Introduction
The golden grey mullet Chelon auratus (Risso, 1810) belongs to the Mugilidae family and is of great importance due to its high commercial value, particularly for its gonads (D'Iglio et al., Reference D'Iglio, Natale, Albano, Savoca, Famulari, Gervasi, Lanteri, Panarello, Spanò and Capillo2022). It is the most abundant species along the northeast Atlantic Ocean and Mediterranean coasts (Bakhshalizadeh et al., Reference Bakhshalizadeh, Liyafoyi, Mora-Medina and Ayala-Soldado2023) and is found at depths of 10–20 m (Thomson, Reference Thomson, Quero, Hureau, Karrer, Post and Saldanha1990). Juveniles feed solely on zooplankton, whereas adults feed mainly on trivial benthic organisms and detritus (Bakhshalizadeh et al., Reference Bakhshalizadeh, Liyafoyi, Mora-Medina and Ayala-Soldado2023). Socially, it is a gregarious species and moves in shoals in coastal marine areas (Fehri-Bedoui et al., Reference Fehri-Bedoui, Gharbi and El Abed2002). Although its adult size is smaller than other mullets, it is very efficient in the early stages of growth. Its finer body and fillets are of better quality, making it a compulsive choice for aquaculture due to its ability to thrive in various ecosystems (Quirós-Pozo et al., Reference Quirós-Pozo, Robaina, Calderón and Filgueira2023). Besides, it is categorized as a euryhaline and eurythermal species because it tolerates an extensive range of salinities and temperatures, where C. auratus enters lagoons and estuaries and rarely migrates to freshwater (Whitfield, Reference Whitfield, Crosetti and Blaber2016). Attaining a length of 59 cm, C. auratus plays a crucial role in the food chain, with a trophic level of 2.8 (Kesiktaş et al., Reference Kesiktaş, Yemişken, Yildi and Eryilmaz2020).
Due to the high economic importance of C. auratus as food and bait, several studies have been carried out worldwide, including on its age and growth (Hotos and Katselis, Reference Hotos and Katselis2011), reproductive biology (Hotos et al., Reference Hotos, Avramidou and Ondrias2000; Fazli et al., Reference Fazli, Janbaz, Taleshian and Bagherzadeh2008; Daryanabard et al., Reference Daryanabard, Shabani, Kaymaram and Gorgin2009; Ghaninejad et al., Reference Ghaninejad, Abdolmalaki and Kuliyev2010; Bekova et al., Reference Bekova, Raikova-Petrova, Panayotova and Prodanov2020; Hasanen et al., Reference Hasanen, Ahmad, EL-Aiatt and Mohamed2021; El-Shenity et al., Reference El-Shenity, El-Dakar, Ahmed, Al-Beak and Ahmed2023), reproductive management (Quirós-Pozo et al., Reference Quirós-Pozo, Robaina, Calderón and Filgueira2023), population dynamics and stock assessment (Çiloğlu, Reference Çiloğlu2023), and morphology and morphometry of saccular otoliths (Fortunato et al., Reference Fortunato, Durà, González-Castro and Volpedo2017; Ferri et al., Reference Ferri, Bartulin and Škeljo2018; Çiçek et al., Reference Çiçek, Avşar, Yeldan and Manaşırlı2020; Kesiktaş et al., Reference Kesiktaş, Yemişken, Yildi and Eryilmaz2020; Reis et al., Reference Reis, Ateş and Jawad2023). However, few studies have been conducted on some aspects of this species in Tunisian and Mauritanian waters. In Tunisian waters, these studies have also focused on its age and growth (Fehri-Bedoui and Gharbi, Reference Fehri-Bedoui and Gharbi2005; Abdallah et al., Reference Abdallah, Ghorbel and Jarboui2012), reproductive biology (Abdallah et al., Reference Abdallah, Ghorbel and Jarboui2013), determination of the reproduction period and sexual maturity (Fehri-Bedoui et al., Reference Fehri-Bedoui, Gharbi and El Abed2002), and mortality pattern and yield per recruit (Fehri-Bedoui et al., Reference Fehri-Bedoui, Ben Meriem and Alemany2013). In addition, Trabelsi et al. (Reference Trabelsi, Aurelle, Bouriga, Quignard, Casanova and Faure2008) identified its juveniles using the cytochrome b gene, whereas Blel et al. (Reference Blel, Chatti, Besbes, Farjallah, Elouaer, Guerbej and Said2008) evaluated the phylogenetic relationships between five mugilid species, including C. auratus, based on the biochemical analysis. Similarly, Blel et al. (Reference Blel, Said and Durand2009) explored the