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Theocharis, Vlachou, Conides, Klaoudatos, Sogunle, and van Wijnen: Population biology of European hake (Merluccius merluccius, Linnaeus, 1758) in Greece

Research article

Population biology of European hake (Merluccius merluccius, Linnaeus, 1758) in Greece

Alexandros Theocharis [1]

Maria Vlachou [1]

Alexis Conides [2]

Dimitris Klaoudatos [1]

Author Affiliations

¹Department of Ichthyology and Aquatic Environment, School of Agricultural Sciences, University of Thessaly, 38446 Volos, Greece.

²Hellenic Centre for Marine Research, Institute of Marine Biological Resources & Inland Waters, 19013 Attika, Greece.

Academic Editor(s):

Olajide Sogunle

Andre J. van Wijnen

Cite paper

Theocharis A, Vlachou M, Conides A, Klaoudatos D. Population biology of European hake (Merluccius merluccius, Linnaeus, 1758) in Greece. Academia Biology 2023;1. https://doi.org/10.20935/AcadBiol6140

DOI: https://doi.org/10.20935/AcadBiol6140

Received: 30 Aug 2023,

Accepted: 06 Oct 2023,

Published: 15 Nov 2023

Open Access

Abstract

The European hake (Merluccius merluccius) is one of the most important demersal species in the Mediterranean Sea. A total of 861 individuals were collected using commercial bottom trawls, between May 2021 and October 2022 from the Aegean Sea (the Eastern Mediterranean) aiming to assess the current state of the population. The male to female ratio (0.92:1) did not significantly depart from 1:1, with length-weight relationships exhibiting positive allometric growth. There were seven age groups identified, with the second age group being the most predominate. The highest reproductive intensity was observed during spring followed by winter. The onset of sexual maturity (L₅₀) for the total population was estimated at 27.58 cm in total length (3.2 years). The asymptotic length was estimated at 65.19 cm for the total population, with females growing larger than males. Longevity was estimated at 22.7 years for the total population (24.9 years for females and 16.1 years for males). The inflection point was estimated at 7.5 years for the total population (8.2 years for females and 5.2 years for males). Length with 50% probability of capture (LC₅₀) was estimated at 17.7 cm, with the respective age (t₅₀) of 1.2 years. The exploitation rate (E = 0.72) indicated that the population is under a high level of exploitation and the Z/K ratio (7.81) further indicated that mortality dominates growth. Fishing mortality at the maximum sustainable yield (F_MSY = 0.29) was estimated considerably lower than the present fishing mortality (F = 0.69). Results indicate the need for enforcement of stricter management measures to protect the stock.

1. Introduction

The European hake (Merluccius merluccius) belongs to the Merlucciidae family and is present in the North-East Atlantic, as well as the Mediterranean Sea with the bathymetric range from 25 to 1,000 m, dwelling near the bottom during daytime and moving to shallow waters at night to feed [1]. The species has been described as one of the most important demersal species both ecologically and commercially in the Mediterranean Sea [2, 3]. European hake is a species with a rather long lifespan that can reach more than 10 years of age [4], with the maximum reported age of 20 years [2]. Females prevail in sizes larger than 30 cm and make up the entire population at 38–40 cm [5]. The species is a multiple batch spawner with indetermined fecundity and a pelagic deposition [6]. Reproduction occurs throughout the year, with intensity and peaks varying among regions. Larger individuals exhibit delayed maturity in colder, nutrient-rich waters like the Atlantic compared to warmer waters of the Mediterranean Sea, and particularly the Adriatic [7].

In both Atlantic and Mediterranean waters, the European hake appears to be overfished or to have reached its maximum potential [8]. Reports throughout the Mediterranean including Algeria [9], Turkish central Aegean Sea [10], Sea of Marmara [11], Turkish northern Aegean Sea [12], and the Atlantic Moroccan coasts [13] indicate that hake populations appear to be heavily exploited or overexploited. Hake landings in Hellenic waters between 1992 and 2022 exhibited a declining trend, with an annual mean of 4,107 ± 889 tons [14] with Aegean catches representing on average (2010–2020) 81% the of the total Hellenic catches [15]. A fact of concern is that numerous reports indicate that the length at first maturity (L₅₀) is higher than 20 cm [10, 16–23] which is the minimum landing size (MLS) in the Mediterranean, whereas the MLS in effect for hake populations of the Atlantic and North Sea is between 27 and 30 cm [24].

This study aims to update information on the present state of European hake’s biology in Hellenic waters, namely the population structure, growth, mortality, reproduction, and exploitation rate to contribute to the improvement of stock assessment and the facilitation of sustainable management of this commercially important species and one of the most exploited demersal species throughout the Mediterranean.

