# Body condition decline in Western european fishes

M Gernez, Marie Savina-Rolland, D Gascuel, Morgane Travers-Trolet

► To cite this version:

M Gernez, Marie Savina-Rolland, D Gascuel, Morgane Travers-Trolet. Body condition decline in Western european fishes. Marine Environmental Research, 2025, 211, pp.107428. 10.1016/j.marenvres.2025.107428. hal-05219033

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Submitted on 22 Aug 2025

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# Body condition decline in Western european fishes

M. Gernez<sup>a, *</sup> , M. Savina-Rolland<sup>b</sup>, D. Gascuel<sup>c</sup>, M. Travers-Trolet<sup>a</sup>

ARTICLE INFO

Keywords:

Bay of biscay

Bottom-up control

Celtic sea

Decadal trends

Density-dependence

Morphometric condition factor

A B S T R A C T

The body condition of small pelagic fish has been declining since the early 2000s in several ecosystems, including the Mediterranean Sea and the Bay of Biscay, probably in response to bottom-up control. Possible trends in body condition of demersal and benthic species in the same regions have so far received little attention. Using a North East Atlantic case study (Bay of Biscay and Celtic Sea), we computed Le Cren's relative body condition index for 264,000 fish individuals from 17 species, based on individual length and weight data collected between 2002 and 2022. Using linear models, a decreasing trend in body condition was evidenced for 12 species, while only two species showed an increase. Anchovy (*Engraulis encrasicolus*), plaice (*Pleuronectes platessa*), megrim (*Lepidorhombus whiffiagonis*) and sardine (*Sardina pilchardus*) have suffered the greatest declines. For these species, individual weight at equivalent size decreased by 3–5 % per decade. The variability between individuals' body condition was mainly explained by sex and sampling season. Among the other variables tested, stock biomass and chlorophyll-a concentration had significant effects on a majority of species, while sea surface temperature did not explain much variability. The declining trend of body condition at the fish community scale could then be partly explained by bottom-up control, but probably also involved complex interactions at the ecosystem scale. Beyond the possible consequences on fish provisioning quality, the prevalence of declining body condition of various fish should be considered as a warning on possible important changes in the overall functioning of marine food-webs.

1. Introduction

Body condition is a fundamental concept in ecology for studying physiological, energetic and nutritional status of animals, and is widely used in marine environments (Stevenson and Woods, 2006). Fish energy reserves can be assessed through various morphological, biogeochemical and physiological metrics, associated with different precision, feasibility constraints and assumptions (see Lloret et al. (2013) for a review). Among them, morphometric body condition, based on the observed weight for a given length, can be interpreted as the well-being of an individual under the hypothesis that heavier fish are in better condition (Le Cren, 1951). Although this morphometric index is not a direct measure of energy reserves, it has been found to reflect the quantity and, to a lesser extent, the quality of lipid reserves, as well as broader physiological status, such as metabolism- and stress-related cortisol levels (Brosset et al., 2023).

Morphometric body condition globally informs on fish health and varies according to various factors. Endogenous factors including the sex of an individual and its stage of maturity can induce variations in body

condition, particularly evidenced for spawning females (Froese, 2006). Individual variations can also result from environmental variability, from intra- and interspecific competition or from the quantity or quality of available food (Lloret et al., 2013). Furthermore, changes in physiological processes, linked to variations in temperature or oxygen levels in the environment (Todd et al., 2008; Limburg and Casini, 2019), or to energy allocation (Beauvieux et al., 2022), as well as the presence of parasites (Timi and Poulin, 2020), can also result in variations of body condition. These variations have been studied to assess the consequences of anthropogenic pressures (Cavraro et al., 2019), climate change (Stevenson and Woods, 2006), habitat quality (Champion et al., 2020) or fisheries management (Lloret et al., 2012). Assessing morphometric body condition offers multiple benefits: it serves as an indicator of both environment and individual fitness, it is inexpensive, non-destructive, it can be rapidly collected and easily calculated from historical datasets (Lloret et al., 2013).

Over the last decade, morphometric body condition has been widely used in studies focusing on one or few species (Gulf of St. Lawrence cod, Lambert and Dutil, 1997; Baltic cod, Limburg and Casini, 2019),

<footnote><sup>a</sup> DECOD, L'Institut Agro, IFREMER, INRAE, 44000, Nantes, France</footnote>

<footnote><sup>b</sup> DECOD, L'Institut Agro, IFREMER, INRAE, 56100, Lorient, France</footnote>

<footnote><sup>c</sup> DECOD, L'Institut Agro, IFREMER, INRAE, 35000, Rennes, France</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: mael.gernez@ifremer.fr (M. Gernez).</footnote>
<figure><img src="image_3.png" /><figcaption>Fig. 1. Location of the Celtic Sea (CS) and Bay of Biscay (BoB) highlighted in grey. Inset in the lower left corner: general location in Western Europe. The orange line represents the 200m isobath.</figcaption></figure>

especially on small pelagic fish in various ecosystems (Mediterranean sea, Albo-Puigserver et al., 2021; Black sea, Gücü et al., 2018; Bay of Biscay, Véron et al., 2020; Northern North Sea, Olafsdottir et al., 2016). The majority of these studies have demonstrated a decline in the condition of small pelagic fish over the past decades, probably due to environmental changes, through bottom-up control (i.e., limitation by resources; opposite of top-down control, regulation by predators). The main hypothesis put forward to explain this common decrease across various ecosystems is a direct effect of a reduction in the quantity and/or quality of prey (Menu et al., 2023), or an indirect effect through density-dependence mechanisms (Olafsdottir et al., 2016; Kamimura et al., 2021).

