Issue |
Aquat. Living Resour.
Volume 33, 2020
|
|
---|---|---|
Article Number | 20 | |
Number of page(s) | 17 | |
DOI | https://doi.org/10.1051/alr/2020021 | |
Published online | 04 December 2020 |
Research Article
Population structure, reproduction and exploitation of the greater forkbeard Phycis blennoides (Brünnich, 1768) from the Algerian basin★
1
Fisheries Laboratory, Faculty of Biological Sciences, University of Sciences and Technology Houari Boumediene (USTHB), BP. 32,
El-Alia Bab-Ezzouar 16111, Algiers, Algeria
2
Pelagic-ecosystem Laboratory, Faculty of Biological Sciences, University of Sciences and Technology Houari Boumediene (USTHB), BP. 32, El-Alia Bab-Ezzouar 16111, Algiers, Algeria
3
Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma, Illes Balears, Spain
* Corresponding author: zakia.alioua@gmail.com
Handling Editor: Richard Nash
Received:
16
December
2019
Accepted:
13
October
2020
The objective of this study was to determine the population distribution and some biological aspects for fish stock assessment of the greater forkbeard Phycis blennoides along the Algerian basin. The distribution of P. blennoides (3418 individuals) was studied using data collected between 170–779 m depth during two bottom trawl surveys developed on 2003 and 2004. Additionally, some biological parameters were obtained from 1050 individuals sampled from commercial fisheries in Algerian ports (i.e. Annaba, Azeffoun, Dellys, Cap Djinet, Zemmouri, Bouharoun, Algiers, La Madrague, Cherchell, Tenes and Mostaganem) during the period 2013–2017. P. blennoides sampled from bottom trawl surveys showed a depth related distribution with the largest individuals being found at 600–800 m depth and the smallest at shallower depths. Density and biomass varied with depth and density also with longitude, while biomass showed no pattern with longitude. Recruitment was recorded in the eastern sector of Algeria during winter, for individuals sampled by bottom trawl surveys. Young P. blennoides entered commercial fisheries in summer, with an overall sex ratio skewed towards males (1F:2.18M). The size at first maturity (L 50) was 24.30 cm and 30.39 cm for males and females, respectively. The age at 50% maturity was 2–3 years for specimens collected by a bottom trawl survey in 2003 and commercial fisheries, but 3–4 years for the bottom trawl survey in 2004.
Key words: Phycis blennoides / density / biomass / maturity / exploitation / Algerian basin
The R-code and data of the population structure and some biological parameters of this species used in this work are available from Alioua et al. (2020a) and can be obtained through SEANOE.
© EDP Sciences 2020
1 Introduction
The general overfishing of Mediterranean stocks requires urgent management measures to ensure the sustainability of resources (Quetglas et al., 2017). Accurate assessment of population parameters related to life history characteristics, including reproductive and growth aspects, is an essential component of effective fisheries management (Brown-Peterson et al., 2011; Saborido-Rey and Trippel, 2013).
The greater forkbeard Phycis blennoides frequents muddy and sandy bottoms and is mainly targeted by trawl fishing and longlines (Matarrese et al., 1998). It has a wide spatial distribution, occurring in the Mediterranean (Cohen et al., 1990, Massutí et al., 1996; Rotllant et al., 2002; Ragonese et al., 2004; Dallarés et al., 2016) and the North-East Atlantic (Clarke, 2005), from Norway and Iceland (Astthorsson and Palsson, 2000) to the White Cape in West Africa. It is a broadcast spawner (Rotllant et al., 2002) with a high total fecundity of 1643899 eggs/female (Fernandez-Arcaya et al., 2013). It is an iteroparous and gonochoristic species with external fertilization (Rotllant et al., 2002), similarly to Phycis phycis from the same genus (Vieira et al., 2016). The latter species presents a group-synchronous ovary development and is a batch spawner (Vieira et al., 2016), while oocytes of P. blennoides do not exhibit synchronous development (Rotllant et al., 2002). Several authors have studied the biology of this species throughout the Mediterranean Sea, e.g. growth (Romdhani et al., 2016), recruitment patterns (Massutí et al., 1996; Matarrese et al., 1998; Lloret and Lleonart, 2002), sexuality (Rotllant et al., 2002), diet composition (Sorbe, 1977; Macpherson, 1978; Sartor, 1995; Morte et al., 2002) and trophic level (Alioua et al., 2018). Moreover, the morpho-histology and histopathology of its digestive organs have recently been studied (Alioua et al., 2020b).
P. blennoides is a low value bycatch in mixed fisheries targeting hakes and shrimps in the Gulf of Lion and Valencia, (Sorbe, 1977; Morte et al., 2002). In contrast it is a species of economic interest in other Mediterranean fishing areas (FAO, 2005), for example on the Turkish coast (Tokaç et al., 2018), in the Catalan Sea (Massutí et al., 1996), and the central region of Algeria (Alioua et al., 2018), where it can fetch 11‑15 USD per kg.
In Algeria, the presence of P. blennoides is very sporadic and the landed quantities are limited in space and time (Alioua et al., 2018). Moreover, scientific assessments of this species are lacking, with no official data available from fisheries services. For better stock management, it seems essential to define sustainable fishing levels and biological reference points. This study aims to contribute knowledge to improve fish stock management in Algeria. It provides informations on population structure, reproduction, growth and exploitation of P. blennoides along the Algerian coast.
The main objectives of this paper are as follow: (1) study density and biomass; (2) analyze the size frequency distribution; (3) characterize the reproduction (sexual maturity stages, physiological indices, histo-morphology and size at first maturity (L50)); (4) estimate growth parameters, exploitation rates and mortalities. For the analyses, we used data from two scientific bottom trawl surveys conducted in 2003 and 2004; supplemented by additional biological data from commercial fisheries, collected 10 years later (2013‑2017).
