Evaluation of growth-dependent survival during early stages of Pacific bluefin tuna using otolith microstructure analysis
Mikio Watai A , Taiki Ishihara A , Osamu Abe A B , Seiji Ohshimo A D and Carlos Augusto Strussmann C
+ Author Affiliations
- Author Affiliations
A National Research Institute of Far Seas Fisheries, Fisheries Research Agency, 5-7-1 Orido, Shimizu-ku, Shizuoka 424-8633, Japan.
B Marine Fishery Resources Development and Management Department, Southeast Asian Fisheries Development Center, Taman Perikanan Chendering, 21080 Kuala Terenhhanu, Malaysia.
C Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo 108-8477, Japan.
D Corresponding author. Email: oshimo@affrc.go.jp
Marine and Freshwater Research 68(11) 2008-2017 https://doi.org/10.1071/MF16337
Submitted: 28 September 2016 Accepted: 4 February 2017 Published: 13 April 2017
Abstract
The present study used otolith analysis-based body size back-calculation to: (1) evaluate the hypothesis of growth-dependent survival in young Pacific bluefin tuna (PBF; Thunnus orientalis) from the north-western Pacific Ocean; (2) identify critical developmental stages for survival; and (3) compare interannual differences in early growth. To this end, we compared the daily growth trajectories of a large number of larvae (standard length (SL) <15 mm), juveniles (15 ≤ SL ≤ 150 mm), and young-of-year (YOY; SL >150 mm) collected between 2011 and 2015. Otolith radius and SL were highly correlated and yielded a single relationship applicable for the five year-classes. Body size back-calculation showed that only larvae with fast, steady growth successfully transitioned to the juvenile stage. The ontogenetic analysis of daily growth rates revealed interannual differences only in larvae, and not in the larval stage of juveniles and YOY. Neither sudden decreases nor increases in growth rates were observed during the larval stage of any of the stages, suggesting that the observed variability in larval body size may be the result of individual differences in growth rates rather than of drastic, one-time events. Overall, the results of the present study indicate that growth-dependent survival of larvae may be the most critical for PBF recruitment.
Additional keywords: Thunnus orientalis.
References
Ashida, H., Suzuki, N., Tanabe, T., Suzuki, N., and Aonuma, Y. (2015). Reproductive condition, batch fecundity, and spawning fraction of large Pacific bluefin tuna Thunnus orientalis landed at Ishigaki Island, Okinawa, Japan. Environmental Biology of Fishes 98, 1173–1183.| Reproductive condition, batch fecundity, and spawning fraction of large Pacific bluefin tuna Thunnus orientalis landed at Ishigaki Island, Okinawa, Japan.Crossref | GoogleScholarGoogle Scholar |
Bradford, M. J., and Cabana, G. (1997). Interannual variability in stage-specific survival rates and the causes of recruitment variation. In ‘Early Life History and Recruitment in Fish Populations’. (Eds C. Chambers and E. Trippel.) pp. 469–493. (Chapman and Hall: London, UK.)
Campana, S. E. (1990). How reliable are growth backcalculations based on otoliths? Canadian Journal of Fisheries and Aquatic Sciences 47, 2219–2227.
| How reliable are growth backcalculations based on otoliths?Crossref | GoogleScholarGoogle Scholar |
Campana, S. E. (1996). Year-class strength and growth rate in young Atlantic cod Gadus morhua. Marine Ecology Progress Series 135, 21–26.
| Year-class strength and growth rate in young Atlantic cod Gadus morhua.Crossref | GoogleScholarGoogle Scholar |
Campana, S. E., and Jones, C. M. (1992). Analysis of microstructure data. In ‘Otolith Microstructure Examination and Analysis’. (Eds D. K. Stevenson and S. E. Campana.) Canadian Special Publication of Fishery Aquatic Sciences 117, pp. 73–100. (Canadian Government Publishing Centre, Canada Communication Group: Ottawa, ON, Canada.)
