Skip to main content
Log in

Ontogenetic changes in the larval condition of Downs herring: use of a multi-index approach at an individual scale

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Evaluating fish larval condition in terms of nutrition and growth is essential as it will influence their development and survival capacity. The present study aims to investigate larval condition of Downs herring (Clupea harengus L.) during winter in the Eastern English Channel and Southern Bight of the North Sea. Four condition indices including ingestion rate based on gut fluorescence, instantaneous growth based on RNA/DNA, DNA/C ratios, and otolith microstructure were combined at an individual scale on herring larvae collected during the 2015 International Bottom Trawl Survey—MIK sampling. The four indices demonstrated a clear shift in the larval condition occurring at a larval size of 13 mm. While smaller larvae were shown to feed and grow, larger larvae exhibited a slower growth rate though actively feeding. This suggests that 13 mm could be a critical size for Downs herring larvae. This ontogenetic shift in the larval condition is discussed regarding environmental conditions, diet shift, and growth strategies. It is concluded that the shift from an omnivorous to a carnivorous diet constitutes an additional critical step besides such as the shift from endogenous to exogenous nutrition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alvarez-Fernandez S, Lindeboom H, Meesters E (2012) Temporal changes in plankton of the North Sea: community shifts and environmental drivers. Mar Ecol Prog Ser 462:21–38. doi:10.3354/meps09817

    Article  Google Scholar 

  • Aminot A, Kérouel R (2004) Hydrologie des écosystèmes marins: paramètres et analyses. Editions Quae, Versailles

    Google Scholar 

  • Anderson JT (1988) A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J Northw Atl Fish Sci 8:55–66

    Google Scholar 

  • Arrhenius F, Hansson S (1996) Growth and seasonal changes in energy content of young Baltic Sea herring (Clupea harengus L.). ICES J Mar Sci J Cons 53:792–801

    Article  Google Scholar 

  • Bailey KM, Houde ED (1989) Predation on eggs and larvae of marine fishes and the recruitment problem. Adv Mar Biol 25:1–83

    Article  Google Scholar 

  • Bakun A (1996) Patterns in the oceans: ocean processes and marine population dynamics. California Sea Grant College System, National Oceanic and Atmospheric Adminstration in cooperation with Centro de Investigaciones Biologicas del Noroeste, La Paz, BCS, Mexico

  • Beaugrand G, Ibañez F, Lindley J (2003) An overview of statistical methods applied to CPR data. Prog Oceanogr 58:235–262. doi:10.1016/j.pocean.2003.08.006

    Article  Google Scholar 

  • Bergeron J-P (1997) Nucleic acids in ichthyoplankton ecology: a review, with emphasis on recent advances for new perspectives. J Fish Biol 51(Supplement A):284–302

    Article  CAS  Google Scholar 

  • Bergeron J-P (2000) Effect of strong winds on the nutritional condition of anchovy (Engraulis encrasicolus L.) larvae in the Bay of Biscay, Northeast Atlantic, as inferred from an early field application of the DNA/C index. ICES J Mar Sci J Cons 57:249–255. doi:10.1006/jmsc.2000.0642

    Article  Google Scholar 

  • Bergeron J-P (2009) Nutritional condition of anchovy Engraulis encrasicolus larvae in connection with mesozooplankton feeding catabolism in the southern Bay of Biscay, NE Atlantic. J Exp Mar Biol Ecol 377:76–83. doi:10.1016/j.jembe.2009.06.019

    Article  CAS  Google Scholar 

  • Bergeron J-P, Boulhic M, Galois R (1991) Effet de la privation de nourriture sur la teneur en ADN de la larve de sole (Solea solea L.). ICES J Mar Sci J Cons 48:127–134

    Article  Google Scholar 

  • Bergeron J-P, Person-Le Ruyet J, Koutsikopoulos C (1997) Use of carbon rather than dry weight to assess the DNA content and nutritional condition index of sole larvae. ICES J Mar Sci J Cons 54:148–151

    Article  Google Scholar 

  • Bigot J-L (1979) Identification des zoés de tourteau (Cancer pagurus L.) et d’étrille (Macropipus puber L.). Comparaison avec d’autres zoés de morphologie très voisine. In: CIEM Conseil International pour l’Exploration de la Mer, Comité de l’Océanographie biologique, CM 1979/L: 17