phylogenetic relationships among these species in addition to Oedalechilus labeo, based on polymorphism in mitochondrial rRNA, COI, CytB, and 12S rRNA, as well as nuclear 5S DNA, rhodopsin gene sequence, and 589 bp of the mitochondrial gene sequence (16S rRNA) (Blel et al., Reference Blel, Said and Durand2013). Moreover, Jmil et al. (Reference Jmil, Ben Faleh, Rebaya, Allaya, Ben Mohamed, Trojette, Chalh, Quignard and Trabelsi2019a) analysed the otolith shape variation in samples collected from the El Biban and Boughrara lagoons and the Bizerte lagoon (Jmil et al., Reference Jmil, Rebaya, Mejri, Chalh, Quignard and Trabelsi2019b). Recently, Mejri et al. (Reference Mejri, Bakkari, Allagui, Rebaya, Jmil, Mili, Shahin, Quignard, Trabelsi and Ben Faleh2022b) assessed the interspecific and intersexual variability of saccular otolith shape between C. auratus and Chelon ramada inhabiting the Boughrara lagoon and Bouriga et al. (Reference Bouriga, Bahri, Bejaoui, Adjibayo Houeto, Shahin, Quignard, Trabelsi and Ben Faleh2023) discriminated among six commercially interesting and ecologically diverse fish species in the Gulf of Tunis by using fatty acid composition and otolith shape analysis.
In Mauritania, however, Ould Mohamed Vall (Reference Ould Mohamed Vall2004) studied the dynamics of the exploitation systems and reproductive eco-biology of C. auratus in addition to Mugil cephalus and Mugil capurrii and analysed their strategies for occupying Mauritanian littoral sectors and their management possibilities.
On the contrary, saccular otoliths or sagittae, the large pair of otoliths found in the inner ear of teleosts, are metabolically inert, i.e. once fully formed, the otolith chemical material is unlikely to be resorbed or altered (Campana, Reference Campana1999). Therefore, the otolith shape remains unaffected by short-term changes in fish conditions or environmental variations (Campana and Casselman, Reference Campana and Casselman1993). However, Tuset et al. (Reference Tuset, Otero-Ferrer, Gómez-Zurita, Venerus, Stransky, Imondi, Orlov, Ye, Santschi, Afanasiev, Zhuang, Farré, Love and Lombarte2016) reported that the size of otoliths increases with the increase of the habitat depths down to about 1000 m, and Volpedo et al. (Reference Volpedo, Tombari and Echeverría2008) indicated that the size decreases in fast swimming fish and is associated with feeding habitats (Lombarte et al., Reference Lombarte, Palmer, Matallanas, Gómez-Zurita and Morales-Nin2010; Tuset et al., Reference Tuset, Otero-Ferrer, Gómez-Zurita, Venerus, Stransky, Imondi, Orlov, Ye, Santschi, Afanasiev, Zhuang, Farré, Love and Lombarte2016). Therefore, saccular otolith morphology has long been employed for the identification of species, i.e. it is species-specific and exhibits high inter- and intra-species local geographic variation in shape and size (Ferri et al., Reference Ferri, Bartulin and Škeljo2018; Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a; Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021; Mejri et al., Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a, Reference Mejri, Bakkari, Allagui, Rebaya, Jmil, Mili, Shahin, Quignard, Trabelsi and Ben Faleh2022b; Ben Mohamed et al., Reference Ben Mohamed, Mejri, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2023; Bouriga et al., Reference Bouriga, Bahri, Bejaoui, Adjibayo Houeto, Shahin, Quignard, Trabelsi and Ben Faleh2023; D'Iglio et al., Reference D'Iglio, Famulari, Albano, Carnevale, Di Fresco, Costanzo, Lanteri, Spanò, Savoca and Capillo2023; Reis et al., Reference Reis, Ateş and Jawad2023; Adjibayo Houeto et al., Reference Adjibayo Houeto, Mejri, Bakkari, Bouriga, Chalh, Shahin, Quiganrd, Trabelsi and Ben Faleh2024). In addition, they have been widely used efficiently to identify local species and populations and to discriminate their stocks in different habitats (Jawad et al., Reference Jawad, Hoedemakers, Ibáñez, Ahmed, Abu El-Regal and Mehanna2018; Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b; Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021; Mejri et al., Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a, Reference