A bottom-up cause of body condition decline of small pelagic fish implies a poorer primary and/or secondary production in the ecosystem, which could also affect the entire food web. Furthermore, as small pelagic fish are a crucial prey group for higher trophic levels (Cury et al., 2000), their declining condition similarly indicates a decreasing quality of food for predators, which in turn could display a decrease in their body condition and/or a diet shift towards richer prey. Surprisingly though, body condition has rarely been studied in multi-species context with prey and predator species at the same time so the ecosystem scale implication of the declining condition of forage fish has not been assessed yet. A comprehensive investigation incorporating a broader

array of species would allow a better identification of the processes at play, whether they are linked to global change, to specific stock exploitation or to habitat perturbation, and could reveal large-scale patterns such as ecosystem-wide trophic cascade, or climate-induced changes in the structure and functioning of marine food-webs.

The Bay of Biscay (BoB) and Celtic Sea (CS) represent a large portion of the Western European continental shelf (Fig. 1). These areas underwent a decrease in fishing pressure over the last two decades, with the average fishing rate almost halved during that period, mainly due to more restrictive catch quota (Gascuel et al., 2016; ICES, 2022a; ICES, 2022b; Kempf et al., 2022). As a consequence, some stocks have improved, but others are still in a poor state (e.g. CS Gadus morhua, BoB Solea solea, Froese et al., 2018). BoB is an ecosystem where growth and body condition have been declining for small pelagic fish since the 2000s (Véron et al., 2020; Taboada et al., 2024), while there are no studies for demersal and benthic species (except seasonal variations for megrim, Lepidorhombus whiffiagonis, evidenced by Landa et al., 2022). Using BoB and CS as a case study, the aim of this work was to explore if the declining condition of small pelagic fish was also observed at the scale of the ecosystem, i.e. considering pelagic, demersal and benthic species, which would reveal a large-scale trend of fish condition.

First, the temporal trends of body condition over the last two decades were characterized for several species using linear models. Then, we
<figure><img src="image_4.png" /><figcaption>Fig. 2. Conceptual diagram summarizing the data processing workflow. Fisheries-dependent and fisheries-independent raw data are filtered and cleaned prior estimation of Length-Weight Relationship (LWR). Selection based on size range, assessment of a sex effect and removal of rare modalities to balance the factorial design are performed before integration of LWR parameters' estimates to produce body condition ($K_n$) data.</figcaption></figure>

sought to determine whether environmental conditions (including temperature and primary production proxy), density-dependence variables, or more complex mechanisms could explain variations in body condition. The overall objective of this multispecies study is to explore the possible propagation of the decline in body condition through the food web, from primary production to predatory fish, in a context of global decrease in fishing pressure (Gascuel et al., 2016; Hernvann and Gascuel, 2020).

## 2. Materials and methods

### 2.1. Study area and data collection

The temporal changes of body condition was studied in the continental shelf of Central-Western European waters, more precisely over the areas referred by the International Council for Exploration of the Sea (ICES) as ICES areas 7e-h,j (hereafter called the Celtic Sea or CS) and ICES areas 8ab (hereafter called the Bay of Biscay or BoB) (Fig. 1). To explore trends in body condition for several species, a large dataset has been compiled, using individual length-weight data from three different sources.

- The first dataset was produced from the French fishery-dependent sampling program, performed on commercial landings coming from thirty-eight English Channel and Atlantic fishing harbours. Individuals were randomly sampled, biological and sampling information were recorded, including individual length-weight, type of measurements, broad fishing area and date.

- The second dataset was compiled from French scientific surveys related to two major observation programs: PELGAS, which monitors the Bay of Biscay pelagic ecosystem during spring, and EVHOE which focusses on benthic and demersal species in the Celtic Sea and the Bay of Biscay in autumn. Additional samples were also obtained from other regular or project-based surveys, detailed in Supporting Information A.

- To complete the French datasets, the third dataset was compiled from international bottom and beam trawl surveys (available from DATRAS, Database of TRAwL Surveys), and contains data provided by Germany, Netherlands, Belgium, United Kingdom, Ireland, and Spain.

From the French dataset collection, a selection of species was made based on the number of individual data available. Only records located in our study area (Celtic Sea and Bay of Biscay) were kept, and only species with more than 1000 data, over 10 years at least and with a minimum of 30 data per year, were selected. Thus, 17 species had sufficient data between 2002 and 2022, and were included in the analysis. The pelagic compartment included European anchovy (Engraulis encrasicolus) and European sardine (Sardina pilchardus), while demersal

species were composed of Atlantic cod (Gadus morhua), greater haddock (Melanogrammus aeglefinus), European hake (Merluccius merluccius), red gurnard (Chelidonichthys cucusulus), European seabass (Dicentrarchus labrax), striped red mullet (Mullus surmuletus), whiting (Merlangius merlangus), and the benthic compartment was represented by black-bellied anglerfish (Lophius budegassa), lemon sole (Microstomus kitt), megrim (Lepidorhombus whiffiagonis), European plaice (Pleuronectes platessa), common sole (Solea solea), white anglerfish (Lophius piscatorius), and witch flounder (Glyptocephalus cynoglossus).

Then, the DATRAS dataset was filtered on the same study area, species list and time span. All length and weight measurements (French commercial and all scientific surveys) were conducted following the same method so that data were comparable and could be combined. A total of 311,711 data, from 2002 to 2022, were gathered for this analysis. In order to analyze the body condition of a large set of species, the dataset only focuses on length and weight measurements, and most of the individual data were not accompanied with age or maturity status observations. Detailed information on data sources, broad spatial distribution of samples and size distribution of samples by year is provided in Supporting Information A.

### 2.2. Relative body condition and data pre-processing

To avoid biases in comparing fish condition across large size ranges, due to potential allometric growth patterns (i.e. where the fish shape changes when its size increases), we used Le Cren (1951) relative condition factor (noted $K_n$) according to Froese (2006) recommendation. It was calculated for every individual fish as:

$$K_n = W / (aL^b) \quad (1)$$

With W the individual weight, L the individual length, a and b the coefficients of the allometric length-weight relationship fitted on our dataset. When $K_n$ is under 1, individuals are in poorer condition than average for a given size, conversely when it is higher than 1 they are in better condition.