  • Bils F, Moyano M, Aberle N et al (2016) Exploring the microzooplankton–ichthyoplankton link: a combined field and modelling study of Atlantic herring (Clupea harengus) in the Irish Sea. J Plankton Res 39:147–163. doi:10.1093/plankt/fbw074

    Article  Google Scholar 

  • Bjørke H (1976) Food and feeding of young herring larvae of Norwegian spring spawners. ICES, Copenhagen

    Google Scholar 

  • Blaxter JHS (1965) The feeding of herring larvae and their ecology in relation to feeding. Calif Coop Ocean Fish Invest Rep 10:79–88

    Google Scholar 

  • Boehlert GW, Yolklavich MM (1984) Carbon assimilation as a function of ingestion rate in larval pacific herring, Clupea harengus pallasi Valenciennes. J Exp Mar Biol Ecol 79:251–262

    Article  CAS  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  • Breiman L (2001) Random forests. Mach Learn 45:5–32

    Article  Google Scholar 

  • Buckley L, Caldarone E, Ong T-L (1999) RNA—DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. In: Zehr JP, Voytek MA (eds) Molecular ecology of aquatic communities. Springer, Netherlands, pp 265–277

    Chapter  Google Scholar 

  • Buckley LJ, Caldarone E, Clemmesen C (2008) Multi-species larval fish growth model based on temperature and fluorometrically derived RNA/DNA ratios: results from a meta-analysis. Mar Ecol Prog Ser 371:221–232. doi:10.3354/meps07648

    Article  Google Scholar 

  • Bulow FJ (1970) RNA-DNA ratios as indicators of recent growth rates of a fish. J Fish Board Can 27:2343–2349

    Article  CAS  Google Scholar 

  • Cahu C, Zambonino J-L (2007) Ontogenèse des fonctions digestives et besoins nutritionnels chez les larves de poissons marins. Cybium 31:217–226

    Google Scholar 

  • Caldarone EM, Clemmesen C, Berdalet E et al (2006) Intercalibration of four spectrofluorometric protocols for measuring RNA/DNA ratios in larval and juvenile fish. Limnol Oceanogr Methods 4:153–163

    Article  CAS  Google Scholar 

  • Campana SE (1990) How reliable are growth back-calculations based on otoliths? Can J Fish Aquat Sci 47:2219–2227

    Article  Google Scholar 

  • Campana SE, Hurley PC (1989) An age-and temperature-mediated growth model for cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) larvae in the Gulf of Maine. Can J Fish Aquat Sci 46:603–613

    Article  Google Scholar 

  • Campana SE, Moksness E (1991) Accuracy and precision of age and hatch date estimates from otolith microstructure examination. ICES J Mar Sci 48:303–316

    Article  Google Scholar 

  • Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032

    Article  Google Scholar 

  • Campana SE, Gagne JA, Munro J (1987) Otolith microstructure of Larval Herring (Clupea harengus): Image or Reality? Can J Fish Aquat Sci 44:1922–1929

    Article  Google Scholar 

  • Catalán IA (2003) Condition indices and their relationship with environmental factors in fish larvae. Thesis, University of Barcelona, Barcelona

  • Checkley DM (1982) Selective feeding by Atlantic herring (Clupea harengus) larvae on zooplankton in natural assemblages. Mar Ecol Prog Ser 9:245–253

    Article  Google Scholar 

  • Checkley DM (1984) Relation of growth to ingestion for larvae of Atlantic herring Clupea harengus and other fish. Mar Ecol Prog Ser 18:215–224

    Article  Google Scholar 

  • Chícharo MA, Chícharo L (2008) RNA:DNA ratio and other nucleic acid derived indices in marine ecology. Int J Mol Sci 9:1453–1471. doi:10.3390/ijms9081453

    Article  CAS  Google Scholar 

  • Chícharo A, Chícharo L, Valdés L et al (1998) Estimation of starvation and diet variation of the RNA/DNA ratios in field-caught Sardina pilchardus larvae off the north of Spain. Mar Ecol Prog Ser 164:273–283

    Article  Google Scholar 

  • Ching FF, Nakagawa Y, Kato K et al (2012) Effects of delayed first feeding on the survival and growth of tiger grouper, Epinephelus fuscoguttatus (Forsskål, 1775), larvae. Aquac Res 43:303–310