2 Materials and methods
2.1 Sampling
Samples were obtained with an experimental bottom trawl (GOC-73) during 160 hauls carried out between 40 and 779 m. Following the protocol generally used in the Mediterranean (MEDITS program; Bertrand et al., 2002), two bottom trawl surveys were performed in March 2003 and February-March 2004. A total of 3418 individuals of P. blennoides were caught between 170 and 779 m depth at three sectors along the Algerian coast: western area (W) from Mostaganem to Ghazaouet, central area (C) from Tenes to Bejaia and eastern area (E) from Bejaia to Annaba (Fig. 1, Table S1). Additionally, monthly samples were collected from commercial trawlers and longliners between 2013 and 2017 (December 2013 to June 2015; February to May 2016; December 2016; March to May 2017) at 11 Algerian ports: Annaba, Azeffoune, Dellys, Cap Djinet, Zemmouri, Bouharoun, Alger, La Madrague, Cherchell, Ténès and Mostaganem (Fig. 1, Table S2).
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Fig. 1 Study area of P. blennoides with sampled landing ports (W: sector west, C: sector center, E: sector east). |
2.2 Population structure
2.2.1 Density, biomass and mean-weight
Numbers and biomass of P. blennoides were standardized to 1 km2 for each trawl haul, accounting for speed and effective horizontal opening of the gear. To identify the geographical gradient of the distribution of this species, density (ind/km2), biomass (kg/km2) and mean-weight were determined by bathymetric range (<200 m, 200‑300 m, 300‑400 m, 400‑500 m, 500‑600 m, 600‑700 m, 700‑800 m) and for the three geographical areas (W: West, C: Central and E: East). Results from 2003 and 2004 were compared globally using the following statistics:
where m is the average across total mean densities, total mean biomasses and total mean weights in each year, s 2 the variance of the mean and n the number of samples. An analysis of variance (ANOVA) was used to test the null hypothesis that there was no difference between the density, biomass and mean weight between bathymetric strata and sectors of both sampling years (2003‑2004). The Tukey post-hoc test “Honest Significant Difference” was used when significant differences were detected. Prior and to minimize heteroscedasticity, the variable density was log10 transformed and a Shapiro-Wilk test was performed to verify normality. To study the effect of depth and longitude, a linear model (LM) was used. In addition, a Generalized additive model (GAM) was also fitted to study the potentially non-linear the effects of longitude on community density and biomass. Cross-validation (GCV) was used to estimate the optimal degrees of freedom. The Akaike Information Criterion (AIC) proved useful as a coarse quantitative aid to choose between models (Wood, 2017). The GAM was implementated with R program version 1.1.383 (R Core Team, 2017) using the mgcv package (Wood, 2006). For studying the spatial distribution, densities, biomasses and mean-weights were mapped.
2.2.2 Size frequency distribution
To characterize population structure, the size frequency distributions of P. blennoides collected by the two bottom trawl surveys carried out in 2003 and 2004 were studied across depth. The size frequency distributions of commercial fisheries were represented by gender and season. A Kolmogorov‑Smirnov test (KS) was used to compare length frequency distributions of P. blennoides from these surveys and commercial fisheries. Furthermore, a KS was used to analyse the difference between sexes and seasons for individuals collected from commercial fisheries.
2.3 Reproduction
For reproduction analysis, a total of 1050 individuals of P. blennoides captured from commercial fisheries were analysed. From each individual, the following informations were collected: total length (TL, 0.01 cm), eviscerated weight (Wevi, 0.01g), liver weight (WL, 0.01g) and gonad weight (WG, 0.01g). Sex and sexual maturity stages were macroscopically determined after opening the abdominal cavity. Macroscopic stages of reproduction were determined using the four-stage scale of Rotllant et al. (2002) for gadiforms as follow: immature (thin/filamentous, transparent); early maturation (small orange pink tube for ovaries, homogeneous tube with a white ivory colour for testes); advanced maturation stage (increased vascularization and volume, ovaries were long orange-red tube, semen is visible for testes); and ripe (much-reduced volume of the gonads richly vascularized: gravid ovaries, dark brown testes). Immature individuals with macroscopically undifferentiated gonads were excluded from reproductive analyses (Sanchez-Vidal et al., 2013).
2.3.1 Sex-ratio
Sex-ratios were compared across seasons and 3-cm size classes using a chi-square test (χ 2). A post hoc test was applied when significance was found applying the function pairwise Nominal Independence, using the rcompanion package (Mangiafico, 2018) in R software version 1.1.383 (R Core Team, 2017).
2.3.2 Reproduction indices and size at maturity
For each individual, the gonadosomatic (GSI), hepatosomatic (HSI) and somatic condition factor (K) indices were estimated using the following formulas:
,
respectively; where WG
is the weight of the gonad, W
evi is the eviscerated weight, WL
is the weight of the liver and TL is the total length. The proportions of mature females by size were fitted by a logistic equation as described by Ashton (1972):
where: P TL is the predicted proportion of mature females at a given total length (TL), and size at first maturity L 50 = –a/b.
2.3.3 Histology
Histological sections were performed on a representative sample (different months and stages) of 151 gonads, covering the entire reproductive cycle. Gonads were fixed in 10% formalin, dehydrated by alcohol solutions with a programmed automat (Spin Tissue Processor STP 120 Myr), impregnated in melted paraffin for 24 h, embedded in paraffin, sectioned by 3 μm using a Leica RM2125 RT microtome and stained with hematoxylin-eosin. The microscopic analysis was carried out using a Premiere T3.15A microscope and a camera, connected to a computer. The image was processed using the TSView image analysis software (version 6.2.4.5. Tucsen, China). Microscopic stages were described using standard terminology from Brown-Peterson et al. (2011). Based on this histological screening, a few oocyte diameters were randomly measured without correcting, for shrinkage.
2.4 Growth
Growth consists in establishing a relationship between a measurable variable (length, weight) characterizing an individual and its age. This relationship was represented by the von Bertalanffy model. From size frequency distributions of P. blennoides, age-length keys were obtained applying Bhattacharya‘s method using the FISAT II version 1.2.0 (Gayanilo et al., 2005).
