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INTRODUCTIONTop

Although juvenile fish is a general concept that spans various stages between birth and adulthood, this period includes numerous important ontogenetic and critical life stages. From an applied perspective, fisheries scientists working in demersal fisheries often refer to the juvenile stage (also referred as post-recruits or sub-adults, Levin and Stunz 2005Levin P.S., Stunz G.W. 2005. Habitat triage for exploited fishes: Can we identify essential “Essential Fish Habitat”? Est. Coast. Shelf Sci. 64: 70-78.) as the period that ranges from settlement to the bottom or from recruitment to the fishery to the first reproductive period (e.g. Ciannelli et al. 2007Ciannelli L., Dingsør G.E., Bogstad O. et al. 2007. Spatial anatomy of species survival: effects of predation and climate-driven environmental variability. Ecology 88: 635-646.). In the case of hake, this period is mainly framed in the second year of life (e.g. 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., Recasens et al. 2008Recasens L., Chiericoni V., Belcari P. 2008. Spawning pattern and batch fecundity of the European hake (Merluccius merluccius (Linnaeus, 1758)) in the western Mediterranean. Sci. Mar. 72: 721-732., see methods for specific details), in which hake already have an active predatory activity, a high food intake of a mainly ichthyophagous diet composed primarily of pelagic fish, and a still high somatic growth rate. Recruits and juveniles are those most impacted by bottom trawl fisheries in the Mediterranean (Colloca et al. 2013Colloca F., Cardinale M., Maynou F., et al. 2013. Rebuilding Mediterranean fisheries: a new paradigm for ecological sustainability. Fish Fish. 14: 89-109.), and juveniles can still be considered relatively well sampled by bottom trawling, through both the monitoring of commercial fisheries and scientific bottom trawl surveys. Larger individuals are less available to bottom trawl gears (thanks to spawning refugia; Colloca et al. 2013Colloca F., Cardinale M., Maynou F., et al. 2013. Rebuilding Mediterranean fisheries: a new paradigm for ecological sustainability. Fish Fish. 14: 89–109., Caddy 2015Caddy J.F. 2015. Criteria for sustainable fisheries on juveniles illustrated for Mediterranean hake: control the juvenile harvest, and safeguard spawning refugia to rebuild population fecundity. Sci. Mar. 79(3): 287-299. and references therein), although they are targeted by other commercial gears such as longlines and gillnets in some Mediterranean areas (Aldebert et al. 1993Aldebert Y., Recasens L., Lleonart J. 1993. Analysis of gear interactions in a hake fishery: the case of the Gulf of Lions (NW Mediterranean). Sci. Mar. 57: 207-217., 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.). All of these findings evidence the high importance of having a complete view of the juvenile life stage to understand how the combination of ecological, environmental and fishing impact shapes natural mortality (Jørgensen et al. 2013Jørgensen C., Holt R.E. 2013. Natural mortality: Its ecology, how it shapes fish life histories, and why it may be increased by fishing. J. Sea Res. 75: 8-18.), a key population dynamics parameter normally assumed to be constant and age-independent in the assessment frameworks (Abella et al. 1997Abella A.J., Caddy J.F., Serena F. 1997. Do natural mortality and availability decline with age? An alternative yield paradigm for juvenile fisheries, illustrated by the hake Merluccius merluccius fishery in the Mediterranean. Aquat. Living Res. 10: 257-269., Caddy 2015Caddy J.F. 2015. Criteria for sustainable fisheries on juveniles illustrated for Mediterranean hake: control the juvenile harvest, and safeguard spawning refugia to rebuild population fecundity. Sci. Mar. 79(3): 287-299.).

Numerous studies have reported size- and growth-dependent survival in juvenile fish (Ciannelli et al. 2007Ciannelli L., Dingsør G.E., Bogstad O. et al. 2007. Spatial anatomy of species survival: effects of predation and climate-driven environmental variability. Ecology 88: 635-646., Le Pape and Bonhommeau et al. 2015Le Pape O., Bonhommeau S. 2015. The food limitation hypothesis for juvenile marine fish. Fish Fish. 16: 373-398. and references therein). The increase of survival at high lengths is often explained as the result of size-selective mortality, a common mechanism in fish population dynamics (‘bigger is better’, e.g. Sogard 1997Sogard S.M. 1997. Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull. Mar. Sci. 60: 1129-1157., Suthers 1998Suthers I.M. 1998. Bigger? Fatter? Or is faster growth better? Considerations on condition in larval and juvenile coral-reef fish. Austral Ecol. 23: 265-273.), for which small fish of a given species or those with slower growth display higher mortality rates. It is indeed expected that food limitation and/or competition can influence survival via density-dependent regulation mechanisms. Density-dependent growth (and size) has been proposed as a primary mechanism of regulation of fish populations (Lorenzen and Enberg 2002Lorenzen K., Enberg K. 2002. Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proc. R. Soc. Lon. B Biol. Sci. 269: 49-54.), including hake (Hidalgo et al. 2014Hidalgo M., Olsen E.M., Ohlberger J. et al. 2014. Contrasting evolutionary demography induced by fishing: the role of adaptive phenotypic plasticity. Ecol. Applic. 24: 1101-1114., Cantafaro et al. 2017Cantafaro A., Ardizzone G., Enea M. et al. 2017. Assessing the importance of nursery areas of European hake (Merluccius merluccius) using a body condition index. Ecol. Indic. 81: 383-389.). However, the literature shows a range of contrasting (and often contradictory) studies from individual to population scale between species (Le Pape and Bonhommeau et al. 2015Le Pape O., Bonhommeau S. 2015. The food limitation hypothesis for juvenile marine fish. Fish Fish. 16: 373-398.). Indeed, contrasting regulatory mechanisms have been described for hake in the Atlantic stocks, with the southern Atlantic stock more dependent on somatic growth to regulate the population dynamics than the northern stock (Hidalgo et al. 2014Hidalgo M., Olsen E.M., Ohlberger J. et al. 2014. Contrasting evolutionary demography induced by fishing: the role of adaptive phenotypic plasticity. Ecol. Applic. 24: 1101-1114.). It is also noteworthy that estimates of survival could be the consequence of transboundary movement of juveniles between areas (geographical sub-areas, GSAs, in the Mediterranean case) used to compile fisheries and ecosystem data, and in some cases to perform analytical fisheries assessment. This implies that the spatial and demographic structure of marine populations is more complex than is currently reported, in accordance with the general acceptance of mismatch between biological and management structures currently used in fisheries assessment frameworks (Kerr et al. 2017Kerr L.A., Hintzen N.T., Cadrin S.X. et al. 2017. Lessons learned from practical approaches to reconcile mismatches between biological population structure and stock units of marine fish. ICES J. Mar. Sci. 74: 1708-1722., Goethel and Berger 2017Goethel D.R., Berger A.M. 2017. Accounting for spatial complexities in the calculation of biological reference points: effects of misdiagnosing population structure for stock status indicators. Can. J. Fish. Aquat. Sci. 74: 1878-1894.).