The Le Cren index requires a length-weight relationship for each species. As a and b refer to the statistical population, all data were used to fit the length-weight relationship. Only data related to the measurement of total length and whole weight were included (i.e. gutted fish weight were not considered). Body weight (W, in g) and total length (L, in cm) were rounded down to the nearest gram, to the nearest half centimeter for small pelagic fish (sardine and anchovy) and the nearest centimeter for other species. Outliers were visually identified and removed. The Nonlinear Least-Square model (NLS, R software package stats, Bates and Watts, 1988) was used to fit the logarithmic relationship. Visual examination of the residual distribution was performed for each model, and the significance of the coefficient was analyzed using a Student t-test. The workflow of data processing is presented in Fig. 2.
<caption>**Table 1**</caption>

List of species used, their ecotype (P: Pelagic, D: Demersal, B: Benthic), data distribution between areas (BoB: CS), time span, length and weight ranges and sample size (N) used in body condition analyses.

<table><thead><tr><th>Species</th><th>Scientific name</th><th>Ecotype</th><th>Percentage of data in BoB: CS</th><th>Year range</th><th>Length range (cm)</th><th>Weight range (g)</th><th>N</th></tr></thead><tbody><tr><td>European anchovy</td><td>Engraulis encrasicolus</td><td>P</td><td>100:0</td><td>2003 - 2022</td><td>10.5 - 18</td><td>4 - 58</td><td>19739</td></tr><tr><td>European sardine</td><td>Sardina pilchardus</td><td>P</td><td>100:0</td><td>2002 - 2022</td><td>13.5 - 22.5</td><td>11 - 144</td><td>27789</td></tr><tr><td>Atlantic cod</td><td>Gadus morhua</td><td>D</td><td>0:100</td><td>2005 - 2022</td><td>37 - 77</td><td>334 - 6205</td><td>2041</td></tr><tr><td>Greater forkbeard</td><td>Phycis blennoides</td><td>D</td><td>41:59</td><td>2011 - 2021</td><td>16 - 47</td><td>13 - 1060</td><td>1329</td></tr><tr><td>Haddock</td><td>Melanogrammus aeglefinus</td><td>D</td><td>0:100</td><td>2003 - 2022</td><td>14 - 62</td><td>19 - 3444</td><td>27612</td></tr><tr><td>European hake</td><td>Merluccius merluccius</td><td>D</td><td>23:77</td><td>2003 - 2022</td><td>7 - 70</td><td>1 - 3310</td><td>18575</td></tr><tr><td>Red gurnard</td><td>Chelidonichthys cuculus</td><td>D</td><td>16:84</td><td>2006 - 2022</td><td>11 - 38</td><td>9 - 655</td><td>7777</td></tr><tr><td>European seabass</td><td>Dicentrarchus labrax</td><td>D</td><td>78:22</td><td>2010 - 2022</td><td>33 - 78</td><td>240 - 5610</td><td>7108</td></tr><tr><td>Striped red mullet</td><td>Mullus surmuletus</td><td>D</td><td>88:12</td><td>2006 - 2022</td><td>10 - 32</td><td>8 - 530</td><td>2757</td></tr><tr><td>Whiting</td><td>Merlangius merlangus</td><td>D</td><td>0:100</td><td>2003 - 2022</td><td>9 - 54</td><td>2 - 1770</td><td>27712</td></tr><tr><td>Black-bellied anglerfish</td><td>Lophius budegassa</td><td>B</td><td>10:90</td><td>2006 - 2022</td><td>9 - 62</td><td>11 - 4348</td><td>6549</td></tr><tr><td>Lemon sole</td><td>Microstomus Kitt</td><td>B</td><td>0:100</td><td>2002 - 2022</td><td>13 - 31</td><td>19 - 545</td><td>10738</td></tr><tr><td>Megrim</td><td>Lepidorhombus whiffiagonis</td><td>B</td><td>11:89</td><td>2003 - 2022</td><td>10 - 50</td><td>1 - 1250</td><td>27230</td></tr><tr><td>European plaice</td><td>Pleuronectes platessa</td><td>B</td><td>0:100</td><td>2002 - 2022</td><td>15 - 42</td><td>17 - 1250</td><td>26834</td></tr><tr><td>Common sole</td><td>Solea solea</td><td>B</td><td>61:39</td><td>2002 - 2022</td><td>9 - 41</td><td>2 - 990</td><td>35085</td></tr><tr><td>White anglerfish</td><td>Lophius piscatorius</td><td>B</td><td>9:91</td><td>2003 - 2022</td><td>9 - 73</td><td>12 - 7285</td><td>10447</td></tr><tr><td>Witch flounder</td><td>Glyptocephalus cynoglossus</td><td>B</td><td>0:100</td><td>2009 - 2022</td><td>20 - 43</td><td>30 - 753</td><td>4817</td></tr></tbody></table>
<figure><img src="image_5.png" /><figcaption>Fig. 3. Temporal changes in body condition for each species. Each line corresponds to the year effect in the linear regression (see Supporting Information D for the equations for each species). The dark orange lines indicate a significant strong decrease (greater than 3 % per decade), light orange lines a significant decrease, the green lines indicate a significant increase, and the black dashed lines indicate no significant trend.</figcaption></figure>

## 2.3. Environmental and density-dependence variables

Satellite-derived Sea Surface Temperature (SST, °C) and Chlorophyll-α (Chla, mg.m⁻³) were identified as available proxies of the environmental conditions possibly impacting individual fish body condition. SST and Chla were extracted from E.U. Copernicus Marine Service (satellite products https://doi.org/10.48670/moi-00153 and 10.48670/moi-00289) and averaged separately over BoB and CS. SST has slightly increased in the BoB over the period, while it displays no trend in the CS between 2002 and 2022. In both regions, Chla has increased from 2002 to around 2009, and decreased since then (Supporting Information B). According to the sampling date and location of each individual biological data, corresponding regional and short term SST and Chla indices were computed as the sum of deviations from monthly averaged SST and Chla, over the three months preceding the sampling date, at the scale of either the BoB or the CS. Because body condition is supposed to respond rapidly to the environmental change, we integrated these deviations over 3 months prior sampling, following results from Rueda et al. (2015). Details of the calculation and time series of environmental indices are presented by region in Supporting Information B. Density-dependence was tested using annual biomass estimates extracted from corresponding stock assessment's outputs. For species without stock assessment, density-dependence was estimated based on a biomass index compiled from the French scientific survey EVHOE. The density-dependence variable (hereafter noted Biomass) was standardized (centered on the mean biomass over the time series and scaled). Details on computation of survey biomass index and time series of species biomass indices are presented in Supporting Information C.

