Mediterranean demersal resources and ecosystems:
25 years of MEDITS trawl surveys
M.T. Spedicato, G. Tserpes, B. Mérigot and E. Massutí (eds)

INTRODUCTIONTop

Multispecies fisheries targeting a large number of species represent a management challenge because several biological and ecological parameters must be incorporated in the assessment (Ekerhovd and Steinshamn 2016Ekerhovd N.-A., Steinshamn S.I. 2016. Economic Benefits of Multi-Species Management: The Pelagic Fisheries in the Northeast Atlantic. Mar. Resour. Econ. 31: 193-210.). This is the case of the Mediterranean fisheries, where the commercial catches are characterized by a high number of target species, among which the most ecologically and economically important one is the European hake, Merluccius merluccius (Linnaeus, 1758) (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38.).

M. merluccius is widely distributed in the Mediterranean Sea and the northeastern Atlantic Ocean, from the coasts of Norway and Iceland to Mauritania. In the Black Sea, it only occurs along the southern coasts. It is a major component of the demersal fish assemblages and can reach depths ranging from 30 to 1000 m, although the most abundant catches are observed especially between 50 and 400 m depth (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38.).

The European hake has always been an important food resource for the population of western Europe throughout history. It is caught in mixed fisheries along with blue whiting, megrim, monkfish, shortfin squid, Norway lobster and deep-water rose shrimp by a multi-rigged fleet. This demersal species is one of the most important commercial resources for trawl and small-scale fisheries (fixed gillnets, bottom longlines) in the Mediterranean basin (STECF 2015Scientific, Technical and Economic Committee for Fisheries (STECF). 2015. Mediterranean assessments part 1 (STECF-15-18). Publications Office of the European Union, Luxembourg, EUR 27638 EN, JRC 98676, 410 pp.). Trawlers mainly catch specimens below 30 cm total length, whereas bottom longlines and gillnets target adults (Sbrana et al. 2007Sbrana M., Belcari P., De Ranieri S., et al. 2007. Comparison of the catches of European hake (Merluccius merluccius, L. 1758) taken with experimental gillnets of different mesh sizes in the northern Tyrrhenian Sea (western Mediterranean). Sci. Mar. 71: 47-56.).

European hake represents about 2% of the average total landings in the Mediterranean Sea (FAO 2016FAO. 2016. Report of the fortieth session of the General Fisheries Commission for the Mediterranean (GFCM), St. Julian’s, Malta, 30 May-3 June 2016. GFCM Report No. 40. Rome, Italy, 144 pp.). However, according to the data series, annual catches decreased from a maximum of ca. 52000 tonnes in 1994-1995 (Maynou et al. 2003Maynou F., Lleonart J., Cartes J.E. 2003. Seasonal and spatial variability of hake (Merluccius merluccius L.) recruitment in the NW Mediterranean. Fish. Res. 60: 65-78.) to 24900 tonnes in the period 2000-2013, indicating an overfishing status in several Mediterranean areas (STECF 2015Scientific, Technical and Economic Committee for Fisheries (STECF). 2015. Mediterranean assessments part 1 (STECF-15-18). Publications Office of the European Union, Luxembourg, EUR 27638 EN, JRC 98676, 410 pp., GFCM 2016GFCM 2016. Working Group on Stock Assessment of Demersal 655 Species (WGSAD). GFCM and FAO headquarters, Rome, Italy, 7-12 November 2016. Final Report, 74 pp.). Several scientists have highlighted the risk of a stock collapse (Russo et al. 2017Russo T., Bitetto I., Carbonara P., et al. 2017. A holistic approach to fishery management: evidence and insights from a central Mediterranean case study (Western Ionian Sea). Front. Mar. Sci. 4: 193.); indeed, European hake stocks in the Mediterranean Sea suffer the highest fishing pressure, with a fishing mortality rate that is on average five times higher than the target fishing mortality level (FAO 2016FAO. 2016. Report of the fortieth session of the General Fisheries Commission for the Mediterranean (GFCM), St. Julian’s, Malta, 30 May-3 June 2016. GFCM Report No. 40. Rome, Italy, 144 pp.).

Studies on M. merluccius have covered aspects such as biology (Papaconstantinou and Stergiou 1995Papaconstantinou C., Stergiou K. 1995. Biology and fisheries of eastern Mediterranean hake (Merluccius merluccius). In: Alheit J., Pitcher T. (eds), Hake: Biology, Fisheries and Markets. Chapman & Hall, London, pp. 149-180.), genetics (Levi et al. 2004Levi D., Patti B., Rizzo P., et al. 2004. Genetic and morphometric variations of Mediterranean hake, Merluccius merluccius, in the Strait of Sicily (Central Mediterranean): implications for stock assessment of shared resources. Ital. J. Zool. 71: 165-170.), recruitment (Fiorentino et al. 2003Fiorentino F., Garofalo G., De Santi J., et al. 2003. Spatio-temporal distribution of recruits (0 group) of Merluccius merluccius and Phycis blennoides (Pisces, Gadiformes) in the Strait of Sicily (Central Mediterranean). Hydrobiologia 503: 223-236., Hidalgo et al. 2008Hidalgo M., Massutí E., Moranta J., et al. 2008. Seasonal and short spatial patterns in European hake (Merluccius merluccius L.) recruitment process at the Balearic Islands (western Mediterranean): the role of environment on distribution and condition. J. Mar. Syst. 71: 367-384., 2009Hidalgo M., Tomas J., Moranta J., et al. 2009. Intra-annual recruitment events of a shelf species around an island system in the NW Mediterranean. Estuar. Coast. Shelf Sci. 83: 227-238.), nurseries modelling (Carlucci et al. 2009Carlucci R., Lembo G., Maiorano P., et al. 2009. Nursery areas of red mullet (Mullus barbatus), hake (Merluccius merluccius) and deep-water rose shrimp (Parapenaeus longirostris) in Eastern-Central Mediterranean Sea. Estuar. Coast. Shelf Sci. 83: 529-538. , Druon et. al. 2015Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204.), reproduction (Al-Absawy 2010Al-Absawy M.A.E.-G. 2010. The reproductive biology and the histological and ultrastructural characteristics in ovaries of the female gadidae fish Merluccius merluccius from the Egyptian Mediterranean water. African J. Biotechnol. 9: 2544-2559.), age and growth (Ligas et al. 2015Ligas A., Colloca F., Lundy M.G., et al. 2015. Modeling the growth of recruits of European hake (Merluccius merluccius) in the northwestern Mediterranean Sea with generalized additive models. Fish. Bull. 113: 69-82. , Pattoura et al. 2015Pattoura P., Lefkaditou E., Megalofonou P. 2015. Age estimation of juvenile European hake Merluccius merluccius based on otolith microstructure analysis: a slow or fast growth pattern? J. Fish Biol. 86: 907-923.), feeding (Carpentieri et al. 2005Carpentieri P., Colloca F., Cardinale M., et al. 2005. Feeding habits of European hake (Merluccius merluccius) in the central Mediterranean Sea. Fish. Bull. 103: 411-416., Mellon-Duval et al. 2017Mellon-Duval C., Vivien M.-H., Métral L., et al. 2017. Trophic ecology of the European hake in the Gulf of Lions, northwestern Mediterranean Sea. Sci. Mar. 81: 7-12.), and exploitation and fishery management (Russo et al. 2017Russo T., Bitetto I., Carbonara P., et al. 2017. A holistic approach to fishery management: evidence and insights from a central Mediterranean case study (Western Ionian Sea). Front. Mar. Sci. 4: 193., Tsagarakis et al. 2017Tsagarakis K., Carbonell A., Bričić J., et al. 2017. Old Info for a New Fisheries Policy: Discard Ratios and Lengths at Discarding in EU Mediterranean Bottom Trawl Fisheries. Front. Mar. Sci. 4: 99. ). These studies on the Mediterranean Sea are regional but most contributions have a local focus.