The MEDITS survey provides a unique opportunity to investigate the spatial and temporal patterns of juvenile survival using information from areas that are regularly sampled on an annual basis according a common and standardized methodology (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., Anonymous 2017Anonymous 2017. MEDITS-Handbook. Version n. 9, MEDITS Working Group, 106 pp.). We here investigate the potential influence of size of juveniles of the current year, size of recruits of the previous year, and differential growth between them, along with information on environmental variables such as sea surface temperature and chlorophyll a, in winter and spring. Given the known sex differences in growth for this species as it approaches the reproductive stage, male and female information was analysed separately. We hypothesize that size can influence juvenile survival, but that this effect differs between sex and geographic subareas over the Mediterranean Sea. The study also discusses the potential utility of the results obtained to improve the current assessment of hake stocks or to implement marine spatial planning in fisheries management.

MATERIALS AND METHODS Top

Sampling

Data have been obtained since 1994 from the EU International Mediterranean Bottom Trawl Survey (MEDITS) conducted on an annual base in spring and early summer on demersal grounds from 10 down to 800 m depth. A stratified random sampling design was adopted with five bathymetric strata: 10-50, 51-100, 101-200, 201-500 and 501-800 m. Specific details of the sampling methods 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 Anonymous (2017)Anonymous 2017. MEDITS-Handbook. Version n. 9, MEDITS Working Group, 106 pp..

The study combines information for 12 geographical subareas (GSA): the northern Alboran Sea (GSA-1), the Balearic Islands (GSA-5), northern Spain (GSA-6), the Gulf of Lions (GSA-7), eastern Corsica (GSA-8), the Ligurian and northern Tyrrhenian seas (GSA-9), the southern and central Tyrrhenian Sea (GSA-10), Sardinia (GSA-11), southern Sicily (GSA-16), the northern-central Adriatic (GSA-17), the southern Adriatic (GSA-18) and the western Ionian (GSA-19).

Density and annual abundances indices

European hake individuals caught in each haul were counted, sexed and measured to the half cm below. Abundance data were standardized to number of individuals per km² using the swept area to obtain density estimates per haul, size class and year. To segregate information of non-sexed individuals into males and females, a sex-ratio vector was calculated for each geographical subarea. Density information for males and females was then grouped into recruits and juveniles according to growth information from García-Rodriguez and Esteban (2002)García-Rodriguez M., Esteban A. 2002. How fast does hake grow? A study on the Mediterranean hake (Merluccius merluccius L.) comparing whole otoliths readings and length frequency distributions data. Sci. Mar. 66: 145-156.: recruits (age 0, ≤15.5 cm), juvenile males (age 1, >15.5 cm and ≤29 cm) and juvenile females (age 1, >15.5 cm and ≤32.5 cm). A weighted mean length per haul, sex, age class and year was also calculated. For plotting purposes, density per haul information was averaged for each year on a 0.5×0.5°grid. The stratified mean equation 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. provided by Anonymous (2017, page 69)Anonymous 2017. MEDITS-Handbook. Version n. 9, MEDITS Working Group, 106 pp. was applied to calculate abundance indices per year, sex and age class. For each year, sex and age class, a weighted mean length was also calculated.

Survival and growth calculations

Survival and growth estimates per year and GSA were calculated separately for males and females using annual abundance and mean length indices, respectively. Given two consecutive years, t–1 and t, we calculated an index of survival (S) between age 0 and the ensuing age 1 as follows:

S_t = X_1,t–X₀,_(t–1)

where X_1,tand X_0,(t–1)are the natural logarithm of the annual abundance index of age 1 and age 0 hake, respectively. Differential growth (G) between years was obtained using the same approach as follows:

G_t = Y_1,t-Y₀,_(t–1)

where Y_1,tand Y₀,_(t–1)are the natural logarithm of the annual mean length of age 1 and age 0 hake, respectively.

Environmental covariates and fishing pressure

To explore the potential influence of inter-annual environmental variability of a given geographical subarea on juvenile survival, satellite data for sea surface temperature and surface chlorophyll a resulted from MODIS-Aqua and NPP-VIIRS sensor measurements already processed with regional ocean colour algorithms (resolution 1 km, daily data) were downloaded from the MyOcean database (http://marine.copernicus.eu/web/69-interactive-catalogue.php) and used as common environmental variables for all the study areas. For each GSA, monthly averages were calculated over the gridded information. To capture potential different seasonal effect of temperature and productivity on survival, sea surface temperature and chlorophyll a were averaged for two contrasting seasons: winter (December-February), which is often related to the population dynamics of several species (e.g. Hidalgo et al. 2011Hidalgo M., Rouyer T., Molinero J. C, et al. 2011. Synergistic effects of fishing-induced demographic changes and climate variation on fish population dynamics. Mar. Ecol. Prog. Ser. 426: 1-12., Puerta et al. 2014Puerta P., Hidalgo M., González M., et al. 2014. Role of hydro-climatic and demographic processes on the spatio-temporal distribution of cephalopods in the western Mediterranean. Mar. Ecol. Prog. Ser. 514: 105-118.); and spring (March-May), concurrent with the MEDITS surveys.

