Abstract
Coastal habitats play a key role in the early life stages of flatfish species, with the quantity and quality of the food they supply being central. However, survival and sufficient development until metamorphosis depend upon obtaining certain essential long-chain polyunsaturated fatty acids (LC-PUFAs). We focused this literature review on flatfish requirements, supplies and availability of three most important LC-PUFAs: DHA (docosahexaenoic acid; 22:6n-3), EPA (eicosapentaenoic acid; 20:5n-3) and ARA (arachidonic acid; 20:4n-6). First, based on aquaculture research, we summarize their importance for larval development and highlight that Solea spp. are the only marine flatfish known to synthesize DHA, which influences their LC-PUFA requirements. Second, analysis of published LC-PUFA contents in the flatfish larvae prey indicates that they most likely cannot synthesize essential LC-PUFA. They show large differences in DHA and EPA content between species, study sites, feeding environments and developmental stages. Third, LC-PUFA contents of phytoplankton, as the main source of essential LC-PUFAs for the prey of flatfish larvae, vary with species, seasons, nutrient availabilities and temperature. However, flatfish larvae prey probably overcome some limiting conditions by targeting species with high LC-PUFA contents through preferential assimilation and/or selective feeding on prey quality as done by flatfish larvae at a higher trophic level. Fourth, in the scarcity of available data, we propose future research avenues. One of them could investigate relations between availability of LC-PUFAs and plankton biodiversity, which appears to be key in meeting flatfish larvae requirements in coastal habitats and may be influenced by the current increasing human pressure.
Similar content being viewed by others
Data Availability
The datasets analyzed during the current study are drawn from numerous previously published articles.
References
Acuña JL, Anadón R (1992) Appendicularian assemblages in a shelf area and their relationship with temperature. J Plankton Res 14:1233–1250. https://doi.org/10.1093/plankt/14.9.1233
Acuña JL, Bedo AW, Harris RP, Anadón R (1995) The seasonal succession of appendicularians (Tunicata: Appendicularia) off Plymouth. J Mar Biol Assoc U K 75:755–758. https://doi.org/10.1017/S0025315400039187
Albaina A, Irigoien X (2007) Fine scale zooplankton distribution in the Bay of Biscay in spring 2004. J Plankton Res 29:851–870. https://doi.org/10.1093/plankt/fbm064
Álvarez E, Moyano M, López-Urrutia Á, Nogueira E, Scharek R (2014) Routine determination of plankton community composition and size structure: a comparison between FlowCAM and light microscopy. J Plankton Res 36:170–184. https://doi.org/10.1093/plankt/fbt069
Amara R, Laffargue P, Dewarumez JM, Maryniak C, Lagardere F, Luzac C (2001) Feeding ecology and growth of 0-group flatfish (sole, dab and plaice) on a nursery ground (Southern Bight of the North Sea). J Fish Biol 58:788–803. https://doi.org/10.1111/j.1095-8649.2001.tb00531.x
Anderson TR, Pond DW (2000) Stoichiometric theory extended to micronutrients: comparison of the roles of essential fatty acids, carbon, and nitrogen in the nutrition of marine copepods. Limnol Oceanogr 45:1162–1167. https://doi.org/10.4319/lo.2000.45.5.1162
Aranda-Burgos JA, da Costa F, Nóvoa S, Ojea J, Martínez-Patiño D (2014) Effects of microalgal diet on growth, survival, biochemical and fatty acid composition of Ruditapes decussatus larvae. Aquaculture 420–421:38–48. https://doi.org/10.1016/j.aquaculture.2013.10.032
Barbut L, Crego CG, Delerue-Ricard S, Vandamme S, Volckaert FAM, Lacroix G (2019) How larval traits of six flatfish species impact connectivity. Limnol Oceanogr 64:1150–1171. https://doi.org/10.1002/lno.11104
Beaugrand G, Ibañez F, Reid P (2000) Spatial, seasonal and long-term fluctuations of plankton in relation to hydroclimatic features in the English Channel, Celtic Sea and Bay of Biscay. Mar Ecol Prog Ser 200:93–102. https://doi.org/10.3354/meps200093
Beaugrand G, Ibañez F, Lindley JA (2001) Geographical distribution and seasonal and diel changes in the diversity of calanoid copepods in the North Atlantic and North Sea. Mar Ecol Prog Ser 219:189–203. https://doi.org/10.3354/meps219189