Mejri, Bakkari, Allagui, Rebaya, Jmil, Mili, Shahin, Quignard, Trabelsi and Ben Faleh2022b; Ben Mohamed et al., Reference Ben Mohamed, Mejri, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2023; Reis et al., Reference Reis, Ateş and Jawad2023). Moreover, the otolith morphology has been used for fisheries management or to estimate population growth and mortality (Cardinale et al., Reference Cardinale, Doerin-Arjes, Kastowsky and Mosegaard2004; Tracey et al., Reference Tracey, Lyle and Duhamelb2006; Burke et al., Reference Burke, Brophy and King2008; Stransky et al., Reference Stransky, Murta, Schlickeisen and Zimmermann2008; Cañás et al., Reference Cañás, Stransky, Schlickeisen, Sampedro and Fariña2012; Morat et al., Reference Morat, Letourneur, Nérini, Banaru and Batjakas2012; Bakkari et al., Reference Bakkari, Mejri, Ben Mohamed, Chalh, Quignard and Trabelsi2020). This is because the otolith morphology and morphometry have been reported to be influenced by many factors, such as sex, growth, maturity, fishery exploitation pattern, and genetic and environmental factors (Begg and Brown, Reference Begg and Brown2000; Volpedo and Echeverría, Reference Volpedo and Echeverría2003; Vignon and Morat, Reference Vignon and Morat2010). Ecologically, otolith shape and morphometry have long been used also as crucial indicators of the ecological characteristics of fish because they provide a wide range of ecology information, including feeding habitat, mobility, substrate association, and water column positioning of fish (Volpedo and Echeverría, Reference Volpedo and Echeverría2003; Assis et al., Reference Assis, da Silva, Souto-Vieira, Lozano, Volpedo and Fabré2020). In addition, earlier studies have shown that the variability in otolith shape is influenced by many factors, such as substrate type (Volpedo and Cirelli, Reference Volpedo and Cirelli2006), feeding habit (Nonogaki et al., Reference Nonogaki, Nelson and Patterson2007; Bouriga et al., Reference Bouriga, Bahri, Bejaoui, Adjibayo Houeto, Shahin, Quignard, Trabelsi and Ben Faleh2023), ontogenetic shifts (Pérez and Fabré, Reference Pérez and Fabré2013), and environmental conditions, including water temperature, depth, and pollution (Lombarte and Lleonart, Reference Lombarte and Lleonart1993; Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b; Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021; Mejri et al., Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a, Reference Mejri, Bakkari, Allagui, Rebaya, Jmil, Mili, Shahin, Quignard, Trabelsi and Ben Faleh2022b; Ben Mohamed et al., Reference Ben Mohamed, Mejri, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2023; Bouriga et al., Reference Bouriga, Bahri, Bejaoui, Adjibayo Houeto, Shahin, Quignard, Trabelsi and Ben Faleh2023; Adjibayo Houeto et al., Reference Adjibayo Houeto, Mejri, Bakkari, Bouriga, Chalh, Shahin, Quiganrd, Trabelsi and Ben Faleh2024).
Among the techniques, elliptical Fourier analysis (EFA) is the most efficient one used for otolith shape analysis, which has been proven to be the most widely used and effective method to describe, characterize, and capture specific information of otoliths outlined in a quantifiable manner (Lord et al., Reference Lord, Morat, Lecomte-Finiger and Leith2012; Mahé et al., Reference Mahé, Ider, Massaro, Hamed, Alba, Patricia, Aiketerini, Angelique, Chryssi, Romain, Zohir, Mahmoud, Rachid, Hélène and Bruno2019).
So far, otolith morphology is poorly studied in fish species of Mauritanian waters, and the variability in the otolith shape is greatly affected by diverse sorts of pressure, such as genetic or ecological influences (Grønkjaer and Sand, Reference Grønkjaer and Sand2003). Therefore, this study was undertaken to compare the saccular otolith shape for the first time between males and females of C. auratus inhabiting two ecologically different geospatial niches in the Ghar El Melh station (Tunisia) and the Etoile Bay station (Mauritania) to evaluate whether the shape and morphometry of saccular otoliths (sagittae) differ between these two niches having different environmental conditions.