2. Materials and methods

2.1. Study area and sampling

A total of 861 individuals (413 males and 448 females) were collected using commercial bottom trawls, between May 2021 and October 2022 from the Aegean Sea (the Eastern Mediterranean) (north Euboean gulf, 38° 47′ 12" Ν 23° 08′ 12" Ε; Pagasitikos gulf 39° 14′ 08" Ν 23° 00′ 42" Ε; central Aegean Sea 39° 01′ 41" Ν 24° 19′ 48" Ε) (Figure 1). The bottom trawl used was a traditional Greek commercial trawl with a square mesh codend with a mesh size (bar length) of 28 mm (stretched). The sampling depth ranged between 80 and 200 m. Mean annual water temperature ranged between 14 and 16°C, salinity ranged at 37–39, pH between 8.40 and 8.46, and oxygen concentration between 5.3 and 5.9 mg/ℓ. Turbidity ranged between 17.4 and 19.8 m. Total length (TL) and total weight (TW) were measured to the nearest 0.01 cm and 0.01 g, respectively. The gonads and otoliths were extracted for further analysis.

Figure 1

Map of the study area.

2.2. Growth parameters

Growth parameters were calculated using the von Bertalanffy growth equation [25]:

L t = L_{\infty} \times (1 - e^{- k \times (t - t_{0})})

(1)

where k (growth coefficient) is the rate at which the asymptotic length, L_∞, is approached, t is the age in years, and t₀ is the hypothetical age at which the fish has zero length.

The index of growth (in length) performance [26] was derived using the von Bertalanffy parameters:

φ ΄ = {log}_{K} + 2 \times {log}_{L_{\infty}}

(2)

The maximum lifespan was estimated according to [27] as:

t_{max} = 3 / K

(3)

2.3. Mortality and exploitation rate

Total mortality (Z) was calculated using Beverton and Holt’s [28] empirical equation:

Z = K \times (L_{\infty} - L_{mean}) / (L_{mean} - L^{'})

(4)

where L_mean is the mean length of all fish in a sample representing a steady-state population and L′ is the cut-off length or the lower limit of the smallest length class included in the computation.

Natural mortality was calculated using Pauly’s [29] empirical equation:

\ln_{M} = - 0.152 - 0.279 \times \ln_{L_{\infty}} + 0.6543 \times \ln_{K} + 0.463 \times \ln_{T}

(5)

Fishing mortality (F) was calculated by subtracting natural from total mortality according to [30]:

F = Z - M

(6)

The exploitation rate (a measure of the amount of fish that are caught from a population each year) was calculated as the ratio of fishing mortality to the total mortality [31]:

E = F / Z

(7)

The balance between population growth and mortality was assessed from the ratio of total mortality to the growth coefficient [13]:

Population growth and mortality balance = Z / K

(8)

The length class with the highest biomass (L_opt) (optimum length) was calculated according to [32]:

L_{opt} = (3 \times L_{\infty}) / (3 + \frac{M}{K})

(9)

The length class at which the fish population can achieve its maximum sustainable yield (MSY) (eumetric length) (L_e) was calculated according to [27, 33]:

L_{e} = \frac{3 L_{\infty}}{3 + \frac{M}{K}}

(10)

The length of first capture (L_c) was the length at initial capture (smallest individual captured). Probability of capture was estimated at 25%, 50%, and 75% level by the linear regression-derived ascending data points of the selectivity curve [34].

2.4. Condition factor

Fulton’s condition factor (K) was used as an estimate of body condition in fish, calculated according to [35]:

K = 100 \times \frac{Weight (in g)}{Length {(in cm)}^{3}}

(11)

2.5. Reproduction

Sex and maturity stage were determined macroscopically for each specimen according to [36] as: I: Virgin; II: Virgin developing; III: Immature; IV: Maturing; V: Mature VI: Spent. Each gonad was removed and was weighed fresh after removal of excess water. The reproductive cycle was assessed seasonally with the use of the gonad-somatic index (GSI) calculated according to [37]:

GSI = \frac{Fresh gonad weight}{Total weight} \times 100

(12)

The length at which 50% of individuals in a population have reached sexual maturity is known as the onset of sexual maturity (L₅₀). To model the link between fish length and the likelihood of sexual maturity, a probit regression model utilizing maximum likelihood estimation based on a linear transformation of a sigmoid type of curve [38] was fitted to the data. Maturity stages I through III were categorized as immature, and stages IV through VI as mature.

2.6. Data analysis

The null hypothesis of no significant temporal (season) and phyletic (sex) effect on the Fulton’s condition factor or their interaction was tested with the ANOVA General Linear Model (GLM) using a least squares regression approach [39]. The chi-square goodness-of-fit test [40] was used to assess the null hypothesis of equal proportions between the male and female ratio and compare our findings with the published literature. Statistical analysis was performed with Jamovi (ver. 2.4.6) [41], at an alpha level of 0.05.