Using the size structure analysis of Powell Wetherall, asymptotic length (L ∞) and Z/K ratios were estimated by FISAT II version 1.2.0 (Gayanilo et al., 2005). To estimate the growth rate (K), we used the empirical relationship between the growth performance index (Φ′) and the asymptotic length L ∞ : Φ′ = log10K+2log10L∞ (Pauly and Munro, 1984). The parameter t 0 is included to adjust the equation for the initial size of the organism and is defined as the age at which the organisms would have had zero size. We used the empirical equation of Pauly (1979) to estimate t0 of the von Bertalanffy growth function: log10(−t0) = −0.3922−0.2752log10L∞−1.038log10K.
2.5 Exploitation
To calculate exploitation indices, it is often impossible to obtain direct and accurate measurements of mortalities. Natural mortality (M) can vary with size, sex, parasitism, food availability and predation (Siegfried and Sansó, 2006). In this study, M was estimated using the empirical equation of Pauly implemented in FISAT II, assuming an average temperature of 13.08 °C for the habitat of P. blennoides (Cartes et al., 2016). Then, the equation developed by Djabali et al. (1994) for Mediterranean fishes and recommended by Bouaziz et al. (2014) was employed: log10 M =−0.0278–0.1172log10L∞+0.5092log10K. Fishing mortality (F) was estimated as F = Z ‑ M and the exploitation rate (E) as E = F/Z (Pauly, 1983). Total mortality (Z) is considered to be the sum of several independent mortality rates. Z was obtained by the linearized catch curve using FISAT II software, version 1.2.2.2 (Gayanilo et al., 2005).
3 Results
3.1 Population structure
The total average density of Phycis blennoides from the Algerian basin possibly decreased (t*= 2.284 > IC: 1.96) between 2003 (412 525 ± 943 327 ind/km2) and 2004 (110 680 ± 191 ind/km2), though uncertainty of mean estimates was large making the confidence intervals of annual estimates overlap. For total average biomass, a slight non-significant decrease was observed (Tab. 1). Average mean-weight of P. blennoides was higher in 2003 than in 2004; though the difference was not significant (p ANOVA= 0.143; Table S3).
The bathymetric distribution of P. blennoides showed different patterns for density, biomass and mean-weight (Table S3, Fig. 2). Mean densities had a modal distribution with a maximum between 300 and 500 m depth, but some variation between the two years, while biomass was highest between 600 and 800 m depth (Fig. 2A, 2B). Only four individuals were caught in 2004 between 100 and 200 m (Fig. 2A). Following the biomass pattern, mean-weight also increased with depth (Fig. 2C). A significant difference between years was found for biomass at shallow depth (200‑300 m) and on the slope (700‑800 m) (p ANOVA= 0.04). In contrast, the ANOVA showed no significant differences in terms of overall density, biomass and mean-weight between sampling years (Table S3).
During both years, the density of P. blennoides increased significantly with longitude (Fig. 2S), reaching its maximum in the eastern sector (Fig. 3a, 3b, 3c). For biomass, the variation was not significant across longitude for both years (Fig. 3c, 3d). The relationship between density and biomass showed a recruitment event in 2003 for a sampling station at 326 m in the east. This sampling station was characterized by a high density (>5000 ind/km2) and low biomass (<20 kg/km2). In 2004 at the same station relatively high density (876.22 ind/km2) and low biomass (<20 kg/km2) were also observed. Mean-weight was 2.24 g in 2003 and 8.81 g in 2004. Also in 2003; a station with large fish was observed at 625 m depth in the eastern sector, characterized by low density (<1000 ind/km2) and high biomass (>50 kg/km2) (Fig. 3a).
The spatial distribution was illustrated by mapping densities, biomasses and mean-weights of both years (Fig. 4).
Analysis of length frequency distributions showed that in both bottom trawl surveys, average length of P. blennoides on the slope was higher than on the continental shelf, indicating bathymetric segregation between adults and juveniles (Fig. S1). Juveniles (3‑7 cm) were found between 200 and 600 m depth, while larger individuals were limited to the deepest areas (600–800 m), with a marked peak in 2003 between 200–400 m. Medium-sized individuals (∼20 cm) were present in all depths for both years, with higher frequencies in 2004. Length-frequency distributions showed a general prevalence of small sizes as expected. Juveniles (<9 cm) were more abundant on the continental shelf (200–400 m depth) than on the slope, as well as in 2003 compared to 2004. Only four individuals were caught between 100–200 m in 2004 (6, 17, 18 and 26 cm). A small portion of larger sizes appeared between 600–800 m in both years (2003 and 2004).
The maximum observed size was 61 cm in 2003; 52 cm in 2004 and 62.7 cm for commercial fisheries (Fig. 5). Winter recruitment (∼6 cm) was identified for fishes caught during the two bottom trawl surveys (2003 and 2004). Small individuals appeared in commercial fisheries at 12 cm in length during summer.
Seasonal lenght frequency distributions of P. blennoides from landings of commercial fisheries are shown in Figure 6. In autumn, sizes around 20 cm were common, representing high percentages of individuals (17.35% for 20 cm and 25.9% for 21 cm). Large individuals (>36 cm) appeared during winter and spring.
The Kolmogorov Smirnov (KS) statistics showed no significant differences in size between P. blennoides caught from bottom trawl surveys in 2003 and 2004 (p 2003-2004 = 0.3742) and commercial fisheries (p 2003-CF = 0.4913; p 2004-CF = 0.7225). Note that sample size was higher for bottom trawl surveys in 2003 (n = 2064) and 2004 (n = 1346) than commercial fisheries (n = 1050) (Fig. 5). For commercial fisheries, we did not observe any differences between seasons (p summer-winter = 0.9794; p summer-autumn = 0.9627; p summer-spring = 0.2032; p autumn-winter = 0.9639; p autumn-spring = 0.9639; p spring-winter = 0.8079) (Fig. 6). In contrast, significant differences in length frequency distributions occurred between sexes (p = 0.03273) (Fig. 7).
Total mean density (ind/km2), total mean biomass (kg/km2) and total mean weight (kg) of P. blennoides caught from bottom trawl surveys (BTS) along the Algerian coast.* Significant.
