Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-28T22:03:29.232Z Has data issue: false hasContentIssue false
  • English
  • Français

Feeding strategies and body condition of juvenile European flounder Platichthys flesus in a nursery habitat

Published online by Cambridge University Press:  28 July 2020

C. Mendes Open the ORCID record for C. Mendes [Opens in a new window] ,
S. Ramos ,
M. Elliott  and
A. A. Bordalo
C. Mendes*
Affiliation:
Laboratory of Hydrobiology and Ecology, Institute of Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208Matosinhos, Portugal Department of Biological and Marine Sciences, University of Hull, HullHU6 7RX, UK International Estuarine & Coastal Specialists Ltd, LevenHU17 5LQ, UK
S. Ramos
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208Matosinhos, Portugal International Estuarine & Coastal Specialists Ltd, LevenHU17 5LQ, UK
M. Elliott
Affiliation:
Department of Biological and Marine Sciences, University of Hull, HullHU6 7RX, UK International Estuarine & Coastal Specialists Ltd, LevenHU17 5LQ, UK
A. A. Bordalo
Affiliation:
Laboratory of Hydrobiology and Ecology, Institute of Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208Matosinhos, Portugal
*
Author for correspondence: C. Mendes, E-mail: claudiavrmendes@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Estuarine habitats are major nurseries for the European flounder Platichthys flesus, with different year classes sharing food and space resources. Hence, an understanding of feeding strategies that optimize resource use and maintain carrying capacity is fundamental for sustainable and successful ecosystem management. The main feeding areas of juvenile European flounder (including 0-group and 1-group age classes) in the Lima estuary (northern Portugal) nursery ground were investigated by integrating stomach content analyses with stable isotopic values (δ13C and δ15N) and fish condition indices (Fulton K and RNA:DNA ratio). The 0-group flounder that were associated with the upstream section of the estuary presented the lowest δ13C value (−25.58 ± 1.86‰), while 1-group flounder exhibited a higher δ13C value (−22.59 ± 2.51‰), indicating use of the more saline areas of the estuary (lower and middle sections). The two age groups did not differ in terms of δ15N (0-group: 13.93 ± 0.29‰; 1-group: 13.50 ± 0.96‰), indicating similar trophic levels. The low salinity upper estuary was the main feeding area of 0-group flounder (74%), while 1-group flounder fed along the estuary both upstream (52%) and downstream (48%). Juvenile flounder showed high individual condition based on the Fulton K index (0-group: 1.05 ± 0.08; 1-group: 1.07 ± 0.05) and RNA:DNA (0-group: 1.70 ± 0.70; 1-group: 1.41 ± 0.47). These indices deal with fish health, and hence indicate nursery habitat quality. It is concluded that in this temperate nursery habitat, different feeding strategies sustained the condition of the European flounder juveniles, compared with other flounder populations.

Keywords

Conditionfeedinghabitat usenursery habitat qualitynursery
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 5 , August 2020 , pp. 795 - 806
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aarnio, K, Bonsdorff, E and Rosenback, N (1996) Food and feeding habits of juvenile flounder Platichthys flesus (L.), and turbot Scophthalmus maximus L. in the Åland archipelago, northern Baltic Sea. Journal of Sea Research 36, 311–320.CrossRefGoogle Scholar
Amara, R, Selleslagh, J, Billon, G and Minier, C (2009) Growth and condition of 0-group European flounder, Platichthys flesus as indicator of estuarine habitat quality. Hydrobiologia 627, 87.CrossRefGoogle Scholar
Amorim, E, Ramos, S, Elliott, M and Bordalo, AA (2016) Immigration and early life stages recruitment of the European flounder (Platichthys flesus) to an estuarine nursery: the influence of environmental factors. Journal of Sea Research 107, 56–66.CrossRefGoogle Scholar
Amorim, E, Ramos, S, Elliott, M, Franco, A and Bordalo, AA (2017) Habitat loss and gain: influence on habitat attractiveness for estuarine fish communities. Estuarine, Coastal and Shelf Science 197(Suppl. C), 244–257.CrossRefGoogle Scholar
Amorim, E, Ramos, S, Elliott, M and Bordalo, AA (2018) Dynamic habitat use of an estuarine nursery seascape: ontogenetic shifts in habitat suitability of the European flounder (Platichthys flesus). Journal of Experimental Marine Biology and Ecology 506, 49–60.CrossRefGoogle Scholar
