First estimates of metabolic rate in Atlantic bluefin tuna larvae.
Edurne Blanco, Patricia Reglero, Aurelio Ortega, Arild Folkvord, Fernando de la Gándara, Alma Hernández de Rojas, Marta Moyano
Author Information
Edurne Blanco: Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Ecosystem Oceanography Group (GRECO), Palma de Mallorca, Spain. ORCID
Patricia Reglero: Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Ecosystem Oceanography Group (GRECO), Palma de Mallorca, Spain.
Aurelio Ortega: Instituto Español de Oceanografía, Centro Oceanográfico de Murcia, Murcia, Spain.
Arild Folkvord: Department of Biological Sciences, University of Bergen, Bergen, Norway.
Fernando de la Gándara: Instituto Español de Oceanografía, Centro Oceanográfico de Murcia, Murcia, Spain.
Alma Hernández de Rojas: Instituto Español de Oceanografía, Centro Oceanográfico de Gijón, Gijón, Spain.
Marta Moyano: Institute of Hydrobiology and Fisheries Science, University of Hamburg, Hamburg, Germany. ORCID
Atlantic bluefin tuna is an iconic scombrid species with a high commercial and ecological value. Despite their importance, many physiological aspects, especially during the larval stages, are still unknown. Metabolic rates are one of the understudied aspects in scombrid larvae, likely due to challenges associated to larval handling before and during respirometry trials. Gaining reliable estimates of metabolic rates is essential to understand how larvae balance their high growth needs and activity and other physiological functions, which can be very useful for fisheries ecology and aquaculture. This is the first study to (a) estimate the relationship between routine metabolic rate (RMR) and larval dry weight (DW) (mass scaling exponent) at a constant temperature of 26°C, (b) measure the RMR under light and darkness and (c) test whether the interindividual differences in the RMR are related to larval nutritional status (RNA/DNA and DNA/DW). The RMR scaled nearly isometrically with body size (b = 0.99, 0.60-31.56 mg DW) in contrast to the allometric relationship observed in most fish larvae (average b = 0.87). The results show no significant differences in larval RMR under light and darkness, suggesting similar larval activity levels in both conditions. The size explained most of the variability in RMR (97%), and nutritional condition was unrelated to the interindividual differences in routine metabolism. This is the first study to report the metabolic rates of Atlantic bluefin tuna larvae and discuss the challenges of performing bioenergetic studies with early life stages of scombrids.
Anderson, J. T. (1988). A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. Journal of Northwest Atlantic Fishery Science, 8, 55-66.
Bergeron, J.-P. (1997). Nucleic acids in Ichthyoplankton ecology: A review, with emphasis on recent advances for new perspectives. Journal of Fish Biology, 51, 284-302.
Blanco, E., Reglero, P., Hernández de Rojas, A., Ortega, A., de la Gándara, F., & Folkvord, A. (2019). The effect of nutritional condition by two nucleic acid derived indices on the growth to post-flexion of Atlantic bluefin tuna and Atlantic bonito larvae. Journal of Experimental Marine Biology and Ecology, 519, 151182.
Blanco, E., Reglero, P., Ortega, A., de la Gándara, F., Fiksen, Ø., & Folkvord, A. (2017). The effects of light, darkness and intermittent feeding on the growth and survival of reared Atlantic Bonito and Atlantic Bluefin tuna larvae. Aquaculture, 479, 233-239.
Brill, R. (1987). On the standard metabolic rates of Tropica tunas, including the effect of body size and acute temperature change. Fishery Bulletin, 85, 25-35.
Brill, R. W. (1979). The effect of body size on the standard metabolic rate of skipjack tuna, Katsuwonus pelamis. Fishery Bulletin, 77, 494-498.
Buckley, L., Caldarone, E., & Ong, T. L. (1999). RNA-DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia, 401, 265-277.
Caldarone, E. M., Clemmesen, C. M., Berdalet, E., Miller, T. J., Folkvord, A., Holt, G. J., … Suthers, I. M. (2006). Intercalibration of four Spectrofluorometric protocols for measuring RNA/DNA ratios in larval and juvenile fish. Limnology and Oceanography: Methods, 4, 153-163.
Chabot, D., McKenzie, D. J., & Craig, J. F. (2016b). Metabolic rate in fishes: definitions, methods and significance for conservation physiology. Journal of Fish Biology, 88, 1-9.
Chabot, D., Steffensen, J. F., & Farrell, A. P. (2016a). The determination of standard metabolic rate in fishes. Journal of Fish Biology, 88, 81-121.