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Fig. 2 Density (ind/km2), biomass (kg/km2) of P. blennoides with depth stratum (m) caught by the bottom trawl surveys in 2003 (A) and 2004 (B) along the Algerian coast and mean weight (kg) (C). |
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Fig. 3 Generalized additive model (GAM) of density (ind/km2) and biomass (kg/km2) of P. blennoides with longitude (°) caught by the bottom trawl surveys in 2003 (A, C) and 2004 (B, D) along the Algerian coast. |
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Fig. 4 Mapping density, biomass and mean-weight of P. blennoides caught by BTS (W: west, C: center, E: east). |
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Fig. 5 Length frequency of P. blennoides caught from bottom trawl surveys in 2003 (A) and 2004 (B) and commercial fisheries in the algerian coast (n: number of individuals). |
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Fig. 6 Seasonal lenght frequency distribution of P. blennoides from landings of commercial fisheries (A: Summer, B: Autumn, C: Winter, D: Spring, n: number of individuals). |
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Fig. 7 Length frequency distribution of P. blennoides by sexes from landing of commercial fisheries (F: female, M: male, nd: undetermined, X axis: Lower limit of size class). |
3.2 Reproduction
Overall, the sex-ratio was skewed towards males (1F:2.18M, χ 2:6.92). This was observed in all seasons (autumn 1:3.64; spring 1:2.15; summer 1:2.53; winter 1:1.60) with significant differences (χ 2:12.393, p = 0.006), between autumn- spring (p = 0.045) and autumn-winter (p < 0.01). The sex-ratio varied with size (χ 2:107.85, p = 4.161 e‑16), with males dominating (1F : 2.72 M) for length classes smaller than 27 cm. Females were dominant (1 F: 0.17 M to 1 F : 0.25M) between 27 and 39 cm (Fig. 7).
The gonado-somatic index (GSI) of males were higher than those of females (Fig. 8a). For males the maximum value was observed in winter, followed by summer, autumn and then spring. For females, highest GSI were in spring and summer, followed by winter and autumn (Fig. 8a). In males, the maximum hepato-somatic index (HSI) was reached in autumn and the minimum in spring, while the peak of somatic condition factor (K) was recorded in summer and the minimum in winter (Fig. 8b). The maximum HSI in females followed the same pattern as for males (Fig. 8c). For K equal values were reported in winter and autumn (Fig. 8c).
The seasonal development of macroscopic stages of P. blennoides's reproduction are represented in Figure 9. The sexual maturity stage evolution of this species revealed a spermatic emission all year round (Fig. 9a) and spring-summer spawning capable females (Fig. 9b). Furthermore, individuals in regressing phase appeared in winter and autumn for both sexes, in addition to spring for males (Fig. 9a). Immature specimens were found in all seasons. Considering developing stage, size at first maturity (L 50) was 24.30 cm for males and 30.39 cm for females (Fig. 10). The description of macroscopic stages of reproduction found in this study is summarized in Table 2.
Histological sections showed that the gonad structure of P. blennoides was similar to that found in most teleost species (Fig. 11). Male gonads presented four distinctive maturity phases in the Algerian greater forkbeard, in contrast to ambiguous ovaries development. Females had cystovarian ovaries characterized by paired lobes that were fused at the caudal end. At immature stage, the ovigerous leg contained primary growth oocytes with many oogonia (Oog) which are the smallest germinal cells of the oogenesis (Fig. 11a). Anatomically, enlarged ovaries contain blood vessels during the developing phase. The histological sections through developing gonads showed oocytes increased in cytoplasmic and nuclear volume together, with the presence of initial vitellogenic oocytes (Vtg I) (109.07 μm) and primary growth oocytes (PG) (Fig. 11b). In early maturing females, the oocyte as well as the nucleus became larger with light cytoplasm. At this stage, the gonads had initial vitellogenic oocytes (Vtg I) containing yolk protein (Fig. 11c). Regenerating ovaries found in the largest Algerian greater forkbeard were flaccid and dark. Their histological structure showed the presence of a thick ovarian wall (Ow) consisting of an outer mesothelium, a layer of smooth muscle, blood vessels and an inner layer of simple columnar epithelium (Fig. 11d). At this stage, primary growth oocytes were mainly present.
Among 200 analysed ovaries, only two spawning capable females were found. Immature/regenerating stages were mainly found for females. Nevertheless, eggs were not observed macroscopically in large females (>39 cm). In contrast to females, all maturing stages were observed in males. Juvenile greater forkbeard, had small and clear testes in primary stage, with spermatogonia (spg) as the largest germinal cells, mainly in the peripherical zone of the spermatogenic cyst (Fig. 11e). At developing stages, testes were ivory white, their spermatogonia, transformed by meiotic division into spermatocytes (Spcy) which are smaller, occupied the periphery part of cysts then, became spermatids (Spd) (Fig. 11f). Males were ready for the spermatic emission when their testes showed spermatozoa (Spz). They were the smallest cells of spermatogenesis located at the central part of the cyst as small black spots (Fig. 11g). Males were reactive to abdominal pressure. The rupture and confluence of seminiferous tubules were observed to release their spermatozoa (Spz: 1.06 μm) in the direction of the deferens duct (Fig. 1h).
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Fig. 8 Physiological indexes of P. blennoides from the Algerian coast (vertical bars are standard deviations). a) gonadosomatic index (GSI); b) hepatosomatic index (HSI) and somatic condition factor (K) for males; c) hepatosomatic index (HSI) and somatic condition factor (K) for females. |
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Fig. 9 Seasonal maturity stages of P. blennoides from the Algerian coast. |
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Fig. 10 Logistic regression model for the proportion of sexually mature males (M) and females (F) of P. blennoides (males L50= 24.30 cm, females L50 = 30.39 cm). |
Macroscopic and microscopic descriptions of the phases in the reproductive cycle of P. blennoides.
