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Ontogenetic shift in the energy allocation strategy and physiological condition of larval plaice (Pleuronectes platessa)


Autoři: Julien Di Pane aff001;  Léa Joly aff001;  Philippe Koubbi aff002;  Carolina Giraldo aff001;  Sébastien Monchy aff003;  Eric Tavernier aff003;  Paul Marchal aff001;  Christophe Loots aff001
Působiště autorů: IFREMER, Channel and North Sea Fisheries Research Unit, Boulogne-sur-Mer, France aff001;  UFR 918 « Terre, Environnement, Biodiversité », Sorbonne Université, Paris, France aff002;  LOG—Laboratoire d’Océanologie et Géosciences, Wimereux, France aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222261

Souhrn

Condition indices aim to evaluate the physiological status of fish larvae by estimating both the level of starvation and potential of survival. Histological indices reveal direct effects of starvation whereas biochemical indices such as lipid classes or RNA:DNA ratios are used as proxies of condition, giving information on the amount of energy reserves and growth rate, respectively. We combined these three indices to evaluate ontogenetic variations of growth performance, lipid dynamics and nutritional condition of plaice larvae caught in the field during winter 2017 in the eastern English Channel and the Southern Bight of the North Sea. RNA:DNA ratios showed that larvae at the beginning of metamorphosis (stage 4) had a lower growth rate than younger individuals (stages 2 and 3). A significant increase in the proportion of triglycerides also occurred at stage 4, indicating energy storage. Histological indices indicated that most of the larvae were in good condition, even younger ones with low lipid reserves. There was, however, an increase in the proportion of healthy individuals over ontogeny, especially with respect to liver vacuoles which were larger and more numerous for stage 4 larvae. Combined together, these condition indices revealed the ontogenetic shift in the energy allocation strategy of plaice larvae. Young larvae (stages 2 and 3) primarily allocate energy towards somatic growth. The decrease in growth performance for stage 4 was not related to poor condition, but linked to a higher proportion of energy stored as lipids. Since the quantity of lipid reserves is particularly important for plaice larvae to withstand starvation during metamorphosis, this could be considered as a second critical period after the one of exogenous feeding for larval survival and recruitment success.

Klíčová slova:

Biology and life sciences – Cell biology – Biochemistry – Developmental biology – Anatomy – Medicine and health sciences – Cellular structures and organelles – Zoology – Nutrition – Lipids – Life cycles – Larvae – Fish biology – Fish physiology – Animal physiology – Vertebrate physiology – Metamorphosis – Fish metamorphosis – Vacuoles – Histology – Malnutrition – Starvation


Zdroje

1. Houde ED. Emerging from Hjort’s Shadow. J Northwest Atl Fish Sci 2008;41:53–70. doi: 10.2960/J.v41.m634

2. Somarakis S, Tsoukali S, Giannoulaki M, Schismenou E, Nikolioudakis N. Spawning stock, egg production and larval survival in relation to small pelagic fish recruitment. Mar Ecol Prog Ser 2017. doi: 10.3354/meps12328

3. Hjort J. Fluctuations in the great fisheries of Northern Europe viewed in the light of biological research 1914. https://brage.bibsys.no/xmlui/handle/11250/109177 (accessed May 7, 2019).

4. Cushing DH. Plankton Production and Year-class Strength in Fish Populations: an Update of the Match/Mismatch Hypothesis. In: Southward JHSB and AJ, editor. Adv. Mar. Biol., vol. 26, Academic Press; 1990, p. 249–93.

5. Iles TD, Sinclair M. Atlantic Herring: Stock Discreteness and Abundance. Science 1982;215:627–33. doi: 10.1126/science.215.4533.627 17842372

6. Bakun A. Ocean triads and radical interdecadal variation: bane and boon to scientific fisheries management | SpringerLink 1998. https://link.springer.com/chapter/10.1007/978-94-011-4433-9_25 (accessed February 2, 2019).

7. Anderson JT. A review of size-dependent survival during pre-recruit stages of fishes in relation to recruitment. J Northwest Atl Fish Sci 1988:55–66.