Since 1994, the MEDITS project (Bertrand et al. 2002Bertrand J.A., Gil de Sola L., Papaconstantinou C., et al. 2002. The general specifications of the MEDITS surveys. Sci. Mar. 66: 9-17.) has provided the opportunity to collect biological and abundance data on demersal species at a Mediterranean Basin scale, by means of large-scale experimental trawl surveys and standardized sampling protocols. In this context, Orsi Relini et al. (2002)Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38. presented data (1994-1999) on abundance, population structure and recruitment pattern of European hake from the Alboran Sea to the Aegean Sea, providing the first integrative picture of European hake over the northern Mediterranean Sea.

The present study aims to provide an update of previous studies, presenting more advanced analyses on several aspects of this species, in terms of both methodological approach and time period of investigation, also analysing several drivers shaping its distribution. Considering MEDITS time series from 1994 to 2015, updated data on occurrence, abundance patterns and mean length of M. merluccius in the northern Mediterranean Sea are presented. Finally, the spatial distribution of biomass of this demersal species as a function of environmental variables was analysed and a predictive map of biomass hotspots was obtained.

MATERIALS AND METHODSTop

Sampling

Since 1994, twenty-two annual bottom trawl surveys have been performed covering the European Union Mediterranean Sea in the framework of the MEDITS project. These surveys mainly aim to obtain estimates of abundance indices and length frequency distributions for a set of target species and have usually been carried out from late spring to mid-summer on demersal grounds from 10 to 800 m depth. A stratified random sampling design was adopted considering five bathymetric strata: 10-50 m, 51-100 m, 101-200 m, 201-500 m and 501-800 m. Details of the survey design and sampling methodology can be found in Bertrand et al. (2002)Bertrand J.A., Gil de Sola L., Papaconstantinou C., et al. 2002. The general specifications of the MEDITS surveys. Sci. Mar. 66: 9-17. and in the MEDITS Handbook (Anonymous 2017Anonymous. 2017. MEDITS-Handbook. Version n. 9, MEDITS Working Group: 106 pp. ).

In the present study, catch data (number and weight) and total length measurements of M. merluccius collected in the period 1994-2015 from 16 geographical sub-areas (GSAs) (FAO 2009FAO. 2009. GFCM Resolution RES-GFCM/33/2009/2 Establishment of Geographical Sub-Areas in the GFCM area amending the resolution GFCM/31/2007/2. In: FAO General Fisheries Commission for the Mediterranean, Report of the thirty-third session. Tunis, 23-27 March 2009. GFCM Report. No. 33. Rome, Italy.) belonging to nine countries (Table 1, Fig. 1) were analysed. In GSAs 5, 17, 20, 22 and 23, the time series are not continuous because MEDITS surveys were not performed for some years; however, they were included in the analysis in order to cover the largest geographical patterns possible.

A total of 23748 valid hauls were carried out during the MEDITS surveys (1994-2015); for each haul, number of specimens and total weight (g) per species were collected. For a list of target species, including European hake, biological sampling consisted in recording size (total length, TL in mm), gonad weight (g), sex and gonad maturation stage.

Data analysis

The frequency of occurrence of European hake (F(%)=N positive hauls/total hauls×100) was computed for each GSA considering the overall depth range (10-800 m). The number of individuals (N) and weight (kg) were standardized to a trawled surface unit (km²) as abundance (N km^–2) and biomass (kg km^–2) indices. Net horizontal opening and recorded distances were used to calculate the swept area. Their distributions were represented graphically for each GSA by means of box plots showing medians, quartiles and ranges (maximum and minimum).

One-way analysis of variance (ANOVA) (Yandell 1997Yandell B.S. 1997. Practical data analysis for designed experiments. Chapman & Hall, London, 440 pp.) was performed on log- transformed abundance (N km^–2) and biomass (kg km^–2), followed by pair-wise post hoc Tukey honestly significant difference tests to investigate for significant differences in terms of abundance and biomass values of M. merluccius among GSAs. Normality assumption of abundance and biomass distributions were previously evaluated using the Shapiro-Wilk test.

The biomass indices (BI, kg km^–2) were modelled using generalized additive models (GAMs), which provides a flexible framework for modelling the relationship between the individual predictors and the dependent variable through smooth functions that can be both linear and nonlinear (Wood 2017Wood S. 2017. Generalized Additive Models. Chapman and Hall/CRC, New York, 496 pp.).