    Article  Google Scholar 

  • Clemmesen CM (1987) Laboratory studies on RNA/DNA ratios of starved and fed herring (Clupea harengus) and turbot (Scophthalmus maximus) larvae. J Cons 43:122–128

    Article  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. Mar Biol 118:377–382

    Article  Google Scholar 

  • Clemmesen C (1996) Importance and limits of RNA/DNA ratios as a measure of nutritional condition in fish larvae. Proceedings of an international workshop, Japan. In: Survival strategies in early life stages of marine resources, pp 67–82

  • Clemmesen C, Doan T (1996) Does otolith structure reflect the nutritional condition of a fish larva? Comparison of otolith structure and biochemical index (RNA/DNA ratio) determined on cod larvae. Mar Ecol Prog Ser 138:33–39

    Article  Google Scholar 

  • Clemmesen C, Bühler V, Carvalho G et al (2003) Variability in condition and growth of Atlantic cod larvae and juveniles reared in mesocosms: environmental and maternal effects. J Fish Biol 62:706–723

    Article  Google Scholar 

  • Cohen S, Diaz MV, Díaz AO (2013) Histological and histochemical study of the digestive system of the Argentine anchovy larvae (Engraulis anchoita) at different developmental stages of their ontogenetic development. Acta Zool 95:409–420. doi:10.1111/azo.12038

    Article  Google Scholar 

  • Corten A (1986) On the causes of the recruitment failure of herring in the central and northern North Sea in the years 1972–1978. J Cons 42:281–294

    Article  Google Scholar 

  • Corten A (2013) Recruitment depressions in North Sea herring. ICES J Mar Sci 70:1–15. doi:10.1093/icesjms/fss187

    Article  Google Scholar 

  • Cushing DH (1969) The regularity of the spawning season of some fishes. J Cons 33:81–92

    Article  Google Scholar 

  • Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:250–293

    Google Scholar 

  • Denis J, Vallet C, Courcot L et al (2016) Feeding strategy of Downs herring larvae (Clupea harengus L.) in the English Channel and North Sea. J Sea Res 115:33–46

    Article  Google Scholar 

  • Doyle MJ (1977) A morphological staging system for the larval development of the herring, Clupea harengus L. J Mar Biol Assoc UK 57:859–867

    Article  CAS  Google Scholar 

  • Fablet R, Pecquerie L, de Pontual H et al (2011) Shedding light on fish otolith biomineralization using a bioenergetic approach. PLoS ONE 6:e27055. doi:10.1371/journal.pone.0027055

    Article  CAS  Google Scholar 

  • Fässler SMM, Payne MR, Brunel T, Dickey-Collas M (2011) Does larval mortality influence population dynamics? An analysis of North Sea herring (Clupea harengus) time series: North Sea herring larval mortality. Fish Oceanogr 20:530–543. doi:10.1111/j.1365-2419.2011.00600.x

    Article  Google Scholar 

  • Feet PØ, Ugland KI, Moksness E (2002) Accuracy of age estimates in spring spawning herring (Clupea harengus L.) reared under different prey densities. Fish Res 56:59–67

    Article  Google Scholar 

  • Ferron A, Leggett WC (1994) An appraisal of condition measures for marine fish larvae. Adv Mar Biol 30:217–303

    Article  Google Scholar 

  • Fiksen Ø, Folkvord A (1999) Modelling growth and ingestion processes in herring Clupea harengus larvae. Mar Ecol Prog Ser 184:273–289

    Article  Google Scholar 

  • Foley CJ, Bradley DL, Höök TO (2016) A review and assessment of the potential use of RNA:DNA ratios to assess the condition of entrained fish larvae. Ecol Indic 60:346–357. doi:10.1016/j.ecolind.2015.07.005

    Article  CAS  Google Scholar 

  • Folkvord A, Rukan K, Johannessen A, Moksness E (1997) Early life history of herring larvae in contrasting feeding environments determined by otolith microstructure analysis. J Fish Biol 51:250–263

    Article  Google Scholar 

  • Folkvord A, Blom G, Johannessen A, Moksness E (2000) Growth-dependent age estimation in herring (Clupea harengus L.) larvae. Fish Res 46:91–103

    Article  Google Scholar 

  • Fossum P, Johannessen A (1979) Field and Laboratory Studies of Herring Larvae (Clupea harengus L.). ICES, Council meeting 1979/H: 28