Andersen, AK, Schou, J, Sparrevohn, CR, Nicolajsen, H and Støttrup, JG (2005 a) The quality of release habitat for reared juvenile flounder, Platichthys flesus, with respect to salinity and depth. Fisheries Management and Ecology 12, 211–219.CrossRefGoogle Scholar
Andersen, BS, Carl, JD, Grønkjær, P and Støttrup, JG (2005 b) Feeding ecology and growth of age 0 year Platichthys flesus (L.) in a vegetated and a bare sand habitat in a nutrient rich fjord. Journal of Fish Biology 66, 531–552.CrossRefGoogle Scholar
Anderson, MJ, Gorley, RN and Clarke, KR (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. Plymouth: Primer-E.Google Scholar
Armitage, PD, Pinder, LC and Cranston, P (1995) The Chironomidae: Biology and Ecology of Non-Biting Midges. London: Chapman and Hall.Google Scholar
Beaumont, WRC and Mann, RHK (1984) The age, growth and diet of a freshwater population of the flounder, Platichthys flesus (L.), in southern England. Journal of Fish Biology 25, 607–616.CrossRefGoogle Scholar
Beck, MW, Heck, KL, Able, KW, Childers, DL, Eggleston, DB, Gillanders, BM, Halpern, B, Hays, CG, Hoshino, K, Minello, TJ, Orth, RJ, Sheridan, PF and Weinstein, MP (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51, 633–641.CrossRefGoogle Scholar
Besyst, B, Cattrijsse, A and Mees, J (1999) Feeding ecology of juvenile flatfishes of the surf zone of a sandy beach. Journal of Fish Biology 55, 1171–1186.CrossRefGoogle Scholar
Boesch, DF and Turner, RE (1984) Dependence of fishery species on salt marshes: the role of food and refuge. Estuaries 7, 460–468.CrossRefGoogle Scholar
Bos, AR (1999) Tidal transport of flounder larvae (Platichthys flesus) in the Elbe River, Germany. Archive of Fishery and Marine Research 47, 47–60.Google Scholar
Buckley, LJ (1984) RNA-DNA ratio: an index of larval fish growth in the sea. Marine Biology 80, 291–298.CrossRefGoogle Scholar
Buckley, L, Caldarone, E 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.CrossRefGoogle Scholar
Buckley, LJ, Caldarone, EM and Clemmesen, C (2008) Multi-species larval fish growth model based on temperature and fluorometrically derived RNA/DNA ratios: results from a meta-analysis. Marine Ecology Progress Series 371, 221–232.CrossRefGoogle Scholar
Bulow, FJ (1970) RNA–DNA ratios as indicators of recent growth rates of a fish. Journal of the Fisheries Research Board of Canada 27, 2343–2349.CrossRefGoogle Scholar
Burrows, MT, Gontarek, SJ, Nash, RDM and Gibson, RN (2001) Shrimp predation on 0-group plaice: contrasts between field data and predictions of an individual-based model. Journal of Sea Research 45, 243–254.CrossRefGoogle Scholar
Cabral, H and Costa, MJ (1999) Differential use of nursery areas within the Tagus Estuary by sympatric soles, Solea solea and Solea senegalensis. Environmental Biology of Fishes 56, 389–397.CrossRefGoogle Scholar
Cabral, HN, Lopes, M and Loeper, R (2002) Trophic niche overlap between flatfishes in a nursery area on the Portuguese coast. Scientia Marina 66, 293–300.CrossRefGoogle Scholar
Cabral, HN, Vasconcelos, R, Vinagre, C, França, S, Fonseca, V, Maia, A, Reis-Santos, P, Lopes, M, Ruano, M, Campos, J, Freitas, V, Santos, PT and Costa, MJ (2007) Relative importance of estuarine flatfish nurseries along the Portuguese coast. Journal of Sea Research 57, 209–217.CrossRefGoogle Scholar
Caldarone, EM, Wagner, M, Onge-Burns, JS and Buckley, LJ (2001) Protocol and Guide for Estimating Nucleic Acids in Larval Fish Using a Fluorescence Microplate Reader. Northeast Fisheries Science Center (Reference Document) 01-11, 1–22.Google Scholar
Caldarone, EM, Clemmesen, CM, Berdalet, E, Miller, TJ, Folkvord, A, Holt, GJ, Olivar, MP and Suthers, IM (2006) Intercalibration of four spectrofluorometric protocols for measuring RNA/DNA ratios in larval and juvenile fish. Limnology and Oceanography: Methods 4, 153–163.Google Scholar
Caldarone, EM, MacLean, SA and Sharack, B (2012) Evaluation of bioelectrical impedance analysis and Fulton's condition factor as nonlethal techniques for estimating short-term responses in postsmolt Atlantic salmon (Salmo salar) to food availability. Fishery Bulletin 110, 257–270.Google Scholar
Chícharo, M and Chícharo, L (2008) RNA:DNA ratio and other nucleic acid derived indices in marine ecology. International Journal of Molecular Sciences 9, 1453–1471.CrossRefGoogle ScholarPubMed