The explanatory variables considered in the model were the geographic coordinates (latitude and longitude) combined in a bidimensional smoother, the mean haul depth (m), sea surface temperature (°C, SST), temperature at the sea bottom (°C, botT) and the surface chlorophyll concentration (mg m^–3, CHL). These variables were selected for the GAM models because they showed considerable variability throughout the study area and were believed to be easier to interpret biologically than some other variables that were available.

The year of the surveys was also included as a factor. Depth grid was obtained from the EMODnet Bathymetry portal (http://www.emodnet.eu/), while data of the other covariates (SST, botT and CHL) were extracted from Mediterranean Monitoring and Forecasting Centre products available on the Copernicus Marine Environment Monitoring Service (CMEMS) web site (http://marine.copernicus.eu). In particular, SST, and botT data were produced using the physical reanalysis component of the Mediterranean Forecasting System (Simoncelli et al. 2014Simoncelli S., Fratianni C., Pinardi N., et al. 2014. Mediterranean Sea physical reanalysis (MEDREA 1987-2015) [Data set]. Copernicus Monitoring Environment Marine Service (CMEMS).), while CHL data were produced using the MedBFM biogeochemical model (Teruzzi et al. 2014Teruzzi A., Bolzon G., Cossarini G., et al. 2014. Mediterranean Sea Reanalysis (CMEMS MED-Biogeochemistry 1999-2015) [Data set]. Copernicus Monitoring Environment Marine Service (CMEMS).).

Absence of collinearity among covariates was checked by means of variance inflation factor (VIF) values (Zuur et al. 2010Zuur A.F., Leno E.N., Elphick C.S. 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1: 3-14.). Only variables with a low Pearson correlation coefficient (r) (|r|<0.5) and a low VIF value (VIF<3) were considered not correlated.

BIs were modelled using Gaussian distribution with a logarithmic link function, according to the following specification:

log (biomass) = α + s₁(lon, lat) + s₂(depth) + s₃(SST) + s₄(botT) + s₅(SAL) + s₆(CHL) + factor(year)

where α represents the intercept, s_i (i=1..., 6) are the smooth functions of the covariates and factor is the step function for the categorical variable year. It is worth noting that, in the model, the smooth function of spatial coordinates represents a residual spatial variation, which is spatially structured. The selection of the best model was realized by minimizing the Akaike information criterion value with the introduction of each variable in the analysis.

Residuals of the model were tested with the Anderson-Darling normality test (Gross and Ligges 2015Gross J., Ligges U. 2015. Nortest: Tests for Normality. R Package Version 1.0-4 (Online).), and the symmetry was assessed by estimating the skewness index of the distribution (Hair et al. 2010Hair J.F., Black W.C., Babin B.J., et al. 2010. Multivariate Data Analysis. Pearson Education, Harlow. 816 pp.). The Spearman rho correlation coefficient was carried out to test the presence of trends in residuals.

For predictions, a 0.03×0.03° resolution grid was used. The bathymetrical extension of the grid was within 10 to 800 m depth. The prediction grid was used to sample the informative layers of the environmental variables (monthly data) used in the model. The grid’s points were also coupled with year and coordinates variables in order to estimate the annual predictive maps throughout the GAM model. In particular, the most representative predictive maps, for the years 1995, 2006, 2011, 2013 and 2015, were chosen to represent biomass values (kg km^–2) of European hake, and to check the model robustness in space, the annual predictions of the model were coupled with the estimation of the mean stratified BIs per GSA obtained following the mean stratified standardization formulas by Souplet (1996)Souplet A. 1996. Calculation of abundance indices and length frequencies in the MEDITS survey. In: Bertrand J.A. et al. (eds), Campagne internationale du chalutage démersal en Méditerraneé. Campagne 1995. EU Final Report, Vol. III..

In order to identify the hotspots of the European hake biomass distribution pattern, prediction maps for the last three years (2013-2015) of the time series were averaged in a single map. This raster map was used to extract the 80^th, 90^th and 95^th percentiles of distribution to draw the actual hotspot contours.

Statistical analyses were performed using R version 3.5.2 (R Development Core Team 2018R Core Development Team. 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.). In particular, GAMs were implemented by means of the mgcv R package (Wood 2017Wood S. 2017. Generalized Additive Models. Chapman and Hall/CRC, New York, 496 pp.). Biomass maps were processed and produced with QGIS software (QGIS Development Team 2017QGIS Development Team. 2017. QGIS Geographic Information System. Open Source Geospatial Foundation Project.).

For each GSA, the length frequencies of M. merluccius were graphically represented by means of box plots of median, quartile, minimum and maximum TLs. An ANOVA test was applied to investigate significant differences among GSAs in terms of size distribution.

RESULTSTop

A total of 1880472 M. merluccius individuals were caught in 18470 hauls of the 23748 valid hauls (F=77.8%) carried out in the overall depth range (10–800 m) during the MEDITS surveys (1994- 2015) (Table 2). The highest frequency of occurrence was recorded in the Gulf of Lions (F=93.6%) and the southern Adriatic Sea (F=90.4%), followed by the northern Adriatic ((F=87.1%), the eastern Ionian Sea (F=85.0%), the Aegean Sea (F=83.4%) and northern Spain (F=81.2%). The highest maximum abundance (N km^–2) and biomass (kg km^–2) indices were observed in Sardinian waters (180493 N km^–2; 4636 kg km^–2) and in the Aegean Sea (129668 N km^–2; 2407 kg km^–2). Significant catches were also reported in the Ligurian and northern central Tyrrhenian seas (124022 N km^–2; 1509 kg km^–2), as well as in the Gulf of Lions (102741 N km^–2; 1588 kg km^–2). The box plots of the log–transformed abundance index (N km^–2) suggested a southwest–northeast increase in the median values in the western areas, from the northern Alboran Sea to the Gulf of Lions (GSAs 1, 5, 6, 7), while in central and eastern Mediterranean areas, the median values remained rather similar (Fig. 2A). The highest median abundance values were found in the Gulf of Lions (1210 N km^–2) and in northern Spain (1092 N km^–2). The box plots of log–transformed BIs (kg km^–2) (Fig. 2B) showed stable median values in the entire investigated area; the highest median biomass value was detected in Sardinian waters (31.83 kg km^–2). The results of the ANOVA (Tables 3 and 4) indicated significant differences among GSAs, in terms of both abundance (F=123.5, p<0.001) and biomass (F=54.98, p<0.001). Furthermore, the post hoc Tukey test performed after the ANOVA indicated significant differences between most pairs of GSAs. No collinearity was detected among covariates, the VIF values being lower than 3 and none of the Pearson correlation coefficients greater than 0.5; therefore, all the covariates were included in the GAM model analysis.