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Fig. 11 Abbreviation: Oog. Oogonia, PG. Primary growth oocyte, Nu. Nucleoli, F.e. Follicular envelope, Lo. Ovarian lumen, VtgI. Primary vitellogenic oocyte, N. Nucleus, Cyt.h. Heterogeneous cytoplasm, St. Ovarian stroma. Ow. Ovarian wall, Spg. Spermatogonia, L.l. Lobular lumen, Cyst. Cyst, Mb.l. The basal membrane of the lobule, Spcy. Spermatocyt, Spd. Spermatid, Spz. Spermatozoa. Histological sections through the gonads of P. blennoides showing different development phases (scale: 100 μm). a. General view of immature female (Gx10, caught 30/04/15, TL: 53.1 cm; WG: 3.86 g, GSI: 0.396). b. Developing female (Gx40, caught 21/12/15, TL: 27.3 cm; WG: 0.12 g, GSI: 0.601). c. Early maturing female with initial stage of vitellogensis and yolk protein (Gx40, caught 29/06/15, TL: 45.1 cm, WG: 3.9 g, GSI: 0.601). d. Histological section through the gonad of the biggest female sampled (Gx10, caught 23/04/2016, TL: 62.7 cm, WG :10.54 g, GSI: 0.61). Thick ovarian wall (Gx4) in regenerating ovaries. e. Immature male with spermatogonia cells (Gx40, caught 10/02/15, TL: 23.6 cm, WG: 0.02 g, GSI: 0.024). f. Male regenerating stage with the appearance of spermatids and spermatozoa (Gx40, caught 26/08/14, TL: 26.1cm, WG: 0.72 g, GSI: 0.373). g. Developing testes (Gx40, caught 6/01/15, TL: 21.1cm, WG: 0.5 g, GSI: 0.990). h. Mature testes with emission of spermatozoa (Gx10, caught 06/01/2015, TL: 24.1 cm, WG: 1.23 g, GSI: 2.13). |
3.3 Growth
The Bhattacharya method isolated seven age classes for the bottom trawl survey in 2003; eight for commercial fishing individuals and nine for specimens from the bottom trawl survey in 2004 (Tab. 3). Age at 50% maturity was 2–3 years for P. blennoides collected by the bottom trawl survey in 2003 and commercial fisheries, but 3-4 years for the bottom trawl survey in 2004. Growth parameters for each sampling type and period are given in Table 4. The largest asymptotic length (L∞) was observed for P. bennoides obtained from commercial fisheries, followed by individuals caught by the bottom trawl surveys in 2003 and in 2004. The opposite pattern was found for growth rate (K).
Mean age-at-length of P. blennoides sampled by bottom trawl surveys (BTS) in 2003 and 2004 and from commercial fisheries (TL: total length in cm) off Algeria.
Growth parameters of P. blennoides estimated by FISAT II software. L∞: asymptotic length (cm) obtained by Powell Wetheral's method. K: growth rate (year−1) obtained applying the equation of Pauly and Munro (1984). t0: size when age is zero, Lmax: Maximum observed size in cm.
3.4 Exploitation
Natural mortalities (M) estimated by Djabali's equation were lower than those obtained by applying Pauly's empirical equation (Tab. 5). The lowest values of total mortality (Z) were found for the bottom trawl survey in 2003; followed by the bottom trawl survey in 2004 and commercial fisheries (Tab. 5). However, the Z estimated by the catch curve showed an optimal situation (E1) for P. blennoides collected by bottom trawl survey in 2003; corresponding to 49% of the exploited stock. The exploitation rate of P. blennoides increase from 2003 to 2004 (Tab. 5), testifying of two overfishing situations (E2 > 0.5).
Exploitation indices for P. blennoides from the Algerian coast. Natural mortality from Djabali's equation (M1) and Pauly's equation (M2); Zc: total mortality from converted catch curve using FISAT II software; F1: fishing mortality using M1 and Zc; F2: fishing mortality using M2 and Zc; E1 and E2 exploitation rates using Zc.
4 Discussion
4.1 Population structure
Population dynamics refer to the processes responsible for changes in density or biomass of a population over time, and are monitored by a subset of possible population parameters (Pope et al., 2010). In this study, the biomass of the greater forkbeard showed distinct distribution pattern for adults and juveniles, with the later found mainly at shallower depths and the former deeper. This bathymetric distribution was already reported for the Phycis genus by several authors (Massutí et al., 1996; Matarrese et al., 1998; Rotllant et al., 2002; Fiorentino et al., 2003b; Santos et al., 2019). It suggests ontogenic migration with the older individuals moving deeper. Similarly to our findings, in the strait of Sicily the main nursery areas for P. blennoides have been observed between 200 and 400 m (Fiorentino et al., 2003b). Maximum density occurred in the 300‑500 m depth stratum and maximum biomass at 600‑800 m. In contrast, Massutí et al. (1996) registered maximum density at 200‑400 m in the Northern Mediterranean. In the context of oligotrophic Mediterranean conditions, density, biomass and mean fish weight have been found to be significantly greater in the Balearic Sea than compared to the western and eastern Ionian Sea (D'Onghia et al., 2004) and similarly in Algeria. This could be attributed to the trophic resources available.
Density decreased significantly from 2003 to 2004; possibly due to fishing, sampling uncertainty or both. The number of fishing trawlers was 494 in 2009 (Roland, 2014) and increased to 688 in 2017. The West sector has the highest number of trawlers (347) followed by the Centre (183) and the East (158) (MPRH, 2017). In this study, a positive gradient of P. blennoides density was found from the western to the eastern Algerian coast. The shape of coast and the lower number of trawlers in the East might explain this pattern. As P. blennoides is of Atlantic origin, the Western sector has a helping flux of Atlantic-current with environmental enrichment. The high number of fishing trawlers in this sector (W) might have contributed to the reduction in density, biomass and mean weight of the species noted in 2004.
In this study, recruitment to commercial fisheries was observed in summer, similar to the north-western Mediterranean (Lloret and Lleonart, 2002). In the survey, winter recruitment was recorded, as was done by Massutí et al. (1996) and Matarrese et al. (1998). Mean biomass and mean weight slightly decreased from 2003 to 2004. A decrease of the Algerian greater forkbeard was also observed during data collecting from commercial fisheries between 2013 and 2017. This is also the case of Portuguese landings in the Atlantic according to ICES (2017). Additionally, juveniles of this species represent an important part of discards in shallower depths (Lorance, 2012). Then, discarded specimens were observed many times in commercial landings of Bouharoun port in summer.