8. Le Pape OL, Bonhommeau S. The food limitation hypothesis for juvenile marine fish. Fish Fish 2015;16:373–98. doi: 10.1111/faf.12063

9. Sogard SM. Size-Selective Mortality in the Juvenile Stage of Teleost Fishes: A Review 1997. https://www.ingentaconnect.com/content/umrsmas/bullmar/1997/00000060/00000003/art00029 (accessed January 31, 2019).

10. Vigliola L, Harmelin-Vivien ML, Biagi F, Galzin R, Garcia-Rubies A, Harmelin J-G, et al. Spatial and temporal patterns of settlement among sparid fishes of the genus Diplodus in the northwestern Mediterranean. Mar Ecol Prog Ser 1998;168:45–56. doi: 10.3354/meps168045

11. Planes S, Romans P. Evidence of genetic selection for growth in new recruits of a marine fish. Mol Ecol 2004;13:2049–60. doi: 10.1111/j.1365-294X.2004.02202.x 15189225

12. Nagelkerken I, Sheaves M, Baker R, Connolly RM. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish Fish 2015;16:362–71. doi: 10.1111/faf.12057

13. Ahlstrom EH, Herpetologists AS of I and, States U. Ontogeny and systematics of fishes: based on an international symposium dedicated to the memory of Elbert Halvor Ahlstrom /. [New York?]: American Society of Ichthyologists and Herpetologists,; 1984.

14. Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, et al. The Identification, Conservation, and Management of Estuarine and Marine Nurseries for Fish and InvertebratesA better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. BioScience 2001;51:633–41. doi: 10.1641/0006-3568(2001)051[0633:TICAMO]2.0.CO;2

15. van Beek FA, Rijnsdorp AD, de Clerck R. Monitoring juvenile stocks of flatfish in the Wadden Sea and the coastal areas of the southeastern North Sea. Helgoländer Meeresunters 1989;43:461–77. doi: 10.1007/BF02365904

16. Hufnagl M, Peck MA, Nash RDM, Pohlmann T, Rijnsdorp AD. Changes in potential North Sea spawning grounds of plaice (Pleuronectes platessa L.) based on early life stage connectivity to nursery habitats. J Sea Res 2013;84:26–39. doi: 10.1016/j.seares.2012.10.007

17. Barbut L, Grego CG, Delerue‐Ricard S, Vandamme S, Volckaert FAM, Lacroix G. How larval traits of six flatfish species impact connectivity. Limnol Oceanogr 2019;0. doi: 10.1002/lno.11104

18. Beverton RJH. Spatial limitation of population size; The concentration hypothesis. Neth J Sea Res 1995;34:1–6. doi: 10.1016/0077-7579(95)90010-1

19. Nash RDM, Geffen AJ. The influence of nursery ground processes in the determination of year-class strength in juvenile plaice Pleuronectes platessa L. in Port Erin Bay, Irish Sea. J Sea Res 2000;44:101–10. doi: 10.1016/S1385-1101(00)00044-7

20. van der Veer HW, Berghahn R, Miller JM, Rijnsdorp AD. Recruitment in flatfish, with special emphasis on North Atlantic species: Progress made by the Flatfish Symposia. ICES J Mar Sci 2000;57:202–15. doi: 10.1006/jmsc.1999.0523

21. Petitgas P, Rijnsdorp AD, Dickey-Collas M, Engelhard GH, Peck MA, Pinnegar JK, et al. Impacts of climate change on the complex life cycles of fish. Fish Oceanogr 2013;22:121–39. doi: 10.1111/fog.12010

22. Levin PS, Stunz GW. Habitat triage for exploited fishes: Can we identify essential “Essential Fish Habitat?” Estuar Coast Shelf Sci 2005;64:70–8. doi: 10.1016/j.ecss.2005.02.007

23. van der Veer HW, Witte JIJ. The “maximum growth/optimal food condition” hypothesis: a test for 0-group plaice Pleuronectes platessa in the Dutch Wadden Sea. Mar Ecol Prog Ser 1993;101:81–90.