The length-weight relationship was calculated separately for females, males, and combined sex according to [42] by fitting the exponential curve (13) to the data, where TW is the total weight (g), TL is the total length (cm), a (growth factor) the intercept of the curve, and b the slope (allometry coefficient).

TW = a \times {TL}^{b}

(13)

The Student’s t-test was used to check the isometry (b = 3) or allometry (b ≠ 3) of the length–weight relationships.

Age classes were initially estimated by length frequency distribution using Bhattacharya’s method [43], with the software FiSAT II (FAO, Rome, Italy) (version 1.2.2.) [44]. Results were refined using the maximum likelihood concept (NORMSEP) [45] separating normally distributed components of size-frequency samples (modal progression analysis). To verify the estimated age classes, 100 otoliths were randomly selected, and annual rings were read by three independent readers according to [46].

Yield and stock predictions (Relative Y/R and B/R analysis: Knife-edge selection) were performed using the relative yield-per-recruit model based on the Beverton and Holt model [47]. Biological reference points including F_0.1, F_MSY, and F_MAX were estimated with the open-source software YPRLEN (V2.1.0) (NOAA Fisheries Integrated Toolbox, Silver Spring, MD, USA).

3. Results

3.1. Population characteristics

Sex ratio

The observed male to female ratio (0.92:1) did not significantly depart from the female to male ratio of 1:1 (X² = 1.42, P > 0.05) or from the reported male to female ratio (0.89:1) [10] in the central Aegean Sea in the Turkish coast (X² = 0.266, P > 0.05).

Length–weight relationship

The length–weight relationships for the total population and males and females, respectively, are shown in Figure 2.

Figure 2

Weight vs length for the entire M. merluccius population sampled (equations and associated coefficient of determination for the total population, and each sex are shown).

Slopes ranged between 3.181 and 3.262, exhibiting positive allometric growth. The t-test confirmed a highly significant difference from isometry for the total population and for each sex (t-test, P < 0.001).

Age composition

The age composition of the entire population is shown in Table 1.

The length-age equation that resulted from the otoliths measured was:

Length = 4.137 \times age + 13.781 (R^{2} = 0.98)

(14)

In total seven age classes were identified, with the most dominant being the second age class (45.6% of the total population) (Table 1).

Table 1

Population characteristics of the age groups identified for the entire M. merluccius population (mean length, standard deviation, and population percentage, at each age class)

Age class	Total length (cm)	Standard deviation	Population %
1	18.20	0.88	18.41
2	20.66	1.54	45.56
3	25.79	2.47	28.34
4	32.29	1.19	3.63
5	35.14	0.68	2.26
6	38.26	1.83	1.42
7	41.96	0.95	0.38

Condition factor

The Fulton’s condition factor exhibited the highest values during winter for the males and during winter and spring for females. The general linear model analysis of variance indicated that both season and sex and their interaction have a significant effect of the condition factor, with season exhibiting the greater effect (F-value 164.78, P < 0.001) followed by sex (F-value 17.19, P < 0.001) and their interaction (F-value 7.99, P < 0.001).

Reproduction

The highest reproductive intensity was exhibited during spring followed by winter (Figure 3).

Six distinct stages of gonadal development were identified in this study.

Figure 3

Mean seasonal GSI (bars indicate 95% confidence interval).

The first stage (immature) was identified at the 8.7% of the population, with the highest abundance during autumn followed by spring. The second stage was identified at 54.3% of the population, with the highest abundance during autumn followed by winter. The third stage was identified at 19.6% of the population, with the highest abundance during winter followed by autumn. The fourth stage was identified at 5.1% of the population, with the highest abundance during winter followed by autumn. The fifth stage was identified at 3.0% of the population, with the highest abundance during spring followed by autumn. The sixth stage was identified at 4.2% of the population, with the highest abundance during summer followed by spring.

All maturity stages were identified throughout every season, apart from stage V (spawning stage) which was not found during summer.

The onset of sexual maturity (L₅₀) for the total population was estimated at 27.58 cm in total length (3.2 years) and 25.41 (2.6 years) and 30.97 (4.0 years) for males and females, respectively (Figure 4). The inflection point was estimated at 7.5 years for the total population (8.2 years for females and 5.2 years for males).

Length at first maturity from other relevant studies is shown in Table 2.

Growth and mortality

The von Bertalanffy growth equations for the total population and each sex were estimated as:

Lt = 65.19 \times (1 - e^{- 0.125 (t + 1.341)}), total population

Lt = 68.33 \times (1 - e^{- 0.113 (t + 1.45)}), females

Lt = 54.00 \times (1 - e^{- 0.175 (t + 1.04)}), males

Growth index (Φ′) was estimated as 2.72.