Bell JG, Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218:491–499. https://doi.org/10.1016/S0044-8486(02)00370-8
Bell MV, Dick JR, Anderson TR, Pond DW (2007) Application of liposome and stable isotope tracer techniques to study polyunsaturated fatty acid biosynthesis in marine zooplankton. J Plankton Res 29:417–422. https://doi.org/10.1093/plankt/fbm025
Bhaud M (1972) Quelques données sur le déterminisme écologique de la reproduction des annélides polychètes. Mar Biol 17:115–136. https://doi.org/10.1007/BF00347302
Boglino A, Darias MJ, Estévez A, Andree KB, Gisbert E (2012) The effect of dietary arachidonic acid during the Artemia feeding period on larval growth and skeletogenesis in Senegalese sole, Solea senegalensis: effects of arachidonic acid in sole bone. J Appl Ichthyol 28:411–418. https://doi.org/10.1111/j.1439-0426.2012.01977.x
Boglino A, Wishkerman A, Darias MJ, Andree KB, de la Iglesia P, Estévez A, Gisbert E (2013) High dietary arachidonic acid levels affect the process of eye migration and head shape in pseudoalbino Senegalese sole Solea senegalensis early juveniles: Ara impairs eye migration in Solea senegalensis. J Fish Biol 83:1302–1320. https://doi.org/10.1111/jfb.12230
Boglino A, Wishkerman A, Darias MJ, de la Iglesia P, Estévez A, Andree KB, Gisbert E (2014) The effects of dietary arachidonic acid on Senegalese sole morphogenesis: a synthesis of recent findings. Aquaculture 432:443–452. https://doi.org/10.1016/j.aquaculture.2014.05.007
Breteler WCMK, Schogt N, Rampen S (2005) Effect of diatom nutrient limitation on copepod development: role of essential lipids. Mar Ecol Prog Ser 291:125–133. https://doi.org/10.3354/meps291125
Cabral HN (2000) Comparative feeding ecology of sympatric Solea solea and S. senegalensis, within the nursery areas of the Tagus estuary. Portugal J Fish Biol 57:1550–1562. https://doi.org/10.1111/j.1095-8649.2000.tb02231.x
Cavallo A, Peck LS (2020) Lipid storage patterns in marine copepods: environmental, ecological, and intrinsic drivers. ICES J Mar Sci 77:1589–1601. https://doi.org/10.1093/icesjms/fsaa070
Chambers RC, Witting DA, Lewis SJ (2001) Detecting critical periods in larval flatfish populations. J Sea Res 45:231–242. https://doi.org/10.1016/S1385-1101(01)00058-2
Cotonnec G (2001) Nutritive value and selection of food particles by copepods during a spring bloom of Phaeocystis sp. in the English Channel, as determined by pigment and fatty acid analyses. J Plankton Res 23:693–703. https://doi.org/10.1093/plankt/23.7.693
Cowles TJ, Olson RJ, Chisholm SW (1988) Food selection by copepods: discrimination on the basis of food quality. Mar Biol 100:41–49. https://doi.org/10.1007/BF00392953
Crowder LB (1985) Optimal foraging and feeding mode shifts in fishes. Environ Biol Fish 12:57–62. https://doi.org/10.1007/BF00007710
Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. In: Blaxter JHS, Southward A.J (eds) Advances in marine biology. Academic Press, pp 249–293
Da Costa F, Nóvoa S, Ojea J, Martínez-Patiño D (2012) Effects of algal diets and starvation on growth, survival and fatty acid composition of Solen marginatus (Bivalvia: Solenidae) larvae. Sci Mar 76:527–537. https://doi.org/10.3989/scimar.03470.18A
Da Costa F, Nóvoa S, Ojea J, Martínez-Patiño D (2013) Biochemical and fatty acid dynamics during larval development in the razor clam Ensis arcuatus (Bivalvia: Pharidae). Aquac Res 44:1926–1939. https://doi.org/10.1111/j.1365-2109.2012.03197.x
Da Costa F, Robert R, Quéré C, Wikfors GH, Soudant P (2015) Essential Fatty Acid Assimilation and Synthesis in Larvae of the Bivalve Crassostrea gigas. Lipids 50:503–511. https://doi.org/10.1007/s11745-015-4006-z
Dahlgren CP, Kellison GT, Adams AJ, Gillanders BM, Kendall MS, Layman CA, Ley JA, Nagelkerken I, Serafy JE (2006) Marine nurseries and effective juvenile habitats: concepts and applications. Mar Ecol Prog Ser 312:291–295. https://doi.org/10.3354/meps312291