As there was no indicator of fishing pressure that was homogeneous in all analysed GSAs for the entire time period, we used the fishing pressure indicators calculated by Kavadas et al. (2015)Kavadas S., Maina I., Damalas, D. et al. 2015. Multi-Criteria Decision Analysis as a tool to extract fishing footprints: application to small scale fisheries and implications for management in the context of the Maritime Spatial Planning Directive. Medit. Mar. Sci. 16: 294-304. for three years (1994, 2004 and 2014; see Supplementary Material for calculation procedure) to indirectly check the influence of fishing on survival using the residuals of the global model (see below).

Statistical analyses

Prior to the statistical analyses, density-dependent relationships were checked for survival, differential growth and mean length (ML) of juveniles, against abundance of recruits and juveniles. In addition, mean survival estimates per GSA were compared against the growth and ML of both recruits and juveniles. Non-linear regressions (general additive models) were used in this study for visual representation of the functional form of these relationships. It is worth noticing that density-dependent relationships were assessed by combining information of males and females, while relationships between mean values per GSA were investigated by sex.

The statistical procedure for analysing the influence of size, growth and environmental variables on survival has two steps and was applied separately for males and females. First, for each GSA, time series of survival were modelled by applying linear models in terms of differential growth, ML of recruits of the previous year (t–1), ML at time t of juveniles and, sea surface temperature and chlorophyll in the two seasons. The best model was obtained by minimizing the Akaike information criterion. For every model, residuals were checked for variance homogeneity and absence of temporal autocorrelation in the residuals. Second, we compared the relative influence of the most recurrent driver observed across all the geographic subareas to assess its relative influence on survival variability. To do that, we applied a global model with all time series (both response and covariate) normalized to mean 0 and variance 1 and pooled in a unique and centred (i.e. intercept equals 0) linear model to compare how the size (slope) of a given effect changes for each geographic subarea. Residuals obtained for these final models for males and females were averaged per GSA and correlated with the fishing pressure indicator (FPI) for each year available (1994, 2004 and 2014) using Spearman rank correlations.

RESULTSTop

Mean spatial pattern of mean densities and mean lengths

Figure 1 shows the spatial information used in this study to calculate survival, such as the mean density of recruits, male and female juveniles, and the estimates of the ML for the same age and sex groups. Given that the spatial pattern of recruits does not differ by sex, they were combined for plotting purposes. High abundance of recruits was observed in the Spanish mainland coasts, the Gulf of Lions, southeast Sardinia and the Italian coasts of the Ligurian and northern Tyrrhenian Sea, coinciding with low ML values of those recruits. By contrast, intermediate to low values of mean density of recruits (consistent with higher ML) were observed in the Alboran Sea, the Balearic Islands, eastern Corsica, northern and eastern Sardinia, the Strait of Sicily, and the western Ionian and the northern Adriatic seas. The highest ML of recruits was found around eastern Corsica and Sardinia and in the western Ionian and northern Adriatic seas, coinciding with the intermediate or lowest values of recruit density. In general, juvenile males and females showed similar patterns with intermediate values of density along the Spanish coast and in the Gulf of Lions and the Ligurian and northern Tyrrhenian seas. The highest density of hake juveniles was found in western Sardinia.

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Fig. 1. – Mean log density (left column) and mean length (right column) per grid (0.5×0.5°) for recruits (above), juvenile males (centre) and juvenile females (bottom) calculated over the whole period. Note that for each map the scale used for the colour legend differs.

The lowest values of ML were observed along the Spanish coast and in the Ligurian and northern Tyrrhenian seas. For females, the lowest ML values were observed in the southern Adriatic Sea, while intermediate to high ML values were found in the Alboran Sea, the Gulf of Lions, the Balearic Islands, the Strait of Sicily and the northern Adriatic Sea.

Temporal patterns of abundance indices and mean lengths

Figure 2 shows for each GSA the time series of abundance indices (in a log scale) and the ML of recruits and juvenile males and females. Time series are segregated into two contiguous plots: the western Mediterranean, including GSAs 1, 5, 6, 7 and 8, and the central Mediterranean, including areas 9, 10, 11, 16, 17, 18 and 19. In general, abundance indices of recruits showed a fluctuating pattern that differed among areas, with larger spatial variation in the western Mediterranean. Males and females showed similar patterns, with higher spatial consistence in the central and western Mediterranean, with the sole exceptions of eastern Corsica (GSA-8) and Sardinia (GSA-11), which displayed stronger fluctuations with lower and higher values than the average, respectively.

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Fig. 2. – Abundance indices (log scale) for recruits (above), juvenile males (centre) and juvenile females (bottom) calculated for each GSA. GSAs of the western Mediterranean (1 to 8) are coded in yellow-red colours and those of the central Mediterranean (9 to 19) are coded in green-blue-black.

The temporal pattern of the ML of recruits displayed large fluctuations (Fig. 3). In the western Mediterranean, the northern Spanish coast and the Gulf of Lion (GSA-6 and GSA-7) showed a coherent fluctuating behaviour and an increasing long-term pattern during the study period. Eastern Corsica showed higher mean values consistent with the lowest densities observed. ML of recruits showed overall higher values in the central Mediterranean than in the western Mediterranean, with the exception of the Ligurian and the northern Tyrrhenian seas (GSA-9). The temporal pattern of ML of juveniles was also generally consistent between sexes in the western Mediterranean, while in the central Mediterranean female ML showed greater fluctuations, particularly in Sardinia (GSA-11) and the Strait of Sicily (GSA-16). The fluctuating pattern of juvenile ML was also generally higher in the western Mediterranean than in the central Mediterranean.