The GAM model of biomass explained 82.2% of the variability in the data (deviance explained). All the smoothing terms were significant (p<0.05). The degrees of freedom estimated for all smoothers are reported in Figure 3.

Although residuals of the model tested with the Anderson-Darling normality test (p<0.05) were not normally distributed, the model was considered sufficiently symmetric because its skewness index (0.023) was within the ±1 range. Moreover, the Spearman rho test carried out on the model’s residuals found no significant trend (p>0.05).

Plots of the smoothers and diagnostic plots of the residuals resulting from the model are presented in Figures 3 and 4. The model indicated that high BI levels of European hake were mainly detected in the northern Spain area, in the Gulf of Lions, on the western side of Sardinia, in the northern Adriatic Sea and in the northern area of the Aegean Sea. The highest biomass of European hake was identified by the model at 200 m depth, although the optimal depth range can extend up to 400 m depth. In relation to sea surface temperature, fairly stable biomass values were observed between 20°C and 22°C. Considering the bottom temperature’s spline shape, the partial effect of the variable shows an increase in the response variable corresponding to temperatures of between 14°C and 18°C, while a progressive reduction of the biomass was expected at higher bottom temperatures. Also, chlorophyll concentration was linked with European hake presence: the partial effect of the CHL variable, as is shown by the spline shape, describes an increase in biomass at chlorophyll concentrations higher than 0.6 mg m^–3, and—albeit for few values—another peak was also evident around higher values than 1.7 mg m^–3. The biomass index showed a fairly stable level over time up to 2002 and large fluctuations thereafter. In particular, an increase of the index recording the highest predicted values was observed in the years 2005, 2006 and 2008 for all GSAs. After this period, a reduction of the BI index was observed, with a relative peak in 2013 and the lowest values in 2011. In relation to the year’s effect (Fig. 3), the most representative predictive maps for the years 1995 (start, medium level), 2006 (high level), 2011 (low level), 2013 (high and recent) and 2015 (low and recent) are shown in Figure 5. For the same years, the observed biomass values from MEDITS data were compared with the predictions of the model; comparable tendencies of biomass values were observed for the different GSAs (Fig. 5).

The areas with the greatest abundance of European hake were located in the Gulf of Lions, the eastern Adriatic Sea, the western side of Sardinia, the south of Sicily and the northern Aegean Sea. This distribution pattern was confirmed and better evidenced by the map showing the biomass hotspots of the European hake for the years 2013-2015 (Fig. 6) calculated at the 80^th, 90^th and 95^th percentiles of the BI distribution.

The length frequencies of M. merluccius are summarized in the box plots shown in Figure 7. In the western Mediterranean, the largest median value was found in Corsica (230 mm TL), while the smallest median values were detected in northern Spain (125 mm TL) and the Gulf of Lions (130 mm TL). Median values lower than 200 mm TL were also observed in the northern Alboran Sea and in the Balearic Islands. In the central Mediterranean, the median values were below 200 mm TL in all areas (the Ligurian and Tyrrhenian seas, Sardinian waters, south of Sicily, the Adriatic Sea and the northwestern Ionian Sea). A prevalence of median values larger than 200 mm TL was observed in the eastern Ionian Sea except the Cretan Sea (160 mm TL). ANOVA results also suggested a significant difference among GSAs in terms of median size (F=1684, p<0.001).

DISCUSSIONTop

The present study provides updated information on the occurrence, abundance and biomass distribution patterns and length frequencies of M. merluccius in the Mediterranean Sea on a large spatial scale during spring-summer over the last two decades. In particular, the use of a GAM model, in which standardized indices of biomass were analysed in relation to the effect of environmental variables, explained how ecological factors could affect the spatio-temporal distribution of European hake biomass in the area.

The results confirm the wide spatial distribution of the species, in terms of both bathymetric range and occurrence, in accordance with previous studies in several Mediterranean areas (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38., Katsanevakis et al. 2009Katsanevakis S., Maravelias C.D., Damalas D., et al. 2009. Spatiotemporal distribution and habitat use of commercial demersal species in the eastern Mediterranean Sea. Fish. Oceanogr. 18: 439-457.). The significant differences among GSAs in terms of both abundance and biomass highlight a high variability in the catches of this demersal species in the whole area, in agreement with the findings by Orsi Relini et al. (2002)Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38..