Ciotti, BJ, Targett, TE and Burrows, MT (2013 a) Decline in growth rate of juvenile European plaice (Pleuronectes platessa) during summer at nursery beaches along the west coast of Scotland. Canadian Journal of Fisheries and Aquatic Sciences 70, 720–734.CrossRefGoogle Scholar
Ciotti, BJ, Targett, TE, Nash, RDM and Burrows, MT (2013 b) Small-scale spatial and temporal heterogeneity in growth and condition of juvenile fish on sandy beaches. Journal of Experimental Marine Biology and Ecology 448, 346–359.CrossRefGoogle Scholar
Clarke, KR and Gorley, RN (2006) Primer V6: User Manual – Tutorial. Plymouth: Plymouth Marine Laboratory.Google 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.CrossRefGoogle Scholar
Dando, PR (2011) Site fidelity, homing and spawning migrations of flounder Platichthys flesus in the Tamar estuary, South West England. Marine Ecology Progress Series 430, 183–196.CrossRefGoogle Scholar
Darnaude, AM, Harmelin-Vivien, ML and Salen-Picard, C (2001) Food partitioning among flatfish (Pisces: Pleuronectiforms) juveniles in a Mediterranean coastal shallow sandy area. Journal of the Marine Biological Association of the United Kingdom 81, 119–127.CrossRefGoogle Scholar
Darnaude, AM, Salen-Picard, C and Harmelin-Vivien, ML (2004) Depth variation in terrestrial particulate organic matter exploitation by marine coastal benthic communities off the Rhone River delta (NW Mediterranean). Marine Ecology Progress Series 275, 47–57.CrossRefGoogle Scholar
De Groot, SJ (1971) On the interrelationships between morphology of the alimentary tract, food and feeding behaviour in flatfishes (Pisces: Pleuronectiformes). Netherlands Journal of Sea Research 5, 121–196.CrossRefGoogle Scholar
DeNiro, MJ and Epstein, S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
DeNiro, MJ and Epstein, S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.CrossRefGoogle Scholar
De Raedemaecker, F, Brophy, D, O'Connor, I and Comerford, S (2012 a) Habitat characteristics promoting high density and condition of juvenile flatfish at nursery grounds on the west coast of Ireland. Journal of Sea Research 73, 7–17.CrossRefGoogle Scholar
De Raedemaecker, F, Brophy, D, O'Connor, I and O'Neill, B (2012 b) Dependence of RNA:DNA ratios and Fulton's K condition indices on environmental characteristics of plaice and dab nursery grounds. Estuarine, Coastal and Shelf Science 98(Suppl. C), 60–70.CrossRefGoogle Scholar
Dias, E, Morais, P, Faria, AM, Antunes, C and Hoffman, JC (2017) Benthic food webs support the production of sympatric flatfish larvae in estuarine nursery habitat. Fisheries Oceanography 26, 507–512.CrossRefGoogle ScholarPubMed
Dinis, MT (1986) Quatre Soleidae de l'estuaire du Tage. Reproduction et croissance. Essai d'elevage de Solea senegalensis Kaup (Ph.D. dissertation). Université de Bretagne Occidentale, Brest, France.Google Scholar
Doornbos, G and Twisk, F (1984) Density, growth and annual food consumption of plaice (Pleuronectes platessa L.) and flounder (Platichthys flesus (L.)) in Lake Grevelingen, the Netherlands. Netherlands Journal of Sea Research 18, 434–456.CrossRefGoogle Scholar
Edwards, R and Steele, JH (1968) The ecology of 0-group plaice and common dabs at Loch Ewe I. Population and food. Journal of Experimental Marine Biology and Ecology 2, 215–238.CrossRefGoogle Scholar
Edwards, RRC, Steele, JH and Trevallion, A (1970) The ecology of 0-group plaice and common dabs in Loch Ewe. III. Prey-predator experiments with plaice. Journal of Experimental Marine Biology and Ecology 4, 156–173.CrossRefGoogle Scholar
Elliott, M and Hemingway, KL (2002) Fishes in Estuaries. Oxford: Blackwell Science.CrossRefGoogle Scholar
Elliott, M, Burdon, D, Hemingway, KL and Apitz, SE (2007) Estuarine, coastal and marine ecosystem restoration: confusing management and science – a revision of concepts. Estuarine, Coastal and Shelf Science 74, 349–366.Google Scholar
Elliott, M, Mander, L, Mazik, K, Simenstad, C, Valesini, F, Whitfield, A and Wolanski, E (2016) Ecoengineering with ecohydrology: successes and failures in estuarine restoration. Estuarine, Coastal and Shelf Science 176, 12–35.CrossRefGoogle Scholar
Evans, S (1983) Production, predation and food niche segregation in a marine shallow soft-bottom community. Marine Ecology Progress Series 10, 147–157.CrossRefGoogle Scholar
Ferron, A and Leggett, WC (1994) An appraisal of condition measures for marine fish larvae. Advances in Marine Biology 30, 217–303.CrossRefGoogle Scholar
Florin, A-B and Lavados, G (2010) Feeding habits of juvenile flatfish in relation to habitat characteristics in the Baltic Sea. Estuarine, Coastal and Shelf Science 86, 607–612.CrossRefGoogle Scholar