4.2 Reproduction
A difference in sex-ratio with size can be explained by females of many slope-dwelling fish becoming mature when they are reaching their maximum total length and then, somatic growth slows down (Gordon et al., 1995). The highly skewed sex-ratio (1F :4.02 M) in this study could be due to the origin of specimens (commercial), which might be selected by the gear, but also that females may not inhabit the depth fisheries are operating in, as reported for other deep-sea species (Morley et al., 2004). Sex segregation has been observed by Gallardo-Cabello (1986) for P. phycis and P. blennoides and by Viana et al. (2000) for Urophycis brasiliensis. In contrast to this study, several authors have report equal sex ratios for greater forkbeard in the Mediterranean Sea (Benghali et al., 2014a; Matarrese et al., 1998; Rotllant et al., 2002; Fernandez-Arcaya et al., 2013).
The reproductive biology of this species has been analysed in the Mediterranean. Its spawning period varies between areas. In the western Ionian Sea, the peak of reproduction occurs between November and January (Matarrese et al., 1998). Similarly, P. blennoides females are mature during autumn in the Balearic Sea (Rotllant et al., 2002) while they are mature in September on the western Algerian coast (Benghali, 2015). Spermatic emission happens between August and March in the western Ionian Sea (Matarrese et al., 1998) and from summer to early autumn in the western Mediterranean (Rotllant et al., 2002). Spawning in the Ionian Sea is observed from November to January (Matarrese et al., 1998). In the Balearic Sea, Rotllant et al. (2002) registered an active reproductive period from autumn to summer, where females spawn in autumn and males release their sperm from summer to early autumn. In the western Algerian coast, the reproductive period of both sexes was observed in September (Benghali, 2015). According to the gonadosomatic index of our study, a peak is found in spring for females, while maturity stages showed regressing females in both winter and autumn. Spermatic emission was registered from summer to winter in this study, similar to the Ionian Sea (Matarrese et al., 1998).
In this study, the somatic condition factor underwent important changes throughout the year for both sexes. Male condition was lowest in winter, while it was lowest in summer for females. This might indicate that P. blennoides stores energy in muscle tissue to meet the energy expenditure caused by reproduction, making it a “fatty type” fish. This is similar to most Gadidae species: e.g. Trisopterus luscus (Alonso-Fernandez et al., 2008).
The description of gonadal development stages is very important for understanding gonad dynamics and evaluation of species reproductive mechanisms (Amira et al., 2019). Values of sexually mature individuals from this work differ from findings reported in previous studies. P. blennoides mature earlier in the Balearic Sea (♂ L50= 19.31; ♀ L50= 24.7 cm) (Rotllant et al., 2002) and along the western Algerian coast (L50♀= 24.7 cm) (Benghali et al., 2014b). Also, 50% of males are mature at 19 cm in the Ionian Sea (Matarrese et al., 1998). Thus, L50 of greater forkbeard reported for females by these authors is almost 7 cm smaller than our findings. In contrast, the estimated L50 value for female Algerian greater forkbeard (30.39 cm) is closer to values recorded in the Atlantic, e.g. 32 cm (Clarke, 2005) and 33 cm (Cohen et al., 1990). Further, in the south-eastern Ligurian sea few mature individuals of P. blennoides have been found in autumn: females ranged between 40 and 63 cm and males between 20 and 26 cm (Rustighi et al., 2004).
No females with eggs have been observed throughout the study period. This finding allows us to consider P. blennoides as skipped spawners. Difficulties in the identification of fecundity, deficient diet and poor nutritional condition can lead to skipped spawning (Rideout and Tomkiewicz, 2011). This phenomenon may considerably affect stock-recruitment and stock-biomass relationships. This process has been found in P. phycis from the Portuguese coast (Vieira et al., 2016). The time and energy required for reproduction is better channelled into growth and survival, to increase future success rather than exacerbating already low energy reserves by spawning in the current year. Moreover, the reproductive potential including the frequency of spawning omission, will play an important role in effective management (Rideout et al., 2006).
4.3 Growth
P. blennoides is an economically important species as are the other Phycidae family members with relatively little information available for growth parameters in the southern Mediterranean (Romdhani et al., 2016). The largest individuals observed in this study were larger than those sampled in Tunisian waters (Lmax=47.7 cm) (Romdhani et al., 2016), western Algeria (Lmax=43.5 cm) (Benghali et al., 2014a) and along the south western Spanish coast (Lmax=47.8 cm) (Torres et al., 2012). However, our Lmax values are close to lengths obtained for the Northern Spanish Shelf (55cm and 67cm) (Ruiz-Pico et al., 2017), the Balearic Islands (Lmax=60 cm) (Rotllant et al., 2002), the eastern Ligurian Sea (Lmax=63 cm) (Rustighi et al., 2004) and the Ionian Sea (Lmax=70.3cm) (D'Onghia et al., 1998). In contrast, Lmax of our study is lower than the largest specimen caught north off the Iberian Peninsula (Lmax=81 cm) (Casas and Piñeiro, 2000). The variability of Lmax is linked to different biotic and abiotic environmental parameters.
Due to sexual dimorphism in size in P. blennoides as reported by Cohen et al., (1990); Rotllant et al., (2002), most researchers treated growth separated by sex. However, greater forkbeard from Tunisian waters does not show sexual dimorphism in growth (Romdhani et al., 2016), even though differences in growth between sexes are a common feature among Phycidae (Casas and Piñeiro, 2000). Therefore, we combined sexes in this study.
Longevity of fish exploited by fisheries is one of the most critical biological parameters (Beverton, 1992). P. blennoides on the Algerian coast was found to live up to seven years (bottom trawl survey in 2003) or nine years (bottom trawl survey in 2004 and commercial fisheries), depending on the data source, in contrast to six years in Tunisia (Romdhani et al., 2016). This is much less than the 14 years found in the north and northwest of the Iberian Peninsula (Casas and Piñeiro, 2000) and the 11 years for individuals of 59 cm in the Strait of Sicily (Fiorentino et al., 2003a).