## 2.4. Statistical analyses

To avoid any biases linked to sampling or changes in size distributions over the course of the time series, the factorial design of the data was checked. Unbalanced years, quarters, regions or sexes were excluded and, for each species, the data were trimmed so that the size range was consistent over the whole time series (Supporting Information A, Fig. A.2). A stratum was considered unbalanced if its number of data was lower than 5 % of the number of data for the richest stratum. Years with less than 30 data, or isolated in the beginning of the time series (with a break of 3 years or more between the considered year and the

next one with data) were also excluded. An independent linear model (log(W) = log(L) × sex) was used to test the impact of sex on the length-weight relationship. If it was significant, data without sex information were removed, and sex was included as an explanatory variable in the body condition model. Synthetic information on the selected fish sample sizes, temporal coverage, length and weight ranges of data by species is provided in Table 1.

As body condition may vary seasonally and since we want to characterize inter-annual trends, the quarter was added as a categorical variable to assess the respective part of seasonal and inter-annual variation. Because the present study concentrates on the primary impact of the factors influencing body condition, we did not consider interactions between the explanatory variables.

In a first step, the temporal changes in body condition were tested with a linear model. The best model was chosen by a stepwise procedure based on the Akaike Information Criterion (AIC, R software package stats, Sakamoto et al., 1986). If the factorial design allowed it, the most complex model tested corresponded to equation (2) (see Supporting Information D for the equations for each species):

$$K_n = \text{Sex} + \text{Quarter} + \alpha \times \text{Year} \quad (2)$$

In a second step, the observed changes in body condition over time were analyzed in relation with SST, Chla and Biomass using linear models. A stepwise procedure based on AIC was also performed to select the optimal model. If the factorial design allowed it (see Supporting Information D for the equations for each species), the most complex model tested was:

$$K_n = \text{Sex} + \text{Quarter} + \alpha \times \text{SST} + \beta \times \text{Chla} + \gamma \times \text{Biomass} \quad (3)$$

For all models, variance inflation factors (VIF) were calculated between all variables to detect high collinearities. Variables associated with the highest VIF values were sequentially removed until all VIF values were lower than 2 (Zuur et al., 2010). The model selected was validated by visual examination of the residuals distributions (i.e. normality, homogeneity and independence). The significance (p < 0.05) of the coefficients of the linear models was checked by a Student t-test. The influence of each variable on the body condition was then assessed by a Fisher test. Finally, a sensitivity analysis regarding the effects of individual length and maturity stage was performed, to check whether the results were robust to ontogenetic changes. All statistical tests were
<caption>**Table 2**</caption>

Results of the linear models selected by the stepwise AIC procedure, representing the effects of year, sex and quarter on K<sub>n</sub>, with percentage (in parentheses) of variance explained for each species. Only significant coefficients are presented, variables tested but not retained by the stepwise procedure or not significant are indicated with ‘-’, variables not tested are indicated by a grey cell. The reference sex is fixed for females, for quarters the reference are indicated with “0”.

<table><thead><tr><th>Species</th><th>Year effect</th><th>Sex (male effect)</th><th>Quarter 1</th><th>Quarter 2</th><th>Quarter 3</th><th>Quarter 4</th></tr></thead><tbody><tr><td>Anchovy</td><td>-0.0049<br>(7.18)</td><td>-0.0113<br>(0.27)</td><td>0<br>(3.41)</td><td>0.021</td><td></td><td>-0.0639</td></tr><tr><td>Plaice</td><td>-0.0035<br>(1.78)</td><td>-0.0462<br>(3.13)</td><td>0<br>(27.76)</td><td></td><td>0.1454</td><td>0.1178</td></tr><tr><td>Megrim</td><td>-0.0033<br>(2.97)</td><td>-</td><td>0<br>(0.9)</td><td></td><td></td><td>0.0229</td></tr><tr><td>Sardine</td><td>-0.0032<br>(3.25)</td><td></td><td>0<br>(21.76)</td><td>0.033</td><td>0.1806</td><td>0.0767</td></tr><tr><td>White anglerfish</td><td>-0.0025<br>(0.53)</td><td>-0.0176<br>(0.28)</td><td>0<br>(0.59)</td><td></td><td>-0.0322</td><td>-0.0296</td></tr><tr><td>Seabass</td><td>-0.0023<br>(0.52)</td><td></td><td>0<br>(2.85)</td><td>-0.0158</td><td>-0.028</td><td>0.0134</td></tr><tr><td>Striped red mullet</td><td>-0.0022<br>(0.69)</td><td>-0.024<br>(0.8)</td><td>0<br>(22.2)</td><td>0.0418</td><td>0.1713</td><td>0.1</td></tr><tr><td>Cod</td><td>-0.0021<br>(0.7)</td><td></td><td>0<br>(0.76)</td><td></td><td></td><td>-0.0243</td></tr><tr><td>Sole</td><td>-0.0019<br>(0.64)</td><td>-0.0389<br>(2.49)</td><td>0<br>(2)</td><td>-0.0158</td><td>0.0253</td><td>0.0086</td></tr><tr><td>Hake</td><td>-0.0016<br>(0.46)</td><td>-0.01<br>(0.18)</td><td>0<br>(2.89)</td><td></td><td></td><td>0.0387</td></tr><tr><td>Whiting</td><td>-0.0016<br>(0.45)</td><td>-</td><td>0<br>(1.04)</td><td></td><td>-0.0203</td><td>0.0119</td></tr><tr><td>Lemon sole</td><td>-0.0007<br>(0.1)</td><td>-0.0543<br>(7.14)</td><td>0<br>(4.03)</td><td>-</td><td>0.0654</td><td>-0.0074</td></tr><tr><td>Witch flounder</td><td>-</td><td>-0.0362<br>(3.09)</td><td>0<br>(0.15)</td><td></td><td></td><td>0.0098</td></tr><tr><td>Red gurnard</td><td>-</td><td>-0.0236<br>(1.07)</td><td>0<br>(1.5)</td><td></td><td>0.0179</td><td>0.0283</td></tr><tr><td>Black-bellied anglerfish</td><td>-</td><td>-0.0219<br>(0.48)</td><td>0<br>(0.39)</td><td></td><td></td><td>0.0196</td></tr><tr><td>Haddock</td><td>0.0003<br>(0.02)</td><td>-0.0057<br>(0.08)</td><td>0<br>(3.86)</td><td>-</td><td>0.0573</td><td>0.0524</td></tr><tr><td>Greater forkbeard</td><td>0.0043<br>(1.49)</td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>
<figure><img src="image_6.png" /><figcaption>Fig. 4. Influence (coefficient of correlation) of exogenous variables (SST, Chla, Biomass) on body condition for each species. Only significant variables are shown. Species are ordered according to the intensity of the observed temporal trend, from highest declining trend (Anchovy), to slightly decreasing (Lemon sole), followed by species without temporal trend (Witch flounder, Red gurnard, Black-bellied anglerfish), and finally species with increasing body condition (Haddock and Greater forkbeard).</figcaption></figure>