Foley, CJ, Bradley, DL and Höök, TO (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.CrossRefGoogle Scholar
Fonds, M, Cronie, R, Vethaak, AD and Van Der Puyl, P (1992) Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and flounder (Platichthys flesus) in relation to fish size and temperature. Netherlands Journal of Sea Research 29, 127–143.CrossRefGoogle Scholar
Fonseca, VF, Vinagre, C and Cabral, HN (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.CrossRefGoogle Scholar
França, S, Vasconcelos, RP, Tanner, S, Máguas, C, Costa, MJ and Cabral, HN (2011) Assessing food web dynamics and relative importance of organic matter sources for fish species in two Portuguese estuaries: a stable isotope approach. Marine Environmental Research 72, 204–215.CrossRefGoogle ScholarPubMed
Freitas, V, Costa-Dias, S, Campos, J, Bio, A, Santos, P and Antunes, C (2009) Patterns in abundance and distribution of juvenile flounder, Platichthys flesus, in Minho estuary (NW Iberian Peninsula). Aquatic Ecology 43, 1143.CrossRefGoogle Scholar
Freitas, V, Kooijman, S and van der Veer, HW (2012) Latitudinal trends in habitat quality of shallow-water flatfish nurseries. Marine Ecology Progress Series 471, 203–214.CrossRefGoogle Scholar
Fry, FEJ (1971) 1 – The effect of environmental factors on the physiology of fish. In Hoar, WS and Randall, DJ (eds), Fish Physiology, vol. 6. London: Academic Press, pp. 1–98.Google Scholar
Fry, B (2002) Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25, 264–271.CrossRefGoogle Scholar
Fry, B and Sherr, EB (1989) Δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. In Rundel, PW, Ehleringer, JR and Nagy, KA (eds), Stable Isotopes in Ecological Research. New York, NY: Springer, pp. 196–229.CrossRefGoogle Scholar
Gerdol, V and Hughes, RG (1995) Feeding behaviour and diet of Corophium volutator in an estuary in southeastern England. Oceanographic Literature Review 42, 391.Google Scholar
Gibson, RN (1973) Tidal and circadian activity rhythms in juvenile plaice, Pleuronectes platessa. Marine Biology 22, 379–386.CrossRefGoogle Scholar
Gibson, RN (1994) Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Netherlands Journal of Sea Research 32, 191–206.CrossRefGoogle Scholar
Gilliers, C, Amara, R and Bergeron, J-P (2004) Comparison of growth and condition indices of juvenile flatfish in different coastal nursery grounds. Environmental Biology of Fishes 71, 189–198.CrossRefGoogle Scholar
Green, BC, Smith, DJ, Grey, J and Underwood, GJC (2012) High site fidelity and low site connectivity in temperate salt marsh fish populations: a stable isotope approach. Oecologia 168, 245–255.CrossRefGoogle ScholarPubMed
Grønkjær, P, Carl, JD, Rasmussen, TH and Hansen, KW (2007) Effect of habitat shifts on feeding behaviour and growth of 0 year-group flounder Platichthys flesus (L.) transferred between macroalgae and bare sand habitats. Journal of Fish Biology 70, 1587–1605.CrossRefGoogle Scholar
Gutt, J (1985) The growth of juvenile flounders (Platichthys flesus L.) at salinities of 0, 5, 15 and 35%%. Journal of Applied Ichthyology 1, 17–26.CrossRefGoogle Scholar
Gwak, WS and Tanaka, M (2001) Developmental change in RNA: DNA ratios of fed and starved laboratory-reared Japanese flounder larvae and juveniles, and its application to assessment of nutritional condition for wild fish. Journal of Fish Biology 59, 902–915.Google Scholar
Hampel, H, Cattrijsse, A and Elliott, M (2005) Feeding habits of young predatory fishes in marsh creeks situated along the salinity gradient of the Schelde estuary, Belgium and the Netherlands. Helgoland Marine Research 59, 151–162.CrossRefGoogle Scholar
Harmelin-Vivien, M, Loizeau, V, Mellon, C, Beker, B, Arlhac, D, Bodiguel, X, Ferraton, F, Hermand, R, Philippon, X and Salen-Picard, C (2008) Comparison of C and N stable isotope ratios between surface particulate organic matter and microphytoplankton in the Gulf of Lions (NW Mediterranean). Continental Shelf Research 28, 1911–1919.CrossRefGoogle Scholar
Haynes, PS, Brophy, D, De Raedemaecker, F and McGrath, D (2011) The feeding ecology of 0 year-group turbot Scophthalmus maximus and brill Scophthalmus rhombus on Irish west coast nursery grounds. Journal of Fish Biology 79, 1866–1882.CrossRefGoogle ScholarPubMed
Henderson, PA and Holmes, RHA (1991) On the population dynamics of dab, sole and flounder within Bridgwater Bay in the lower Severn Estuary, England. Netherlands Journal of Sea Research 27, 337–344.CrossRefGoogle Scholar