All environmental factors were significant drivers affecting European hake distribution. The application of the GAM model, which considers the effect of some environmental variables, has significantly improved knowledge of the spatio-temporal variations of M. merluccius in the Mediterranean Sea. The high biomass levels predicted by the model in northern Spain (the Catalan Sea), the Gulf of Lions, the western side of Sardinia, south of Sicily, the eastern Adriatic Sea (mainly Croatian waters) and the northern Aegean Sea are in accordance with previous studies carried out in the Mediterranean Sea (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38., Hidalgo et al. 2008Hidalgo M., Massutí E., Moranta J., et al. 2008. Seasonal and short spatial patterns in European hake (Merluccius merluccius L.) recruitment process at the Balearic Islands (western Mediterranean): the role of environment on distribution and condition. J. Mar. Syst. 71: 367-384., Druon et al. 2015Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204.). Furthermore, the predictive model showed a biomass peak at 200 m depth, most likely correlated to the presence of nursery grounds in many Mediterranean areas (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38., Druon et al. 2015Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204.). The optimal depth range for BI was observed between 200 and 400 m, beyond which a consistent decrease in biomass was evident throughout the time period. These results are in agreement with previous studies using the MEDITS protocol, which indicate that abundance of European hake increases especially at depths ranging from 100 to 400 m, but decreases at depths greater than 500 m (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38., Katsanevakis et al. 2009Katsanevakis S., Maravelias C.D., Damalas D., et al. 2009. Spatiotemporal distribution and habitat use of commercial demersal species in the eastern Mediterranean Sea. Fish. Oceanogr. 18: 439-457., Garofalo et al. 2018Garofalo G., Fezzani S., Gargano F., et al. 2018. Predictive distribution models of European hake in the south-central Mediterranean Sea. Hydrobiologia 821: 153-172. ). This demersal species shows an optimal bottom temperature range of between 14°C and 18°C, with noticeably lower biomass for higher bottom temperatures. The GAM model confirms the results obtained by De Pontual et al. (2013)De Pontual H., Jolivet A., Garren F., et al. 2013. New insights on European hake biology and population dynamics from a sustained tagging effort in the Bay of Biscay. ICES J. Mar. Sci. 70: 1416-1428. concerning the preference of the species for cold waters, as it has a limited tolerance to warm temperature.

The CHL covariate also has a significant effect: an increase in biomass occurs with increasing CHL concentration, which might be considered a proxy of primary production, thus indicating areas where favourable feeding conditions would attract the species (Brosset et al. 2017Brosset P., Fromentin J.M., Van Beveren E., et al. 2017. Spatio-temporal patterns and environmental controls of small pelagic fish body condition from contrasted Mediterranean areas. Prog. Oceanogr. 151: 149-162.). M. merluccius is an opportunistic feeder (Hidalgo et al. 2008Hidalgo M., Massutí E., Moranta J., et al. 2008. Seasonal and short spatial patterns in European hake (Merluccius merluccius L.) recruitment process at the Balearic Islands (western Mediterranean): the role of environment on distribution and condition. J. Mar. Syst. 71: 367-384.) that is able to feed on a wide range of trophic resources. In the central Mediterranean, Carpentieri et al. (2005)Carpentieri P., Colloca F., Cardinale M., et al. 2005. Feeding habits of European hake (Merluccius merluccius) in the central Mediterranean Sea. Fish. Bull. 103: 411-416. reported that European hake size classes are differentiated along food niche dimensions according to different prey sizes or different prey taxa. During its early demersal life, the species feeds on crustaceans (mostly euphausiids and mysids); subsequently the juvenile hakes migrate from the nursery areas to the parental stock, and when they reach between 18 and 32 cm TL, they shift their diet towards pelagic and necto-benthic fish (Carrozzi et al. 2019Carrozzi V., Di Lorenzo M., Massi D., et al. 2019. Prey preferences and ontogenetic diet shift of European hake Merluccius merluccius (Linnaeus, 1758) in the central Mediterranean Sea. Reg. Stud. Mar. Sci. 25: 100440.). The predicted biomass hotspots of the European hake could be linked to areas characterized by high availability of crustaceans and small pelagic fish consumed mostly by individuals of age 0 and large specimens of European hake respectively.

This study highlights that the effect of environmental factors such as the range of preferred bottom temperature (14°C-18°C) and the increase in chlorophyll concentration could offer favourable conditions for a productive habitat, enhancing the prey availability and consequently increasing the biomass levels of European hake in Mediterranean areas. The results confirm the potential distribution of juvenile European hake habitats reported by Druon et al. (2015)Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204., with the highest biomass levels of M. merluccius occurring in nursery areas located near the shelf break in the northern Catalan Sea, the eastern Gulf of Lions, southwestern Sardinia, the northern Tyrrhenian Sea, southeastern Sicily, the semi-enclosed part of the eastern Ionian Sea and fragmented areas of the Aegean Sea. The prediction of both important nursery habitats (Druon et al. 2015Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204.) and biomass hotspots in the northern Aegean Sea is not revealed by MEDITS survey data (Tserpes et al. 2008Tserpes G., Politou C.Y., Peristeraki P., et al. 2008. Identification of hake distribution pattern and nursery grounds in the Hellenic seas by means of generalized additive models. Hydrobiologia 612: 125.). The low presence of juveniles in the northern Aegean is rather due to a time lag between the MEDITS sampling period and the seasonal recruitment peak in autumn-winter (Hellenic Centre for Marine Research, unpublished data). The high biomass observed in the present study may confirm the presence of a nursery area in the southern Adriatic Sea (Pomo Pit), as hypothesized by Arneri and Morales-Nin (2000)Arneri E., Morales-Nin B. 2000. Aspects of the early life history of European hake from the central Adriatic. J. Fish Biol. 56: 1368-1380.. The high biomass of small pelagic fish in the Mediterranean basin (Palomera et al. 2007Palomera I., Olivar M.P., Salat J., et al. 2007. Small pelagic fish in the NW Mediterranean Sea: an ecological review. Prog. Oceanogr. 74: 377-396. , Giannoulaki et al. 2011Giannoulaki M., Pyrounaki M.M., Liorzou B., et al. 2011. Habitat suitability modelling for sardine (Sardina pilchardus) juveniles in the Mediterranean Sea. Fish. Oceanogr. 20: 367-382.) offers a great lure of food for the species. In the southern-central Mediterranean Sea, Garofalo et al. (2018)Garofalo G., Fezzani S., Gargano F., et al. 2018. Predictive distribution models of European hake in the south-central Mediterranean Sea. Hydrobiologia 821: 153-172. reported that high small pelagic fish biomass related to the high primary production had led to the presence of large adult European hakes in the Gulf of Gabes. The strong relationship between productive fronts and demersal resources especially linked to fish preys of low trophic level has been observed in other marine areas (Alemany et al. 2014Alemany D., Acha E.M., Iribarne O. 2014. Marine fronts are important fishing areas for demersal species at the Argentine Sea (Southwest Atlantic Ocean). J. Sea Res. 87: 56-67.).

