Ontogenetic changes in DNA and RNA content of laboratory-reared Prochilodus lineatus larvae: use of RNA/DNA ratios as indicators of nutritional condition
M. V. Diaz A B E , M. I. Gómez C , S. Sánchez D and C. M. Fuentes CA Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo V. Ocampo 1, Escollera Norte, Mar del Plata, B7602HSA, Buenos Aires, Argentina.
B Instituto de Investigaciones Marinas y Costeras, Consejo Nacional de Investigaciones Científicas y Técnicas (IIMyC-CONICET), Rodríguez Peña 4002-4100, Mar del Plata, B7602GSD, Buenos Aires, Argentina.
C Dirección de Pesca Continental, Ministerio de Agroindustria, Avenida Paseo Colón 982, C1063ACJ, Ciudad Autónoma de Buenos Aires, Argentina.
D Facultad de Ciencias Veterinarias, Instituto de Ictiología del Nordeste, Universidad Nacional del Nordeste. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Sargento Cabral 2139, Corrientes, W3402BKG, Corrientes, Argentina.
E Corresponding author. Email: mdiaz@inidep.edu.ar
Marine and Freshwater Research 69(3) 455-463 https://doi.org/10.1071/MF17178
Submitted: 11 June 2017 Accepted: 9 October 2017 Published: 12 January 2018
Abstract
The aims of the present study were to describe the ontogenetic performance of DNA and RNA content, as well as to assess the nutritional condition of Prochilodus lineatus larvae reared under different feeding treatments. The experiment consisted of two parts, the first 6–14 days after hatching (DAH) and the second 15–21 DAH. In the first part of the experiment, larvae were kept under one of two feeding treatments: fed or starved. During the second part of the experiment, larvae were kept under one of four treatments: fed, fed until 14 DAH and later starved, starved until 14 DAH and fed later or starved. It is of note that the size and weight reached of larvae that were starved during early development and later received food were higher than those of than larvae in the other feeding treatments. In addition, instantaneous growth rates were higher and nutritional condition was better in larvae that were initially starved and fed later. The availability of food following a period of starvation seems to trigger larval metabolism and cellular division. Consequently, we recommend maintaining appropriate food provision in the aquaculture of P. lineatus larvae, especially in advanced developmental stages. We verified that RNA/DNA ratio is affected by the feeding condition and that it is sensitive enough to promptly reflect changes in feeding conditions of P. lineatus larvae. Thus, the RNA/DNA ratio could be used to assess nutritional condition of both wild and cultured P. lineatus larvae.
Additional keywords: fish larvae, fresh water, laboratory calibration, nucleic acids content, starvation.
References
Agostinho, A. A., De Vazzoler, A. E. A., Gomes, L. C., and Okada, O. (1993). Estratificación espacial y comportamiento de Prochilodus scrofa en distintas fases del ciclo de vida, en la planicie de inundación del alto río Paraná y embalse de Itaipú, Paraná, Brasil. Revue d’Hydrobiologie Tropicale 26, 79–90.Araújo, F. G., and Rosa, P. V. (2017). Docosahexaenoic acid (C22:6n-3) alters cortisol response after air exposure in Prochilodus lineatus (Valenciennes) larvae fed on enriched Artemia. Aquaculture Nutrition 23, 1216–1224.
| Docosahexaenoic acid (C22:6n-3) alters cortisol response after air exposure in Prochilodus lineatus (Valenciennes) larvae fed on enriched Artemia.Crossref | GoogleScholarGoogle Scholar |
Baigún, C., Puig, A., Minotti, P. G., Kandus, P., Quintana, R., Vicari, R., Bo, R., Oldani, N., and Nestler, J. (2008). Resource use in the Paraná River delta (Argentina): moving away from an ecohydrological approach? Ecohydrology & Hydrobiology 8, 245–262.
| Resource use in the Paraná River delta (Argentina): moving away from an ecohydrological approach?Crossref | GoogleScholarGoogle Scholar |
Baigún, C., Minotti, P., and Oldani, N. (2013). Assessment of sábalo (Prochilodus lineatus) fisheries in the lower Paraná River basin (Argentina) based on hydrological, biological, and fishery indicators. Neotropical Ichthyology 11, 199–210.
| Assessment of sábalo (Prochilodus lineatus) fisheries in the lower Paraná River basin (Argentina) based on hydrological, biological, and fishery indicators.Crossref | GoogleScholarGoogle Scholar |
Bailey, K. M., Canino, M. F., Napp, J. N., Spring, S. M., and Brown, A. L. (1995). Contrasting years of prey levels, feeding conditions and mortality of larval walleye pollock Theragra chalcogramma in the western Gulf of Alaska. Marine Ecology Progress Series 119, 11–23.
| Contrasting years of prey levels, feeding conditions and mortality of larval walleye pollock Theragra chalcogramma in the western Gulf of Alaska.Crossref | GoogleScholarGoogle Scholar |
Bonetto, A. A. (1986). Fish of the Paraná system. In ‘The Ecology of River Systems’. (Eds B. R. Davies and K. F. Walker.) pp. 573–588. (Dr. W. Junk Publishers: Dordrecht, Netherlands.)