Herzka, SZ (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuarine, Coastal and Shelf Science 64, 58–69.CrossRefGoogle Scholar
Hoffman, JC, Kelly, JR, Peterson, GS and Cotter, AM (2015) Landscape-scale food webs of fish nursery habitat along a river-coast mixing zone. Estuaries and Coasts 38, 1335–1349.CrossRefGoogle Scholar
Hyslop, EJ (1980) Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411–429.CrossRefGoogle Scholar
Jager, Z, Kleef, HL and Tydeman, P (1995) Mortality and growth of 0-group flatfish in the brackish dollard (Ems Estuary, Wadden Sea). Netherlands Journal of Sea Research 34, 119–129.CrossRefGoogle Scholar
Kennedy, P, Kennedy, H and Papadimitriou, S (2005) The effect of acidification on the determination of organic carbon, total nitrogen and their stable isotopic composition in algae and marine sediment. Rapid Communications in Mass Spectrometry 19, 1063–1068.CrossRefGoogle ScholarPubMed
Kerstan, M (1991) The importance of rivers as nursery grounds for 0- and 1-group flounder (Platichthys flesus L.) in comparison to the Wadden Sea. Netherlands Journal of Sea Research 27, 353–366.CrossRefGoogle Scholar
Kopp, D, Le Bris, H, Grimaud, L, Nérot, C and Brind'Amour, A (2013) Spatial analysis of the trophic interactions between two juvenile fish species and their preys along a coastal–estuarine gradient. Journal of Sea Research 81, 40–48.CrossRefGoogle Scholar
Kostecki, C, Roussel, JM, Desroy, N, Roussel, G, Lanshere, J, Le Bris, H and Le Pape, O (2012) Trophic ecology of juvenile flatfish in a coastal nursery ground: contributions of intertidal primary production and freshwater particulate organic matter. Marine Ecology Progress Series 449, 221–232.CrossRefGoogle Scholar
Laffargue, P, Lagardère, F, Rijnsdorp, AD, Fillon, A and Amara, R (2007) Growth performances of juvenile sole Solea solea under environmental constraints of embayed nursery areas. Aquatic Living Resources 20, 213–221.CrossRefGoogle Scholar
Le Pape, O and Bonhommeau, S (2015) The food limitation hypothesis for juvenile marine fish. Fish and Fisheries 16, 373–398.CrossRefGoogle Scholar
Le Pape, O and Cognez, N (2016) The range of juvenile movements of estuarine and coastal nursery dependent flatfishes: estimation from a meta-analytical approach. Journal of Sea Research 107(Part 1), 43–55.CrossRefGoogle Scholar
Le Pape, O, Modéran, J, Beaunée, G, Riera, P, Nicolas, D, Savoye, N, Harmelin-Vivien, M, Darnaude, AM, Brind'Amour, A, Le Bris, H, Cabral, H, Vinagre, C, Pasquaud, S, França, S and Kostecki, C (2013) Sources of organic matter for flatfish juveniles in coastal and estuarine nursery grounds: a meta-analysis for the common sole (Solea solea) in contrasted systems of Western Europe. Journal of Sea Research 75, 85–95.CrossRefGoogle Scholar
Lonsdale, J-A, Weston, K, Barnard, S, Boyes, SJ and Elliott, M (2015) Integrating management tools and concepts to develop an estuarine planning support system: a case study of the Humber Estuary, eastern England. Marine Pollution Bulletin 100, 393–405.CrossRefGoogle ScholarPubMed
Malloy, KD and Targett, TE (1994) The use of RNA:DNA ratios to predict growth limitation of juvenile summer flounder (Paralichthys dentatus) from Delaware and North Carolina estuaries. Marine Biology 118, 367–375.CrossRefGoogle Scholar
Marshall, S and Elliott, M (1997) A comparison of univariate and multivariate numerical and graphical techniques for determining inter- and intraspecific feeding relationships in estuarine fish. Journal of Fish Biology 51, 526–545.CrossRefGoogle Scholar
Martinho, F, Leitão, R, Neto, JM, Cabral, HN, Marques, JC and Pardal, MA (2007) The use of nursery areas by juvenile fish in a temperate estuary, Portugal. Hydrobiologia 587, 281–290.CrossRefGoogle Scholar
Martinho, F, Leitão, R, Neto, JM, Cabral, H, Lagardère, F and Pardal, MA (2008) Estuarine colonization, population structure and nursery functioning for 0-group sea bass (Dicentrarchus labrax), flounder (Platichthys flesus) and sole (Solea solea) in a mesotidal temperate estuary. Journal of Applied Ichthyology 24, 229–237.CrossRefGoogle Scholar
McLusky, DS and Elliott, M (2004) The Estuarine Ecosystem: Ecology, Threats and Management. Oxford: Oxford University Press.CrossRefGoogle Scholar
Mendes, C, Ramos, S and Bordalo, AA (2014) Feeding ecology of juvenile flounder Platichthys flesus in an estuarine nursery habitat: influence of prey–predator interactions. Journal of Experimental Marine Biology and Ecology 461, 458–468.CrossRefGoogle Scholar