Figure 4

Probit regression for the proportion of mature M. merluccius in relation to its total length (L₂₅, L₅₀, L₇₅ and associated age are also indicated).

Table 2

Comparative table of length at first maturity among relevant studies

Authors	L₅₀ males (cm)	L₅₀ females (cm)	Area of study
Present study	25.41	30.97	Hellenic waters
Khoufi et al. [19]	–	29	Tunisian coast
Soykan et al. [10]	25.6	21.4	central Aegean Sea
Kahraman et al. [11]	22.5	29.9	Sea of Marmara
Carbonara et al. [21]	–	30.03	Sardinia
		31.95	Southern Adriatic Sea
		33.03	South and central Tyrrhenian Sea
		32.94	Western Ionian Sea
Candelma et al. [22]	–	30.81 (macroscopic) 33.73 (histological)	Central Adriatic Sea
ELGazzar et al. [23]	–	31.95	Southern Adriatic
ELGazzar et al. [23]	–	34.4	Egyptian Mediterranean

Natural mortality (M) was estimated as 0.284, total mortality (Z) as 0.975, and fishing mortality (F) as 0.69. The exploitation rate (E) was estimated at 0.72. The length class with the highest biomass (L_opt) was estimated at 38.16 cm. The ratio of total mortality to growth coefficient (Z/k) was calculated as 7.81. Eumetric length (length class at which the fish population can achieve its maximum sustainable yield) was estimated at 37.04 cm. Longevity was estimated at 22.7 years for the total population (24.9 years for females and 16.1 years for males).

Growth and mortality parameters from other relevant studies are shown in Table 3.

Probability of capture

Probability of capture was estimated at 25% (LC₂₅), 50% (LC₅₀), and 75% (LC₇₅) levels as 16.7, 17.7, and 18.5 cm, respectively (Figure 5), with age at 50% probability of capture (t₅₀) being estimated at 1.2 years.

Relative Y/R and B/R analysis: Knife-edge selection

The yield per recruit (Y/R) against the fishing mortality and exploitation rate for different levels of natural mortality are shown in Figures 6 and 7, respectively.

Results of the yield-per-recruit analysis and biological reference points are shown in Table 4.

Figure 5

Probability of capture for different length classes (LC₂₅, LC₅₀, LC₇₅).

Table 3

Comparative table of growth and mortality parameters among relevant studies

Author	Sex	L_∞	K	t₀	Φ′	Z	M	F	E	Area of study
This study	Both	65.19	0.125	−1.341	2.72	0.975	0.284	0.69	0.72	Hellenic waters
Soykan et al. [10]	Both	54.53	0.315	−0.223	2.97	1.539	0.579	0.959	0.62	Central Aegean Sea
Kahraman et al. [11]	Both	103.97	0.087	−0.926	2.97	2.01	0.19	1.81	0.9	Marmara Sea
Uzer et al. [12]	Both	102.6	0.0992	−0.8	3.01	2.21	0.57	1.61	0.72	North Aegean Sea
Boudjadi and Rachedi [48]	Both	44.08	0.29	−0.517	2.7	1.53	0.61	0.92	0.6	North-East of Algeria
El Bouzidi et al. [13]	Both	77.39	0.3	−0.427	3.25	1.49	0.51	0.98	0.66	North of Moroccan Atlantic coasts
Slimani et al. [49]	Both	76.65	0.11	−1.21	2.81	0.65	0.28	0.37	0.57	Moroccan Mediterranean coast

Figure 6

Sensitivity analysis of yield per recruit against fishing mortality for different levels of natural mortality.

Figure 7

Sensitivity analysis for yield per recruit against exploitation rate for different levels of natural mortality (green line E_0.1, red line E_0.5 and yellow line E_max).

Table 4

Relative yield/recruit analysis (knife edge) and biological reference points of the population

	E	Y/R	B/R
	0.01	0.007	0.801
	0.20	0.012	0.623
	0.30	0.016	0.496
	0.40	0.018	0.337
	0.50	0.018	0.229
	0.60	0.017	0.144
	0.70	0.015	0.081
	0.80	0.012	0.039
	0.90	0.009	0.013
	0.99	0.007	0.001
Biological reference points		Y/R	B/R
E _max	0.473	0.018	0.256
E _0.1	0.354	0.016	0.403
E _0.5	0.279	0.014	0.505
F _0.1	0.1657	0.021	0.130
F _MAX	0.2972	0.022	0.073
F _MSY	0.2972	0.022	0.073

E, exploitation rate; YPR, yield per recruit; B/R, biomass per recruit; E_max, exploitation rate which produces the maximum yield; E_0.1, exploitation rate at which the marginal increase of relative yield-per-recruit is 1/10th of its value at E = 0; E_0.5, value of E under which the stock has been reduced to 50% of its unexploited biomass; F_MSY, level of fishing mortality that will allow a fish population to achieve MSY; F_MAX, fishing mortality rate at maximum sustainable yield; F_0.1, level of fishing mortality where the slope of the YPR curve is reduced to 10% of the value at the origin; F_MAX, fishing effort where yield is maximum.