Campana, S. E., and Neilson, J. D. (1985). Microstructures of fish otoliths. Canadian Journal of Fisheries and Aquatic Sciences 42, 1014–1032.
| Microstructures of fish otoliths.Crossref | GoogleScholarGoogle Scholar |
Folkvord, A., Blom, G., Johannessen, A., and Moksness, E. (2000). Growth-dependent age estimation in herring (Clupea harengus L.) larvae. Fisheries Research 46, 91–103.
| Growth-dependent age estimation in herring (Clupea harengus L.) larvae.Crossref | GoogleScholarGoogle Scholar |
Fujioka, K., Oshima, K., Tei, Y., Ichinokawa, M., and Takeuchi, Y. (2014). Recruitment abundance indices of young Pacific bluefin tuna revealed by Japanese troll fisheries. ISC Pacific Bluefin Tuna Working Group report ISC/14/PBFWG-1/07. (International Scientific Committee for Tuna and Tuna-Like Species in the North Pacific Ocean, ISC: Shizuoka, Japan). Available at http://isc.fra.go.jp/pdf/PBF/ISC_2014_PBF/ISC_14_PBFWG1_07.pdf [Verified 23 February 2017].
Fukuda, H., Torisawa, S., and Takagi, T. (2014). Ontogenetic changes in schooling behavior and visual sensitivity during larval and juvenile stages in Pacific bluefin tuna, Thunnus orientalis. Suisan Sougou Kenkyuu Senta Kenkyuu Houkoku 38, 135–139.
García, A., Cortés, D., Quintanilla, J., Rámirez, T., Quintanilla, L., Rodríguez, J. M., and Alemany, F. (2013). Climate-induced environmental conditions influencing interannual variability of Mediterranean bluefin (Thunnus thynnus) larval growth. Fisheries Oceanography 22, 273–287.
| Climate-induced environmental conditions influencing interannual variability of Mediterranean bluefin (Thunnus thynnus) larval growth.Crossref | GoogleScholarGoogle Scholar |
Govoni, J. J., Chester, J. A., Hoss, D. E., and Ortner, B. P. (1985). An observation of episodic feeding and growth of larval Leiostomus xanthurus in the northern Gulf of Mexico. Journal of Plankton Research 7, 137–146.
| An observation of episodic feeding and growth of larval Leiostomus xanthurus in the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Hare, J. A., and Cowen, R. K. (1995). Effect of age, growth rate, and ontogeny on the otolith size–fish size relationship in bluefish, Pomatomus saltatrix, and the implications for backcalculation of size in fish early life history stages. Canadian Journal of Fisheries and Aquatic Sciences 52, 1909–1922.
| Effect of age, growth rate, and ontogeny on the otolith size–fish size relationship in bluefish, Pomatomus saltatrix, and the implications for backcalculation of size in fish early life history stages.Crossref | GoogleScholarGoogle Scholar |
Hunter, J. R. (1981). Feeding ecology and predation of marine fish larvae. In ‘Marine Fish Larvae’. (Ed. R. Lasker.) pp. 33–77. (University of Washington Press: Seattle, WA, USA.)
Ichinokawa, M., Okamura, H., Oshima, K., Yokawa, K., and Takeuchi, Y. (2014). Spatiotemporal catch distribution of age-0 Pacific bluefin tuna Thunnus orientalis caught by the Japanese troll fishery in relation to surface sea temperature and seasonal migration. Fisheries Science 80, 1181–1191.
| Spatiotemporal catch distribution of age-0 Pacific bluefin tuna Thunnus orientalis caught by the Japanese troll fishery in relation to surface sea temperature and seasonal migration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFKms73P&md5=3eec9bd49d6724f954b88a23932d40d3CAS |
Itoh, T., Shiina, Y., Tsuji, S., Endo, F., and Tezuka, N. (2000). Otolith daily increment formation in laboratory reared larval and juvenile bluefin tuna Thunnus thynnus. Fisheries Science 66, 834–839.
| Otolith daily increment formation in laboratory reared larval and juvenile bluefin tuna Thunnus thynnus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsl2qurs%3D&md5=79b940e700f05ec8573aca7d9ba84b50CAS |
Kaji, T., Tanaka, M., Takahashi, Y., Oka, M., and Ishibashi, N. (1996). Preliminary observations on development of Pacific bluefin tuna Thunnus thynnus (Scombridae) larvae reared in the laboratory, with special reference to the digestive system. Marine and Freshwater Research 47, 261–269.