Clarke, A., & Johnston, N. M. (1999). Scaling of metabolic rate with body mass and in teleost temperature fish. Journal of Animal Ecology, 68, 893-905.
Clemmesen, C. M. (1987). Laboratory studies on Rna Dna ratios of starved and fed herring (Clupea-Harengus) and turbot (Scophthalmus-Maximus) larvae. Journal du Conseil, 43, 122-128.
Cushing, D. H. (1990). Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Advances in Marine Biology, 26, 249-293.
Davenport, J., & Lonning, S. (1980). Oxygen uptake in developing eggs and larvae of the cod Gadus morhua. Journal of Fish Biology, 16, 249-256.
De la Gándara, F., Mylonas, C. & Bridges, C. (2010) SELFDOTT Report 2009.
De Silva, C. D., Premawansa, S., & Keembiyahetty, C. N. (1986). Oxygen consumption in Oreochromis niloticus (L.) in relation to development, salinity, temperature and time of day. Journal of Fish Biology, 29, 267-277.
Dewar, H., Graham, J. B., & Brill, R. W. (1994a). Studies of Tropical tuna swimming Performance in a large water tunnel-Thermoregulation. Journal of Experimental Biology, 192(1), 33-44.
Dewar, H., Graham, J. B., & Brill, R. W. (1994b). Studies of tropical tuna swimming performance in a large water tunnel-Energetics. Journal of Experimental Biology, 192(1), 13-31.
Finn, R., Fyhn, H., & Evjen, M. (1995). Physiological energetics of developing embryos and yolk-sac larvae of Atlantic cod (Gadus morhua) .I. respiration and nitrogen metabolism. Marine Biology, 124, 355-369.
Finn, R. N., Rønnestad, I., Van Der Meeren, T., & Fyhn, H. J. (2002). Fuel and metabolic scaling during the early life stages of Atlantic cod Gadus morhua. Marine Ecology-Progress Series, 243, 217-234.
Foley, C., Bradley, D., & HooK, T. (2016). A review and assessment of the potential use of RNA: DNA ratios to assess the condition of entrained fish larvae. Ecological Indicators, 60, 346-357.
Folkvord, A., Ystanes, L., Johannessen, A., & Moksness, E. (1996). RNA: DNA ratios and growth of herring (Clupea harengus) larvae reared in Mesocosms. Marine Biology, 126, 591-602.
García, A., Cortés, D., Ramírez, T., Fehri-Bedoui, R., Alemany, F., Rodríguez, J. M., … Álvarez, J. P. (2006). First data on growth and nucleic acid and protein content of field-captured Mediterranean bluefin (Thunnus thynnus) and albacore (Thunnus alalunga) tuna larvae: a comparative study. Scientia Marina, 70, 67-78.
Giguere, L., Cote, B., & Pierre, J. F. S. (1988). Metabolic rates scale Isometrically. Marine Ecology Progress Series, 50, 13-19.
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M., & Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science, 2001, 2248-2251.
Gooding, R. M., Neill, W. H., & Dizon, A. E. (1981). Respiration rates and low-oxygen tolerance limits in skipjack tuna, Katsuwonus pelamis. Fishery Bulletin, 79, 31-48.
Graham, J. B., & Laurs, R. M. (1982). Metabolic rate of the albacore tuna Thunnus alalunga. Marine Biology, 72, 1-6.
Graham, J. B., & Dickson, K. A. (2004). Tuna comparative physiology. Journal of Experimental Biology, 207, 4015-4024.
Hjort, J. (1914). Fluctuations in the great fisheries of northern Europe viewed in light of biological research. Rapports et Procès-verbaux des Réunions. Conseil international pour l'Exploration de la Mer, 20, 1-228.
Houde, E.-D., & Schekter, R. (1983). Oxygen uptake and comparative energetics among eggs and larvae of three subtropical marine fishes. Marine Biology, 72, 283-293.
Houde, E. D. (1989). Subtleties and episodes in the early life of fishes. Journal of Fish Biology, 35, 29-38.
Houlihan, D., Pedersen, B., Steffensen, J., & Brechin, J. (1995). Protein synthesis, growth and energetics in larval herring (Clupea harengus) at different feeding regimes. Fish Physiology and Biochemistry, 14, 195-208.
Hunter, J. R., & Kimbrell, C. A. (1980). Early life history of Pacific mackerel, Scomber japonicus. Fishery Bulletin, 78, 89-101.
ICES. (2004). Recruitment studies: Manual on precision and accuracy of tools. In M. Belchier, C. Clemmesen, D. Cortes, T. Doan, A. Folkvord, A. Garcia, A. Geffen, H. Høie, A. Johannessen, E. Moksness, H. de Pontual, T. Ramirez, D. Schnack, & B. Sveinsbo (Eds.), ICES Techniques in Marine Environmental Sciences, No. 33. 35 pp.