24. Gibson RN. Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Neth J Sea Res 1994;32:191–206. doi: 10.1016/0077-7579(94)90040-X

25. Craig JK, Rice JA, Crowder LB, Nadeau DA. Density-dependent growth and mortality in an estuary-dependent fish: an experimental approach with juvenile spot Leiostomus xanthurus. Mar Ecol Prog Ser 2007;343:251–62. doi: 10.3354/meps06864

26. Nash RDM, Geffen AJ. The influence of nursery ground processes in the determination of year-class strength in juvenile plaice Pleuronectes platessa L. in Port Erin Bay, Irish Sea. J Sea Res 2000;44:101–10. doi: 10.1016/S1385-1101(00)00044-7

27. Nash RDM, Geffen AJ, Burrows MT, Gibson RN. Dynamics of shallow-water juvenile flatfish nursery grounds: application of the self-thinning rule. Mar Ecol Prog Ser 2007;344:231–44. doi: 10.3354/meps06933

28. Fonds M, Cronie R, Vethaak AD, Van Der Puyl P. Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and flounder (Platichthys flesus) in relation to fish size and temperature. Neth J Sea Res 1992;29:127–43. doi: 10.1016/0077-7579(92)90014-6

29. Ciotti BJ, Targett TE, Nash RDM, Batty RS, Burrows MT, Geffen AJ. Development, validation and field application of an RNA-based growth index in juvenile plaice Pleuronectes platessa. J Fish Biol 2010;77:2181–209. doi: 10.1111/j.1095-8649.2010.02786.x 21155778

30. Selleslagh J, Amara R. Effect of starvation on condition and growth of juvenile plaice Pleuronectes platessa: nursery habitat quality assessment during the settlement period. J Mar Biol Assoc U K 2013;93:479–88. doi: 10.1017/S0025315412000483

31. Wennhage H, Gibson RN. Influence of food supply and a potential predator (Crangon crangon) on settling behaviour of plaice (Pleuronectes platessa). J Sea Res 1998;39:103–12. doi: 10.1016/S1385-1101(97)00011-7

32. Veer HW van der, Freitas V, Koot J, Witte JI, Zuur AF. Food limitation in epibenthic species in temperate intertidal systems in summer: analysis of 0-group plaice Pleuronectes platessa. Mar Ecol Prog Ser 2010;416:215–27. doi: 10.3354/meps08786

33. Ferron A, Leggett WC. An Appraisal of Condition Measures for Marine Fish Larvae*. In: Southward JHSB and AJ, editor. Adv. Mar. Biol., vol. 30, Academic Press; 1994, p. 217–303.

34. Gisbert E, Ortiz-Delgado JB, Sarasquete C. Nutritional cellular biomarkers in early life stages of fish. Histol Histopathol 2008.

35. O’Connell CP. Histological criteria for diagnosing the starving condition in early post yolk sac larvae of the northern anchovy, Engraulis mordax Girard. J Exp Mar Biol Ecol 1976;25:285–312. doi: 10.1016/0022-0981(76)90130-1

36. Theilacker GH, Watanabe Y. Midgut Cell Height Defines Nutritional Status of Laboratory Raised Larval Northern Anchovy,. Fish Bull 1989;87:457–69.

37. Koubbi P, Vallet C, Razouls S, Grioche A, Hilde D, Courcot L, et al. Condition and diet of larval Pleuragramma antarcticum (Nototheniidae) from Terre Adélie (Antarctica) during summer. Cybium 2007;31:67–76.

38. Diaz MV, Olivar MP, Macchi GJ. Larval condition of Merluccius hubbsi (Marini, 1933) in the northern Patagonian spawning ground. Fish Res 2014;160:60–8. doi: 10.1016/j.fishres.2013.11.009

39. Clemmesen CM. Laboratory studies on RNA/DNA ratios of starved and fed herring (Clupea harengus) and turbot (Scophthalmus maximus) larvae. J Cons 1987;43:122–8. doi: 10.1093/icesjms/43.2.122

40. Robinson SMC, Ware DM. Ontogenetic Development of Growth Rates in Larval Pacific Herrings, Clupea harengus pallasi, Measured with RNA–DNA Ratios in the Strait of Georgia, British Columbia. Can J Fish Aquat Sci 1988;45:1422–9. doi: 10.1139/f88-166

41. Buckley LJ. Relationships Between RNA–DNA Ratio, Prey Density, and Growth Rate in Atlantic Cod (Gadus morhua) Larvae. J Fish Res Board Can 1979;36:1497–502. doi: 10.1139/f79-217