| Preliminary observations on development of Pacific bluefin tuna Thunnus thynnus (Scombridae) larvae reared in the laboratory, with special reference to the digestive system.Crossref | GoogleScholarGoogle Scholar |
Le Pape, O., and Bonhommeau, S. (2015). The food limitation hypothesis for juvenile marine fish. Fish and Fisheries 16, 373–398.
| The food limitation hypothesis for juvenile marine fish.Crossref | GoogleScholarGoogle Scholar |
Meekan, M. G., and Fortier, L. (1996). Selection for fast growth during the larval life of Atlantic cod Gadus morhua on the Scotian shelf. Marine Ecology Progress Series 137, 25–37.
| Selection for fast growth during the larval life of Atlantic cod Gadus morhua on the Scotian shelf.Crossref | GoogleScholarGoogle Scholar |
Miyashita, S. (2002). Studies on the seedling production of the Pacific bluefin tuna, Thunnus thynnus orientalis. Bulletin of the Fisheries Laboratory of Kinki University Kinki University 8, 1–171.
Miyashita, S., Sawada, Y., Okada, T., Murata, O., and Kumai, H. (2001). Morphological development and growth of laboratory-reared larval and juvenile Thunnus thynnus (Pisces: Scombridae). Fishery Bulletin 99, 601–616.
Okiyama, M. (1974). Occurrence of the postlarvae of bluefin tuna, Thunnus thynnus, in the Japan Sea. Nihonkai-ku Suisan Kenkyujo Kenkyu Hokoku 11, 9–21.
Okochi, Y., Abe, O., Tanaka, S., Ishihara, Y., and Shimizu, A. (2016). Reproductive biology of female Pacific Bluefin tuna, Thunnus orientalis, in the Sea of Japan. Fisheries Research 174, 30–39.
| Reproductive biology of female Pacific Bluefin tuna, Thunnus orientalis, in the Sea of Japan.Crossref | GoogleScholarGoogle Scholar |
Peterman, R. M., Bradford, M. J., Lo, N. C. H., and Methot, R. D. (1988). Cotribution of early life stages to interannual variability in recruitment of northern anchovy (Engraulis mordax). Canadian Journal of Fisheries and Aquatic Sciences 45, 8–16.
| Cotribution of early life stages to interannual variability in recruitment of northern anchovy (Engraulis mordax).Crossref | GoogleScholarGoogle Scholar |
Peterson, I., and Wroblewski, J. S. (1984). Mortality rates of fishes in the pelagic ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 41, 1117–1120.
| Mortality rates of fishes in the pelagic ecosystem.Crossref | GoogleScholarGoogle Scholar |
Robert, D., Catonguay, M., and Fortier, L. (2007). Early growth and recruitment in Atlantic mackerel Scomber scombrus: discriminating the effects of fast growth and selection for fast growth. Marine Ecology Progress Series 337, 209–219.
| Early growth and recruitment in Atlantic mackerel Scomber scombrus: discriminating the effects of fast growth and selection for fast growth.Crossref | GoogleScholarGoogle Scholar |
Satoh, K., Tanaka, Y., and Iwahashi, M. (2008). Variation in the instantaneous mortality rate between larval patches of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean. Fisheries Research 89, 248–256.
| Variation in the instantaneous mortality rate between larval patches of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Satoh, K., Tanaka, Y., Masujima, M., Okazaki, M., Kato, Y., Shono, H., and Suzuki, K. (2013). Relationship between the growth and survival of larval Pacific bluefin tuna, Thunnus orientalis. Marine Biology 160, 691–702.
| Relationship between the growth and survival of larval Pacific bluefin tuna, Thunnus orientalis.Crossref | GoogleScholarGoogle Scholar |
Suzuki, N., Tanabe, T., Nohara, K., Doi, W., Ashida, H., Kameda, T., and Aonuma, Y. (2014). Annual fluctuation in Pacific bluefin tuna (Thunnus orientalis) larval catch from 2007 to 2010 in waters surrounding the Ryukyu Archipelago, Japan. Bulletin of Fisheries Research Agency 38, 87–99.