Dâmaso-Rodrigues ML, Pousão-Ferreira P, Ribeiro L, Coutinho J, Bandarra NM, Gavaia PJ, Narciso L, Morais S (2010) Lack of essential fatty acids in live feed during larval and post-larval rearing: effect on the performance of juvenile Solea senegalensis. Aquac Int 18:741–757. https://doi.org/10.1007/s10499-009-9296-9
De Figueiredo GM, Nash RDM, Montagnes DJS (2005) The role of the generally unrecognised microprey source as food for larval fish in the Irish Sea. Mar Biol 148:395–404. https://doi.org/10.1007/s00227-005-0088-0
Deibel D, Cavaletto J, Riehl M, Gardner W (1992) Lipid and lipid class content of the pelagic tunicate Oikopleura vanhoeffeni. Mar Ecol Prog Ser 88:297–302. https://doi.org/10.3354/meps088297
Déniel C (1974) Régime alimentaire des jeunes turbots Scophthalmus maximus L. de la classe 0 dans leur milieu naturel. Cah Biol Mar XV:551–556
Dessier A, Bustamante P, Chouvelon T, Huret M, Pagano M, Marquis E, Rousseaux F, Pignon-Mussaud C, Mornet F, Bréret M, Dupuy C (2018) The spring mesozooplankton variability and its relationship with hydrobiological structure over year-to-year changes (2003–2013) in the southern Bay of Biscay (Northeast Atlantic). Prog Oceanogr 166:76–87. https://doi.org/10.1016/j.pocean.2018.04.011
Duffy-Anderson JT, Bailey KM, Cabral HN, Nakata H, van der Veer HW (2014) The planktonic stages of flatfishes: physical and biological interactions in transport processes. In: Gibson RN, Nash RDM, Geffen AJ, van der Veer HW (eds) Flatfishes: biology and exploitation. Wiley, Chichester, pp 132–170
Ellis T, Gibson R (1995) Size-selective predation of 0-group flatfishes on a Scottish coastal nursery ground. Mar Ecol Prog Ser 127:27–37. https://doi.org/10.3354/meps127027
Estévez A, Kanazawa A (1995) Effect of (n-3) PUFA and vitamin A Artemia enrichment on pigmentation success of turbot, Scophthalmus maximus (L). Aquac Nutr 1:159–168. https://doi.org/10.1111/j.1365-2095.1995.tb00040.x
Estévez A, McEvoy LA, Bell JG, Sargent JR (1999) Growth, survival, lipid composition and pigmentation of turbot (Scophthalmus maximus) larvae fed live-prey enriched in Arachidonic and Eicosapentaenoic acids. Aquaculture 180:321–343. https://doi.org/10.1016/S0044-8486(99)00209-4
Evjemo JO, Reitan KI, Olsen Y (2003) Copepods as live food organisms in the larval rearing of halibut larvae (Hippoglossus hippoglossus L.) with special emphasis on the nutritional value. Aquaculture 227:191–210. https://doi.org/10.1016/S0044-8486(03)00503-9
Evjemo JO, Tokle N, Vadstein O, Olsen Y (2008) Effect of essential dietary fatty acids on egg production and hatching success of the marine copepod Temora longicornis. J Exp Mar Biol Ecol 365:31–37. https://doi.org/10.1016/j.jembe.2008.07.032
Fanjul A, Villate F, Uriarte I, Iriarte A, Atkinson A, Cook K (2017) Zooplankton variability at four monitoring sites of the Northeast Atlantic Shelves differing in latitude and trophic status. J Plankton Res 39:891–909. https://doi.org/10.1093/plankt/fbx054
Fanjul A, Iriarte A, Villate F, Uriarte I, Atkinson A, Cook K (2018) Zooplankton seasonality across a latitudinal gradient in the Northeast Atlantic Shelves Province. Cont Shelf Res 160:49–62. https://doi.org/10.1016/j.csr.2018.03.009
Félix PM, Vinagre C, Cabral HN (2011) Life-history traits of flatfish in the Northeast Atlantic and Mediterranean Sea. J Appl Ichthyol 27:100–111. https://doi.org/10.1111/j.1439-0426.2010.01623.x
Fernández-Reiriz MJ, Pérez-Camacho A, Peteiro LG, Labarta U (2011) Growth and kinetics of lipids and fatty acids of the clam Venerupis pullastra during larval development and postlarvae. Aquac Nutr 17:13–23. https://doi.org/10.1111/j.1365-2095.2009.00701.x
Franco-Santos RM, Auel H, Boersma M, Troch MD, Graeve M, Meunier CL, Niehoff B (2019) You are not always what you eat—fatty acid bioconversion and lipid homeostasis in the larvae of the sand mason worm Lanice conchilega. PLoS ONE 14:e0218015. https://doi.org/10.1371/journal.pone.0218015
Fuiman LA, Faulk CK (2013) Batch spawning facilitates transfer of an essential nutrient from diet to eggs in a marine fish. Biol Lett 9:20130593. https://doi.org/10.1098/rsbl.2013.0593
Furuita H, Takeuchi T, Uematsu K (1998) Effects of eicosapentaenoic and docosahexaenoic acids on growth, survival and brain development of larval Japanese flounder Paralichthys olivaceus. Aquaculture 161:269–279
