Investigating environmental influence and temporal changes in sole (Solea solea) larvae condition using histology

https://doi.org/10.1016/j.ecss.2020.107161Get rights and content

Highlights

  • First feeding stage corresponds to the critical most period during sole larval ontogeny.

  • Good larval condition was related to estuarine areas in the Eastern English Channel.

  • Lower sole larval abundances in spring 2017 compared to spring 1995.

  • Environment suitable for a good sole larvae condition was more limited in 2017.

Abstract

In the eastern part of the English Channel, common sole (Solea solea) has strong interests in fisheries research. Low recruitment along with a decline in spawning stock biomass have been observed for several years. According to the recruitment hypotheses, larval survival may play an important role that needs to be considered. The fish larval condition can be assessed using histology which has been recognised as the most appropriate method to provide a reliable index of the nutritional status. Based on this approach, this study aimed to identify critical periods of wild-collected sole larvae and to determine sources of variations of their condition between two periods separated by more than 20 years. In line with other studies, the transition from endogenous to exogenous feeding was identified as the most critical period with the lowest proportion of healthy larvae observed. During this first feeding stage, good larval conditions were located in sampling stations close to the coast and at the end of the spring season, in relation to higher temperature and fluorescence values. This highlights the need for sole larvae survival to cross the coastal front, which splits the central and coastal waters, to reach more stable and productive areas. This coastal migration pattern was consistent between 1995 and 2017, with however significantly lower larval abundances in the recent period. Multivariate analyses showed that the spring environmental conditions of 1995, characterised with lower temperature and higher fluorescence values were more favourable to larval condition, compared to the spring in 2017. Areas providing suitable environmental conditions in 2017 were more restricted and limited to sampling stations in front of estuaries. Since small differences in larval survival can lead to large fluctuations in recruitment, the larval condition should be studied in a more long-term approach. This would provide a better understanding of the environmental influence on larval survival and recruitment success.

Introduction

In the eastern English Channel (EEC), common sole (Solea solea) spawning occurs from February to June close to the coasts (Eastwood et al., 2001). The pelagic phase lasts about six weeks (Vaz et al., 2019). Dispersion, nychthemeral and tidal migrations drive larval settlement in the coastal and estuarine nursery grounds during metamorphosis (Grioche et al., 2000, 2001; Koutsikopoulos et al., 1989; Rochette et al., 2012). There is some evidence that the population is supplied by a pool of three distinct nurseries: along the English coast, the Seine Bay area, and the nurseries along the south-east coasts of the EEC including the three estuaries Somme, Authie and Canche (Du Pontavice et al., 2018; Rochette et al., 2013). Juveniles settle down for two years before recruiting into the adult population, with very low connectivity between the different nursery pools mentioned above (Le Pape and Cognez, 2016). This strong spatial structuration seems to persist during the adult phase (Du Pontavice et al., 2018; Lecomte et al., 2019; Randon et al., 2018, 2020). However, the EEC sole stock remains assessed and managed as a single, spatially homogeneous population (ICES division 107D).

The ECC common sole is a stock of high economic value in the area (Gibson et al., 2014). Since many fleets rely on it, the stock has been the subject of particular attention for several years. Low recruitment along with a decline in spawning stock biomass, which is now around Blim (i.e stock size below which there is a high risk of reduced recruitment), have been observed since 2011 (ICES, 2018) despite the stock management being close to Maximum Sustainable Yield (MSY). Likewise, the potential role of the larval phase, especially its survival rate, remains misunderstood and needs to be considered.

Many hypotheses for recruitment success rely on larval survival which requires favourable transport as well as a spatial and temporal coincidence of fish larvae with their trophic resources (Somarakis et al., 2017). Since the number of offspring recruiting in the adult population is not necessarily proportional to the spawning biomass (Anderson, 1988; Houde, 2008), larval starvation and predation have been accepted as major sources of variability in larval survival and recruitment (Peck et al., 2012).

Food deprivation in fish larvae can be assessed using condition indices (Ferron and Leggett, 1994). Many indices are available to highlight the effects of starvation on growth and nutritional condition (Buckley, 1979; Clemmesen, 1994; Diaz et al., 2018), energy reserves (Fraser, 1989; Giraldo et al., 2011) or tissue integrity (Diaz et al., 2013; O'Connell, 1976; Theilacker, 1978). The latter is an integrative approach of the level of starvation and can be evaluated using histology. Histological-based observations have been recognised as the most appropriate method to provide a reliable index of the larval nutritional status (Di Pane et al., 2019; Ferron and Leggett, 1994; Gisbert et al., 2008). It informs on the direct effects of starvation on the organs state, especially those related to nutrition (e.g guts, liver, and pancreas). Indeed, food deprivation leads to abnormal development and degeneration of cells and tissues regardless of stages or species. (McFadzen et al., 1997; O'Connell, 1976; Sieg, 1998).