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Fig. 3. – Mean lengths for recruits (above), juvenile males (centre) and juvenile females (bottom) calculated for each GSA. GSAs of the western Mediterranean (1 to 8) are coded in yellow-red colours and those of the central Mediterranean (9 to 19) are coded in green-blue-black.

Temporal and large-scale patterns of survival and growth per GSA

Figure 4 shows the time series estimates of survival and growth per sex and GSA. Survival values ranged between –5 and 2. Values above zero indicate that for a given GSA, the number of juveniles in a given year was higher than the number of recruits in the previous year. This is the case for most years in Corsica (GSA-8) and Sardinia (GSA-11), and for few years in the Balearic Islands (GSA-5) and the western Ionian Sea (GSA-19). The lowest values of survival in the western Mediterranean occurred along the northern Spanish (GSA-6) coast and in the Gulf of Lions (GSA-7), which showed a similar temporal pattern. In the central Mediterranean, the lowest values of survival were observed in the Ligurian and northern Tyrrhenian seas (GSA-9). The fluctuation pattern was very similar between sexes in all GSAs, with a slightly higher degree of variability in the western than in the central Mediterranean.

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Fig. 4. – Juvenile survival (left) and growth (right) for males (above) and females (bottom) calculated for each GSA. GSAs of the western Mediterranean (1 to 8) are coded in yellow-red colours and those of the central Mediterranean (9 to 19) are coded in green-blue-black.

In the case of growth (Fig. 4), the western Mediterranean GSAs also displayed higher variability within and among areas than the central Mediterranean. As observed in the survival and ML pattern, the northern Spanish coast and the Gulf of Lions displayed a similar fluctuating pattern. The growth rates in the recruit to juvenile phase observed in eastern Corsica were the lowest, despite a very high growth rate during the first year of life, as proved by the higher ML of recruits in this area.

On a broad Mediterranean scale, GSAs with higher ML of recruits and juveniles yielded higher survival for both sexes (Fig. 5), with this pattern being more clearly observed in the ML of recruits. As a consequence, survival was higher in areas with smaller differential growth between consecutive years (Fig. 5).

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Fig. 5. – Relationships between mean survival and recruit mean length at time t–1 (above), juvenile mean length at time t (centre) and growth (bottom) for each GSA (colour codes consistent with Figs. 2 and 3). Male relationships are represented on the left and female relationships on the right. Red dotted lines represent non-linear regression fit using a general additive model – in all the models the covariates showed a significant effect. Bars represent the standard deviation over the whole time series.

Density dependence in survival, growth and size

Significant density-dependent survival was observed in all GSAs, though it was stronger in the western areas, Sardinia and the western Ionian Sea (Fig. 6). While the density-dependent effect on ML of juveniles was generally significant in the central Mediterranean GSAs and non-significant in the western Mediterranean, the density-dependent effect on growth was, in contrast, significant in most areas of the western Mediterranean (Fig. 6).

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Fig. 6. – Strength of density dependence plotted as the value of the slope of the relationship with density estimates: density-dependent effect of recruit density on survival (top), density-dependent effect of juvenile density on mean length of juveniles (middle), and growth (bottom). Black symbols represent significant effects (p<0.05) and grey symbols non-significant effects (p>0.05).

Drivers of temporal variation of survival for each GSA

Table 1 shows the best models for juvenile survival of males, females and the combination of both sexes in each GSA. A negative effect of the ML on the juvenile survival of a given year was the most recurrent pattern observed (GSAs 5, 7, 8, 10 and 16). A negative effect of growth was observed in the western Ionian (GSA-19) and northern Spain (GSA-6), while a positive effect of the ML of recruits was observed in the Alboran Sea (GSA-1) and northern Spain. A positive effect of chlorophyll in winter was observed in the Alboran Sea, while a significant negative effect of chlorophyll in spring was observed in the whole Adriatic. A marginal effect of sea surface temperature in spring was observed in female survival in the western Ionian. Figure S2 (Supplementary material) presents the residuals of all the best models included in Table 1.

Table 1. – Covariates of the best linear models obtained to model juvenile survival as response variables. Models were independently performed for all individuals, males and females for each geographical subarea (GSA) (see Statistical Analyses in the Methods section). As model covariates, Chl-w and Chl-s are respectively chlorophyll in winter and spring; ML rec and ML juv, the mean length in recruits and juveniles respectively; Growth, the differential growth; and SST-s, the mean sea surface temperature in spring. Signs in parenthesis represents the direction of the effect in the response variable. Adjusted R² (R²_adj) for each model is also reported in parenthesis.**, p<0.005; *, p<0.05.

Geographic Subarea	All	Males	Females
GSA-1 - Northern Alboran	Chl-w** (+), ML rec (t–1)* (+) (R²_adj=0.64)	Chl–w** (+), ML rec (t–1)* (+) (R²_adj=0.66)	Chl–w** (+) (R²_adj=0.46)
GSA-5 - Balearic Islands	ML juv (t)* (–) (R²_adj=0.33)	ML juv (t)* (–) (R²_adj=0.35)	-
GSA-6 - Northern Spain	ML rec (t–1)* (+) (R²_adj=0.23)	Growth* (–) (R²_adj=0.25)	Growth* (–) (R²_adj=0.22)
GSA-7 - Gulf of Lion	ML juv (t)** (–) (R²_adj=0.32)	ML juv (t)** (–)(R²_adj=0.25)	ML juv (t)** (–) (R²_adj=0.38)
GSA-8 - Corsica	-	ML juv (t)** (–) (R²_adj=0.28)	-
GSA-9 - Ligurian-North Tyrrhenian	-	-	ML juv (t)* (–) (R²_adj=0.19)
GSA-10 - South-Cenrtral Tyrrhenian	ML juv (t)** (–) (R²_adj=0.39)	ML juv (t)** (–) (R²_adj=0.38)	ML juv (t)** (–) (R²_adj=0.34)
GSA-11 - Sardinia	-	-	-
GSA-16 - South Sicily	ML juv (t)* (–) (R²_adj=0.19)	ML juv (t)** (–) (R²_adj=0.29)	-
GSA-17 - Northern Adriatic	Chl-s* (–) (R²_adj=0.25)	Chl-s* (–) (R²_adj=0.25)	Chl-s* (–) (R²_adj=0.24)
GSA-18 - Southern Adriatic	Chl-s* (–) (R²_adj=0.25)	Chl-s* (–) (R²_adj=0.25)	Chl-s* (–) (R²_adj=0.24)
GSA-19 - Western Ionian	Growth* (–) (R²_adj=0.22)	Growth* (–) (R²_adj=0.28)	-