Takahashi, M., and Watanabe, Y. (2004). Growth rate-dependent recruitment of Japanese anchovy Engraulis japonicus in the Kuroshio–Oyashio transitional waters. Marine Ecology Progress Series 266, 227–238.
| Growth rate-dependent recruitment of Japanese anchovy Engraulis japonicus in the Kuroshio–Oyashio transitional waters.Crossref | GoogleScholarGoogle Scholar |
Takasuka, A., Aoki, I., and Mitani, I. (2003). Evidence of growth-selective predation on larval Japanese anchovy Engraulis japonicus in Sagami Bay. Marine Ecology Progress Series 252, 223–238.
| Evidence of growth-selective predation on larval Japanese anchovy Engraulis japonicus in Sagami Bay.Crossref | GoogleScholarGoogle Scholar |
Tanaka, M., Kaji, T., Nakamura, Y., and Takahashi, Y. (1996). Developmental strategy of scombrid larvae: high growth potential related to food habits and precocious digestive system development. In ‘Survival Strategies in Early Life Stages of Marine Resources’. (Eds Y. Watanabe, Y. Yamashita, and Y. Oozeki.) pp. 125–139. (AA Balkema: Rotterdam, Netherlands.)
Tanaka, Y., Satoh, K., Iwahashi, M., and Yamada, H. (2006). Growth-dependent recruitment of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean. Marine Ecology Progress Series 319, 225–235.
| Growth-dependent recruitment of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Tanaka, Y., Mohri, M., and Yamada, H. (2007). Distribution, growth and hatch date of juvenile Pacific bluefin tuna Thunnus orientalis in the coastal area of the Sea of Japan. Fisheries Science 73, 534–542.
| Distribution, growth and hatch date of juvenile Pacific bluefin tuna Thunnus orientalis in the coastal area of the Sea of Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntlGitr0%3D&md5=94e63d7e9a218e4f6ede7a8a5111e61aCAS |
Tanaka, Y., Satoh, K., Yamada, H., Takebe, T., Nikaido, H., and Shiozawa, S. (2008). Assessment of the nutritional status of field-caught larval Pacific bluefin tuna by RNA/DNA ratio based on a starvation experiment of hatchery-reared fish. Journal of Experimental Marine Biology and Ecology 354, 56–64.
| Assessment of the nutritional status of field-caught larval Pacific bluefin tuna by RNA/DNA ratio based on a starvation experiment of hatchery-reared fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFehtA%3D%3D&md5=374df229c5e69715dadbaa2783c489b0CAS |
Tanaka, Y., Minami, H., Ishihi, Y., Kumon, K., Eba, T., Nishi, A., Nikaido, H., and Shiozawa, S. (2010). Prey utilization by hatchery-reared Pacific bluefin tuna larvae in mass culture tank estimated using stable isotope analysis, with special reference to their growth variation. Aquaculture Science 58, 501–508.
| Prey utilization by hatchery-reared Pacific bluefin tuna larvae in mass culture tank estimated using stable isotope analysis, with special reference to their growth variation.Crossref | GoogleScholarGoogle Scholar |
Tanaka, Y., Minami, H., Ishihi, Y., Kumon, K., Higuchi, K., Eba, T., Nishi, A., Nikaido, H., and Shiozawa, S. (2014). Relationship between prey utilization and growth variation in hatchery-reared Pacific bluefin tuna, Thunnus orientalis (Temminck et Schlegel), larvae estimated using nitrogen stable isotope analysis. Aquaculture Research 45, 537–545.
| Relationship between prey utilization and growth variation in hatchery-reared Pacific bluefin tuna, Thunnus orientalis (Temminck et Schlegel), larvae estimated using nitrogen stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXit12gurg%3D&md5=b764902b6fcbe67270401409c4485cecCAS |
Ueyanagi, S. (1969). Observations on the distribution of tuna larvae in the Indo-Pacific Ocean with emphasis on the delineation of the spawning areas of albacore, Thunnus alalunga. Nihonkai-ku Suisan Kenkyujo Kenkyu Hokoku 2, 177–256.
Wexler, J. B., Chow, S., Wakabayashi, T., Nohara, K., and Margulies, D. (2007). Temporal variation in growth of yellowfin tuna (Thunnus albacares) larvae in the Panama Bight, 1990–97. Fish Bulletin 105, 1–18.
Yabe, H., Ueyanai, S., and Watanabe, H. (1966). Studies on the early life history of bluefin tuna Thunnus thynnus and on the larvae of the southern bluefin tuna T. maccoyii. Report of the Nankai Regional Fishery Research Laboratory 23, 95–129.