42. Buckley L, Caldarone E, Ong T-L. RNA—DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. In: Zehr JP, Voytek MA, editors. Mol. Ecol. Aquat. Communities, Springer Netherlands; 1999, p. 265–77. doi: 10.1007/978-94-011-4201-4_20

43. Clemmesen C. The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Mar Biol 1994;118:377–82. doi: 10.1007/BF00350294

44. Caldarone EM. Estimating growth in haddock larvae Melanogrammus aeglefinus from RNA:DNA ratios and water temperature. Mar Ecol Prog Ser 2005;293:241–52. doi: 10.3354/meps293241

45. Foley CJ, Bradley DL, Höök TO. A review and assessment of the potential use of RNA:DNA ratios to assess the condition of entrained fish larvae. Ecol Indic 2016;60:346–57. doi: 10.1016/j.ecolind.2015.07.005

46. Denis J, Mahe K, Tavernier E, Monchy S, Vincent D, Vallet C, et al. Ontogenetic changes in the larval condition of Downs herring: use of a multi-index approach at an individual scale. Mar Biol 2017;164:154. doi: 10.1007/s00227-017-3180-3

47. Diaz MV, Gómez MI, Sánchez S, Fuentes CM. Ontogenetic changes in DNA and RNA content of laboratory-reared Prochilodus lineatus larvae: use of RNA/DNA ratios as indicators of nutritional condition. Mar Freshw Res 2018. doi: 10.1071/MF17178

48. Meyer S, Caldarone EM, Chícharo MA, Clemmesen C, Faria AM, Faulk C, et al. On the edge of death: Rates of decline and lower thresholds of biochemical condition in food-deprived fish larvae and juveniles. J Mar Syst 2012;93:11–24. doi: 10.1016/j.jmarsys.2011.09.010

49. Ehrlich KF. Chemical Changes during Growth and Starvation of Herring Larvae. In: Sc JHSBMA D, editor. Early Life Hist. Fish, Springer Berlin Heidelberg; 1974, p. 301–23. doi: 10.1007/978-3-642-65852-5_26

50. Ehrlich KF. Chemical changes during growth and starvation of larval Pleuronectes platessa. Mar Biol 1974;24:39–48. doi: 10.1007/BF00402845

51. Giraldo C, Boutoute M, Mayzaud P, Tavernier E, Quang AV, Koubbi P. Lipid dynamics in early life stages of the icefish Chionodraco hamatus in the Dumont d’Urville Sea (East Antarctica). Polar Biol 2016:1–8. doi: 10.1007/s00300-016-1956-4

52. Lazo JP, Darias MJ, Gisbert E. Ontogeny of the Digestive Tract. Larval Fish Nutr., John Wiley & Sons, Ltd; 2011, p. 3–46. doi: 10.1002/9780470959862.ch1

53. Enes P, Panserat S, Kaushik S, Oliva-Teles A. Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 2009;35:519–39. doi: 10.1007/s10695-008-9259-5 18791853

54. Deplano M, Diaz JP, Connes R, Kentouri-Divanach M, Cavalier F. Appearance of lipid-absorption capacities in larvae of the sea bass Dicentrarchus labrax during transition to the exotrophic phase. Mar Biol 1991;108:361–71. doi: 10.1007/BF01313645

55. Segner H, Storch V, Reinecke M, Kloas W, Hanke W. The development of functional digestive and metabolic organs in turbot, Scophthalmus maximus. Mar Biol 1994;119:471–86. doi: 10.1007/BF00347544

56. Giraldo C, Cherel Y, Vallet C, Mayzaud P, Tavernier E, Moteki M, et al. Ontogenic changes in the feeding ecology of the early life stages of the Antarctic silverfish (Pleuragramma antarcticum) documented by stable isotopes and diet analysis in the Dumont d’Urville Sea (East Antarctica). Polar Sci 2011;5:252–63. doi: 10.1016/j.polar.2011.04.004

57. Costalago D, Tecchio S, Palomera I, Álvarez-Calleja I, Ospina-Álvarez A, Raicevich S. Ecological understanding for fishery management: Condition and growth of anchovy late larvae during different seasons in the Northwestern Mediterranean. Estuar Coast Shelf Sci 2011;93:350–8. doi: 10.1016/j.ecss.2011.05.005