The global model, which analyses exclusively the most recurrent covariate (mean length of juveniles, ML_juv), showed a clear effect of ML_juv on male survival, with a significant effect in all the GSAs with the exception of the Alboran Sea (GSA-1) (Fig. 7). This effect was stronger in the Balearic Islands (GSA-5), the Gulf of Lions (GSA-7), eastern Corsica (GSA-8), the Ligurian and northern Tyrrhenian seas (GSA-9), the Strait of Sicily (GSA-16), the northern Adriatic (GSA-17) and the western Ionian (GSA-19). In females, the effect was only significant in the Balearic Islands, the Gulf of Lions, the Ligurian and Tyrrhenian seas and the western Ionian. Finally, the negative correlations obtained between the FPIs were not considered of relevance (Supplementari material Fig. S2).

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Fig. 7. – Size of effect of juvenile mean length on juvenile survival (male model on the left and female model on the right) for each GSA, applying a linear model to the standardized variables (mean 0 and variance 1). No overlapping of horizontal bars (standard error of the model estimates) with zero vertical lines reveals statistical significance of the effect.

DISCUSSIONTop

Our study indicates that the spatial and temporal coverage of the MEDITS programme can provide significant insights into the survival of juvenile hake in Mediterranean populations, despite sampling and ecological constraints. These constraints are associated with the seasonality of the information and the consequent lack of information of intra-annual recruitment events occurring later (i.e. autumn) than the period covered by the survey, along with the fast ontogenetic changes in the behaviour of the species. At a basin scale, the results support our expectations with higher survival in areas (i.e. GSAs) with higher ML. However, at an interannual level, the most recurrent pattern contrasts with higher survival at smaller MLs, which may have several explanations (see below). In addition, the results suggest that the relationship between survival and length (and growth) can be indirectly mediated by the strength of the density dependence, at least for the western Mediterranean areas. Finally, important elements of the study are the identification of areas with hake survival that is highly sensitive to primary production variability, such as the Alboran and Adriatic seas, and areas with positive survival values that could indicate movement of recruits and juvenile fish to these areas (i.e. eastern Corsica and Sardinia) or strong intra-annual recruitment events later in the year that were not detected during the survey. In general, analyses performed by sex provided the same message.

Although there is no geographical segregation in the mean patterns, survival and growth time series in the western areas (from the Alboran Sea, GSA-1, to Sardinia, GSA 11) show a more fluctuating and variable pattern both at an interannual scale and between areas. This may indicate a more complex combination of environmental and ecological processes, but also a more heterogeneous effect of fishing. In contrast, in the central areas (from the Strait of Sicily, GSA-16, to the western Ionian, GSA-19), the fluctuation pattern is greatly reduced for both survival and growth. The geographical pattern of mean survival reveals that the areas with higher ML of recruits are consistent with those of higher ML of juveniles, yielding higher survival. This finding suggests a fast-growth pattern during the pre-recruitment to fishery stages (first six months of life, including early life stages, bottom settlement and arrival at the nursery areas) that has been shown to lead to size-selective processes, as pre-recruits spend less time in smaller size classes, which are more vulnerable to predation (e.g. Houde 1997Houde E.D. 1997. Patterns and consequences of selective processes in teleost early life histories. In: Chambers R.C. and Trippel E.A. (eds), Early Life History and Recruitment in Fish Populations. Chapman & Hall Fish and Fish. Series, vol 21. Springer, Dordrecht., Sogard 1997Sogard S.M. 1997. Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull. Mar. Sci. 60: 1129-1157., Conover 2007Conover D.O. 2007. Nets versus nature. Nature 450: 179-180.). This pattern can be additionally affected by geographical differences in the bottom settlement peak. The opposite relationship observed between juvenile growth and survival must represent the ‘compensatory growth’, an ecological strategy observed in several species in which high energetic investment in the growth rates during the first year to maximize survival is compensated with reduced growth in the second year of life (Sogard 1997Sogard S.M. 1997. Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull. Mar. Sci. 60: 1129-1157., Ali et al. 2003Ali M., Nicieza A., Wootton R.J. 2003. Compensatory growth in fishes: a response to growth depression. Fish Fish. 4: 147-190.). Under this strategy, fish allocate energy preferentially to increase protein before lipids are restored (Schultz and Conover 1997Schultz E.T., Conover D.O. 1997. Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia 109: 516-529.), and was already suggested for hake in the Mediterranean Sea as a mechanism for maximizing recruitment in populations that are highly dependent on recruitment success (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. Est. Coast. Shelf Sci. 83: 227-238.).