Furuita H, Tanaka H, Yamamoto T, Shiraishi M, Takeuchi T (2000) Effects of n-3 HUFA levels in broodstock diet on the reproductive performance and egg and larval quality of the Japanese flounder, Paralichthys olivaceus. Aquaculture 187:387–398
Gailhard I, Gros P, Durbec J, Beliaeff B, Belin C, Nézan E, Lassus P (2002) Variability patterns of microphytoplankton communities along the French coasts. Mar Ecol Prog Ser 242:39–50. https://doi.org/10.3354/meps242039
Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS ONE 10:e0130053. https://doi.org/10.1371/journal.pone.0130053
García-Isarch E, Juárez A, Ruiz J, Romero Z, Jiménez P, Baldó F (2006) Spawning and nursery habitat of the wedge sole Dicologlossa cuneata (Moreau, 1881) in the Gulf of Cadiz (SW Spain). Sci Mar 70:123–136. https://doi.org/10.3989/scimar.2006.70s2123
Gibson RN (1994) Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Neth J Sea Res 32:191–206. https://doi.org/10.1016/0077-7579(94)90040-X
Grosse J, Brussaard CPD, Boschker HTS (2019) Nutrient limitation driven dynamics of amino acids and fatty acids in coastal phytoplankton: compound synthesis under N and P limitation. Limnol Oceanogr 64:302–316. https://doi.org/10.1002/lno.11040
Hays G, Richardson A, Robinson C (2005) Climate change and marine plankton. Trends Ecol Evol 20:337–344. https://doi.org/10.1016/j.tree.2005.03.004
Hermant M, Lobry J, Bonhommeau S, Poulard J-C, Le Pape O (2010) Impact of warming on abundance and occurrence of flatfish populations in the Bay of Biscay (France). J Sea Res 64:45–53. https://doi.org/10.1016/j.seares.2009.07.001
His E, Maurer D (1988) Shell growth and gross biochemical composition of oyster larvae (Crassostrea gigas) in the field. Aquaculture 69:185–194. https://doi.org/10.1016/0044-8486(88)90195-0
Hixson SM, Arts MT (2016) Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton. Glob Change Biol 22:2744–2755. https://doi.org/10.1111/gcb.13295
Hunter JR (1981) Feeding ecology and predation of marine fish larvae. In: Lasker R (ed) Marine fish larvae: morphology, ecology, and relation to fisheries. Washington Sea Grant Program, Seattle, pp 33–77
Ishizaki Y, Masuda R, Uematsu K, Shimizu K, Arimoto M, Takeuchi T (2001) The effect of dietary docosahexaenoic acid on schooling behaviour and brain development in larval yellowtail. J Fish Biol 58:1691–1703. https://doi.org/10.1111/j.1095-8649.2001.tb02323.x
Izquierdo MS (1996) Essential fatty acid requirements of cultured marine fish larvae. Aquac Nutr 2:183–191. https://doi.org/10.1111/j.1365-2095.1996.tb00058.x
Izquierdo MS, Arakawa T, Takeuchi T, Haroun R, Watanabe T (1992) Effect of n-3 HUFA levels in Artemia on growth of larval Japanese flounder (Paralichthys olivaceus). Aquaculture 105:73–82. https://doi.org/10.1016/0044-8486(92)90163-F
Jónasdóttir SH (2019) Fatty acid profiles and production in marine phytoplankton. Mar Drugs 17:151. https://doi.org/10.3390/md17030151
Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol Oceanogr 49:1784–1793. https://doi.org/10.4319/lo.2004.49.5.1784
Kattner G, Krause M (1987) Changes in lipids during the development of Calanus finmarchicus s.l. from Copepodid I to adult. Mar Biol 96:511–5018
Kattner G, Krause M, Trahms J (1981) Lipid composition of some typical North Sea copepods. Mar Ecol Prog Ser 4:69–74. https://doi.org/10.3354/meps004069
Kim S-K, Takeuchi T, Yokoyama M, Murata Y, Kaneniwa M, Sakakura Y (2005) Effect of dietary taurine levels on growth and feeding behavior of juvenile Japanese flounder Paralichthys olivaceus. Aquaculture 250:765–774. https://doi.org/10.1016/j.aquaculture.2005.04.073
Knutsen JA (1992) Feeding behaviour of North Sea turbot (Scophthalmus maximus) and Dover sole (Solea solea) larvae elicited by chemical stimuli. Mar Biol 113:543–548. https://doi.org/10.1007/BF00349697
Kreibich T, Saborowski R, Hagen W, Niehoff B (2008) Short-term variation of nutritive and metabolic parameters in Temora longicornis females (Crustacea, Copepoda) as a response to diet shift and starvation. Helgol Mar Res 62:241–249. https://doi.org/10.1007/s10152-008-0112-0