Bonetto, A. A., Cannon Veron, M., and Roldán, D. (1981). Nuevos aportes al conocimiento de las migraciones de peces en el río Paraná. Ecosur 8, 29–40.
Brown, D. R., and Fuentes, C. M. (2010). Daily increments in otoliths of sábalo (Prochilodus lineatus) larvae. Journal of Applied Ichthyology 26, 123–125.
| Daily increments in otoliths of sábalo (Prochilodus lineatus) larvae.Crossref | GoogleScholarGoogle Scholar |
Buckley, L. (1984). RNA/DNA ratio: an index of larval fish growth in the sea. Marine Biology 80, 291–298.
| RNA/DNA ratio: an index of larval fish growth in the sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhsVKnt7w%3D&md5=ce17aa1aa12ce9c17eeb9997ad78a460CAS |
Buckley, B. A., Caldarone, E. M., and Ong, T.-L. (1999). RNA–DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia 401, 265–277.
| RNA–DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotV2ht7k%3D&md5=d46508de2e0aadd32bf3c23b27f5e5d8CAS |
Bulow, F. J. (1970). RNA–DNA ratios as indicators of recent growth rates of a fish. Journal of the Fisheries Research Board of Canada 27, 2343–2349.
| RNA–DNA ratios as indicators of recent growth rates of a fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXps1SgsQ%3D%3D&md5=bafeee0759de6874d398e2153d0b8517CAS |
Caldarone, E. M., Wagner, M., St. Onge-Burns, J., and Buckley, L. J. (2001). Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Reference Document 11. (Northeast Fisheries Science Center.) Available at https://www.nefsc.noaa.gov/nefsc/publications/crd/crd0111/crd0111.pdf [Verified 8 November 2017].
Caldarone, E. M., Clemmesen, M. C., Berdalet, E., Miller, T. J., Folkvord, A., Holt, G. J., Olivar, M. P., and 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.
| Intercalibration of four spectrofluorometric protocols for measuring RNA:DNA ratios in larval and juvenile fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xntlertbs%3D&md5=c0e17c3627bf8c0d0c62d392cbbb7f40CAS |
Camargo, M. M. P., and Martinez, B. R. (2006). Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil. Environmental Toxicology and Pharmacology 21, 61–69.
| Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1OnurvF&md5=e8328a1a30ef7ed7f6927c8d6fa8311cCAS |
Chícharo, L., and Chícharo, M. A. (1995). The DNA/RNA ratio as a useful indicator of the nutritional condition in juveniles of Ruditapes decussatus. Scientia Marina 59, 95–101.
Chícharo, M. A., and Chícharo, L. (2008). RNA:DNA ratio and other nucleic acid derived indices in marine ecology. International Journal of Molecular Sciences 9, 1453–1471.
| RNA:DNA ratio and other nucleic acid derived indices in marine ecology.Crossref | GoogleScholarGoogle Scholar |
Clemmesen, C. (1994). The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Marine Biology 118, 377–382.
| The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration.Crossref | GoogleScholarGoogle Scholar |
Dahlhoff, E. P. (2004). Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annual Review of Physiology 66, 183–207.
| Biochemical indicators of stress and metabolism: applications for marine ecological studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1emtr8%3D&md5=b6620e015c0eb0b630b1b4ea0824140eCAS |
Diaz, M. V., and Pájaro, M. (2012). Protocolo para la determinación de ácidos nucleicos en larvas de peces. INIDEP Technical report 20. Instituto Nacional de Investigación y Desarrollo Pesquero, Mar del Plata, Buenos Aires, Argentina.
Diaz, M. V., Olivar, M. P., and Macchi, G. J. (2014). Larval condition of Merluccius hubbsi (Marini, 1933) in the northern Patagonian spawning ground. Fisheries Research 160, 60–68.
| Larval condition of Merluccius hubbsi (Marini, 1933) in the northern Patagonian spawning ground.Crossref | GoogleScholarGoogle Scholar |
Espinach Ros, A., and Sánchez, R. P. (2006). Proyecto de evaluación del recurso sábalo en el Paraná. Informe de los resultados de la primera etapa (2005–2006) y medidas de manejo recomendadas. Serie Pesca y Acuicultura: Estudios e Investigaciones Aplicadas 1, Secretaría de Agricultura Ganadería, Pesca y Alimentación, Buenos Aires, Argentina. Available at https://www.agroindustria.gob.ar/sitio/areas/pesca_continental/informes/baja/index.php [Verified 7 November 2017].