The analyses at temporal scale of all GSAs show a negative effect of ML of juveniles, with higher survival at lower lengths—an opposite pattern to that observed at biogeographical scale. While this response seems counterintuitive a priori, it has previously been observed in analyses of juvenile survival using information of seasonal scientific surveys (Ciannelli et al. 2007Ciannelli L., Dingsør G.E., Bogstad O. et al. 2007. Spatial anatomy of species survival: effects of predation and climate-driven environmental variability. Ecology 88: 635-646.). Ciannelli et al. (2007)Ciannelli L., Dingsør G.E., Bogstad O. et al. 2007. Spatial anatomy of species survival: effects of predation and climate-driven environmental variability. Ecology 88: 635-646. reported a similar pattern in pollock juvenile survival and argued a potential under-representation of larger and older juvenile fish. The ontogenetic changes in catchability have been demonstrated to be progressive and often with non-linear forms that maximize catchability in juvenile stages, as has been observed in several gadoid species, including hake (Fraser et al. 2007Fraser H.M., Greenstreet S.P.R., Piet G.J. 2007. Taking account of catchability in groundfish survey trawls: implications for estimating demersal fish biomass. ICES J. Mar. Sci. 64: 1800-1819.). This means that escapement capabilities and aggregation behaviour of juvenile hakes around 20 cm are not the same as those of larger individuals of the same age class, i.e. close to 30 cm (Mahévas et al. 2011Mahévas S., Trenkel V.M., Doray M. 2011. Hake catchability by the French trawler fleet in the Bay of Biscay: estimating technical and biological components. ICES J. Mar. Sci. 68: 107-118.): this decrease in catchability with size could partially affect the juvenile stage. In addition, the lack of information of cohorts (intra-annual recruitment events) recruiting to the nursery grounds after the survey (late summer or autumn) could also affect survival estimates. Although spring-early summer is the seasonal window for the main recruitment peak over the whole Mediterranean (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. Progr. Oceanogr. 130: 188-204. and references therein), several intra-annual recruitment events have been reported in the Mediterranean in certain areas (e.g. Arneri and Morales-Nin 2000Arneri E., Morales-Nin B. 2000. Aspects of the early life history of European hake from the central Adriatic. J. Fish Biol. 56: 1368-1380., Rey and Gil de Sola 2004Rey J., Árbol J., Gil de Sola L. 2004. Seasonal recruitment of hake in the Alboran Sea (SW Mediterranean). Rapp. Comm. Int. Mer Medit. 37: 427., Belcari et al. 2006Belcari P., Ligas A., Viva C. 2006. Age determination and growth of juveniles of the European hake, Merluccius merluccius (L., 1758), in the northern Tyrrhenian Sea (NW Mediterranean). Fish. Res. 78: 211-217.). Thus, a certain amount of recruits of secondary intra-annual recruitment events that are not captured in a given year could be captured as juveniles the year after.

In addition to this general pattern, our analyses also indicate a positive effect of recruit length and a negative effect of juvenile growth on survival in the Alboran Sea (GSA-1), northern Spain (GSA-6) and western Ionian Sea (GSA-19). This finding evidences a size-dependent mortality shaping the regional population dynamics of hake for these areas, similarly to what has been observed in other species (Lorenzen and Enberg 2002Lorenzen K., Enberg K. 2002. Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proc. R. Soc. Lon. B Biol. Sci. 269: 49-54.). In addition, the significant density-dependent effect on growth observed in the western Mediterranean areas provides an additional element of the indirect influence of growth on survival, as growth limitation under high densities can be linked to competition and mortality related to food limitation (Le Pape and Bonhommeau et al. 2015Le Pape O., Bonhommeau S. 2015. The food limitation hypothesis for juvenile marine fish. Fish Fish. 16: 373-398.). This is also in agreement with a recent theoretical framework by Andersen et al. (2017)Andersen H. Jacobsen N.S., Jansen T. et al. 2017. When in life does density dependence occur in fish populations? Fish Fish. 18: 656-667., who argue that, in habitats of small and medium size, density-dependent regulation of populations does not occur only in early life stages, but also late during life. Andersen et al. (2017)Andersen H. Jacobsen N.S., Jansen T. et al. 2017. When in life does density dependence occur in fish populations? Fish Fish. 18: 656-667. show that competition in the juvenile stages may lead to stunted growth, as we here observe in hake, and to overcompensation regulation of the populations at small scales. This finding underlines the fact that density dependence in marine fish population is more complex than can be captured by models of spatially homogeneous population dynamics or by models based on stock-recruitment relationships.

Our results show two areas (the Alboran and Adriatic seas) in which survival of juveniles is strongly controlled by environmental variability, and particularly by primary production. However, the season of the environmental effect differs in the two regions and the direction of the effect appears to be opposite. In the Alboran Sea, the increase in primary production due to the influence of the Atlantic inflow and the meandering and mesoscale circulation is known to fuel the whole trophic chain (Oguz et al. 2014Oguz T., Macias D., Garcia-Lafuente J.et al. 2014. Fueling plankton production by a meandering frontal jet: a case study for the Alboran Sea (Western Mediterranean). PloS ONE 9: e111482.). In winter, this oceanographic scenario impacts the recruitment dynamics of several species in the Alboran Sea (Catalán et al. 2013Catalán I.A., Macías D., Solé J. et al. 2013. Stay off the motorway: resolving the pre-recruitment life history dynamics of the European anchovy in the SW Mediterranean through a spatially-explicit individual-based model (SEIBM). Progr. Oceanog. 111: 140-153., Ruiz et al. 2013Ruiz J., Macias D., Rincon M.M. et al. 2013. Atlantic inflow controls fish recruitment at the Western Mediterranean. Rapp. Comm. Int. Mer Medit. 40: 158.), and is consistent with our results suggesting more food availability that favours hake survival. By contrast, survival in the Adriatic Sea is negatively correlated with strength of primary production in spring. This negative relationship between primary production and marine resources production has already been observed in the Mediterranean and attributed to inter-specific competition (Puerta et al. 2015Puerta P., Hunsicker M.E., Quetglas A. et al. 2015. Spatially explicit modeling reveals cephalopod distributions match contrasting trophic pathways in the western Mediterranean Sea. PloS ONE 10: e0133439.). Thus, we could interpret that years with high productivity in the Adriatic in spring increase the overall abundance of the nektobenthic community, increasing the competition between hake and other species that may trigger food limitation and low survival (or active movements of hake juveniles to other areas with less competition).