Illing, B., Moyano, M., Berg, J., Hufnagl, M., & Peck, M. A. (2018). Behavioral and physiological responses to prey match-mismatch in larval herring. Estuarine, Coastal and Shelf Science, 201, 82-94.
Javahery, S., Nekoubin, H., & Moradlu, A. H. (2012). Effect of Anaesthesia with clove oil in fish (review). Fish Physiology and Biochemistry, 38, 1545-1552.
Jørgensen, C., Enberg, K., & Mangel, M. (2016). Modelling and interpreting fish bioenergetics: a role for behaviour, life-history traits and survival trade-offs. Journal of Fish Biology, 88, 389-402.
Juan-Jordá, M. J., Mosqueira, I., Freire, J. & Dulvy, N. K. (2013) Life history correlates of marine fisheries vulnerability: A review and a test with tunas and mackerel species. Marine extinctions - patterns and processes. CIESM Workshop Monograph no. 45 113-128.
Kaji, T. (2003). Bluefin tuna larval rearing and development: State of the art. Cahiers Options Mediterranéennes, 89, 85-89.
Kendall, A. W., Ahlstrom, E. H., & Moser, H. G. (1984). Early life History stages of fishes and their characters. In H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, J. A. W. Kendall, Jr, & S. L. Richardson, (Eds), Ontogeny and Systematics of Fishes, 1, (pp. 11-22). Allen Press, Lawrence: American Society of Ichthyologists and Herpetologists.
Killen, S. S., Costa, I., Brown, J. A., & Gamperl, A. K. (2007). Little left in the tank: metabolic scaling in marine Teleosts and its implications for aerobic scope. Proceedings of the Royal Society B: Biological Sciences, 274, 431-438.
Killen, S. S., Atkinson, D., & Glazier, D. S. (2010). The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. Ecology Letters, 13, 184-193.
Kiorbøe, T., Munk, P., & Richardson, K. (1987). Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Marine Ecology Progress Series, 40, 1-10.
Kiørboe, T., & Hirst, A. G. (2014). Shifts in mass scaling of respiration, feeding, and growth rates across life-form transitions in marine pelagic organisms. American Naturalist, 183, E118-E130.
Korsmeyer, K. E., & Dewar, H. B. T.-F. P. (2001). Tuna metabolism and energetics. In B. Block & E. Stevens (Eds.), Tuna: Physiology, ecology, and evolution (pp. 35-78). San Diego, California, USA: Academic Press.
Margulies, D. (1997). Development of the visual system and inferred Performance capabilities of larval and early juvenile Scombrids. Marine and Freshwater Behaviour and Physiology, 30, 75-98.
McCarthy, I. D., & Fuiman, L. A. (2011). Post-prandial changes in protein synthesis in red drum (Sciaenops ocellatus) larvae. Journal of Experimental Biology, 214, 1821-1828.
McKenzie, D. J., Lund, I., & Pedersen, P. B. (2008). Essential fatty acids influence metabolic rate and tolerance of hypoxia in Dover sole (Solea solea) larvae and juveniles. Marine Biology, 154, 1041-1051.
McLeod, I. M., & Clark, T. D. (2016). Limited capacity for faster digestion in larval coral reef fish at an elevated temperature. PLoS One, 11, 1-13.
McLeod, I. M., Rummer, J. L., Clark, T. D., Jones, G. P., McCormick, M. I., Wenger, A. S., & Munday, P. L. (2013). Climate change and the Performance of larval coral reef fishes: the interaction between temperature and food availability. Conservation Physiology, 1, 1-12.
Meyer, S., Caldarone, E. M., Chícharo, M. A., Clemmesen, C., Faria, A. M., Faulk, C., … Peck, M. A. (2012). On the edge of death: rates of decline and lower thresholds of biochemical condition in food-deprived fish larvae and juveniles. Journal of Marine Systems, 93, 11-24.
Miyashita, S., Hattori, N., Sawada, Y., Ishibashi, Y., Nakatsukasa, H., Okada, T., … Kumai, H. (1999). Ontogenetic change in oxygen consumption of Bluefin tuna. Thunnus thynnus. Suisanzoshoku, 47, 269-275.
Moyano, M., Garrido, S., Teodósio, M. A., & Peck, M. A. (2014). Standard metabolism and growth dynamics of laboratory-reared larvae of Sardina pilchardus. Journal of Fish Biology, 84, 1247-1255.