Minagawa, M and Wada, E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.CrossRefGoogle Scholar
Modin, J and Pihl, L (1996) Small-scale distribution of juvenile plaice and flounder in relation to predatory shrimp in a shallow Swedish bay. Journal of Fish Biology 49, 1070–1085.CrossRefGoogle Scholar
Molinero, A and Flos, R (1992) Influence of season on the feeding habits of the common sole Solea solea. Marine Biology 113, 499–507.CrossRefGoogle Scholar
Moore, JW and Moore, IA (1976) The basis of food selection in flounders, Platichthys flesus (L.), in the Severn Estuary. Journal of Fish Biology 9, 139–156.CrossRefGoogle Scholar
Muus, BJ and Nielsen, JG (1999) Sea Fish. Hedehusene: Scandinavian Fishing Year Book.Google Scholar
Ng, JSS, Wai, T-C and Williams, GA (2007) The effects of acidification on the stable isotope signatures of marine algae and molluscs. Marine Chemistry 103, 97–102.CrossRefGoogle Scholar
Nielsen, JG (1986) Pleuronectidae. In Whitehead, PJP, Bauchot, ML, Hureau, JC, Nielsen, J and Tortonese, E (eds), Fishes of the North-Eastern Atlantic and Mediterranean. Paris: UNESCO, pp. 1299–1307.Google Scholar
Nunn, AD, Tewson, LH and Cowx, IG (2012) The foraging ecology of larval and juvenile fishes. Reviews in Fish Biology and Fisheries 22, 377–408.CrossRefGoogle Scholar
O'Neill, B, De Raedemaecker, F, McGrath, D and Brophy, D (2011) An experimental investigation of salinity effects on growth, development and condition in the European flounder (Platichthys flesus L.). Journal of Experimental Marine Biology and Ecology 410, 39–44.CrossRefGoogle Scholar
Palmer, SCF, Coulon, A and Travis, JMJ (2014) Inter-individual variability in dispersal behaviours impacts connectivity estimates. Oikos 123, 923–932.CrossRefGoogle Scholar
Parnell, AC, Inger, R, Bearhop, S and Jackson, AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5, e9672.CrossRefGoogle ScholarPubMed
Parnell, AC, Phillips, DL, Bearhop, S, Semmens, BX, Ward, EJ, Moore, JW, Jackson, AL, Grey, J, Kelly, DJ and Inger, R (2013) Bayesian stable isotope mixing models. Environmetrics 24, 387–399.Google Scholar
Pasquaud, S, Elie, P, Jeantet, C, Billy, I, Martinez, P and Girardin, M (2008) A preliminary investigation of the fish food web in the Gironde estuary, France, using dietary and stable isotope analyses. Estuarine, Coastal and Shelf Science 78, 267–279.CrossRefGoogle Scholar
Peterson, BJ and Fry, B (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.CrossRefGoogle Scholar
Phillips, DL, Inger, R, Bearhop, S, Jackson, AL, Moore, JW, Parnell, AC, Semmens, BX and Ward, EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92, 823–835.CrossRefGoogle Scholar
Piet, GJ, Pfisterer, AB and Rijnsdorp, AD (1998) On factors structuring the flatfish assemblage in the southern North Sea. Journal of Sea Research 40, 143–152.CrossRefGoogle Scholar
Pihl, L, Cattrijsse, A, Codling, I, Mathieson, S, McLusky, DS and Roberts, C (2007) Habitat use by fishes in estuaries and other brackish areas. Fishes in Estuaries. Oxford: Blackwell Science, pp. 10–53.Google Scholar
Poiesz, SSH, de Vries, A, Cardoso, JFMF, Witte, JIJ, van der Veer, HW and Freitas, V (2019) A comparison of growth in two juvenile flatfish species in the Dutch Wadden Sea: searching for a mechanism for summer growth reduction in flatfish nurseries. Journal of Sea Research 144, 39–48.CrossRefGoogle Scholar
Post, DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.CrossRefGoogle Scholar
Potter, IC, Tweedley, JR, Elliott, M and Whitfield, AK (2015) The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish and Fisheries 16, 230–239.CrossRefGoogle Scholar
Power, M, Attrill, MJ and Thomas, RM (2000) Environmental factors and interactions affecting the temporal abundance of juvenile flatfish in the Thames Estuary. Journal of Sea Research 43, 135–149.CrossRefGoogle Scholar
Preston, T and Owens, NJP (1983) Interfacing an automatic elemental analyser with an isotope ratio mass spectrometer: the potential for fully automated total nitrogen and nitrogen-15 analysis. The Analyst 108, 971–977.CrossRefGoogle Scholar
Primo, AL, Azeiteiro, UM, Marques, SC, Martinho, F, Baptista, J and Pardal, MA (2013) Colonization and nursery habitat use patterns of larval and juvenile flatfish species in a small temperate estuary. Journal of Sea Research 76(Suppl. C), 126–134.CrossRefGoogle Scholar
