean). Prog Oceanogr 2010; 86: 21–38.
- 19. Nishikawa Y. Distribution atlas of larval tunas, billfishes and related species: results of larval surveys by R/V Shunyo Maru, and Syoyo Maru. Far Seas Fish Res Lab S Ser 1978; 9: 1–99.
- 20. Nishikawa Y. Average distribution of larvae of oceanic species of scombroid fishes, 1956–1981. NRIFSF S-Ser 1985; 12: 1–99.
- 21. Reglero P, Tittensor DP, Álvarez-Berastegui D, Aparicio-González A, Worm B. Worldwide distributions of tuna larvae: revisiting hypotheses on environmental requirements for spawning habitats. Mar Ecol Prog Ser 2014; 501: 207–224.
- 22. Heberer LN, Snodgrass OE. The NOAA Pacific Bluefin Tuna Port Sampling Program, 2014–2019. NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC-651 2021.
- 23. Schaefer KM Reproductive biology of yellowfin tuna Thunnus albacares in the eastern Pacific Ocean. Bull I-ATCC 1998; 21: 201–272.
- 24. Lavaniegos BE, Jiménez-Pérez LC, Gaxiola-Castro G. Plankton response to El Niño 1997–1998 and La Niña 1999 in the southern region of the California Current. Prog Oceanogr 2002; 54: 33–58.
- 25. Gallo ND, Drenkard E, Thompson AR, Weber ED, Wilson-Vendenberg D, McClatchie S, et al. Bridging from monitoring to solutions-based thinking: Lessons from CalCOFI for understanding and adapting to marine climate change impacts. Front Mar Sci 2019; 6: 695.
- 26. Huang B, Liu C, Banzon V, Freeman E, Graham G, Hankins B et al. Improvements of the Daily Optimum Interpolation Sea Surface Temperature (OISST) Version 2.1. J Climate 2021; 34: 2923–2939.
- 27.
Richards WJ (2006). Early Stages of Atlantic Fishes: An Identification Guide for Western Central North Atlantic. Taylor and Francis: Boca Raton, FL.
- 28. Brown‐Peterson NJ, Wyanski DM, Saborido‐Rey F, Macewicz BJ, Lowerre‐Barbieri SK. A standardized terminology for describing reproductive development in fishes. Mar Coast Fish 2011; 3: 52–70.
- 29. Schaefer KM Spawning time, frequency, and batch fecundity of yellowfin tuna, Thunnus albacares near Clipperton Atoll in the eastern Pacific Ocean. Fish Bull 1996; 94: 98–112.
- 30. Farley JH, Davis TL, Bravington MV, Andamari R, Davies CR. Spawning dynamics and size related trends in reproductive parameters of southern bluefin tuna, Thunnus maccoyii. PLoS One 2015; 10(5), e0125744. pmid:25993276
- 31. Boustany AM, Matteson R, Castleton M, Farwell C, Block BA. Movements of Pacific Bluefin Tuna (Thunnus orientalis) in the Eastern North Pacific revealed with archival tags. Prog Oceanogr 2010; 86: 94–104.
- 32. Runcie RM, Muhling B, Hazen EL, Bograd SJ, Garfield T, DiNardo G. Environmental associations of Pacific bluefin tuna (Thunnus orientalis) catch in the California Current system. Fish Oceanogr 2019; 28: 372–388.
- 33. Block BA, Teo SL, Walli A, Boustany A, Stokesbury MJW, Farwell CJ et al. Electronic tagging and population structure of Atlantic Bluefin Tuna. Nature 2005; 434: 1121–1127. pmid:15858572
- 34. Corriero A, Karakulak S, Santamaria N, Deflorio M, Spedicato D, Addis P et al. Size and age at sexual maturity of female bluefin tuna (Thunnus thynnus L. 1758) from the Mediterranean Sea. J Appl Ichthyol 2005; 21: 483–486.
- 35. McGowan MF, Richards WJ. Bluefin tuna, Thunnus thynnus, larvae in the Gulf Stream off the Southeastern United States: satellite and shipboard observations of their environment. Fish Bull 1989; 87: 615–631.