The present work aims to evaluate the sole larval condition on the French side of the EEC. Using a histological condition index developed and calibrated experimentally on sole larvae, the objectives are (1) to evaluate larval condition and identify the critical period(s); (2) to determine environmental sources of variation in the condition; and (3) to study temporal changes in these factors and their impact on the larval condition between two periods more than 20 years apart. In line with the recruitment assumptions, we expect a higher starvation incidence for first feeding larvae. Moreover, in a context of changing environment and low recruitment observed for sole since 2011, we expect individuals collected in 2017 to display poorer condition and/or lower abundances than cohorts from two decades ago.

Section snippets

Data origins

Data used in this study come from oceanographic surveys conducted in spring 1995 and 2017 (Fig. 1). Histological data on sole larvae captured during spring 1995 are based on work carried out by Grioche (1998). The same methodology for sampling and larval condition analyses was used for the two periods to ensure comparability.

Surveys

Data come from five ichthyoplanktonic surveys that were conducted in the EEC between March and May in 1995 and 2017 (Table 1, see Grioche et al. (2001) and Di Pane et al.

Sole larvae abundances

Abundances and proportions of the different developmental stages of sole larvae were calculated and compared between surveys. An effect of the survey on abundances was observed (ANOVA: F = 13.27; df = 4; P < 0.01). The results of the differences highlighted by the Tukey post-hoc test are shown in Appendix A.1. Maps of the different developmental stages proportions are also given in appendix (Appendix A.2).

In April 1995 (REISE 1), no stage 1 larvae were captured and stage 2 larvae were largely

Discussion

In this study, abundances and the influence of the environment on the nutritional condition of sole larvae during the spring were investigated. Differences between 1995 and 2017 were studied. According to our hypothesis, we observed lower larval abundances in 2017. A higher starvation incidence for first feeding larvae was also highlighted. This poor condition was even more pronounced in 2017 compared to 1995 due to a lower availability of suitable area.

Conclusion

The present study confirmed that transition from endogenous to exogenous feeding corresponded to a critical step. Also, transition from pelagic to benthic life appeared to be potentially another major critical period in early-life history of flatfish. These two transitional stages could represent bottlenecks in larval survival and, as a consequence, to the number of fishes recruiting in the adult population. This study also provided a methodological example of how the larval condition

Author statement

Julien Di Pane: Conceptualization, Data curation, Formal analysis, Investigation; Methodology; Visualization; Software; Writing - original draft; Writing - review & editing.

Philippe Koubbi: Conceptualization, Data curation, Funding acquisition, Investigation; Methodology, Resources, Project administration, Supervision; Validation.

Felix Gendrot: Formal analysis.

Carolina Giraldo: Conceptualization; Supervision; Validation.

Stephane Karasiewicz: Formal analysis; Software; Validation; Visualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We would like to thank the Pôle Metropolitain de la Côte d'Opale and the SMAC (Sole de Manche Est) project (supported by France Filière Pêche and the Hauts-de-France region) for their financial support. Our acknowledgments are also dedicated to all persons involved in the three recent surveys, especially Eric Tavernier, Léa Joly, Romain Causse, Ugo Werner and Felipe Artigas as scientist in charge of the PHYCO survey.

References (81)

  • A. Ferron et al.

    An appraisal of condition measures for marine fish larvae*

  • A.J. Geffen et al.

    The cost of metamorphosis in flatfishes

    J. Sea Res.

    (2007)
  • C. Giraldo et al.

    Ontogenic changes in the feeding ecology of the early life stages of the Antarctic silverfish (Pleuragramma antarcticum) documented by stable isotopes and diet analysis in the Dumont d'Urville Sea (East Antarctica)

    Pol. Sci.

    (2011)
  • A. Grioche et al.

    Spatial patterns of ichthyoplankton assemblages along the eastern English channel French coast during spring 1995

    Estuar. Coast Shelf Sci.

    (1999)
  • W.S. Gwak et al.