The predictive maps showing the European hake biomass index along a temporal scale highlighted a strong reduction of biomass since the year 2009 according to FAO (2016)FAO. 2016. Report of the fortieth session of the General Fisheries Commission for the Mediterranean (GFCM), St. Julian’s, Malta, 30 May-3 June 2016. GFCM Report No. 40. Rome, Italy, 144 pp., which reports a decrease in European hake landings in Spain, Italy and France since 2009. Also, in the ecological niche modelling developed by Druon et al. (2015)Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204. on a Mediterranean scale, a substantial decrease in biomass of recruits and adults in 2010 and 2011 was detected, probably due to the strengthening of the seasonal thermocline that had greatly reduced the availability of food. Also, a recent report by the GFCM (2019)GFCM 2019. Report of the third meeting of the Working Group on Marine Protected Areas (WGMPA), FAO HQ, Italy, 18-21 February 2019, 53 pp. highlights that the increase in sea bottom temperature could likely be responsible for the decrease in hake nurseries in recent years.

Environmental factors such as temperature and food availability can also affect the spatial distribution of the biomass of European hake through indirect effects. The general decrease in biomass of several stocks of anchovy and sardine observed at a Mediterranean scale (Vasilakopoulos et al. 2014Vasilakopoulos P., Maravelias C.D., Tserpes G. 2014. The alarming decline of Mediterranean fish stocks. Curr. Biol. 24: 1643-1648.) might be connected to the decreasing M. merluccius biomass detected in the present study along the time series. The effects of climate change (e.g. increase in mean SST, sea surface salinity and water stratification) are favouring smaller size classes in the zooplankton community (Herrmann et al. 2013Herrmann M., Diaz F., Estournel C., et al. 2013. Impact of atmospheric and oceanic interannual variability on the Northwestern Mediterranean Sea pelagic planktonic ecosystem and associated carbon cycle. J. Geophys. Res. Oceans 118: 5792-5813.). Since smaller plankton has lower energy values (Zarubin et al. 2014Zarubin M., Farstey V., Wold A., et al. 2014. Intraspecific differences in lipid content of calanoid copepods across fine-scale depth ranges within the photic layer. PLoS ONE 9: e92935., Brosset et al. 2017Brosset P., Fromentin J.M., Van Beveren E., et al. 2017. Spatio-temporal patterns and environmental controls of small pelagic fish body condition from contrasted Mediterranean areas. Prog. Oceanogr. 151: 149-162.), the condition of small pelagic fish may remain poor or even continue to decline, in turn having a negative effect on the European hake biomass, which would tend to decrease over time due to the reduced quality and/or quantity of food. Other investigations document that the decrease in biomass of small pelagic fish could arise from the combined effect of exploitation and environmental changes, especially in areas where anchovy and sardine were clearly overexploited, such as the Adriatic Sea (FAO 2014FAO. 2014. The State of World Fisheries and Aquaculture (SOFIA). FAO Fisheries and Aquaculture Department, Rome, 223 pp.). Indeed, such decrease in the biomass of anchovy and sardine stocks could have negative effects on many Mediterranean fisheries, hindering productivity of both small pelagic stocks and species preying on small pelagic fish, such as European hake.

The length analysis confirms, as other studies have reported (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38., Ligas et al. 2015Ligas A., Colloca F., Lundy M.G., et al. 2015. Modeling the growth of recruits of European hake (Merluccius merluccius) in the northwestern Mediterranean Sea with generalized additive models. Fish. Bull. 113: 69-82.), that trawl fisheries in Mediterranean waters mainly target first age classes (0-1) corresponding to sizes of between 100 and 180 mm TL. The smaller median sizes of M. merluccius observed in the western Mediterranean (northern Spain and the Gulf of Lions) and in the central Mediterranean, mostly in the Ligurian and Cretan seas, probably confirm concentrations of juveniles in these areas (Hidalgo et al. 2009Hidalgo M., Tomas J., Moranta J., et al. 2009. Intra-annual recruitment events of a shelf species around an island system in the NW Mediterranean. Estuar. Coast. Shelf Sci. 83: 227-238.), whereas the largest median values, appearing in Corsican waters, the Aegean Sea and Cyprus waters, reflect the lack/low presence of recruits in these areas (Orsi Relini et al. 2002Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38., Druon et al. 2015Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204.) due to the recruitment seasonal peak (autumn-winter), which escapes from MEDITS sampling.

The present study has shown good predictive results highlighting how environmental factors can affect the spatio-temporal distribution pattern of the European hake in the Mediterranean basin. The results emphasize the importance of integrating any existing knowledge about environmental drivers in the assessments of the ecosystems and fisheries, in line with the ecosystem approach to fisheries management and the requirements of the European Commission (EC 2008European Commission (EC). 2008. The role of CFP in implementing an ecosystem approach to marine management, 187 pp.) to the Scientific, Technical and Economic Committee for Fisheries (STECF) and the International Council for the Exploration of the Sea (ICES). Furthering knowledge of the spatio-temporal distribution pattern of European hake and identifying persistent areas of high abundance of juveniles and spawners in relation to environmental factors are key elements for the management of this important commercial species that has long been overfished and is now subject to multi-annual management plans in several GSAs of the Mediterranean Sea (FAO 2016FAO. 2016. Report of the fortieth session of the General Fisheries Commission for the Mediterranean (GFCM), St. Julian’s, Malta, 30 May-3 June 2016. GFCM Report No. 40. Rome, Italy, 144 pp.).

ACKNOWLEDGEMENTSTop

The MEDITS scientific survey is supported by the European Union Data Collection Framework and the Member States of the EU.

REFERENCESTop

Al-Absawy M.A.E.-G. 2010. The reproductive biology and the histological and ultrastructural characteristics in ovaries of the female gadidae fish Merluccius merluccius from the Egyptian Mediterranean water. African J. Biotechnol. 9: 2544-2559.