performed with R v.4.3.2 (R Core Team, 2023).

## 3. Results

The parameters of the length-weight relationships were estimated for all species, and the visual examination of the diagnostic plots allowed validation of all models. The values of parameters a and b, as well as the 95 % confidence intervals, the length and weight ranges and the time span of the data, are given for each species in Supporting Information E. Sex had a significant effect on the length-weight relationship for most species, but not for greater forkbeard, sardine, seabass and cod.

### 3.1. Temporal changes of body condition

Computation of variance inflection factors (VIF) did not detect collinearity among covariates (all VIF <2). The visual examination of the diagnostic plots allowed validation of all models.

The body condition significantly decreased through time for 12 species out of 17 (Fig. 3). Anchovy, plaice, megrim and sardine showed the strongest trends, with relative body condition and thus mean weight at a given length decreasing by 6–10 % over the twenty years studied,

while lemon sole showed the most limited decline (Table 2). Two species (greater forkbeard and haddock) showed an increase in body condition over time and three species (black-bellied anglerfish, witch flounder and red gurnard) showed no significant trends.

Most species for which the sex variable could be tested exhibited a significant correlation between sex and body condition, and all indicated a poorer condition for males (Table 2). Similarly, all species for which the quarter variable could be tested showed a significant correlation. However, the seasonal optimum is reached at different times of the year depending on the species. The sex effect is particularly important for flatfish: plaice, sole, lemon sole, witch flounder, while the quarter effect is particularly important for plaice, sardine, striped red mullet, with better conditions in quarter 3 and poorer conditions in quarter 1. These two effects had a strong explanatory power in our models, reflecting both the anatomical differences between males and females and the seasonal variation, which means that only the inter-annual variation was included in the proportion explained by the year variable.
## 3.2. Influence of environmental and density-dependence variables

The results of the second series of linear models, which include environmental and density-dependence variables, are presented in Fig. 4. Here, the computation of VIF also did not detect collinearity (all VIF <2), and the visual examination of the diagnostic plots allowed validation of all models. The impact of biomass on body condition is significant for all species, except for seabass and lemon sole. For nine species, stock biomass negatively impacted body condition, while for six species this effect was positive. Among the species whose condition declined through time, seven had a negative correlation with biomass, while only three had a positive correlation (sardine, cod, whiting). Changes were observed in environmental variables over the period, with a declining trend in Chla in the CS and an increasing SST in the BoB (Supporting Information B). Chlorophyll-α showed a fairly consistent pattern with $K_n$ across species, with ten species exhibiting a positive correlation, while only three (anchovy, sardine and red gurnard) exhibited a negative correlation. SST was correlated either positively (five species) or negatively (four species) with body condition. Coefficient and percentage of variance explained by each variable, including sex and quarter, for each species are provided in Supporting Information F. The effects of sex and quarter are similar to those observed in the first temporal model.

Models including exogenous variables (SST, Chla, Biomass) had a slightly improved explanatory power compared to our previous series of models for eleven species (Supporting Information D). Environmental variables SST and Chla were found to explain less than 1 % of variations in body condition across the species studied, while the biomass effect appeared to be slightly more important (>1 % of variations for anchovy, sardine, megrim and cod, Supporting Information F).

## 3.3. Influence of individual length and ontogenic change

The sensitivity analysis regarding the effects of individual length and maturity stage was performed to assess whether the results were robust to ontogenetic changes (Supporting Information G). The inclusion of individual length in the temporal model (Eq. (2)) only barely changed the effect of year and slightly enhanced explanatory power. In a second step, the temporal model was applied to a subset of data containing only immature/mature or smaller/larger individuals in order to assess the consistency of the temporal trend. All species show consistent trends regardless of the subgroup considered, except for hake, for which the condition of mature individuals increases while condition of immatures decreases. All other species that exhibited a significant temporal trend with the entire dataset also demonstrated a consistent trend across both immature and mature, or smaller and larger, individuals.