  • Fox CJ, Folkvord A, Geffen AJ (2003) Otolith micro-increment formation in herring Clupea harengus larvae in relation to growth rate. Mar Ecol Prog Ser 264:83–94

    Article  Google Scholar 

  • Gasparini S, Antajan E (2013) PLANKTON IDENTIFIER: a software for automatic recognition of planktonic organisms. http://www.obs-vlfr.fr/~gaspari/Plankton_Identifier/index.php. Accessed 30 Nov 2016

  • Geffen AJ (1982) Otolith ring deposition in relation to growth rate in herring (Clupea harengus) and turbot (Scophthalmus maximus) larvae. Mar Biol 71:317–326

    Article  Google Scholar 

  • Geffen AJ (1986) The growth of herring larvae, Clupea harengus L., in the Clyde: an assessment of the suitability of otolith ageing methods. J Fish Biol 28:279–288

    Article  Google Scholar 

  • Giraldo C (2012) Ecologie trophique du poisson Pleuragramma antarcticum dans l’Est Antarctique. Thesis, Université Pierre et Marie Curie-Paris VI

  • Giraldo C, Mayzaud P, Tavernier E et al (2015) Lipid dynamics and trophic patterns in Pleuragramma antarctica life stages. Antarct Sci 27:429–438. doi:10.1017/S0954102015000036

    Article  Google Scholar 

  • Giraldo C, Boutoute M, Mayzaud P et al (2016) Lipid dynamics in early life stages of the icefish Chionodraco hamatus in the Dumont d’Urville Sea (East Antarctica). Polar Biol. doi:10.1007/s00300-016-1956-4

    Google Scholar 

  • Gorsky G, Ohman MD, Picheral M et al (2010) Digital zooplankton image analysis using the ZooScan integrated system. J Plankton Res 32:285–303. doi:10.1093/plankt/fbp124

    Article  Google Scholar 

  • Grioche A (1998) Dynamique de l’écophase ichtyoplanctonique en Manche orientale et sud Mer du Nord. Approche multispécifique et description de deux espèces cibles : Solea solea (L.) et Pleuronectes flesus (L.). Thesis, Université du Littoral Côte d’Opale

  • Grosjean P, Picheral M, Warembourg C, Gorsky G (2004) Enumeration, measurement, and identification of net zooplankton samples using the ZOOSCAN digital imaging system. ICES J Mar Sci 61:518–525. doi:10.1016/j.icesjms.2004.03.012

    Article  Google Scholar 

  • Harden-Jones FR (1968) Fish migration. St. Martin’s, New York

    Google Scholar 

  • Harlay X, Koubbi P, Grioche A (2001) Ecology of plaice (Pleuronectes platessa) in fish assemblages of beaches of the Opale coast (North of France) during spring 1997. Cybium 25:67–80

    Google Scholar 

  • Haslob H, Rohlf N, Schnack D (2009) Small scale distribution patterns and vertical migration of North Sea herring larvae (Clupea harengus, Teleostei: Clupeidea) in relation to abiotic and biotic factors. Sci Mar 73:13–22. doi:10.3989/scimar.2009.73s1013

    Article  Google Scholar 

  • Hay DE (1981) Effects of capture and fixation on gut contents and body size of Pacific herring larvae. Rapp P-V Reun Cons 178:395–400

    Google Scholar 

  • Heath M, Scott B, Bryant AD (1997) Modelling the growth of herring from four different stocks in the North Sea. J Sea Res 38:413–436

    Article  Google Scholar 

  • Hempel G (1960) Untersuchungen über die Verbreitung der Heringslarven im Englischen Kanal und der südlichen Nordsee im Januar 1959. Helgoländer Wiss Meeresunters 7:72

    Article  Google Scholar 

  • Hoff GR, Fuiman LA (1995) Environmentally induced variation in elemental composition of red drum (Sciaenops ocellatus) otoliths. Bull Mar Sci 56:578–591

    Google Scholar 

  • Høie H, Folkvord A, Johannessen A (1999) Maternal, paternal and temperature effects on otolith size of young herring (Clupea harengus L.) larvae: an experimental study. J Exp Mar Biol Ecol 234:167–184