    Nutritional condition, as evaluated by RNA/DNA ratios, of hatchery-reared Japanese flounder from hatch to release

    Aquaculture

    (2003)
  • O. Le Pape et al.

    The range of juvenile movements of estuarine and coastal nursery dependent flatfishes: estimation from a meta-analytical approach

    J. Sea Res.

    (2016)
  • W.C. Leggett et al.

    Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages?

    Neth. J. Sea Res.

    (1994)
  • I.R.B. McFadzen et al.

    Histological indices of the nutritional condition of sardine, Sardina pilchardus (Walbaum) larvae off the north coast of Spain

    J. Exp. Mar. Biol. Ecol.

    (1997)
  • C.P. O'Connell

    Histological criteria for diagnosing the starving condition in early post yolk sac larvae of the northern anchovy, Engraulis mordax Girard

    J. Exp. Mar. Biol. Ecol.

    (1976)
  • M.A. Peck et al.

    Chapter 3 - intrinsic and extrinsic factors driving match–mismatch dynamics during the early life history of marine fishes

  • M. Randon et al.

    Could we consider a single stock when spatial sub-units present lasting patterns in growth and asynchrony in cohort densities? A flatfish case study

    J. Sea Res.

    (2018)
  • E.H. Ahlstrom

    Ontogeny and Systematics of Fishes: Based on an International Symposium Dedicated to the Memory of Elbert Halvor Ahlstrom

    (1984)
  • S. Alvarez-Fernandez et al.

    Temporal changes in plankton of the North Sea: community shifts and environmental drivers

    Mar. Ecol. Prog. Ser.

    (2012)
  • J.T. Anderson

    A review of size-dependent survival during pre-recruit stages of fishes in relation to recruitment

    J. Northwest Atl. Fish. Sci.

    (1988)
  • A. Auber et al.

    Regime shift in an exploited fish community related to natural climate oscillations

    PloS One

    (2015)
  • M. Boulhic

    Recherches d’indices de jeûne chez la larve de sole, Solea solea (Linnaeus, 1758): approche expérimentale et application dans le golfe de Gascogne

    (1991)
  • P. Brosset et al.

    A fine-scale multi-step approach to understand fish recruitment variability

    Sci. Rep.

    (2020)
  • J.-M. Brylinski et al.

    L’interface eaux côtières/eaux du large dans le Pas-de-Calais (côte française) : une zone frontale

    Comptes Rendus Académie Sci. Sér. 2 Mécanique Phys. Chim. Sci. Univers Sci. Terre

    (1990)
  • L.J. Buckley

    Relationships between RNA–DNA ratio, prey density, and growth rate in atlantic cod (Gadus morhua) larvae

    J. Fish. Res. Board Can.

    (1979)
  • I.A. Catalán

    Condition Indices and Their Relationship with Environmental Factors in Fish Larvae

    (2003)
  • I. Catalán et al.

    Link between environmental anomalies, growth and condition of pilchard Sardina pilchardus larvae in the northwestern Mediterranean

    Mar. Ecol. Prog. Ser.

    (2006)
  • C. Clemmesen

    The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration

    Mar. Biol.

    (1994)
  • J. Di Pane et al.

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

    PloS One

    (2019)
  • M.V. Diaz et al.

    The use of morphological and histological features as nutritional condition indices of Pagrus pagrus larvae

    Neotrop. Ichthyol.

    (2013)
  • M.V. Diaz et al.

    Ontogenetic changes in DNA and RNA content of laboratory-reared Prochilodus lineatus larvae: use of RNA/DNA ratios as indicators of nutritional condition

    Mar. Freshw. Res.

    (2018)
  • S. Dolédec et al.

    Niche separation in community analysis: a new method

    Ecology

    (2000)
  • M. Dufrêne et al.

    Species assemblages and indicator species: the need for a flexible asymmetrical approach

    Ecol. Monogr.

    (1997)
  • J.P. Dupont et al.

    La dynamique des masses d’eaux et des matieres en suspension en Manche Orientale

    Oceanol. Acta

    (1991)
  • S. Dray et al.

    The ade4 package: implementing the duality diagram for ecologists

    J. Stat. Software

    (2007)
  • P.D. Eastwood et al.

    Modelling spatial variations in spawning habitat suitability for the sole Solea solea using regression quantiles and GIS procedures

    Mar. Ecol. Prog. Ser.

    (2001)
  • Cited by (0)

    View full text