4. Discussion

A wide range of variables, such as temperature, salinity, habitat variation, food availability, maturity stage, fishing season, high fishing mortality, and genetic factors, affect a teleost’s sex ratio, GSI, and spawning period [50]. At smaller sizes (less than 30 cm in total length), the sex ratio favored males, but at larger sizes (more than 30 cm in total length), the sex ratio favored females. While the opposite pattern was noted in the Sea of Marmara (Turkey) by Yildiz [51], this pattern was also noticed by Piñeiro and Saínza [4], El Habouz [52], and Costa [53] in Iberian Atlantic waters, Eastern Central Atlantic, and Portuguese coast, respectively. The disparity in growth rates between sexes, the higher natural mortality rate of older males relative to females, or the overfishing-related decrease in catch availability may all contribute to the sex ratio’s unpredictability [54].

The highest reproductive intensity in this study was observed during spring followed by winter. A number of studies in the region have reported spawning between November and March, including the Mediterranean coastline in Egypt [23], Central, and Western Mediterranean [21], the Sea of Marmara Turkey [11], and the Atlantic Moroccan coast [52]. Spawning season can be affected by several factors including temperature, food availability, and the condition factor [55].

The males’ length at first maturity was comparable to that measured in the central Aegean [10]. According to [21, 52], variations in L₅₀ could be attributed to phenotypic responses to environmental factors (such as competition, population distribution, space, and food availability) or to selective pressure, such as fishing effort, which leads to overexploitation of the stock and lower spawning biomass in various areas. The observed difference between males and females in the length at first maturity (L₅₀) with females maturing in larger size compared to males (30.97 cm versus 25.41 cm) could be attributed to the stock’s level of exploitation [56]. The effect of growth and mortality could also lead to a higher proportion of larger-sized females if males grow at a slower rate, especially following the onset of maturity [57].

Asymptotic length (L∞) was lower than those obtained in similar studies from the Strait of Gibraltar [4], Atlantic [52], Tunisian coast [19], Sea of Marmara [20], and the North Aegean [12], with the maximum size in the Mediterranean reportedly limited to 80–90 cm [7]. Growth index (Φ′) in this study (2.7) was lower than those observed in previous studies (between 2.8 and 3.4). The growth rate for the European hake may vary according to genetic variance, biotic factors including food availability and longevity, and regional environmental differences such as temperature, salinity, and depth [58].

This study estimated a relatively high fishing mortality (F = 0.69/year) with the calculated Z/K ratio (7.81) greater than the population equilibrium (Z/K ratio = 1) where mortality is balanced by growth [59], indicating that mortality dominates growth, similarly to [13] (4.97) in the Moroccan Atlantic coast. The exploitation rate calculated in this study (E = 0.72) indicated that the population is under a high level of exploitation, indicating that the species is overfished or at best case fully exploited [60]. Similar exploitation rates were estimated in the north and central Aegean Sea along the Turkish coastline (0.72 and 0.74, respectively) [12, 61]. The optimal exploitation rate for a fish population will vary depending on the species, environment, and management practices in place. However, a general rule of thumb is that exploitation should not exceed 0.5, as this could lead to overfishing. Thus, values greater than 0.5 are an indication that the stock is overfished [30, 62].

Length at first capture (LC₅₀) was estimated at 17.7 cm, with age at probability of capture (t₅₀) being estimated at 1.2 years, whereas the onset of sexual maturity (L₅₀) of the population was estimated at 27.58 cm in total length (3.2 years) and 25.41 (2.6 years) and 30.97 (4.0 years) for males and females, respectively, indicating that the population is exploited from an early age and size, well before sexual maturity. It is noteworthy that despite the minimum landing size (MLS) for M. merluccius in the Eastern Mediterranean of 20 cm total length [24], roughly 64% of the present population was comprised of 1- and 2-year old individuals, the vast majority of which with the total length lower than the MLS. Furthermore, the length class with the highest biomass in an unfished population (L_opt) estimated at 38.16 cm (greater than 5-year-old individuals in this study) comprises less than 4% of the total population, indicating that the target of capturing individuals with an average length equal to this size, theoretically allowing the stock to yield MSY level, would be unattainable.