Lagardère F, Aboussouan A (1981) Développement du céteau, Dicologoglossa cuneata (Moreau, 1881) (Pisces, Pleuronectiformes, Soleidae): II.–Description des larves. Cybium 5:53–72
Laing I, Child AR, Janke A (1990) Nutritional value of dried algae diets for larvae of Manila clam (Tapes philippinarum). J Mar Biol Assoc U K 70:1–12. https://doi.org/10.1017/S0025315400034147
Langdon CJ, Waldock MJ (1981) The effect of algal and artificial diets on the growth and fatty acid composition of Crassostrea gigas Spat. J Mar Biol Assoc U K 61:431–448. https://doi.org/10.1017/S0025315400047056
Last JM (1978) The food of four species of pleuronectiform larvae in the eastern English Channel and southern North Sea. Mar Biol 45:359–368. https://doi.org/10.1007/BF00391822
Last JM (1979) The food of larval turbot Scophthalmus maximus L. from the west central North Sea. ICES J Mar Sci 38:308–313. https://doi.org/10.1093/icesjms/38.3.308
Le Bourg B, Cornet-Barthaux V, Pagano M, Blanchot J (2015) FlowCAM as a tool for studying small (80–1000 µm) metazooplankton communities. J Plankton Res 37:666–670. https://doi.org/10.1093/plankt/fbv025
Lee RF, Nevenzel JC, Paffenhöfer G-A (1971) Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Mar Biol 9:99–108. https://doi.org/10.1007/BF00348249
Lee R, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306. https://doi.org/10.3354/meps307273
Leonardos N, Lucas IAN (2000) The use of larval fatty acids as an index of growth in Mytilus edulis L. larvae. Aquaculture 184:155–166. https://doi.org/10.1016/S0044-8486(99)00320-8
Llopiz JK (2013) Latitudinal and taxonomic patterns in the feeding ecologies of fish larvae: a literature synthesis. J Mar Syst 109–110:69–77. https://doi.org/10.1016/j.jmarsys.2012.05.002
López-Urrutia Á, Acuña JL, Irigoien X, Harris R (2003) Food limitation and growth in temperate epipelagic appendicularians (Tunicata). Mar Ecol Prog Ser 252:143–157. https://doi.org/10.3354/meps252143
López-Urrutia Á, Harris RP, Acuña JL, Bämstedt U, Fyhn HJ, Gasser B, Gorsky G, Irigoien X, Martinussen M (2005) A comparison of appendicularian seasonal cycles in four contrasting European coastal environments. In: Gorsky G, Youngbluth M, Deibel D (eds) Response of marine ecosystem to global change: ecological impact of appendicularians. Contemporary Publishing International, p 43
Lund I, Steenfeldt SJ, Hansen BW (2007) Effect of dietary arachidonic acid, eicosapentaenoic acid and docosahexaenoic acid on survival, growth and pigmentation in larvae of common sole (Solea solea L.). Aquaculture 273:532–544. https://doi.org/10.1016/j.aquaculture.2007.10.047
MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609
Marshall R, McKinley S, Pearce CM (2010) Effects of nutrition on larval growth and survival in bivalves. Rev Aquac 2:33–55. https://doi.org/10.1111/j.1753-5131.2010.01022.x
Martinez-Silva MA, Audet C, Winkler G, Tremblay R (2018) Prey quality impact on the feeding behavior and lipid composition of winter flounder (Pseudopleuronectes americanus) larvae. Aquac Fish 3:145–155. https://doi.org/10.1016/j.aaf.2018.06.003
Marty Y, Delaunay F, Moal J, Samain J-F (1992) Changes in the fatty acid composition of Pecten maximus (L.) during larval development. J Exp Mar Biol Ecol 163:221–234. https://doi.org/10.1016/0022-0981(92)90051-B
Masuda R, Ziemann DA, Ostrowski AC (2001) Patchiness formation and development of schooling behavior in Pacific threadfin Polydactylus sexfilis reared with different dietary highly unsaturated fatty acid contents. J World Aquac Soc 32:309–316. https://doi.org/10.1111/j.1749-7345.2001.tb00454.x
Matsushita Y, Miyoshi K, Kabeya N, Sanada S, Yazawa R, Haga Y, Satoh S, Yamamoto Y, Strüssmann CA, Luckenbach JA, Yoshizaki G (2020) Flatfishes colonised freshwater environments by acquisition of various DHA biosynthetic pathways. Commun Biol 3:1–9. https://doi.org/10.1038/s42003-020-01242-3
Meunier CL, Boersma M, Wiltshire KH, Malzahn AM (2016) Zooplankton eat what they need: copepod selective feeding and potential consequences for marine systems. Oikos 125:50–58. https://doi.org/10.1111/oik.02072
Monroig Ó, Tocher DR, Navarro JC (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs 11:3998–4018. https://doi.org/10.3390/md11103998