Alemany D., Acha E.M., Iribarne O. 2014. Marine fronts are important fishing areas for demersal species at the Argentine Sea (Southwest Atlantic Ocean). J. Sea Res. 87: 56-67.
https://doi.org/10.1016/j.seares.2013.12.006

Anonymous. 2017. MEDITS-Handbook. Version n. 9, MEDITS Working Group: 106 pp.
http://www.sibm.it/MEDITS%202011/principaledownload.htm

Arneri E., Morales-Nin B. 2000. Aspects of the early life history of European hake from the central Adriatic. J. Fish Biol. 56: 1368-1380.
https://doi.org/10.1111/j.1095-8649.2000.tb02149.x

Bertrand J.A., Gil de Sola L., Papaconstantinou C., et al. 2002. The general specifications of the MEDITS surveys. Sci. Mar. 66: 9-17.
https://doi.org/10.3989/scimar.2002.66s29

Brosset P., Fromentin J.M., Van Beveren E., et al. 2017. Spatio-temporal patterns and environmental controls of small pelagic fish body condition from contrasted Mediterranean areas. Prog. Oceanogr. 151: 149-162.
https://doi.org/10.1016/j.pocean.2016.12.002

Carlucci R., Lembo G., Maiorano P., et al. 2009. Nursery areas of red mullet (Mullus barbatus), hake (Merluccius merluccius) and deep-water rose shrimp (Parapenaeus longirostris) in Eastern-Central Mediterranean Sea. Estuar. Coast. Shelf Sci. 83: 529-538.
https://doi.org/10.1016/j.ecss.2009.04.034

Carpentieri P., Colloca F., Cardinale M., et al. 2005. Feeding habits of European hake (Merluccius merluccius) in the central Mediterranean Sea. Fish. Bull. 103: 411-416.

Carrozzi V., Di Lorenzo M., Massi D., et al. 2019. Prey preferences and ontogenetic diet shift of European hake Merluccius merluccius (Linnaeus, 1758) in the central Mediterranean Sea. Reg. Stud. Mar. Sci. 25: 100440.
https://doi.org/10.1016/j.rsma.2018.100440

De Pontual H., Jolivet A., Garren F., et al. 2013. New insights on European hake biology and population dynamics from a sustained tagging effort in the Bay of Biscay. ICES J. Mar. Sci. 70: 1416-1428.
https://doi.org/10.1093/icesjms/fst102

Druon J.N., Fiorentino F., Murenu M., et al. 2015. Modelling of European hake nurseries in the Mediterranean Sea: an ecological niche approach. Prog. Oceanogr. 130: 188-204.
https://doi.org/10.1016/j.pocean.2014.11.005

Ekerhovd N.-A., Steinshamn S.I. 2016. Economic Benefits of Multi-Species Management: The Pelagic Fisheries in the Northeast Atlantic. Mar. Resour. Econ. 31: 193-210.
https://doi.org/10.1086/685383

European Commission (EC). 2008. The role of CFP in implementing an ecosystem approach to marine management, 187 pp.

FAO. 2009. GFCM Resolution RES-GFCM/33/2009/2 Establishment of Geographical Sub-Areas in the GFCM area amending the resolution GFCM/31/2007/2. In: FAO General Fisheries Commission for the Mediterranean, Report of the thirty-third session. Tunis, 23-27 March 2009. GFCM Report. No. 33. Rome, Italy.

FAO. 2014. The State of World Fisheries and Aquaculture (SOFIA). FAO Fisheries and Aquaculture Department, Rome, 223 pp.

FAO. 2016. Report of the fortieth session of the General Fisheries Commission for the Mediterranean (GFCM), St. Julian’s, Malta, 30 May-3 June 2016. GFCM Report No. 40. Rome, Italy, 144 pp.

Fiorentino F., Garofalo G., De Santi J., et al. 2003. Spatio-temporal distribution of recruits (0 group) of Merluccius merluccius and Phycis blennoides (Pisces, Gadiformes) in the Strait of Sicily (Central Mediterranean). Hydrobiologia 503: 223-236.
https://doi.org/10.1007/978-94-017-2276-6_23

Garofalo G., Fezzani S., Gargano F., et al. 2018. Predictive distribution models of European hake in the south-central Mediterranean Sea. Hydrobiologia 821: 153-172.
https://doi.org/10.1007/s10750-017-3338-5

GFCM 2016. Working Group on Stock Assessment of Demersal 655 Species (WGSAD). GFCM and FAO headquarters, Rome, Italy, 7-12 November 2016. Final Report, 74 pp.

GFCM 2019. Report of the third meeting of the Working Group on Marine Protected Areas (WGMPA), FAO HQ, Italy, 18-21 February 2019, 53 pp.

Giannoulaki M., Pyrounaki M.M., Liorzou B., et al. 2011. Habitat suitability modelling for sardine (Sardina pilchardus) juveniles in the Mediterranean Sea. Fish. Oceanogr. 20: 367-382.
https://doi.org/10.1111/j.1365-2419.2011.00590.x

Gross J., Ligges U. 2015. Nortest: Tests for Normality. R Package Version 1.0-4 (Online).
https://cran.r-project.org/web/packages/nortest/index.html

Hair J.F., Black W.C., Babin B.J., et al. 2010. Multivariate Data Analysis. Pearson Education, Harlow. 816 pp.

Herrmann M., Diaz F., Estournel C., et al. 2013. Impact of atmospheric and oceanic interannual variability on the Northwestern Mediterranean Sea pelagic planktonic ecosystem and associated carbon cycle. J. Geophys. Res. Oceans 118: 5792-5813.
https://doi.org/10.1002/jgrc.20405

Hidalgo M., Massutí E., Moranta J., et al. 2008. Seasonal and short spatial patterns in European hake (Merluccius merluccius L.) recruitment process at the Balearic Islands (western Mediterranean): the role of environment on distribution and condition. J. Mar. Syst. 71: 367-384.
https://doi.org/10.1016/j.jmarsys.2007.03.005

Hidalgo M., Tomas J., Moranta J., et al. 2009. Intra-annual recruitment events of a shelf species around an island system in the NW Mediterranean. Estuar. Coast. Shelf Sci. 83: 227-238.
https://doi.org/10.1016/j.ecss.2009.03.037

Katsanevakis S., Maravelias C.D., Damalas D., et al. 2009. Spatiotemporal distribution and habitat use of commercial demersal species in the eastern Mediterranean Sea. Fish. Oceanogr. 18: 439-457.
https://doi.org/10.1111/j.1365-2419.2009.00523.x