    Article  Google Scholar 

  • Houde ED (1987) Fish early life dynamics and recruitment variability. R Hoyt Am Fish Soc Symp 2:17–29

    Google Scholar 

  • Houde ED (1997) Patterns and trends in larval-stage growth and mortality of teleost fish. J Fish Biol 51:52–83

    Article  Google Scholar 

  • Houde ED (2008) Emerging from Hjort’s shadow. J Northw Atl Fish Sci 41:53–70. doi:10.2960/J.v41.m634

    Article  Google Scholar 

  • Hufnagl M, Peck MA (2011) Physiological individual-based modelling of larval Atlantic herring (Clupea harengus) foraging and growth: insights on climate-driven life-history scheduling. ICES J Mar Sci 68:1170–1188. doi:10.1093/icesjms/fsr078

    Article  Google Scholar 

  • Hufnagl M, Peck MA, Nash RDM, Dickey-Collas M (2015) Unravelling the Gordian knot! Key processes impacting overwintering larval survival and growth: a North Sea herring case study. Prog Oceanogr 138:486–503. doi:10.1016/j.pocean.2014.04.029

    Article  Google Scholar 

  • ICES (2015) Report of the Herring Assessment Working Group for the Area South of 62°N (HAWG). ICES HQ, Copenhagen

    Google Scholar 

  • Irigoien X, Cotano U, Boyra G et al (2008) From egg to juvenile in the Bay of Biscay: spatial patterns of anchovy (Engraulis encrasicolus) recruitment in a non-upwelling region. Fish Oceanogr 17:446–462. doi:10.1111/j.1365-2419.2008.00492.x

    Article  Google Scholar 

  • John EH, Batten SD, Harris RP, Hays GC (2001) Comparison between zooplankton data collected by the Continuous Plankton Recorder survey in the English Channel and by WP-2 nets at station L4, Plymouth (UK). J Sea Res 46:223–232

    Article  Google Scholar 

  • Kimura R (2000) Nutritional condition of first-feeding larvae of Japanese sardine in the coastal and oceanic waters along the Kuroshio Current. ICES J Mar Sci 57:240–248. doi:10.1006/jmsc.2000.0663

    Article  Google Scholar 

  • Kiørboe T, Møhlenberg F, Nicolajsen H (1982) Ingestion rate and gut clearance in the planktonic copepod Centropages hamatus (Lilljeborg) in relation to food concentration and temperature. Ophelia 21:181–194. doi:10.1080/00785326.1982.10426586

    Article  Google Scholar 

  • Kiørboe T, Munk P, Støttrup JG (1985) First feeding by larval herring Clupea harengus L. Dana 5:95–107

    Google Scholar 

  • Kiørboe T, Munk P, Richardson K (1987) Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Mar Ecol Prog Ser 40:1–10

    Article  Google Scholar 

  • Kiørboe T, Munk P, Richardson K et al (1988) Dynamics and larval herring growth, drift and survival in a frontal area. Mar Ecol Prog Ser 44:205–219

    Article  Google Scholar 

  • Koubbi P, Vallet C, Razouls S et al (2007) Condition and diet of larval Pleuragramma antarcticum (Nototheniidae) from Terre Adélie (Antarctica) during summer. Cybium 31:67–76

    Google Scholar 

  • Le Pape O, Bonhommeau S (2015) The food limitation hypothesis for juvenile marine fish. Fish Fish 16:373–398. doi:10.1111/faf.12063

    Article  Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR, an R package for multivariate analysis. J Stat Softw 25:1–18

    Article  Google Scholar 

  • Lebour MV (1924) The food of young herring. J Mar Biol 13:325–330

    Article  Google Scholar 

  • Legendre P, Legendre LF (2012) Numerical ecology, vol 24. Elsevier, New York

    Google Scholar 

  • Lelièvre S, Verrez-Bagnis V, Jerome M, Vaz S (2010) PCR-RFLP analyses of formalin-fixed fish eggs for the mapping of spawning areas in the Eastern Channel and Southern North Sea. J Plankton Res 32:1527–1539. doi:10.1093/plankt/fbq067

    Article  CAS  Google Scholar 

  • Lelièvre S, Antajan E, Vaz S (2012) Comparison of traditional microscopy and digitized image analysis to identify and delineate pelagic fish egg spatial distribution. J Plankton Res 34:470–483. doi:10.1093/plankt/fbs015