# 4. Discussion

## 4.1. Overall decline in body condition

From the observed temporal changes in body condition between 2002 and 2022 in the Bay of Biscay and Celtic Sea, we evidenced a prevailing declining trend at the fish community scale (observed for 12 out of 17 species). Body condition has deteriorated for small pelagic fish (−5 % per decade for anchovy and −3 % per decade for sardine) in Western Europe over the past 20 years. Recent decreasing body condition has already been reported for sardine and anchovy in the Bay of Biscay (Véron et al., 2020; Taboada et al., 2024), but this pattern has also been documented at a wider scale: decrease in body condition of anchovy and sardine in the Mediterranean Sea (Brosset et al., 2017), and in other small pelagic fish such as Baltic sprat (Casini et al., 2014), Northeast Atlantic mackerel (Olafsdottir et al., 2016) and Western North Pacific chub mackerel (Kamimura et al., 2021). However, some ecosystems have exhibited an increase in small pelagic's body condition (overwintering Black Sea anchovy, Gücü et al., 2018). The novelty of our

study lies in the evidence of a declining trend in body condition at a larger fish community scale, including demersal and benthic species, with plaice and megrim experiencing stronger declines in body condition than sardine.

Across all the studied species, the results concerning greater fork-beard differ from the others species. This deepwater species has a different ecology than the shelf species studied here, and is weakly connected to the Celtic Sea food web (Merillet, 2020). This species relies partly on different trophic resources than species living on the shelf, and may be impacted by different environmental factors. Conversely to our results, a decreasing trend in body condition has been found for deep-sea species (Molva species) in adjacent regions (Lloret et al., 2021). These contrasted results together with the reduced amount of available data and their limited time span should lead to caution when interpreting the results obtained for this particular species.

Climate change may contribute to reduction in phytoplankton size (Winder and Sommer, 2012), and potentially induces a shift towards smaller-sized zooplankton (as evidenced in the Baltic Sea, Suikkanen et al., 2013; Viitasalo and Bonsdorff, 2022). The hypothesis of a shift in phytoplankton production (Litzow et al., 2006; Biton-Porsmoguer et al., 2020) or towards reduction in zooplankton food quantity (Brosset et al., 2015; Saraux et al., 2019) or quality (Menu et al., 2023) has been mainly retained to explain the decline in body condition of small pelagic fish. Small pelagic fish species are a crucial prey group for top predators (Cury et al., 2000). The declining body condition of small pelagics due to a depletion of the pelagic pathway could similarly extend up to predators, resulting in an overall worsening condition at the fish community scale. The consequences of a reduction in the energy value, approximated by body condition (Brosset et al., 2023), of small pelagic fish on their predators including seabirds have already been demonstrated in other ecosystems (Wanless et al., 2005). Here, the predators of small pelagic fish, such as megrim, white anglerfish, seabass, cod, whiting and hake (Du Built, 1992; Preciado et al., 2008; Spitz et al., 2013; Issac et al., 2017; Rault et al., 2017) displayed a worsening body condition. The total biomass of small pelagics has not changed much in Celtic Sea and Bay of Biscay in the last two decades (ICES, 2022a; ICES, 2022b), favoring the hypothesis of a reduction in food quality rather than quantity to explain the decreasing body condition of predators.

Two mechanisms can lead to a reduction of food quality: a reduction of preys' individual energy content and/or a modification of the species composition in the diet, from energetically rich species to poorer ones. In this study, the reduction in individual prey energy content can be approximated by the decreasing body condition of both sardine and anchovy. More generally a decline in forage fish quality has been evidenced in Bay of Biscay forage fish by Amelot et al. (2025), based on a comparison of direct lipid measurements between the 2000s and the early 2020s. Simultaneously, the decline in sardine biomass (Supporting Information C), a lipid-rich species, concomitant with an increase of anchovy biomass, which display lower lipid concentration than sardine (Spitz et al., 2010; Albo-Puigserver et al., 2021), results in a decreasing overall quality of available prey. A decline in lipid-rich prey in the diet of post-smolt salmon has for instance been identified as a cause for the decline in condition observed in the Norwegian Sea (Utne et al., 2021). This hypothesis is in line with the essential fatty acid limitation (Litzow et al., 2006).

Furthermore, in combination with the hypothesis of a pelagic pathway depletion, piscivorous fish might have partly shifted their diet from forage fish to other organisms, such as crustaceans. Amelot et al. (2023) highlighted a change in the diet of some Celtic Sea Gadiformes, between 1980, 1990 and 2010, with a decrease of Pisces and an increase of Crustaceans in stomach content, especially for whiting and hake. According to Spitz et al. (2010), fish generally have higher lipid contents than Crustacean species. Moreover, pelagic feeders are generally richer in lipids than demersal feeders (Litzow et al., 2006). Piscivorous fish that have undergone a diet shift would therefore display a worse condition when feeding on invertebrates compared to forage fish. However, our
results are based on a simple morphometric index, interpreted as proxy for energy reserve (Brosset et al., 2023). A comparison with temporal change in lipids contents, unfortunately not available to our knowledge, would provide a more accurate view of the mechanisms underlying this widespread decline.

Our hypotheses based on a pelagic pathway depletion and a dietary shift are not sufficient to explain the decreasing condition of some other demersal and benthic species, such as plaice, stripped red mullet, sole, and lemon sole, which are not piscivores and do not feed directly on the pelagic pathway after larval stage. The decline in condition of these species should be further explored, as it could be linked to a similar depletion of the benthic pathway, either linked to the pelagic production through benthopelagic coupling (as benthic organisms rely on sinking pelagic particles), or to other factors affecting benthic invertebrates or habitats. Climate change could reduce the size of phytoplankton (Lewandowska and Sommer, 2010), but also increase stratification, leading to a decrease in sediment flux (Winder and Sommer, 2012), involving a reduction in benthic production (Viitasalo and Bonsdorff, 2022). Therefore, we suggest that benthic pathway might have been partially influenced by pelagic impoverishment, resulting in a potential ecosystem-wide trophic cascade.

## 4.2. Effect of sex, season and environmental variables on body condition

Among the explanatory variables tested, season and sex were the most important variables, followed by chlorophyll-α and intra-specific density-dependence, which were shown to be significantly correlated to body condition for the majority of species, while sea surface temperature did not explain much of the body condition variability.