Compared to previous works, whatever the method and samples used in our study, all asymptotic length (L∞) and t0 estimates were lower than values obtained for Iberian Peninsula; conversely for K. Asymptotic length for combined sexes estimated in Tunisia was 65.73 cm (Romdhani et al., 2016) which is close to our L∞ values for bottom trawl survey in 2003 and commercial fisheries.
Conversely to K, t0 in our study was different from values obtained for Tunisian coast (Romdhani et al., 2016) and the Strait of Sicily (Ragonese et al., 2004). Observed differences can be due to different size compositions of the populations (Romdhani et al., 2016) and method used for estimating growth parameters. These results also indicated that bias and precision were influenced by fish life history type, which may allow for standardization of field collection methods across a wide range of fish species. Any factor that acts to obscure modal structure makes length frequency analysis more difficult (Bjorndal and Bolten, 1995). Fish growth, i.e., the size increment with time, varies greatly with food quality and availability, temperature and other environmental factors and the fish will reach the different stages in development more dependent on size than on age (Amara and Lagardère, 1995; Aritaki and Seikai, 2004; Sæle and Pittman, 2010). Furthermore, factors include long spawning season, variation in individual growth rates that result in variation in length-at-age, cessation or near cessation of growth in older age classes, and high rates of exploitation (Bjorndal and Bolten, 1995). Geographic location and some environmental condition, such as the date and time of capture, index of condition, disease and parasites loads can also affect age estimates (Bagenal and Tesch, 1978).
The estimated age at 50% maturity corresponded to 3–4 years for individuals sampled by the bottom trawl survey in 2004 and 2–3 years for the bottom trawl survey in 2003 and commercial fisheries. This is in agreement with 3-4 years reported before for the Mediterranean Sea (Muus and Nielsen, 1999).
4.4 Exploitation
In this study, estimated total mortality values exceeded 1, similarly to values reported for the western Algerian coast (Benghali et al., 2014a) and Sicily (Ragonese et al., 2004) (Tab. 6). The estimates might have been influenced by the dominance of juveniles in our samples. Estimated natural mortality is comparable to Ragonese et al. (2004). The reliability of estimated M was confirmed using the M/K ratio reported to be within the range of 1.12–2.25 for most fishes (Beverton and Holt, 1959). Natural mortality depends closely on growth parameters, which differ according to the approach used. Moreover, the stock structure of P. blennoides is complex and requires further studies (ICES, 2017). However, the main issue in estimating fishing mortality F from Z is the actual impossibility to get reliable, consistent, precise, unbiased and verifiable M estimates when dealing with “mature and long-time steady-state overfished” stocks (Ragonese and Jereb, 2018). This is the case for the majority of Mediterranean demersal fish stocks (Farrugio et al., 1993; Lleonart and Maynou, 2003).
Demersal fisheries are characterized by high fishing pressure on few young age classes, which leaves only a reduced fraction of the adult population at sea (Fiorentino et al., 2003a). For P. blennoides, the amount of juveniles discarded by fisheries is larger than the landings of adult fishes (Lorance, 2012). Indeed, trawl mesh size affects stocks. A comparative analysis was made in the northern Tyrrhenian Sea to compare the catches and 0.3 kg were captured with 62.5 cm mesh size (Sbrana et al., 2007).
The presence of this species is very sporadic on the Algerian market, and the landed quantities are limited in space and time (Alioua et al., 2018). As immatures are present throughout the year in the catches, the annual sperm emissions with a peak of GSI in winter and summer, the short laying period (spring, summer) when the sexual activity of females is highest in spring with the absence of females able to lay eggs, suggest reproductive difficulties and therefore pressure on the population. As a result, egg fertilization is less frequent and can lead to poor recruitment and inefficient renewal of this stock. However, the development of a database with multi-year monitoring could permit estimating spawning stock biomass by modal prediction, taking into account the spawning period. Lastly, P. blennoides should be capable of renewal if caught individuals are larger than 30 cm.
Biogeographic comparison of mortalities and exploitation rates of P. blennoides. Natural mortality (M), total mortality (Z), fishing mortality (F), and exploitation rate (E).
5 Conclusion
Stock assessment of P. blennoides is necessary to define its status. The IUCN Red List considered it as Least Concern in 2015, but today, P. blennoides is no longer listed, known as “Not Evaluated” according to FishBase. Our study should be useful to design new scenarios for sustainable exploitation of Phycidae in the Mediterranean. We also suggest the use of mark and recapture techniques to determine age and analyse growth rates more accurately, to confirm that females grow faster than males.
Supplementary Material
Fig. S1. Length frequency of P. blennoides caught from 52 hauls in 2003 (A) and from 109 hauls in 2004 (B) (n: number of individuals).
Fig. S2. Linear model (LM) of log density of P. blennoides with depth (m) and longitude (°) caught by the bottom trawl surveys in 2003 (A1, A2) and 2004 (B1, B2) along the Algerian coast (*:significant).
Fig. S3. Residual plot of linear model (LM) of log density of P. blennoides with longitude (A1, B1) and depth (A2, B2) caught by the bottom trawl surveys in 2003 (A1, A2) and 2004 (B1, B2) along the Algerian coast.
Table S1. Sampling of P. blennoides from bottom trawl surveys.
Table S2. Sampling of P. blennoides from commercial fisheries (pooled sampling: 2013–2017).
Table S3. Density (ind/km2), biomass (kg/km2) and mean-weight (kg) of P. blennoides across depth (m) caught from bottom trawl surveys in 2003 and 2004.
Table S4. Density, biomass and mean-weight of P. blennoides by sectors caught from bottom trawl surveys in 2003 and 2004.
Table S5. Generalized additive model (GAM) of density (ind/km2) and biomass (kg/km2) of P. blennoides with longitude (°) caught from bottom trawl surveys in 2003 and 2004 along the Algerian coast.