Studies of crucial biological characteristics, namely growth [4], and the exploitation rate [63] are essential for stock assessment and development of management strategies. Results of this study indicated that further management measures need to be enforced to protect the stock and in particular the juveniles to prevent possible stock depletion. Possible measures could include the increase of MLS through alteration in mesh size, application of nets with a different geometry (square vs. diamond), seasonal closures, closed areas (spawning grounds; nursery areas), improved management of illegal and unregulated fishing (increased coastguard policing) or a combination of the above.

5. Conclusion

This study aimed to assess the population characteristics of the commercially important European hake (Merluccius merluccius) in Hellenic waters (the Eastern Mediterranean). Length at first maturity was estimated at a larger total length compared to the MLS and length at first capture with asymptotic length smaller than those observed in other studies (the Mediterranean). Results indicated that the population is overexploited with mortality dominating growth. It is recommended that further management measures can be put in place to avoid overfishing, given the importance of this highly prized commercial species.

Funding

The authors declare no financial support for the research, authorship, or publication of this article.

Author contributions

Conceptualization, A.T. and D.K.; methodology, A.K. and D.K.; software, A.K. and D.K.; formal analysis, A.T., M.V., A.K., and D.K.; investigation, A.T. and M.V.; resources, D.K.; data curation, A.T. and M.V.; writing—original draft preparation, A.T., M.V., and D.K.; writing—review and editing, A.T., M.V., A.K., and D.K.; supervision, D.K.; project administration, D.K.; All authors have read and agreed to the published version of the manuscript.

Conflict of interest

The authors declare no conflict of interest.

Data availability statement

Data supporting these findings are available within the article or upon reasonable request from the corresponding author.

Institutional review board statement

Not applicable.

Informed consent statement

Not applicable.

Sample availability

Sampling was conducted using commercial bottom trawls across various locations in the Eastern Mediterranean as detailed in section 2.1 of the Materials and Methods.

Publisher’s note

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References

Bozzano A, Sardà F, Ríos J. Vertical distribution and feeding patterns of the juvenile European hake, Merluccius merluccius in the NW Mediterranean. Fish Res. 2005;73:29–36.

Cohen DM, Inada T, Iwamoto T, Scialabba N. Gadiform fishes of the world. FAO Fish Synop. 1990;10:I.

Philips AE. Comparison of some biological aspects between the two sexes of the European hake Merluccius merluccius from the Egyptian Mediterranean waters. Egypt J Aquat Res. 2014;40:309–15.

Piñeiro C, Saínza M. Age estimation, growth and maturity of the European hake (Merluccius merluccius (Linnaeus, 1758)) from Iberian Atlantic waters. ICES J Mar Sci. 2003;60:1086–102.

Zorica B, et al. Reproduktivna biologija oslića, Merluccius merluccius (L. 1758), u Jadranskom moru. Acta Adriat Int J Mar Sci. 2021;62:183–98.

Murua H, Motos L, Lucio P. Reproductive modality and batch fecundity of the European hake (Merluccius merluccius L.) in the Bay of Biscay. Calif Coop Ocean Fish Investig Rep. 1998;196–203.

Mascoli A, Candelma M, Santojanni A, Carnevali O, Colella S. Reproductive biology of male European hake (Merluccius merluccius) in Central Mediterranean Sea: an overview from macroscopic to molecular investigation. Biology (Basel). 2023;12:562.

Colloca F, et al. Rebuilding Mediterranean fisheries: a new paradigm for ecological sustainability. Fish Fish. 2013;14:89–109.

Belhoucine F. Etude de la biologie de la croissance et de la reproduction d’un poisson téléostéen le merlu (Merluccius merluccius L., 1758) et son utilisation comme indicateur biologique de la pollution par les métaux lourds (Zinc, Plomb et Cadmium) dans la baie d’Oran [Thèse de Doctorat]. Oran: Université d’Oran; 2012.

Soykan O, Ilkyaz AT, Metın G, Kinacigıl HT. Age, growth and reproduction of European hake (Merluccius merluccius (Linn., 1758)) in the Central Aegean Sea, Turkey. J Mar Biol Assoc UK. 2015;95:829–37.

Kahraman AE, Yıldız T, Uzer U, Karakulak FS. Sexual maturity and reproductive patterns of European hake Merluccius merluccius (Linnaeus, 1758) (Actinopterygii: Merlucciidae) from the Sea of Marmara, Turkey. Acta Zool Bulg. 2017;69:385–92.

Uzer U, Öztürk B, Yıldız T. Age composition, growth, and mortality of European hake Merluccius merluccius (Actinopterygii: Gadiformes: Merlucciidae) from the northern Aegean Sea, Turkey. Acta Ichthyol Piscat. 2019;49:109–17.