Raffaelli, D, Conacher, A, McLachlan, H and Emes, C (1989) The role of epibenthic crustacean predators in an estuarine food web. Estuarine, Coastal and Shelf Science 28, 149–160.CrossRefGoogle Scholar
Raffaelli, D, Richner, H, Summers, R and Northcott, S (1990) Tidal migrations in the flounder (Platichthys flesus). Marine Behaviour and Physiology 16, 249–260.CrossRefGoogle Scholar
Ramos, S, Cowen, RK, Ré, P and Bordalo, AA (2006) Temporal and spatial distributions of larval fish assemblages in the Lima estuary (Portugal). Estuarine, Coastal and Shelf Science 66, 303–314.CrossRefGoogle Scholar
Ramos, S, Ré, P and Bordalo, AA (2009) Environmental control on early life stages of flatfishes in the Lima Estuary (NW Portugal). Estuarine. Coastal and Shelf Science 83, 252–264.CrossRefGoogle Scholar
Ramos, S, Ré, P and Bordalo, AA (2010) Recruitment of flatfish species to an estuarine nursery habitat (Lima Estuary, NW Iberian Peninsula). Journal of Sea Research 64, 473–486.CrossRefGoogle Scholar
Ramos, S, Paris, CB and Angélico, MM (2017) Larval fish dispersal along an estuarine–ocean gradient. Canadian Journal of Fisheries and Aquatic Sciences 74, 1462–1473.CrossRefGoogle Scholar
R Development Core Team (2007) R: A Language and Environment for Statistical Computing. Vienna: R foundation for Statistical Computing.Google Scholar
Richard, P, Bergeron, J-P, Boulhic, M, Galois, R and Person-Le Ruyet, J (1991) Effect of starvation on RNA, DNA and protein content of laboratory-reared larvae and juveniles of Solea solea. Marine Ecology Progress Series 72, 69–77.CrossRefGoogle Scholar
Ricker, WE (1975) Computation and Interpretation of Biological Statistics of Fish Populations. Ottawa: Bulletin of the Fisheries Research Board of Canada.Google Scholar
Rijnsdorp, AD, Berghahn, R, Miller, JM and Van Der Veer, HW (1995) Recruitment mechanisms in flatfish: what did we learn and where do we go? Netherlands Journal of Sea Research 34, 237–242.CrossRefGoogle Scholar
Russo, T, Pulcini, D, O'Leary, Á, Cataudella, S and Mariani, S (2008) Relationship between body shape and trophic niche segregation in two closely related sympatric fishes. Journal of Fish Biology 73, 809–828.CrossRefGoogle Scholar
Selleslagh, J and Amara, R (2013) Effect of starvation on condition and growth of juvenile plaice Pleuronectes platessa: nursery habitat quality assessment during the settlement period. Journal of the Marine Biological Association of the United Kingdom 93, 479–488.CrossRefGoogle Scholar
Selleslagh, J, Blanchet, H, Bachelet, G and Lobry, J (2015) Feeding habitats, connectivity and origin of organic matter supporting fish populations in an estuary with a reduced intertidal area assessed by stable isotope analysis. Estuaries and Coasts 38, 1431–1447.CrossRefGoogle Scholar
Sheaves, M (2009) Consequences of ecological connectivity: the coastal ecosystem mosaic. Marine Ecology Progress Series 391, 107–115.CrossRefGoogle Scholar
Sheaves, M, Baker, R, Nagelkerken, I and Connolly, RM (2015) True value of estuarine and coastal nurseries for fish: incorporating complexity and dynamics. Estuaries and Coasts 38, 401–414.CrossRefGoogle Scholar
Sogard, SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bulletin of Marine Science 60, 1129–1157.Google Scholar
Sousa, R, Dias, S and Antunes, JC (2006) Spatial subtidal macrobenthic distribution in relation to abiotic conditions in the Lima Estuary, NW of Portugal. Hydrobiologia 559, 135–148.CrossRefGoogle Scholar
Souza, AT, Dias, E, Nogueira, A, Campos, J, Marques, JC and Martins, I (2013) Population ecology and habitat preferences of juvenile flounder Platichthys flesus (Actinopterygii: Pleuronectidae) in a temperate estuary. Journal of Sea Research 79(Suppl. C), 60–69.CrossRefGoogle Scholar
Summers, RW (1979) Life cycle and population ecology of the flounder Platichthys flesus (L.) in the Ythan estuary, Scotland. Journal of Natural History 13, 703–723.CrossRefGoogle Scholar
Summers, RW (1980) The diet and feeding behaviour of the flounder Platichthys flesus (L.) in the Ythan estuary, Aberdeenshire, Scotland. Estuarine and Coastal Marine Science 11, 217–232.CrossRefGoogle Scholar
Suthers, IM, Fraser, A and Frank, KT (1992) Comparison of lipid, otolith and morphometric condition indices of pelagic juvenile cod Gadus morhua from the Canadian Atlantic. Marine Ecology Progress Series 84, 31–40.CrossRefGoogle Scholar