Moyano, M., Illing, B., Christiansen, L., & Peck, M. A. (2018). Linking rates of metabolism and growth in marine fish larvae. Marine Biology, 165(5).
Nelson, J. A. (2016). Oxygen consumption rate v. rate of energy utilization of fishes: a comparison and brief history of the two measurements. Journal of Fish Biology, 88, 10-25.
Ortega, A. & de la Gándara, F. (2017) Closing the Life Cycle of the Atlantic Bluefin Tuna Thunnus thynnus in Captivity. In Aquaculture Europe, Dubrovnik, Croatia, October 17-20.
Peck, M. A., & Buckley, L. J. (2008). Measurements of larval Atlantic cod (Gadus morhua) routine metabolism: temperature effects, Diel differences and individual-based modeling. Journal of Applied Ichthyology, 24, 144-149.
Peck, M. A., & Moyano, M. (2016). Measuring respiration rates in marine fish larvae: challenges and advances. Journal of Fish Biology, 88, 173-205.
Peck, M. A., Reglero, P., Takahashi, M., & Catalán, I. A. (2013). Life cycle Ecophysiology of small pelagic fish and climate-driven changes in populations. Progress in Oceanography, 116, 220-245.
Porter, S. M. (2001). Effects of size and light on respiration and activity of walleye Pollock (Theragra chalcogramma) larvae. Journal of Experimental Marine Biology and Ecology, 256, 253-265.
Post, J., & Lee, J. (1996). Metabolic ontogeny of teleost fishes. Canadian Journal of Fisheries and Aquatic Sciences, 53, 910-923.
Reglero, P., Ortega, A., Blanco, E., Fiksen, T., Viguri, F. J., de la Gándara, F., … Folkvord, A. (2014). Size-related differences in growth and survival in Piscivorous fish larvae fed different prey types. Aquaculture, 433, 94-101.
Reglero, P., Ortega, A., Balbín, R., Abascal, F. J., Medina, A., Blanco, E., et al. (2018). Atlantic Bluefin tuna spawn at suboptimal temperatures for their offspring. Proceedings of the Royal Society B: Biological Sciences, 285(1870), 20171405.
Reglero, P., Balbín, R., Abascal, F. J., Medina, A., Alvarez-Berastegui, D., Rasmuson, L., et al. (2019). Pelagic habitat and offspring survival in the eastern stock of Atlantic Bluefin tuna. ICES Journal of Marine Science.76(2), 549-558.
Rodgers, G. G., Tenzing, P., & Clark, T. D. (2016). Experimental methods in aquatic Respirometry: the importance of mixing devices and accounting for background respiration. Journal of Fish Biology, 88, 65-80.
Ruzicka, J. J., & Gallager, S. M. (2006a). The importance of the cost of swimming to the foraging behavior and ecology of larval cod (Gadus morhua) on Georges Bank. Deep-Sea Research Part II: Topical Studies in Oceanography, 53, 2708-2734.
Ruzicka, J. J., & Gallager, S. M. (2006b). The Saltatory search behavior of larval cod (Gadus morhua). Deep-Sea Research Part II: Topical Studies in Oceanography, 53, 2735-2757.
Wexler, J. B., Margulies, D., & Scholey, V. P. (2011). Temperature and dissolved oxygen requirements for survival of Yellowfin tuna, Thunnus albacares, larvae. Journal of Experimental Marine Biology and Ecology, 404, 63-72.
Wieser, W. (1995). Energetics of fish larvae, the smallest vertebrates. Acta Physiologica Scandinavica, 154, 279-290.
Wieser, W., Forstner, H., Medgyesy, N., & Hinterleitner, S. (1988). To switch or not to switch: partitioning of energy between growth and activity in larval cyprinids (Cyprinidae: Teleostei). Functional Ecology, 2, 499-507.
Yamashita, Y., & Bailey, K. M. (1989). A laboratory study of the bioenergetics of larval walleye Pollock Theragra -Chalcogramma. Fishery Bulletin, 87, 525-536.
Yúfera, M., Ortiz-Delgado, J. B., Hoffman, T., Siguero, I., Urup, B., & Sarasquete, C. (2014). Organogenesis of digestive system, visual system and other structures in Atlantic Bluefin tuna (Thunnus thynnus) larvae reared with copepods in Mesocosm system. Aquaculture, 426-427, 126-137.
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57381332/German Academic Exchange Service
678193 (CERES)/European Union's Horizon 2020 research and innovation programme
773713 (PANDORA)/European Union's Horizon 2020 research and innovation programme
652831/European Union's Horizon 2020 research and innovation programme