58. Peters J, Diekmann R, Clemmesen C, Hagen W. Lipids as a proxy for larval starvation and feeding condition in small pelagic fish: a field approach on match-mismatch effects on Baltic sprat. Mar Ecol Prog Ser 2015;531:277–92. doi: 10.3354/meps11292

59. Ackman RG. Marine Biogenic Lipids, Fats & Oils. CRC Press; 1989. doi: 10.1016/j.plefa.2016.02.004

60. Sargent JR, Whittle KJ. Lipids and hydrocarbons in the marine food web 1981.

61. Hâkanson JL. Analysis of lipid components for determining the condition of anchovy larvae, Engraulis mordax. Mar Biol 1989;102:143–51. doi: 10.1007/BF00428274

62. Fraser AJ, Gamble JC, Sargent JR. Changes in lipid content, lipid class composition and fatty acid composition of developing eggs and unfed larvae of cod (Gadus morhua). Mar Biol 1988;99:307–13. doi: 10.1007/BF02112122

63. Giraldo C. Ecologie trophique du poisson Pleuragramma antarcticum dans l’Est Antarctique. Paris 6; 2012.

64. Shelbourne JE. The feeding and condition of plaice larvae in good and bad plankton patches. J Mar Biol Assoc U K 1957;36:539–52. doi: 10.1017/S0025315400025832

65. Ryland JS. Observations on the Development of Larvae of the Plaice, Pleuronectes platessa L., in Aquaria. J Cons 1966;30:177–95. doi: 10.1093/icesjms/30.2.177

66. Yandi I, Altinok I. Defining the starvation potential and the influence on RNA/DNA ratios in horse mackerel (Trachurus mediterraneus) larvae. Helgol Mar Res 2015;69:25–35. doi: 10.1007/s10152-014-0414-3

67. Buckley L, Caldarone E, Clemmesen C. Multi-species larval fish growth model based on temperature and fluorometrically derived RNA/DNA ratios: results from a meta-analysis. Mar Ecol Prog Ser 2008;371:221–32. doi: 10.3354/meps07648

68. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497–509. 13428781

69. Martoja R, Martoja-Pierson M. Initiation aux techniques de l’histologie animale 1967.

70. Theilacker G. Starvation-induced mortality of young sea-caught jack mackerel, Trachurus symmetricus, determined with histological and morphological methods. Fish Bull 1986;84:17.

71. Margulies D. Assessment of the nutritional condition of larval and early juvenile tuna and Spanish mackerel (Pisces: Scombridae) in the Panamá Bight. Mar Biol 1993;115:317–30. doi: 10.1007/BF00346350

72. Yúfera M, Pascual E, Polo A, Sarasquete MC. Effect of starvation on the feeding ability of gilthead seabream (Sparus aurata L.) larvae at first feeding. J Exp Mar Biol Ecol 1993;169:259–72. doi: 10.1016/0022-0981(93)90196-U

73. McFadzen IRB, Coombs SH, Halliday NC. Histological indices of the nutritional condition of sardine, Sardina pilchardus (Walbaum) larvae off the north coast of Spain. J Exp Mar Biol Ecol 1997;212:239–58. doi: 10.1016/S0022-0981(96)02755-4

74. Sieg A. A study on the histological classification of the in situ nutritional condition of larval south-west Atlantic anchovy, Engraulis anchoita Hubbs and Marini, 1935. Oceanogr Lit Rev 1998;9:1693–4.

75. Catalán I, Olivar M, Palomera I, Berdalet E. Link between environmental anomalies, growth and condition of pilchard Sardina pilchardus larvae in the northwestern Mediterranean. Mar Ecol Prog Ser 2006;307:219–31. doi: 10.3354/meps307219

76. Diaz MV, Arano MF, Pájaro M, Aristizábal EO, Macchi GJ, Diaz MV, et al. The use of morphological and histological features as nutritional condition indices of Pagrus pagrus larvae. Neotropical Ichthyol 2013;11:649–60. doi: 10.1590/S1679-62252013000300018