It is worth noting that eastern Corsica and Sardinia (and, to a lesser degree, western Ionian) show many years with positive survival values (more juveniles than recruits the year before), with no clear temporal trend. In addition to the potential influence of late-in-year recruitment pulses discussed above, another plausible explanation is that this pattern is a consequence of an active movement of recruits and juveniles from neighbouring areas. The high ML values of recruits for these two areas (eastern Corsica and Sardinia) support this hypothesis, suggesting that this active feeding migration could start during the second year of life of the species, once the ontogenetic bathymetric migration is finished. Although bathymetric migrations of juvenile hake have been described as part of the ontogenetic changes in habitat selection for this species (Bartolino et al. 2008bBartolino V., Ottavi A., Colloca F. et al. 2008b. Bathymetric preferences of juvenile European hake (Merluccius merluccius). ICES J Mar. Sci. 65: 963-969., 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.), they are compatible with potential geographic juvenile feeding migrations in the Mediterranean to neighbouring geographic subareas. Active migratory movements across management areas have been evidenced for the Atlantic hake stocks (Pita et al. 2016Pita A., Leal A., Santafé-Muñoz A., et al. 2016. Genetic inference of demographic connectivity in the Atlantic European hake metapopulation (Merluccius merluccius) over a spatio-temporal framework. Fish. Res. 179: 291-301.), whose habitats are considerably larger than those in the Mediterranean and those of other hake species worldwide (e.g. Agostini et al. 2006Agostini V.N., Francis R.C., Hollowed A.B. et al. 2006. The relationship between Pacific hake (Merluccius productus) distribution and poleward subsurface flow in the California Current System. Can. J. Fish. Aquat. Sci. 63: 2648-2659.), suggesting that this may also happen in the Mediterranean. This would provide an additional element for the consideration of transboundary assessment of hake in certain regions of the Mediterranean Sea beyond the geographical limits of the GSAs (e.g. Fiorentino et al. 2014Fiorentino F., Massutí E., Tinti S. et al. 2014. Stock units: Identification of distinct biological units (stock units) for different fish and shellfish species and among different GFCM-GSA. STOCKMED Deliverable 03: FINAL REPORT. September 2014, 310 pp., STECF 2015Scientific, Technical and Economic Committee for Fisheries (STECF). 2015. Mediterranean assessments part 1 (STECF-15-18). Publ. Off. Europ. Union, Luxembourg, EUR 27638 EN, JRC 98676, 410 pp., among others, see below). However, the hypothesis of transboundary feeding migration certainly requires additional research using complementary and additional data in order to be well supported.

Fishing impact, assessment and management implications

Improving knowledge of the distribution and abundance patterns of exploited resources is a key element for offering better advice for fishing management. Doing so requires increasing the knowledge on life stages sensitive to climate forcing or fishing impact, such as recruits and juveniles of hake, for which conservative management measures play an important role in the Mediterranean Sea. Although we did not detect a robust sign of fishing impact in this study, the influence of fishing activity cannot be disregarded, as hake trawl fisheries in the Mediterranean Sea are mainly sustained by the exploitation of juveniles (Colloca et al. 2013Colloca F., Cardinale M., Maynou F., et al. 2013. Rebuilding Mediterranean fisheries: a new paradigm for ecological sustainability. Fish Fish. 14: 89–109., 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., STECF 2015Scientific, Technical and Economic Committee for Fisheries (STECF). 2015. Mediterranean assessments part 1 (STECF-15-18). Publ. Off. Europ. Union, Luxembourg, EUR 27638 EN, JRC 98676, 410 pp.). For stock assessment purposes, a correct computation of mortality rates, considering both fishing mortality and natural mortality, is essential. The modelling of juvenile harvest and how to estimate and implement realistic vectors of natural mortality in the assessment and management of this species have been important topics of research in the last two decades (e.g. Abella et al. 1997Abella A. J., Caddy J. F., Serena F. 1997. Do natural mortality and availability decline with age? An alternative yield paradigm for juvenile fisheries, illustrated by the hake Merluccius merluccius fishery in the Mediterranean. Aquat. Living Res. 10: 257-269., Caddy and Abella 1999Caddy J.F., Abella A.J. 1999. Reconstructing reciprocal M vectors from length cohort analysis (LCA) of commercial size frequencies of hake, and fine mesh trawl surveys over the same grounds. Fish. Res. 41: 169-175., Caddy 2015Caddy J.F. 2015. Criteria for sustainable fisheries on juveniles illustrated for Mediterranean hake: control the juvenile harvest, and safeguard spawning refugia to rebuild population fecundity. Sci. Mar. 79(3): 287-299.). To this end, scientifically-based information is required to disentangle ecological processes that affect their survival (i.e. natural mortality) from those that can be spatially and/or temporally managed (i.e. fishing mortality). The present study provides new insights into these challenges and into the integration of ecological processes affecting hake survival in a more holistic assessment of this species towards the operationalization and implementation of the ecosystem approach to fisheries (Link and Browman 2017Link J. S., Browman H.I. 2017. Operationalizing and implementing ecosystem-based management. ICES J. Mar. Sci. 74: 379-381.). New generation fisheries assessment may also reflect the increasing importance of the structural complexity of populations and the heterogeneity of processes at regional scale: habitat selection, density dependence, (passive) connectivity or active movements/migrations. Although the first exercises of assessments combining several GSAs have been already carried out by STECF and GFCM WGs since 2015 (e.g. GSA 1-7; GSA 9-10-11; GSA 17-18; STECF 2015Scientific, Technical and Economic Committee for Fisheries (STECF). 2015. Mediterranean assessments part 1 (STECF-15-18). Publ. Off. Europ. Union, Luxembourg, EUR 27638 EN, JRC 98676, 410 pp., GFCM 2016GFCM. 2016. Working Group on Stock Assessment of Demersal Species (WGSAD). GFCM and FAO headquarters, Rome, Italy, 7-12 November 2016. Final Report. 74 pp.), these combinations are supported by evolutionary connectivity (i.e. absence of genetic differences), and few of them support demographic connectivity (i.e. effective number of individuals exchange at inter-annual scale between close sub-populations). The spatial scale of management can be different to the spatial scale of the assessment (Cadrin and Secor 2009Cadrin S., Secor D. 2009. Accounting for spatial population structure in stock assessment: past, present, and future. In: Beamish R., Rothschild B. (eds), The Future of Fisheries Science in North America. Springer Publishing, Dordrecht, pp. 405-426.), and neighbouring areas must be combined only if they demographically interact at an interannual scale and the cross-boundary movement of individuals impacts the population dynamics principles (and equations) that sustain fisheries assessment methods (Kerr et al. 2017Kerr L.A., Hintzen N.T., Cadrin S.X. et al. 2017. Lessons learned from practical approaches to reconcile mismatches between biological population structure and stock units of marine fish. ICES J. Mar. Sci. 74: 1708-1722., Goethel et al. 2017Goethel D.R., Berger A.M. 2017. Accounting for spatial complexities in the calculation of biological reference points: effects of misdiagnosing population structure for stock status indicators. Can. J. Fish. Aquat. Sci. 74: 1878-1894.).