Levi D., Patti B., Rizzo P., et al. 2004. Genetic and morphometric variations of Mediterranean hake, Merluccius merluccius, in the Strait of Sicily (Central Mediterranean): implications for stock assessment of shared resources. Ital. J. Zool. 71: 165-170.
https://doi.org/10.1080/11250000409356568

Ligas A., Colloca F., Lundy M.G., et al. 2015. Modeling the growth of recruits of European hake (Merluccius merluccius) in the northwestern Mediterranean Sea with generalized additive models. Fish. Bull. 113: 69-82.
https://doi.org/10.7755/FB.113.1.7

Maravelias C.D., Papaconstantinou C. 2006. Geographic, seasonal and bathymetric distribution of demersal fish species in the eastern Mediterranean. J. Appl. Ichthyol. 22: 35-42.
https://doi.org/10.1111/j.1439-0426.2006.00695.x

Maynou F., Lleonart J., Cartes J.E. 2003. Seasonal and spatial variability of hake (Merluccius merluccius L.) recruitment in the NW Mediterranean. Fish. Res. 60: 65-78.
https://doi.org/10.1016/S0165-7836(02)00062-0

Mellon-Duval C., Vivien M.-H., Métral L., et al. 2017. Trophic ecology of the European hake in the Gulf of Lions, northwestern Mediterranean Sea. Sci. Mar. 81: 7-12.
https://doi.org/10.3989/scimar.04356.01A

Orsi Relini L., Papaconstantinou C., Jukic-Peladic S., et al. 2002. Distribution of the Mediterranean hake populations (Merluccius merluccius smiridus Rafinesque, 1810) (Osteichthyes: Gadiformes) based on six years monitoring by trawl surveys: some implications for management. Sci. Mar. 66: 21-38.
https://doi.org/10.3989/scimar.2002.66s221

Palomera I., Olivar M.P., Salat J., et al. 2007. Small pelagic fish in the NW Mediterranean Sea: an ecological review. Prog. Oceanogr. 74: 377-396.
https://doi.org/10.1016/j.pocean.2007.04.012

Papaconstantinou C., Stergiou K. 1995. Biology and fisheries of eastern Mediterranean hake (Merluccius merluccius). In: Alheit J., Pitcher T. (eds), Hake: Biology, Fisheries and Markets. Chapman & Hall, London, pp. 149-180.
https://doi.org/10.1007/978-94-011-1300-7_6

Pattoura P., Lefkaditou E., Megalofonou P. 2015. Age estimation of juvenile European hake Merluccius merluccius based on otolith microstructure analysis: a slow or fast growth pattern? J. Fish Biol. 86: 907-923.
https://doi.org/10.1111/jfb.12598

QGIS Development Team. 2017. QGIS Geographic Information System. Open Source Geospatial Foundation Project.

R Core Development Team. 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

Russo T., Bitetto I., Carbonara P., et al. 2017. A holistic approach to fishery management: evidence and insights from a central Mediterranean case study (Western Ionian Sea). Front. Mar. Sci. 4: 193.
https://doi.org/10.3389/fmars.2017.00193

Sbrana M., Belcari P., De Ranieri S., et al. 2007. Comparison of the catches of European hake (Merluccius merluccius, L. 1758) taken with experimental gillnets of different mesh sizes in the northern Tyrrhenian Sea (western Mediterranean). Sci. Mar. 71: 47-56.
https://doi.org/10.3989/scimar.2007.71n147

Scientific, Technical and Economic Committee for Fisheries (STECF). 2015. Mediterranean assessments part 1 (STECF-15-18). Publications Office of the European Union, Luxembourg, EUR 27638 EN, JRC 98676, 410 pp.

Simoncelli S., Fratianni C., Pinardi N., et al. 2014. Mediterranean Sea physical reanalysis (MEDREA 1987-2015) [Data set]. Copernicus Monitoring Environment Marine Service (CMEMS).
https://doi.org/10.25423/MEDSEA_REANALYSIS_PHYS_006_004

Souplet A. 1996. Calculation of abundance indices and length frequencies in the MEDITS survey. In: Bertrand J.A. et al. (eds), Campagne internationale du chalutage démersal en Méditerraneé. Campagne 1995. EU Final Report, Vol. III.

Teruzzi A., Bolzon G., Cossarini G., et al. 2014. Mediterranean Sea Reanalysis (CMEMS MED-Biogeochemistry 1999-2015) [Data set]. Copernicus Monitoring Environment Marine Service (CMEMS).
https://doi.org/10.25423/MEDSEA_REANALYSIS_BIO_006_008

Tsagarakis K., Carbonell A., Bričić J., et al. 2017. Old Info for a New Fisheries Policy: Discard Ratios and Lengths at Discarding in EU Mediterranean Bottom Trawl Fisheries. Front. Mar. Sci. 4: 99.
https://doi.org/10.3389/fmars.2017.00099

Tserpes G., Politou C.Y., Peristeraki P., et al. 2008. Identification of hake distribution pattern and nursery grounds in the Hellenic seas by means of generalized additive models. Hydrobiologia 612: 125-133.
https://doi.org/10.1007/s10750-008-9486-x

Vasilakopoulos P., Maravelias C.D., Tserpes G. 2014. The alarming decline of Mediterranean fish stocks. Curr. Biol. 24: 1643-1648.
https://doi.org/10.1016/j.cub.2014.05.070

Wood S. 2017. Generalized Additive Models. Chapman and Hall/CRC, New York, 496 pp.
https://doi.org/10.1201/9781315370279

Yandell B.S. 1997. Practical data analysis for designed experiments. Chapman & Hall, London, 440 pp.
https://doi.org/10.1201/9780203742563

Zarubin M., Farstey V., Wold A., et al. 2014. Intraspecific differences in lipid content of calanoid copepods across fine-scale depth ranges within the photic layer. PLoS ONE 9: e92935.
https://doi.org/10.1371/journal.pone.0092935

Zuur A.F., Leno E.N., Elphick C.S. 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1: 3-14.
https://doi.org/10.1111/j.2041-210X.2009.00001.x