El Bouzidi C, Abid N, Awadh H, Bakkali M, Zerrouk MH. Growth and mortality of the European hake Merluccius merluccius (Linnaeus, 1758) from the North of Moroccan Atlantic coasts. Egypt J Aquat Res. 2022;48:233–9.

ELSTAT. Hellenic Statistical Authority Sea fisheries [Internet]. ELSTAT. 2023 [cited 2023 Mar 12]. Available from: http://www.statistics.gr/

GFCM. (Mediterranean and Black Sea) Capture Production. Fisheries and Aquaculture Division [Internet]. FAO. 2023 [cited 2023 Mar 12]. Available from: https://www.fao.org/fishery/statistics-query/en/gfcm_capture/gfcm_capture_quantity

Ragonese S, Morizzo G, De Santi A, Bianchini ML. Rapid-response indicators of changes in resource state based on Mediterranean bottom-trawl surveys. ICES J Mar Sci. 2005;62:511–5.

Recasens L, Chiericoni V, Belcari P. Spawning pattern and batch fecundity of the European hake (Merluccius merluccius (Linnaeus, 1758)) in the western Mediterranean. Sci Mar. 2008;72:721–32.

Al-Absawy MAE-G. 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. 2010;9:2544–59.

Khoufi W, et al. Reproductive traits and seasonal variability of Merluccius merluccius from the Tunisian coast. J Mar Biol Assoc UK. 2014;94:1545–56.

Kahraman AE, Yıldız T, Uzer U, Karakulak FS. Age composition, growth and mortality of European hake Merluccius merluccius (Linnaeus, 1758) (Actinopterygii: Merlucciidae) from the Sea of Marmara, Turkey. Acta Zool Bulg. 2017;69:377–84.

Carbonara P, et al. The spawning strategy of European hake (Merluccius merluccius, L. 1758) across the Western and Central Mediterranean Sea. Fish Res. 2019;219:105333.

Candelma M, et al. Aspects of reproductive biology of the European hake (Merluccius merluccius) in the Northern and Central Adriatic Sea (GSA 17-Central Mediterranean Sea). J Mar Sci Eng. 2021;9:389.

ELGazzar HM, Mahmoud HH, Abdel-Rahman SA, Hussein EEM. Maturity and gonadosomatic index of uropean hake Merluccius merluccius (Linnaeus, 1758) from the Egyptian Mediterranean water. Menoufia J Anim Poult Fish Prod. 2022;6:143–52.

Commission E. Council Regulation (EC) No 1967/2006 concerning management measures for the sustainable exploitation of fishery resources in the Mediterranean Sea. EC Brussels; 2006.

Von Bertalanffy L. A quantitative theory of organic growth (inquiries on growth laws. II). Hum Biol. 1938;10:181–213.

Munro JL, Pauly D. A simple method for comparing the growth of fishes and invertebrates. Fishbyte. 1983;1:5–6.

Froese R, Binohlan C. Empirical relationships to estimate asymptotic length, length at first maturity and length at maximum yield per recruit in fishes, with a simple method to evaluate length frequency data. J Fish Biol. 2000;56:758–73.

Beverton RJH, Holt SJ. On the dynamics of exploited fish populations. Switzerland: Springer Science & Business Media; 2012.

Pauly D. On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. ICES J Mar Sci. 1980;39:175–92.

Sparre P, Venema SC. Introduction to fish stock assessment. Part 1: Manual. FAO Fisheries Technical Paper; 1998. p. 306.

Pauly D. Some simple methods for the assessment of tropical fish stocks. Rome: FAO; 1983.

Beverton RJH. Spatial limitation of population size; the concentration hypothesis. Netherlands J Sea Res. 1995;34:1–6.

Hoggarth DD. Stock assessment for fishery management: a framework guide to the stock assessment tools of the fisheries management and science programme. Rome: Food & Agriculture Org.; 2006.

Pauly D. Theory and management of tropical multispecies stocks: a review, with emphasis on the Southeast Asian demersal fisheries. Manila: ICLARM; 1979.

Fulton TW. The rate of growth of fishes. Twenty-second Annual Reports, Part III. Edinburgh: Fisheries Board of Scotland; 1904. p. 141–241.

Nikolsky CV. The ecology of fishes. London and New York: Academic Press; 1963.

Guillou M, Lumingas LJL. Variation in the reproductive strategy of the sea urchin Sphaerechinus granularis (Echinodermata: Echinoidea) related to food availability. J Mar Biol Assoc UK. 1999;79:131–6.

Trippel EA, Harvey HH. Comparison of methods used to estimate age and length of fishes at sexual maturity using populations of white sucker (Catostomus commersoni). Can J Fish Aquat Sci. 1991;48:1446–59.