From the spatial management perspective (i.e. marine spatial planning), and its application to fisheries, the present study provides useful insights for implementing marine spatial planning in fisheries management in close communication with temporal fisheries assessment. As natural populations are highly dynamic in space and time, there is an increased need to include such spatiotemporal transboundary scenarios in a more flexible and adaptive fishing management (e.g. fisheries restricted areas or marine protected areas). For instance, management measures such as the recent protection of essential fish habitats for recruitment for hake and shrimps in the central Mediterranean (Strait of Sicily, Vielmini et al. 2017Vielmini I., Perry A.L., Cornax M.J. 2017. Untying the Mediterranean Gordian knot: a twenty first century challenge for fisheries management. Front. Mar. Sci. 4: 195. ) must be further expanded to the whole Mediterranean basin.

In addition, European fisheries are transitioning to new rules aimed at reducing discards and mandatorily bringing all catches to land (the “discard ban” or “landing obligation”: Art. 15 of the new Common Fisheries Policy, Reg. EU No 1380/2013). These new rules are likely to affect fishery activities in Europe. As it is impossible to completely avoid unwanted catches, and the Common Fisheries Policy will progressively phase out discards of regulated species (i.e. those subject to quotas and species with a minimum conservation reference size in the Mediterranean; see Reg. EC No 1967/2006), it is essential to know the spatial patterns of the juvenile stage to characterize areas that may have high quantities and persistence of unwanted catches (Paradinas et al. 2016Paradinas I., Martín M., Pennino M.G. et al. 2016. Identifying the best fishing-suitable areas under the new European discard ban. ICES J. Mar. Sci. 73: 2479-2487., Maeda et al. 2017Maeda E.E., Mäntyniemi S., Despoti S. et al. 2017. A Bayesian model of fisheries discards with flexible structure and priors defined by experts. Ecol. Mod. 366: 1-14., Pennino et al. 2017Pennino M.G., Vilela R., Valeiras J. et al. 2017. Discard management: A spatial multi-criteria approach. Mar. Policy 77: 144-151.).

All these elements are well framed in the essence of the Mid-Term Strategy 2017-2020 (MTS, Resolution GFCM/40/2016/2) launched by the GFCM to implement new fisheries governance in the Mediterranean Sea and to ensure the conservation and sustainable exploitation of living marine resources while protecting habitats and vulnerable species from fishing. Indeed, the results of the present study may contribute to two of the five structured targets of the MST: i) reverse the declining trend of fish stocks through strengthened scientific advice in support of management, and ii) minimize and mitigate unwanted interactions between fisheries and marine ecosystems and environment. The present study provides information to improve the quantification of the survival in the recruit and juvenile stages of hake, which are the stages most harvested by commercial fleets, especially bottom trawlers. Our study also highlights the importance of size- and growth-dependent survival in the juvenile stages of hake in the Mediterranean Sea and the contribution that scientific surveys can regularly make to the understanding of these processes.

ACKNOWLEDGEMENTSTop

We thank all the dedicated people who have worked since 1994 on the research and fishing vessels conducting the MEDITS surveys throughout the Mediterranean Sea. MEDITS data were co-funded by the EU through the European Maritime and Fisheries Fund (EMFF) within the national programme of collection, management and use of data in the fisheries sector and support for scientific advice regarding the Common Fisheries Policy. MH also thanks P. Tugores for her help on the mapping and coding.

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SUPPLEMENTARY MATERIAL

The following supplementary material is available through the online version of this article and at the following link:
http://scimar.icm.csic.es/scimar/supplm/sm04857esm.pdf

Material and methods supplementary text.

Table S1. – Rankingof the criteria taken into account in MCDA per length overall (LOA) segmentation. The higher the grade, the more favourable the area is for trawl fishing activities.

Fig. S1. – Model residuals against response variable for the best linear model obtained for each GSA (Table 1) for all individuals (left), males (centre) and females (right). Here, models for GSA-1, GSA-5, GSA-6 and GSA-7 are shown.

Fig. S2. – Scatter plot of the residuals of the global survival model for females applying a linear model on the standardized variables (mean 0 and variance 1) and the fishing pressure indicator for 1994 (left), 2004 (centre) and 2014 (right). While the negative correlations obtained between the fishing pressure indices and the residuals of the global model were very low (–0.23<rho≤0.17, right), those correlations for females were relatively high (–0.62<rho≤0.60, left). However, these high correlation values are forced by two extreme values of FPI: the lowest in the Balearic Islands (GSA-5) and the highest in the northern Adriatic (GSA-17).