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