77. Silva L, Moyano M, Illing B, Faria AM, Garrido S, Peck MA. Ontogeny of swimming capacity in plaice (Pleuronectes platessa) larvae. Mar Biol 2015;162:753–61. doi: 10.1007/s00227-015-2621-0

78. Fernández‐Díaz C, Yýfera M, Cañavate JP, Moyano FJ, Alarcón FJ, Díaz M. Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory. J Fish Biol 2001;58:1086–97. doi: 10.1111/j.1095-8649.2001.tb00557.x

79. Chambers RC, Leggett WC. Event Analysis Applied to Timing in Marine Fish Ontogeny. Can J Fish Aquat Sci 1989;46:1633–41. doi: 10.1139/f89-208

80. Benoît HP, Pepin P. Individual variability in growth rate and the timing of metamorphosis in yellowtail flounder Pleuronectes ferrugineus. Mar Ecol Prog Ser 1999;184:231–44. doi: 10.3354/meps184231

81. Benoît HP, Pepin P, Brown JA. Patterns of metamorphic age and length in marine fishes, from individuals to taxa. Can J Fish Aquat Sci 2000;57:856–69. doi: 10.1139/f00-019

82. Comerford S, Brophy D, Fox CJ, Taylor N, Veer HW van der, Nash RDM, et al. Temperature effect on growth and larval duration of plaice Pleuronectes platessa in three regions of the Northeast Atlantic. Mar Ecol Prog Ser 2013;476:215–26. doi: 10.3354/meps10118

83. Christensen MN, Korsgaard B. Protein metabolism, growth and pigmentation patterns during metamorphosis of plaice (Pleuronectes platessa) larvae. J Exp Mar Biol Ecol 1999;237:225–41. doi: 10.1016/S0022-0981(98)00215-9

84. Amara R, Paul C. Seasonal patterns in the fish and epibenthic crustaceans community of an intertidal zone with particular reference to the population dynamics of plaice and brown shrimp. Estuar Coast Shelf Sci 2003;56:807–18. doi: 10.1016/S0272-7714(02)00315-3

85. Hovenkamp F. Growth-dependent mortality of larval plaice Pleuronectes platessa in the North Sea. Mar Ecol Prog Ser 1992;82:95–101.

86. Houde ED. Patterns and trends in larval-stage growth and mortality of teleost fish*. J Fish Biol 1997;51:52–83. doi: 10.1111/j.1095-8649.1997.tb06093.x

87. Bailey KM, Houde ED. Predation on Eggs and Larvae of Marine Fishes and the Recruitment Problem. In: Southward JHSB and AJ, editor. Adv. Mar. Biol., vol. 25, Academic Press; 1989, p. 1–83.

88. Pepin P. Effect of Temperature and Size on Development, Mortality, and Survival Rates of the Pelagic Early Life History Stages of Marine Fish. Can J Fish Aquat Sci 1991;48:503–18. doi: 10.1139/f91-065

89. Pepin P. Death from near and far: alternate perspectives on size-dependent mortality in larval fish. ICES J Mar Sci 2016;73:196–203. doi: 10.1093/icesjms/fsv160

90. Brewster B. Eye migration and cranial development during flatfish metamorphosis: a reappraisal (Teleostei: Pleuronectiformes). J Fish Biol 1987;31:805–33. doi: 10.1111/j.1095-8649.1987.tb05281.x

91. Riley JD. Marine Fish Culture in BritainVII. Plaice (Pleuronectes platessa L.) Post-larval Feeding on Artemia salina L. Nauplii and the Effects of Varying Feeding Levels. ICES J Mar Sci 1966;30:204–21. doi: 10.1093/icesjms/30.2.204

92. Geffen AJ, van der Veer HW, Nash RDM. The cost of metamorphosis in flatfishes. J Sea Res 2007;58:35–45. doi: 10.1016/j.seares.2007.02.004

93. Rønnestad I, Yúfera M, Ueberschär B, Ribeiro L, Sæle Ø, Boglione C. Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquac 2013;5:S59–98. doi: 10.1111/raq.12010

94. Infante MFLJLZ, Gisbert E, Sarasquete C, Navarro I, Cahu JG and CL. Ontogeny and Physiology of the Digestive System of. Feed Dig Funct Fishes 2008. doi: 10.1201/b10749-8


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