Morais S, Conceição LEC (2009) A new method for the study of essential fatty acid requirements in fish larvae. Br J Nutr 101:1564–1568. https://doi.org/10.1017/S0007114508111436
Morais S, Narciso L, Dores E, Pousão-Ferreira P (2004) Lipid enrichment for Senegalese sole (Solea senegalensis) larvae: effect on larval growth, survival and fatty acid profile. Aquac Int 12:281–298. https://doi.org/10.1023/B:AQUI.0000036184.13187.6b
Morais S, Castanheira F, Martinez-Rubio L, Conceição LEC, Tocher DR (2012) Long chain polyunsaturated fatty acid synthesis in a marine vertebrate: ontogenetic and nutritional regulation of a fatty acyl desaturase with Δ4 activity. Biochim Biophys Acta 1821:660–671. https://doi.org/10.1016/j.bbalip.2011.12.011
Munroe TA (2014) Systematic diversity of the Pleuronectiformes. In: Gibson RN, Geffen AJ, van der Veer HW (eds) Flatfishes, biology and exploitation. Wiley, pp 13–51
Nott PL (1980) Reproduction in Abra alba (Wood) and Abra tenuis (Montagu) (Tellinacea: Scrobiculariidae). J Mar Biol Assoc U K 60:465–479. https://doi.org/10.1017/S0025315400028484
Nunn AD, Tewson LH, Cowx IG (2012) The foraging ecology of larval and juvenile fishes. Rev Fish Biol Fish 22:377–408. https://doi.org/10.1007/s11160-011-9240-8
Oboh A, Kabeya N, Carmona-Antoñanzas G, Castro LFC, Dick JR, Tocher DR, Monroig O (2017) Two alternative pathways for docosahexaenoic acid (DHA, 22:6n–3) biosynthesis are widespread among teleost fish. Sci Rep 7:3889. https://doi.org/10.1038/s41598-017-04288-2
Palazzi R, Richard J, Bozzato G, Zanella L (2006) Larval and juvenile rearing of common sole (Solea solea L.) in the Northern Adriatic (Italy). Aquaculture 255:495–506. https://doi.org/10.1016/j.aquaculture.2006.01.042
Parma L, Bonaldo A, Pirini M, Viroli C, Parmeggiani A, Bonvini E, Gatta P (2015) Fatty acid composition of eggs and its relationships to egg and larval viability from domesticated common sole (Solea solea) breeders. Reprod Domest Anim 50:186–194. https://doi.org/10.1111/rda.12466
Pedersen TM, Hansen JLS, Josefson AB, Hansen BW (2008) Mortality through ontogeny of soft-bottom marine invertebrates with planktonic larvae. J Mar Syst 73:185–207. https://doi.org/10.1016/j.jmarsys.2007.10.008
Peltomaa E, Hällfors H, Taipale SJ (2019) Comparison of diatoms and dinoflagellates from different habitats as sources of PUFAs. Mar Drugs 17:1–17. https://doi.org/10.3390/md17040233
Pepin P, Dower JF (2007) Variability in the trophic position of larval fish in a coastal pelagic ecosystem based on stable isotope analysis. J Plankton Res 29:727–737. https://doi.org/10.1093/plankt/fbm052
Pinto W, Engrola S, Conceição LEC (2018) Towards an early weaning in Senegalese sole: a historical review. Aquaculture 496:1–9. https://doi.org/10.1016/j.aquaculture.2018.06.077
Pond D, Harris R, Head R, Harbour D (1996) Environmental and nutritional factors determining seasonal variability in the fecundity and egg viability of Calanus helgolandicus in coastal waters off Plymouth, UK. Mar Ecol Prog Ser 143:45–63. https://doi.org/10.3354/meps143045
Poulet SA, Laabir M, Chaudron Y (1996) Characteristic features of zooplankton in the Bay of Biscay. Sci Mar 60:77–95
Quéro JC, Vayne JJ (1997) Les Poissons de Mer des Pêches françaises. 304 p. Ifremer/Delachaux et niestlé., Ifremer / Delachaux et Niestlé
Rainuzzo JR, Reitan KI, Jørgensen L, Olsen Y (1994) Lipid composition in turbot larvae fed live feed cultured by emulsions of different lipid classes. Comp Biochem Physiol A Physiol 107:699–710. https://doi.org/10.1016/0300-9629(94)90372-7
Rajasilta M, Vuorinen I (1983) A field study of prey selection in planktivorous fish larvae. Oecologia 59:65–68. https://doi.org/10.1007/BF00388074
Reading BJ, Sullivan CV (2011) Vitellogenesis in fishes. In: Farrell AP, Cech JJ, Richard JG, Stevens ED (eds) Encyclopedia of fish physiology. Academic Press, San Diego, pp 635–646
Reitan KI, Rainuzzo JR, Olsen Y (1994a) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979. https://doi.org/10.1111/j.0022-3646.1994.00972.x
Reitan KI, Rainuzzo JR, Olsen Y (1994b) Influence of lipid composition of live feed on growth, survival and pigmentation of turbot larvae. Aquac Int 2:33–48. https://doi.org/10.1007/BF00118531