Espinach Ros, A., Sverlij, S., Amestoy, F., and Spinetti, M. (1998). Migration pattern of the sábalo Prochilodus lineatus (Pisces, Prochilodontidae) tagged in the lower Uruguay River. Verhandlungen des Internationalen Verein Limnologie 26, 2234–2236.
Ferron, A., and Leggett, W. C. (1994). An appraisal of condition measures for marine fish larvae. Advances in Marine Biology 30, 217–303.
| An appraisal of condition measures for marine fish larvae.Crossref | GoogleScholarGoogle Scholar |
Foley, C. J., Bradleyc, D. L., and Hööka, T. O. (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.
| A review and assessment of the potential use of RNA:DNA ratios to assess the condition of entrained fish larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Krs73E&md5=cc9f93eeb1a4b4bc3c48b7544350dc8bCAS |
Folkvord, A., Ystanes, L., and Moksness, E. (1996). RNA:DNA ratios and growth of herring (Clupea harengus) larvae reared in mesocosms. Marine Biology 126, 591–602.
| RNA:DNA ratios and growth of herring (Clupea harengus) larvae reared in mesocosms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntFOrurw%3D&md5=65bcab7ef0b936b1912b4eefcb6e0882CAS |
Fonseca, V. F., Vinagre, C., and Cabral, H. N. (2006). Growth variability of juvenile soles Solea solea and Solea senegalensis, and comparison with RNA:DNA ratios in the Tagus estuary, Portugal. Journal of Fish Biology 68, 1551–1562.
| Growth variability of juvenile soles Solea solea and Solea senegalensis, and comparison with RNA:DNA ratios in the Tagus estuary, Portugal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1OnsLo%3D&md5=46b6dc2ac6daba44331beac9fd5b05cdCAS |
Fuentes, C. M. (1998). Deriva de larvas de Sabalo, Prochilodus lineatus (Valenciennes, 1847) y otras especies de peces de interés comercial, en el Río Paraná Inferior. Ph.D. Thesis, Buenos Aires University, Buenos Aires, Argentina.
Fuentes, C. M., Gómez, M. I., Brown, D. R., Arcelus, A., and Espinach Ros, A. (2016). Downstream passage of fish larvae at the Salto Grande dam on the Uruguay River. River Research and Applications 32, 1879–1889.
| Downstream passage of fish larvae at the Salto Grande dam on the Uruguay River.Crossref | GoogleScholarGoogle Scholar |
Gómez, M. I., Sánchez, S., and Fuentes, C. M. (2014). Shrinkage of Prochilodus lineatus (Valenciennes, 1847) larvae preserved in either ethyl-alcohol or formalin in relation to their developmental stage and feeding condition. Journal of Applied Ichthyology 30, 140–144.
| Shrinkage of Prochilodus lineatus (Valenciennes, 1847) larvae preserved in either ethyl-alcohol or formalin in relation to their developmental stage and feeding condition.Crossref | GoogleScholarGoogle Scholar |
Gwak, W. S., Tsusaki, T., and Tanaka, M. (2003). Nutritional condition, as evaluated by RNA/DNA ratios, of hatchery-reared Japanese flounder from hatch to release. Aquaculture 219, 503–514.
| Nutritional condition, as evaluated by RNA/DNA ratios, of hatchery-reared Japanese flounder from hatch to release.Crossref | GoogleScholarGoogle Scholar |
Hopkins, K. D. (1992). Reporting fish growth: a review of the basics. Journal of the World Aquaculture Society 23, 173–179.
| Reporting fish growth: a review of the basics.Crossref | GoogleScholarGoogle Scholar |
Houde, E. D., and Zastrow, C. E. (1993). Ecosystem- and taxon-especific dynamic and energetics properties of larval fish assemblages. Bulletin of Marine Science 53, 290–335.
Hunter, J. R. (1981). Feeding ecology and predation of marine fish larvae. In ‘Marine Fish Larvae. Morphology, Ecology and Relation to Fisheries’. (Ed. R. Lasker.) pp. 33–77. (Washington Press: Seattle, WA, USA.)