    Article  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    Article  CAS  Google Scholar 

  • Lough RG, Pennington M, Bolz GR, Rosenberg AA (1982) Age and growth of larval Atlantic herring, Clupea harengus L., in the Gulf of Maine-Georges Bank region based on otolith growth increments. Fish Bull (Wash DC) 80:187–199

    Google Scholar 

  • Mackas D, Bohrer R (1976) Fluorescence analysis of zooplankton gut contents and an investigation of diel feeding patterns. J Exp Mar Biol Ecol 25:77–85

    Article  Google Scholar 

  • Mastail M, Battaglia A (1978) Amélioration de la conservation des pigments du zooplancton. In: CIEM Conseil International pour l’Exploration de la Mer, Comité de l’Océanographie biologique, CM 1978/L: 20

  • Mathers EM, Houlihan DF, Burren LJ (1994) RNA, DNA and protein concentrations in fed and starved herring Clupea harengus larvae. Mar Ecol Prog Ser 107:223–231

    Article  CAS  Google Scholar 

  • Maucorps A (1969) Biologie et pêche du hareng en mer du nord, son exploitation rationnelle. Sci Pêche 186:1–8

    Google Scholar 

  • McGurk MD (1984) Effects of delayed feeding and temperature on the age of irreversible starvation and on the rates of growth and mortality of Pacific herring larvae. Mar Biol 84:13–26

    Article  Google Scholar 

  • McGurk MD (1986) Natural mortality of marine pelagic fish eggs and larvae: role of spatial patchiness. Mar Ecol Prog Ser 34:227–242

    Article  Google Scholar 

  • Moksness E (1992) Validation of daily increments in the otolith microstructure of Norwegian spring-spawning herring (Clupea harengus L.). ICES J Mar Sci J Cons 49:231–235

    Article  Google Scholar 

  • Moksness E, Butler J, Radtke RL (1987) Estimation of age and growth rate in Norwegian spring spawning herring (Clupea harengus) larvae and juveniles. Sarsia 72:341–342

    Article  Google Scholar 

  • Mosegaard H, Svedäng H, Taberman K (1988) Uncoupling of somatic and otolith growth rates in arctic char (Salvelinus alpinus) as an effect of differences in temperature response. Can J Fish Aquat Sci 45:1514–1524. doi:10.1139/f88-180

    Article  Google Scholar 

  • Motoda S (1959) Devices of simple plankton apparatus. Mem Fac Fish Hokkaido Univ 7:73–94

    Google Scholar 

  • Munk P, Kiørboe T (1985) Feeding behaviour and swimming activity of larval herring (Clupea harengus) in relation to density of copepod nauplii. Mar Ecol Prog Ser 24:15–21

    Article  Google Scholar 

  • Munk P, Nielsen JL (2005) Eggs and larvae of North Sea fishes. Biofolia, Frederiksberg

    Google Scholar 

  • Munk P, Kiørboe T, Christensen V (1989) Vertical migrations of herring, Clupea harengus, larvae in relation to light and prey distribution. Environ Biol Fish 26:87–96

    Article  Google Scholar 

  • Oeberst R, Dickey-Collas M, Nash RD (2009) Mean daily growth of herring larvae in relation to temperature over a range of 5–20°C, based on weekly repeated cruises in the Greifswalder Bodden. ICES J Mar Sci 66:1696–1701

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2013) Package “vegan”. R Packag Ver 254:20–28

    Google Scholar 

  • Pannella G (1971) Fish otoliths: daily growth layers and periodical patterns. Science 173:1124–1127

    Article  Google Scholar 

  • Pannella G (1974) Otolith growth patterns: an aid in age determination in temperate and tropical fishes. In: Bagenal TB (ed) The aging of fish. Unwin Brothers, Old Woking, pp 28–39

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis, vol 395. Pergamon Press, Oxford, pp 475–490

    Google Scholar 

  • Pasternak AF (1994) Gut fluorescence in herbivorous copepods: an attempt to justify the method. Hydrobiol 292:241–248

    Article  Google Scholar 

  • Paulsen M, Clemmesen C, Hammer C et al (2016) Food-limited growth of larval Atlantic herring Clupea harengus recurrently observed in a coastal nursery area. Helgol Mar Res 70:17. doi:10.1186/s10152-016-0470-y