Richard N, Colen R, Aragão C (2017) Supplementing taurine to plant-based diets improves lipid digestive capacity and amino acid retention of Senegalese sole (Solea senegalensis) juveniles. Aquaculture 468:94–101. https://doi.org/10.1016/j.aquaculture.2016.09.050
Rico-Villa B, Le Coz JR, Mingant C, Robert R (2006) Influence of phytoplankton diet mixtures on microalgae consumption, larval development and settlement of the Pacific oyster Crassostrea gigas (Thunberg). Aquaculture 256:377–388. https://doi.org/10.1016/j.aquaculture.2006.02.015
Riemann L, Alfredsson H, Hansen MM, Als TD, Nielsen TG, Munk P, Aarestrup K, Maes GE, Sparholt H, Petersen MI, Bachler M, Castonguay M (2010) Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding. Biol Lett 6:819–822. https://doi.org/10.1098/rsbl.2010.0411
Rodríguez F, Fernández E, Head RN, Harbour DS, Bratbak G, Heldal M, Harris RP (2000) Temporal variability of viruses, bacteria, phytoplankton and zooplankton in the western English Channel off Plymouth. J Mar Biol Assoc U K 80:575–586. https://doi.org/10.1017/S0025315400002393
Russel FS (1976) The eggs and planktonic stages of British marine fishes. Academic Press, London
Sadoul B, Foucard A, Valotaire C, Labbé L, Goardon L, LeCalvez JM, Médale F, Quillet E, Dupont-Nivet M, Geurden I, Prunet P, Colson V (2016) Adaptive capacities from survival to stress responses of two isogenic lines of rainbow trout fed a plant-based diet. Sci Rep 6:35957. https://doi.org/10.1038/srep35957
Sánchez-Velasco L (1998) Diet composition and feeding habits of fish larvae of two co-occurring species (Pisces: Callionymidae and Bothidae) in the North-western Mediterranean. ICES J Mar Sci 55:299–308. https://doi.org/10.1006/jmsc.1997.0278
Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199. https://doi.org/10.1016/S0044-8486(99)00083-6
Schreiber AM (2001) Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): an osmoregulatory perspective. Comp Biochem Physiol B Biochem Mol Biol 129:587–595. https://doi.org/10.1016/S1096-4959(01)00346-3
Shawky WA, El-Sayed HS, Saleh NE, Ismael AA, El-Sayed A-FM (2021) Evaluation of microalgae-supplemented diets and enriched decapsulated artemia cyst powder as novel diets for post-weaned common sole (Solea solea) larvae. Aquac Nutr 27:1042–1051. https://doi.org/10.1111/anu.13245
Sheaves M, Baker R, Nagelkerken I, Connolly RM (2015) True value of estuarine and coastal nurseries for fish: Incorporating complexity and dynamics. Estuaries Coasts 38:401–414. https://doi.org/10.1007/s12237-014-9846-x
Shields RJ, Bell JG, Luizi FS, Gara B, Bromage NR, Sargent JR (1999) Natural copepods are superior to enriched artemia nauplii as feed for halibut larvae (Hippoglossus hippoglossus) in terms of survival, pigmentation and retinal morphology: relation to dietary essential fatty acids. J Nutr 129:1186–1194. https://doi.org/10.1093/jn/129.6.1186
Sumule O, Koshio S, Teshima S, Ishikawa M (2003) Energy budget of the Japanese flounder Paralichthys olivaceus (Temminck & Schlegel) larvae fed HUFA-enriched and non-enriched Artemia nauplii. Aquac Res 34:877–886. https://doi.org/10.1046/j.1365-2109.2003.00896.x
Tableau A, Bris HL, Saulnier E, Pape OL, Brind’Amour A (2019) Novel approach for testing the food limitation hypothesis in estuarine and coastal fish nurseries. Mar Ecol Prog Ser 629:117–131. https://doi.org/10.3354/meps13090
Takeuchi T, Dedi J, Ebisawa C, Watanabe T, Seikai T, Hosoya K, Nakazoe J-I (1995) The effect of β-carotene and vitamin A enriched Artemia Nauplii on the malformation and color abnormality of larval Japanese flounder. Fish Sci 61:141–148. https://doi.org/10.2331/fishsci.61.141
Tiselius P, Hansen B, Calliari D (2012) Fatty acid transformation in zooplankton: from seston to benthos. Mar Ecol Prog Ser 446:131–144. https://doi.org/10.3354/meps09479
Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquac Res 41:717–732. https://doi.org/10.1111/j.1365-2109.2008.02150.x
Trivedi S, Aloufi AA, Ansari AA, Ghosh SK (2016) Role of DNA barcoding in marine biodiversity assessment and conservation: An update. Saudi J Biol Sci 23:161–171. https://doi.org/10.1016/j.sjbs.2015.01.001