Kalous, L., The Bui, A., Petrtyl, M., Bohlen, J., and Chaloupkova, P. (2012). The South American freshwater fish Prochilodus lineatus (Actinopterygii: Characiformes: Prochilodontidae): new species in Vietnamese aquaculture. Aquaculture Research 43, 955–958.
| The South American freshwater fish Prochilodus lineatus (Actinopterygii: Characiformes: Prochilodontidae): new species in Vietnamese aquaculture.Crossref | GoogleScholarGoogle Scholar |
Ma, Z., Zheng, P., Guo, H., Zhang, N., Wang, L., Jiang, S., Qin, J. G., and Zhang, D. (2015). Effect of weaning time on the performance of Trachinotus ovatus (Linnaeus 1758) larvae. Aquaculture Nutrition 21, 670–678.
| Effect of weaning time on the performance of Trachinotus ovatus (Linnaeus 1758) larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVykt7nO&md5=b0350bad8bbd4e0f49fd22c784b531b7CAS |
Malzahn, A. M., Clemmesen, C. M., and Rosenthal, H. (2003). Temperature effects on growth and nucleic acids in laboratory-reared larval coregonid fish. Marine Ecology Progress Series 259, 285–293.
| Temperature effects on growth and nucleic acids in laboratory-reared larval coregonid fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVCqurY%3D&md5=1050e283abdbb3db7317791857b5e847CAS |
McGurk, M. D., Warburton, H. D., Galbraith, M., and Kusser, W. C. (1992). RNA–DNA ratio of herring and sand lance larvae from Port Moller, Alaska: comparison with prey concentration and temperature. Fisheries Oceanography 1, 193–207.
| RNA–DNA ratio of herring and sand lance larvae from Port Moller, Alaska: comparison with prey concentration and temperature.Crossref | GoogleScholarGoogle Scholar |
Olivar, M. P., Diaz, M. V., and Chícharo, M. A. (2009). Tissue effect on RNA:DNA ratios of marine fish larvae. Scientia Marina 73, 171–182.
| Tissue effect on RNA:DNA ratios of marine fish larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVeru7zI&md5=8e6cf36d84a5e05623e4fc294ec4c9d2CAS |
Paolucci, E. M., Cataldo, D. H., Fuentes, C. M., and Boltovskoy, D. (2007). Larvae of the invasive species Limnoperna fortunei (Bivalvia) in the diet of fish larvae in the Paraná River, Argentina. Hydrobiologia 589, 219–233.
| Larvae of the invasive species Limnoperna fortunei (Bivalvia) in the diet of fish larvae in the Paraná River, Argentina.Crossref | GoogleScholarGoogle Scholar |
Pereira Maduenho, L., and Martinez, C. B. R. (2008). Acute effects of diflubenzuron on the freshwater fish Prochilodus lineatus. Comparative Biochemistry and Physiology – C. Toxicology & Pharmacology 148, 265–272.
| Acute effects of diflubenzuron on the freshwater fish Prochilodus lineatus.Crossref | GoogleScholarGoogle Scholar |
Quirós, R., and Baigún, C. (1985). Fish abundance related to organic matter in the Plata River Basin, South America. Transactions of the American Fisheries Society 114, 377–387.
| Fish abundance related to organic matter in the Plata River Basin, South America.Crossref | GoogleScholarGoogle Scholar |
Robinson, S. M., and Ware, D. (1988). Ontogenetic development of growth, rates in larval Pacific herring, Clupea harengus pallasi, measured with RNA/DNA ratios in the Strait of Georgia, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 45, 1422–1429.
| Ontogenetic development of growth, rates in larval Pacific herring, Clupea harengus pallasi, measured with RNA/DNA ratios in the Strait of Georgia, British Columbia.Crossref | GoogleScholarGoogle Scholar |
Sverlij, S. B., Espinach Ros, A., and Orti, G. (1993). Sinopsis de los datos biológicos y pesqueros del sábalo Prochilodus lineatus (Valenciennes, 1847). FAO Sinopsis sobre la Pesca 154, FAO, Rome, Italy.
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=bd9355c2ba8aeee4e167d288c0c1cbdeCAS |
Uriarte, I., and Balbontín, F. (1987). Caracterización del estado de hambruna en las larvas de sardina Sardinops sagax musica (Pisces, Clupeiformes) mediante criterios morfométricos e histológicos. Revista de Biología Marina 23, 77–106.
Winkaler, E. U., Santos, T. R. M., Machado-Neto, J. G., and Martinez, C. B. R. (2007). Acute lethal and sublethal effects of neem leaf extract on the neotropical freshwater fish Prochilodus lineatus. Comparative Biochemistry and Physiology – C. Toxicology & Pharmacology 145, 236–244.
| Acute lethal and sublethal effects of neem leaf extract on the neotropical freshwater fish Prochilodus lineatus.Crossref | GoogleScholarGoogle Scholar |
Yandi, I., and Altinok, I. (2015). Defining the starvation potential and the influence on RNA/DNA ratios in horse mackerel (Trachurus mediterraneus) larvae. Helgoland Marine Research 69, 25–35.
| Defining the starvation potential and the influence on RNA/DNA ratios in horse mackerel (Trachurus mediterraneus) larvae.Crossref | GoogleScholarGoogle Scholar |