Rutherford A. Introducing ANOVA and ANCOVA: a GLM approach. Thousand Oaks (CA): Sage; 2001.

Rolke W, Gongora CG. A chi-square goodness-of-fit test for continuous distributions against a known alternative. Comput Stat. 2021;36:1885–900.

Şahin M, Aybek E. Jamovi: an easy to use statistical software for the social scientists. Int J Assess Tools Educ. 2019;6:670–92.

Quinn TJ, Deriso RB. Quantitative fish dynamics. Oxford: Oxford University Press; 1999.

Bhattacharya CG. A simple method of resolution of a distribution into Gaussian components. Biometrics. 1967;115–35.

Gayanilo F, Sparre P, Pauly D. FAO-ICLARM Stock Assessment Tools II (FiSAT II) user’s guide. Rome: FAO; 2005.

Pauly D, Caddy JF. A modification of Bhattacharya’s method for the analysis of mixtures of normal distributions. Rome: FAO; 1985.

Rodríguez MG, Esteban A. How fast hake grows? A study on the Mediterranean hake (Merluccius merluccius, L.) comparing whole otoliths readings and length frequency distributions data. Sci Mar. 2002;66:145–56.

Berverton RJH, Holt SJ. Manual of methods for fish stock assessment. Part II Tables yield Functions Fisheries Technical Paper No 38. Food and Agriculture Organization of the United Nations; 1966. p. 10.

Boudjadi Z, Rachedi M. Age, growth, and mortality of the European hake Merluccius merluccius (Linnaeus, 1758) from El-Kala coastline (the extreme North-East of Algeria). Egypt J Aquat Biol Fish. 2021;25:523–37.

Slimani D, et al. Age, growth and exploitation rate of European hake, Merluccius merluccius, from the Moroccan Mediterranean coastline. AACL Bioflux. 2023;16:635–49.

Rajendiran P, et al. Sex determination and differentiation in teleost: roles of genetics, environment, and brain. Biology (Basel). 2021;10:973.

Yildiz T, Kesiktaş M, Yemisken E, Sonmez B, Eryilmaz L. Modeling the trajectories of growth and reproduction in European Hake (Merluccius merluccius, L. 1758) from the Sea of Marmara, Turkey. Iran J Fish Sci. 2022;21:445–62.

El Habouz H, et al. Maturity and batch fecundity of the European hake (Merluccius merluccius, Linnaeus, 1758) in the eastern central Atlantic. Sci Mar. 2011;75:447–54.

Costa AM. Somatic condition, growth and reproduction of hake, Merluccius merluccius L., in the Portuguese coast. Open J Mar Sci. 2013;3:12–30.

Piñeiro-Álvarez CG. Edad y crecimiento de la merluza europea Merluccius merluccius (Linnaeus, 1758) del Noroeste de la Península Ibérica: evolución de un paradigma. Centro Oceanográfico de Vigo; 2011.

Ferrer-Maza D, et al. Parasitism, condition and reproduction of the European hake (Merluccius merluccius) in the northwestern Mediterranean Sea. ICES J Mar Sci. 2014;71:1088–99.

Lappalainen A, et al. Length at maturity as a potential indicator of fishing pressure effects on coastal pikeperch (Sander lucioperca) stocks in the northern Baltic Sea. Fish Res. 2016;174:47–57.

Martin I. A preliminary analysis of some biological aspects of hake Meluccius merluccius L. 1758) in the Bay of Biscay. International Council for the Exploration of the Sea. C.M. 1991/G:54; 1991.

Mellon-Duval C, De Pontual H, Métral L, Quemener L. Growth of European hake (Merluccius merluccius) in the Gulf of Lions based on conventional tagging. ICES J Mar Sci. 2010;67:62–70.

Barry JP. Inferring demographic processes from size-frequency distributions: simple models indicate specific patterns of growth and mortality. Fish Bull. 1989;88:13–9.

Fiorentino F. A compilation of information on stock assessment in the GFCM areas presented in standard forms. IRMA, Istituto di ricerche sulle Risorse Marine e l’Ambiente, Consiglio …; 2000.

Gurbet R, Akyol O, Yalçın E. Exploitation and mortality rates of European hake (Merluccius merluccius) in the Aegean Sea (Izmir Bay, Turkey). J Appl Ichthyol. 2013;29:569–72.

Froese R, Stern-Pirlot A, Winker H, Gascuel D. Size matters: how single-species management can contribute to ecosystem-based fisheries management. Fish Res. 2008;92:231–41.

Martin P, Sartor P, Garcia-Rodriguez M. Exploitation patterns of the European hake Merluccius merluccius, red mullet Mullus barbatus and striped red mullet Mullus surmuletus in the western Mediterranean. J Appl Ichthyol. 1999;15:24–8.