Troedsson C, Grahl-Nielsen O, Thompson E (2005) Variable fatty acid composition of the pelagic appendicularian Oikopleura dioica in response to dietary quality and quantity. Mar Ecol Prog Ser 289:165–176. https://doi.org/10.3354/meps289165
Troedsson C, Bouquet J-M, Lobon CM, Novac A, Nejstgaard JC, Dupont S, Bosak S, Jakobsen HH, Romanova N, Pankoke LM, Isla A, Dutz J, Sazhin AF, Thompson EM (2013) Effects of ocean acidification, temperature and nutrient regimes on the appendicularian Oikopleura dioica: a mesocosm study. Mar Biol 160:2175–2187. https://doi.org/10.1007/s00227-012-2137-9
Twining CW, Bernhardt JR, Derry AM, Hudson CM, Ishikawa A, Kabeya N, Kainz MJ, Kitano J, Kowarik C, Ladd SN, Leal MC, Scharnweber K, Shipley JR, Matthews B (2021) The evolutionary ecology of fatty-acid variation: Implications for consumer adaptation and diversification. Ecol Lett 24:1709–1731. https://doi.org/10.1111/ele.13771
Vallet C, Dauvin J-C (2004) Spatio-temporal changes of the near-bottom mesozooplankton from the English Channel. J Mar Biol Assoc U K 84:539–546. https://doi.org/10.1017/S0025315404009543h
van der Meeren T, Olsen RE, Hamre K, Fyhn HJ (2008) Biochemical composition of copepods for evaluation of feed quality in production of juvenile marine fish. Aquaculture 274:375–397. https://doi.org/10.1016/j.aquaculture.2007.11.041
Villalta M, Estévez A, Bransden MP, Bell JG (2005) The effect of graded concentrations of dietary DHA on growth, survival and tissue fatty acid profile of Senegal sole (Solea senegalensis) larvae during the Artemia feeding period. Aquaculture 249:353–365. https://doi.org/10.1016/j.aquaculture.2005.03.037
Villalta M, Estévez A, Bransden MP, Bell JG (2008) Effects of dietary eicosapentaenoic acid on growth, survival, pigmentation and fatty acid composition in Senegal sole (Solea senegalensis) larvae during the Artemia feeding period. Aquac Nutr 14:232–241. https://doi.org/10.1111/j.1365-2095.2007.00522.x
Vinagre C, Maia A, Amara R, Cabral HN (2013) Spawning period of Senegal sole, Solea senegalensis, based on juvenile otolith microstructure. J Sea Res 76:89–93. https://doi.org/10.1016/j.seares.2012.11.004
Vizcaíno-Ochoa V, Lazo JP, Barón-Sevilla B, Drawbridge MA (2010) The effect of dietary docosahexaenoic acid (DHA) on growth, survival and pigmentation of California halibut Paralichthys californicus larvae (Ayres, 1810). Aquaculture 302:228–234. https://doi.org/10.1016/j.aquaculture.2010.02.022
Williams R, Conway DVP, Hunt HG (1994) The role of copepods in the planktonic ecosystems of mixed and stratified waters of the European shelf seas. Hydrobiologia 292–293:521–530. https://doi.org/10.1007/BF00229980
Winder M, Bouquet J-M, Rafael Bermúdez J, Berger SA, Hansen T, Brandes J, Sazhin AF, Nejstgaard JC, Båmstedt U, Jakobsen HH, Dutz J, Frischer ME, Troedsson C, Thompson EM (2017) Increased appendicularian zooplankton alter carbon cycling under warmer more acidified ocean conditions. Limnol Oceanogr 62:1541–1551. https://doi.org/10.1002/lno.10516
Yacoob SY, Browman HI (2007) Olfactory and gustatory sensitivity to some feed-related chemicals in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 263:303–309. https://doi.org/10.1016/j.aquaculture.2006.11.005
Zhukova NV, Kharlamenko VI (1999) Sources of essential fatty acids in the marine microbial loop. Aquat Microb Ecol 17:153–157. https://doi.org/10.3354/ame017153
Acknowledgements
The authors thank Ms. C. Cliquet for her help in bibliographic research and M. Corson for proofreading the English. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
All authors contributed to the review conception and writing, and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
This article does not contain any studies with animals performed by any of the authors.
Additional information
Responsible Editor: S. Shumway.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Le Bris, H., Brosset, P. & Sadoul, B. Quality of the food of flatfish larvae: requirements, supplies and availability of essential fatty acids in coastal marine areas. Mar Biol 170, 127 (2023). https://doi.org/10.1007/s00227-023-04263-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-023-04263-8