Access hereAcknowledgments
The authors would like to thank the master and PhD students of the Faculty of Biological Science especially KHELIFA Kenza, MOKHTARI Sonia, MANSEUR Hakim, BOUFEKANE Bilal, BENSARI Billel, LAMALI Imene, MABCOUT Narimene Ouiza and MOULAI Amina; for helping in collecting commercial samples and the histological study. We express our gratitude to the Department of Ecology and Environment (USTHB) for the internship financial at the Spanish institute of Palma (Instituto Español de Oceanografía). Also, we would like to express our acknowledgements to Verena Trenkel (co-editor-in-Chief, Aquatic Living Resources) and two anonymous referees for their useful comments.
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Cite this article as: Alioua Z, Amira S, Khames GEY, Fernandez-Arcaya U, Guijarro B, Ordines F, Massutí E, Zerouali-Khodja F. 2020. Population structure, reproduction and exploitation of the greater forkbeard Phycis blennoides (Brünnich, 1768) from the Algerian basin. Aquat. Living Resour. 33: 20
All Tables
Total mean density (ind/km2), total mean biomass (kg/km2) and total mean weight (kg) of P. blennoides caught from bottom trawl surveys (BTS) along the Algerian coast.* Significant.
Macroscopic and microscopic descriptions of the phases in the reproductive cycle of P. blennoides.
Mean age-at-length of P. blennoides sampled by bottom trawl surveys (BTS) in 2003 and 2004 and from commercial fisheries (TL: total length in cm) off Algeria.
Growth parameters of P. blennoides estimated by FISAT II software. L∞: asymptotic length (cm) obtained by Powell Wetheral's method. K: growth rate (year−1) obtained applying the equation of Pauly and Munro (1984). t0: size when age is zero, Lmax: Maximum observed size in cm.
Exploitation indices for P. blennoides from the Algerian coast. Natural mortality from Djabali's equation (M1) and Pauly's equation (M2); Zc: total mortality from converted catch curve using FISAT II software; F1: fishing mortality using M1 and Zc; F2: fishing mortality using M2 and Zc; E1 and E2 exploitation rates using Zc.
Biogeographic comparison of mortalities and exploitation rates of P. blennoides. Natural mortality (M), total mortality (Z), fishing mortality (F), and exploitation rate (E).
All Figures
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Fig. 1 Study area of P. blennoides with sampled landing ports (W: sector west, C: sector center, E: sector east). |
In the text |
![]() |
Fig. 2 Density (ind/km2), biomass (kg/km2) of P. blennoides with depth stratum (m) caught by the bottom trawl surveys in 2003 (A) and 2004 (B) along the Algerian coast and mean weight (kg) (C). |
In the text |
![]() |
Fig. 3 Generalized additive model (GAM) of density (ind/km2) and biomass (kg/km2) of P. blennoides with longitude (°) caught by the bottom trawl surveys in 2003 (A, C) and 2004 (B, D) along the Algerian coast. |
In the text |
![]() |
Fig. 4 Mapping density, biomass and mean-weight of P. blennoides caught by BTS (W: west, C: center, E: east). |
In the text |
![]() |
Fig. 5 Length frequency of P. blennoides caught from bottom trawl surveys in 2003 (A) and 2004 (B) and commercial fisheries in the algerian coast (n: number of individuals). |
In the text |
![]() |
Fig. 6 Seasonal lenght frequency distribution of P. blennoides from landings of commercial fisheries (A: Summer, B: Autumn, C: Winter, D: Spring, n: number of individuals). |
In the text |
![]() |
Fig. 7 Length frequency distribution of P. blennoides by sexes from landing of commercial fisheries (F: female, M: male, nd: undetermined, X axis: Lower limit of size class). |
In the text |
![]() |
Fig. 8 Physiological indexes of P. blennoides from the Algerian coast (vertical bars are standard deviations). a) gonadosomatic index (GSI); b) hepatosomatic index (HSI) and somatic condition factor (K) for males; c) hepatosomatic index (HSI) and somatic condition factor (K) for females. |
In the text |
![]() |
Fig. 9 Seasonal maturity stages of P. blennoides from the Algerian coast. |
In the text |
![]() |
Fig. 10 Logistic regression model for the proportion of sexually mature males (M) and females (F) of P. blennoides (males L50= 24.30 cm, females L50 = 30.39 cm). |
In the text |
![]() |
Fig. 11 Abbreviation: Oog. Oogonia, PG. Primary growth oocyte, Nu. Nucleoli, F.e. Follicular envelope, Lo. Ovarian lumen, VtgI. Primary vitellogenic oocyte, N. Nucleus, Cyt.h. Heterogeneous cytoplasm, St. Ovarian stroma. Ow. Ovarian wall, Spg. Spermatogonia, L.l. Lobular lumen, Cyst. Cyst, Mb.l. The basal membrane of the lobule, Spcy. Spermatocyt, Spd. Spermatid, Spz. Spermatozoa. Histological sections through the gonads of P. blennoides showing different development phases (scale: 100 μm). a. General view of immature female (Gx10, caught 30/04/15, TL: 53.1 cm; WG: 3.86 g, GSI: 0.396). b. Developing female (Gx40, caught 21/12/15, TL: 27.3 cm; WG: 0.12 g, GSI: 0.601). c. Early maturing female with initial stage of vitellogensis and yolk protein (Gx40, caught 29/06/15, TL: 45.1 cm, WG: 3.9 g, GSI: 0.601). d. Histological section through the gonad of the biggest female sampled (Gx10, caught 23/04/2016, TL: 62.7 cm, WG :10.54 g, GSI: 0.61). Thick ovarian wall (Gx4) in regenerating ovaries. e. Immature male with spermatogonia cells (Gx40, caught 10/02/15, TL: 23.6 cm, WG: 0.02 g, GSI: 0.024). f. Male regenerating stage with the appearance of spermatids and spermatozoa (Gx40, caught 26/08/14, TL: 26.1cm, WG: 0.72 g, GSI: 0.373). g. Developing testes (Gx40, caught 6/01/15, TL: 21.1cm, WG: 0.5 g, GSI: 0.990). h. Mature testes with emission of spermatozoa (Gx10, caught 06/01/2015, TL: 24.1 cm, WG: 1.23 g, GSI: 2.13). |
In the text |
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