Suzuki, KW, Kasai, A, Isoda, T, Nakayama, K and Tanaka, M (2008) Distinctive stable isotope ratios in important zooplankton species in relation to estuarine salinity gradients: potential tracer of fish migration. Estuarine, Coastal and Shelf Science 78, 541–550.CrossRefGoogle Scholar
Tableau, A, Brind'Amour, A, Woillez, M and Le Bris, H (2016) Influence of food availability on the spatial distribution of juvenile fish within soft sediment nursery habitats. Journal of Sea Research 111, 76–87.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Teal, LR, de Leeuw, JJ, van der Veer, HW and Rijnsdorp, AD (2008) Effects of climate change on growth of 0-group sole and plaice. Marine Ecology Progress Series 358, 219–230.CrossRefGoogle Scholar
van der Veer, HW and Bergman, MJN (1987) Predation by crustaceans on a newly settled 0-group plaice Pleuronectes platessa population in the western Wadden Sea. Marine Ecology Progress Series 35, 203–215.CrossRefGoogle Scholar
van der Veer, HW, Bergman, MJN, Dapper, R and Witte, JIJ (1991) Population dynamics of an intertidal 0-group flounder Platichthys flesus population in the western Dutch Wadden Sea. Marine Ecology Progress Series 73, 141–148.CrossRefGoogle Scholar
van der Veer, HW, Berghahn, R, Miller, JM and Rijnsdorp, AD (2000) Recruitment in flatfish, with special emphasis on North Atlantic species: progress made by the Flatfish Symposia. ICES Journal of Marine Science 57, 202–215.CrossRefGoogle Scholar
van der Veer, HW, Freitas, V, Koot, J, Witte, JIJ and Zuur, AF (2010) Food limitation in epibenthic species in temperate intertidal systems in summer: analysis of 0-group plaice Pleuronectes platessa. Marine Ecology Progress Series 416, 215–227.CrossRefGoogle Scholar
van der Veer, HW, Jung, AS, Freitas, V, Philippart, CJM and Witte, JIJ (2016) Possible causes for growth variability and summer growth reduction in juvenile plaice Pleuronectes platessa L. in the western Dutch Wadden Sea. Journal of Sea Research 111, 97–106.CrossRefGoogle Scholar
Vander Zanden, MJ, Cabana, G and Rasmussen, JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences 54, 1142–1158.CrossRefGoogle Scholar
Vasconcelos, RP, Reis-Santos, P, Fonseca, V, Ruano, M, Tanner, S, Costa, MJ and Cabral, HN (2009) Juvenile fish condition in estuarine nurseries along the Portuguese coast. Estuarine, Coastal and Shelf Science 82, 128–138.CrossRefGoogle Scholar
Vasconcelos, RP, Reis-Santos, P, Maia, A, Fonseca, V, França, S, Wouters, N, Costa, MJ and Cabral, HN (2010) Nursery use patterns of commercially important marine fish species in estuarine systems along the Portuguese coast. Estuarine, Coastal and Shelf Science 86, 613–624.CrossRefGoogle Scholar
Vaslet, A, Phillips, DL, France, CAM, Feller, IC and Baldwin, CC (2015) Trophic behaviour of juvenile reef fishes inhabiting interlinked mangrove–seagrass habitats in offshore mangrove islets. Journal of Fish Biology 87, 256–273.CrossRefGoogle ScholarPubMed
Vinagre, C, França, S, Costa, MJ and Cabral, HN (2005) Niche overlap between juvenile flatfishes, Platichthys flesus and Solea solea, in a southern European estuary and adjacent coastal waters. Journal of Applied Ichthyology 21, 114–120.CrossRefGoogle Scholar
Vinagre, C, Cabral, H and Costa, MJ (2008) Prey selection by flounder, Platichthys flesus, in the Douro estuary, Portugal. Journal of Applied Ichthyology 24, 238–243.CrossRefGoogle Scholar
Vinagre, C, Salgado, J, Cabral, HN and Costa, MJ (2011) Food web structure and habitat connectivity in fish estuarine nurseries – impact of river flow. Estuaries and Coasts 34, 663–674.CrossRefGoogle Scholar
Vizzini, S, Sarà, G, Michener, RH and Mazzola, A (2002) The role and contribution of the seagrass Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecologica 23, 277–285.CrossRefGoogle Scholar
Wirjoatmodjo, S and Pitcher, TJ (1984) Flounders follow the tides to feed: evidence from ultrasonic tracking in an estuary. Estuarine, Coastal and Shelf Science 19, 231–241.Google Scholar
Wolanski, E and Elliott, M (2015) Estuarine Ecohydrology: An Introduction. Boston, MA: Elsevier.Google Scholar
Złoch, I and Sapota, M (2010) Trophic interactions between preadult and adult Pomatoschistus minutus and Pomatoschistus microps and young Platichthys flesus occurring in inshore waters of the Gulf of Gdańsk (Southern Baltic). Oceanological and Hydrobiological Studies 39, 37–53.CrossRefGoogle Scholar
Supplementary material: File

Mendes et al. supplementary material

Mendes et al. supplementary material

Download Mendes et al. supplementary material(File)
File 21.9 KB