    Article  Google Scholar 

  • Payne MR, Hatfield EM, Dickey-Collas M et al (2009) Recruitment in a changing environment: the 2000s North Sea herring recruitment failure. ICES J Mar Sci J Cons 66:272–277

    Article  Google Scholar 

  • Peck MA, Baumann H, Clemmesen C et al (2015) Calibrating and comparing somatic-, nucleic acid-, and otolith-based indicators of growth and condition in young juvenile European sprat (Sprattus sprattus). J Exp Mar Biol Ecol 471:217–225. doi:10.1016/j.jembe.2015.06.011

    Article  Google Scholar 

  • Pedersen BH (1984) The intestinal evacuation rates of larval herring (Clupea harengus L) predating on wild plankton. Dana 3:1–30

    Article  Google Scholar 

  • Pepin P, Evans GT, Shears TH (1999) Patterns of RNA/DNA ratios in larval fish and their relationship to survival in the field. ICES J Mar Sci J Cons 56:697–706

    Article  Google Scholar 

  • Pepin P, Robert D, Bouchard C et al (2015) Once upon a larva: revisiting the relationship between feeding success and growth in fish larvae. ICES J Mar Sci 72:359–373. doi:10.1093/icesjms/fsu201

    Article  Google Scholar 

  • Petitgas P, Rijnsdorp AD, Dickey-Collas M et al (2013) Impacts of climate change on the complex life cycles of fish. Fish Oceanogr 22:121–139. doi:10.1111/fog.12010

    Article  Google Scholar 

  • Radtke RL, Fey DP (1996) Environmental effects on primary increment formation in the otoliths of newly hatched Arctic charr. J Fish Biol 48:1238–1255

    Google Scholar 

  • Radtke RL, Townsend DW, Folsom SD, Morrison MA (1990) Strontium: calcium concentration ratios in otoliths of herring larvae as indicators of environmental histories. Environ Biol Fishes 27:51–61

    Article  Google Scholar 

  • Rooker JR, Holt GJ (1996) Application of RNA:DNA ratios to evaluate the condition and growth of larval and juvenile red drum (Sciaenops ocellatus). Mar Freshw Res 47:283–290

    Article  CAS  Google Scholar 

  • Russell FS (1976) The eggs and Planktonic stages of British Marine Fishes. Academic, London

    Google Scholar 

  • Secor DH, Dean JM, Laban EH (1993) Otolith removal and preparation for microstructural examination. Can Spec Publ Fish Aquat Sci 117:19

    Google Scholar 

  • Suthers IM (1998) Bigger? Fatter? Or is faster growth better? Considerations on condition in larval and juvenile coral-reef fish. Aust J Ecol 23:265–273

    Article  Google Scholar 

  • Theilacker GH, Bailey KM, Canino MF, Porter SM (1996) Variations in larval walleye pollock feeding and condition: a synthesis. Fish Oceanogr 5:112–123

    Article  Google Scholar 

  • Tranter DJ, Smith PE (1996) Filtration performance. Fiheries Oceanogr 2:27–56

    Google Scholar 

  • Waldman JR (1961) Untersuchungen an Heringslarven und Zooplankton des Greifswalder Boddens in den Jahren 1958 und 1959. Zeitschriften Für Fischerei 10:523–536

    Google Scholar 

  • Weber W (1971) Die Laichplätze des Herings (Clupea harengus L.) der westlichen Ostsee. Kiel Meeresforsch 27:197–208

    Google Scholar 

  • Wright PJ (1991) The influence of metabolic rate on otolith increment width in Atlantic salmon parr, Salmo salar L. J Fish Biol 38:929–933

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge IFREMER and the Pôle Métropolitain de la Côte d’Opale for their financial supports. They also would like to thank the scientific staff and crew of the RV Thalassa involved each year in the IBTS survey. Finally, the authors are very grateful to the two anonymous referees and the editor, who helped to greatly improve the initial manuscript with their positive and constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christophe Loots.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: C. Harrod.

Reviewed by M. Paulsen and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Denis, J., Mahe, K., Tavernier, E. et al. Ontogenetic changes in the larval condition of Downs herring: use of a multi-index approach at an individual scale. Mar Biol 164, 154 (2017). https://doi.org/10.1007/s00227-017-3180-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3180-3

Navigation