For the majority of species, sex has an impact on condition, with females exhibiting better condition. This result is coherent with other studies focusing either on black-bellied and white anglerfish in the Bay of Biscay (Landa and Antolínez, 2018), or on a large set of species in Europe from the North Sea to the Bay of Biscay (Mahé et al., 2018) and for some demersal species in the north-western Mediterranean (Lloret et al., 2002). As total weight data were used rather than eviscerated weight data, the better condition of females is probably linked to the weight of female gonads as suggested by Lloret et al. (2013). Reproduction and gonadal development can also explain seasonal variations in body condition, which has been highlighted for all species that were tested. Other documented factors may exert an influence on the seasonal variability in body condition, including migration, wintering, environmental conditions and temperature (Lloret et al., 2013; Albo-Puigserver et al., 2021). In this study we specifically used monthly anomalies of chlorophyll-α and temperature to focus on the inter-annual variability rather than the seasonal one, therefore the seasonal pattern of these variables was, at least partially, entangled in the ‘quarter’ variable. Changes in gonadal development, reproduction phenology and/or in energy allocation between reproduction and growth could also lead to seasonal variation in body condition. As individual maturity development data were not available for the set of species studied, we conducted a sensitivity analysis based on length-at-maturity. This analysis revealed consistent trends between all immature and mature individuals across all species exhibiting significant trends except hake, for which immature and mature individuals showed divergent trends (Supporting Information G). In the case of hake, further studies are needed to better understand this species-specific response, although some hypotheses can be advanced. During the study period, mature hake may have changed their energy allocation toward somatic growth, resulting in an increase in their body condition. Another hypothesis could be related to the level of parasites in hake and their influence on weight measurements. This species exhibits a high degree of parasitism (Pascual et al., 2018), with a positive correlation between infestation level and body length, resulting in all individuals being infested at maturity length (Diez et al., 2022). The infestation rate seems to increase for this species during the study period in the Bay of Biscay (Diez et al., 2022). As suggested by Timi and

Poulin (2020), ignoring parasite weight may lead to an overestimation of individual weight, ultimately resulting in a misinterpretation of body condition.

Chlorophyll-α was used to estimate surface primary production, considered as proxy for available trophic resource at the basis of the food web. For all demersal and benthic species studied (except red gurnard), interannual variability of Chla was positively correlated with body condition. This suggests that higher surface productivity creates favorable conditions for maintaining good body condition, even for species feeding near the sea bottom. Surprisingly, for small pelagic fish the correlation between Chla concentration and body condition is negative, and opposite to the results obtained for sardine in the Bay of Biscay by Véron et al. (2020). These authors used the averaged Chla concentration of the sampling month, whereas we used the sum of deviations from the monthly average over the past three months prior to the sampling date, therefore discarding the seasonal signal and focusing on the interannual variability. This difference in methodology might explain the difference of correlation. In any case, response time of body condition to change in prey remains poorly quantified. The negative correlation we obtained for anchovy and sardine, together with its low explanatory power suggest that factors other than Chla concentration, such as quality more than quantity, can lead to a decrease in body condition despite high Chla concentration, as shown in several studies (Brosset et al., 2017; Queiros et al., 2019; Menu et al., 2023). Phytoplankton quality is expected to deteriorate with climate change, which would impact the entire food web (Hixson and Arts, 2016). The quality of phytoplankton in the BoB and CS has been studied through the composition of diatoms and dinoflagellates species, which has displayed temporal shifts in the mid-2000s in the Bay of Biscay (Houliez et al., 2021) and showed spatially variable trends in the Celtic Sea (Bedford et al., 2020). In line with essential fatty acid limitation, such a change in the proportion of diatoms (rich in eicosapentaenoic acid, EPA) and dinoflagellates (rich in docosahexaenoic acid, DHA) may lead to a shift in the food web DHA: EPA ratio, which can propagate throughout the entire marine food web (Litzow et al., 2006), potentially resulting in an ecosystem-wide trophic cascade. At the consumer level, a decline in individual zooplankton size has been demonstrated in the Bay of Biscay together with an increase in the abundance of small copepods (Grandremy, 2023). This resulted in an apparent stability in total biomass, while masking a shift in community structure towards smaller individuals, i.e., poorer food quality for foraging fish that rely extensively on copepods.

The inconsistency of body condition response to sea surface temperature across species either in terms of significance, or in terms of having a consistent positive or negative sign of the estimated coefficient was also found in another multispecies study (28 species) in California with bottom temperature (Thorson, 2015). Inconsistency across species can be explained by the potential multiple effects of temperature on fish condition: a direct physiological effect, depending on the optimum temperature of the species, and indirect effects, i.e., via changes in the abundance (or quality) of prey and predators (Brett, 1979; Lloret et al., 2013).

## 4.3. Effect of fishing and fisheries management

The Bay of Biscay and Celtic Sea have experienced a global decrease in fishing pressure during the study period (Gascuel et al., 2016; Hernvann and Gascuel, 2020; STECF, 2024), associated with a global increase in biomass (ICES, 2022a; ICES, 2022b). The Celtic Sea has been described as partially recovering since 2010 (Hernvann and Gascuel, 2020; Hernvann et al., 2020). An increase in global fish biomass can lead to stronger inter- and intra-specific competition for food, leading to a decline in body condition. Our results showed a negative correlation between body condition and biomass indices for seven out of the twelve species experiencing a declining body condition, thus suggesting intra-specific competition. Such density-dependence has been previously highlighted for megrim (Landa et al., 2022), chub mackerel (Kamimura
<figure><img src="image_7.png" /><figcaption>**Fig. 5.** Conceptual diagram of the mechanisms possibly responsible for the widespread decrease in body condition ($K_n$) observed for small pelagic fish (represented by the anchovy cartoon) for demersal and piscivorous species (seabass cartoon) and for benthic species (plaice cartoon). 1. Pelagic pathway depletion indicates a poorer quality of plankton food that propagates to the food web resulting in generalized declining trend in body condition ($K_n$) of pelagic, demersal and piscivorous species. 2. A diet shift of piscivorous species from lipid-rich organisms towards less energetic organisms (e.g. sardine towards anchovy or pelagic forage fish towards benthic invertebrates). 3. Hypothetic benthic pathway depletion, either due to external perturbation or to benthopelagic coupling. 4. Reduction in global fishing pressure may result in an increase in intraspecific density-dependence (tested in this study) but also interspecific density-dependence (not tested), which may affect body condition.</figcaption></figure>

et al., 2021), hake (Bensebaini et al., 2022), and for anchovy (Bay of Biscay, Boëns et al., 2023; Black sea, Gücü et al., 2018). In the case of Black sea anchovy, an increasing trend in body condition was found to be negatively correlated with a decline in the abundance of the population. The study focused on wintering anchovy, during a season when food supply is limited, and the release of intraspecific competition was retained as a main factor determining condition. Negative correlation between condition and biomass was also highlighted in our study, but in an opposite pattern, i.e., a decline in condition in a context of increasing biomass.

Conversely, a positive correlation between body condition and biomass (as observed in our study for sardine, cod and whiting) suggests a low level of intraspecific competition but greater control of the environment. For example, a decrease in food availability may decrease recruitment, growth and condition without causal relationship with density (Orlova et al., 2010; Rueda et al., 2015; Rindorf et al., 2022). Similar positive correlation between growth this time and biomass has been evidenced for sardine in the Bay of Biscay (Boëns et al., 2023) and for cod in the Celtic Sea (Rindorf et al., 2022).

More generally, it should be noted that the recovery of certain stocks during the period remains limited and that stock abundances are still lower than those observed in the 1970s or 1980s. Therefore, the hypothesis of a density-dependent effect must be interpreted with great caution, especially due to the difficulty of distinguishing density-dependent and fisheries effects from environmental drivers (Rindorf et al., 2022). Thus, another interpretation of our results may be to consider the observed correlations as fortuitous, with some stocks recovering due to decreased fishing pressure, while body condition declined due to climate-induced changes in the food web, but with no direct link between these two concomitant processes.

Finally, a last hypothesis can be mentioned to explain this overall worsening condition at the fish community scale. The fishing pressure picked up in the 1990s and early 2000s, and many stocks were considered to be in a severe state of recruitment overfishing (Hernvann and

Gascuel, 2020). In such a situation, genetic drift or fishing-induced selection may intervene, generally favoring individuals with early reproduction, which spend more energy on sexual maturation and less on somatic growth (Ernande et al., 2004; Olsen et al., 2004; Marty et al., 2015). The majority of the literature on fishing-induced evolution concerns the effects on length or maturity rather than directly on body condition.

Interannual variation in body condition could be caused by other features at the ecosystem scale, like multispecies interactions, including interspecific density-dependence (Kamimura et al., 2021; Olafsdottir et al., 2016), pollution (Lopes et al., 2023), or habitat suitability (Champion et al., 2020). Moreover, only linear relationships were tested in our study, which may not reflect more complex interactions, particularly given that ecological processes are often non-linear. Ecosystem models representing trophic interactions and energy allocation within the ecosystem would be interesting to disentangle all these hypotheses. However, the hypothesis of a degradation of trophic conditions appears to be the most supported at the moment, to explain our results. It suggests a massive effect of climate change on the functioning of marine trophic networks.

## 4.4. Conclusion

This study analyzed a long-time series of individual length-weight data to assess the temporal trend in body condition for species other than small pelagics, already extensively studied. As far as we know, this is the first time that a multidecadal decrease in body condition is demonstrated at the scale of an entire ecosystem for the majority of finfish, including both small pelagic and benthodemersal species. Although the underlying mechanisms driving body condition variations remain complex and require further study, we have highlighted the importance of bottom-up control. Four major non-exclusive mechanisms appeared to be the most likely to explain the general decline in body condition at the scale of the fish community: 1. depletion of the pelagic
pathway, 2. change in the diet of piscivorous species, 3. hypothetic benthic pathway depletion, and 4. effect of fishing pressure through density dependence. The links between the aforementioned mechanisms are illustrated in Fig. 5.

In addition to the potential impact on fish provisioning quality, the prevalence of declining body condition over several fish communities at the regional scale should be considered as a warning of important climate-induced changes in the trophic functioning of these marine ecosystems. Furthermore, this study emphasises the necessity of investigating body condition at a large scale, rather than focusing on a few selected species, in order to gain a comprehensive understanding of the diverse mechanisms that can perturb the ecosystem. Such an overview of ecosystem dynamics is an essential component for the implementation of effective management strategies. The expected benefits of fishing management, mainly based on regulating fishing pressure, may be limited by other factors, such as larger-scale bottom-up processes. Furthermore, if not properly accounted for in stock assessments, a declining body condition can lead to biased estimates of stock biomass and exploitation status, impairing fisheries management.

Finally, this approach should encourage large-scale studies in other ecosystems, particularly where a decline in body condition has been evidenced in small pelagic species, to potentially identify ecosystem-wide trophic cascades.

### CRediT authorship contribution statement

**M. Gernez:** Writing – review & editing, Writing – original draft, Software, Methodology, Investigation, Data curation, Conceptualization. **M. Savina-Rolland:** Writing – original draft, Methodology, Investigation, Funding acquisition, Conceptualization. **D. Gascuel:** Writing – original draft, Methodology, Investigation, Conceptualization. **M. Travers-Trolet:** Writing – original draft, Methodology, Investigation, Funding acquisition, Conceptualization.

### Funding

This project has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 101000318 (SEAwise) and Region Pays de la Loire, France. A CC-BY public copyright license has been applied by the authors to the present document and will be applied to all subsequent versions up to the Author Accepted Manuscript arising from this submission, in accordance with the grant's open access conditions.

### 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.

### Acknowledgements

The authors would like to thank Léa Simonet for her contribution during her end-of-study internship, which led to this study.

### Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.marenvres.2025.107428.

### Data availability

International data are available on datras website, and national data on request from the SIH (Système d'Informations Halieutiques, IFREMER).

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