Materials and methods
Study area
The Ghar El Melh station is located in the Ghar El Melh lagoon (32°28′33°45″N, 10°45′10°57″E), which ranks first among the Tunisian lagoons because it has an area of 50,000 ha (Guetat et al., Reference Guetat, Sellem, Akrout, Brahim, Atoui, Ben Romdhane and Daly Yahia2012). It is located south of Djerba Island on the southern edge of the Gulf of Gabes and communicates with the seawater of the Gulf of Gabes through the El Kantara in the north-eastern part and the Ajim channels in the north-western part (Figure 1A). The water surface temperature ranges from 11.2°C in winter and 24.7°C in summer (Feki et al., Reference Feki, Hamza, Frossard, Abdennadher, Hannachi, Jacquot, Bel Hassen and Aleya2013) and the salinity mostly varies between 38 and 43‰ in winter (Sellem et al., Reference Sellem, Guetat, Enaceur, Ghorbel-Ouannes, Othman, Harki, Lakuireb and Rafrafi2019), while it oscillates between 42.19 and 53.3‰ in summer (Khedhri et al., Reference Khedhri, Djabou and Afli2015). In addition, the pH of the water fluctuates between 7.92 in winter and 8.31 in summer (Ben Aoun et al., Reference Ben Aoun, Farhat, Chouba and Hadjali2007). Moreover, the lagoon is polluted with organic discharges through harbour-related activities in its southern part (Guetat et al., Reference Guetat, Sellem, Akrout, Brahim, Atoui, Ben Romdhane and Daly Yahia2012), as well as with sewage resulting from the transportation of the surrounding ports and the entry of seawater loaded with phosphorous from the Gulf of Gabes (Sellem et al., Reference Sellem, Guetat, Enaceur, Ghorbel-Ouannes, Othman, Harki, Lakuireb and Rafrafi2019).
Figure 1. C. auratus Risso, 1810: (A) the Ghar El Melh (Tunisia) and (B) Etoile Bay (Mauritania) stations (●) from which the males and females were collected.
The Etoile Bay station is situated in the Etoile Bay (21°2′12″N, 17°1′1″W) that lies north of Nouadhibou and is identified as an aesthetic site where a variety of space and ecosystem uses coexist (Amadou, Reference Amadou2009). It is an enclave of Bay Lévrier on the Cap Blanc Peninsula and covers a marine area of 1200 ha, and its width ranges between 100 and 150 m in the loop-shaped downstream area and between 150 and 550 m in the slightly straight middle and upstream part (Figure 1B). The seabed consists of shoals with a submerged sandbank, with a maximum depth of 4.5 m in the central-western part, gradually decreasing around the periphery, and the depth does not exceed 1 m at the pass. The bay experiences constant water renewal because the tidal currents dominate the circulation of water masses and due to the small volume of water (Brêthes and Mayif, Reference Brêthes and Mayif2013). In addition, the Etoile Bay receives several sources of chronic pollution that could be responsible for its eutrophication, including the Nouadhibou slaughterhouse, the Tarhil districts, the flour factories in Bountiya, the wreckage dump accumulated by the Société hollandaise in Bountiya, the salting, drying, and smoking of fish on the Nouadhibou inlet, as well as domestic discharges from Cabanons (Berque et al., Reference Berque, Ould Taleb, Ould Hamadi, M'bengue, Ould Abed and Diop2012). The water surface temperature and salinity are 26.5°C and 37.9‰, respectively, in the warm season (August–October) and 19.4°C and 35.8‰, respectively, in the cold season (January–May), whereas the pH is over 8 in both seasons (Legraa, Reference Legraa2019).
Sampling
A total of 120 adult individuals of C. auratus (60 individuals from each station; 30 males and 30 females) were collected between June and October 2023 from the Ghar El Melh station located in northeast Tunisia (37°10′10″N, 10°11′16″E) (Figure 1A) and the Etoile Bay station situated in Mauritania (21°00′15″N, 17°00′45″W) (Figure 1B). All individuals were caught alive by coastal artisanal fishermen using gillnets. Immediately after catching, the sexual maturity status of each individual was examined macroscopically, using the scale of Kesteven (Reference Kesteven1960) and Treasurer (Reference Treasurer1990), or microscopically in the case of small gonads, to ensure that all individuals chosen for this study were fully mature. Afterwards, all individuals were weighed for the total weight (TW; g) using a digital balance, and the standard length (SL; mm) was measured using an ichthyometer, and the values from both parameters were rounded to the nearest 0.01 (online Table S).
Otolith extraction and imaging
Sagittal otoliths were extracted using a sharp-bladed knife, soaked in distilled water, dried, and stored in an Eppendorf tube. The left and right otoliths were placed on their convex side, more precisely with the grooves positioned upwards and the rostrum below, with an inclination to avoid errors during the normalization process, and digital images were captured using a binocular loupe with a Canon IXUS 185 digital camera, with a resolution of 20 megapixels (Figure 2A, B). After that, all images were sent to an image analyzer equipped with an incorporated millimetre scale.
Figure 2. C. auratus Risso, 1810: images of the left (L) and right (R) sagittal otoliths showing the length (Lo) and width (Wo) parameters examined among individuals collected from the (A) Ghar El Melh (Tunisia) and (B) Etoile Bay (Mauritania) stations. Scale bar: 2 mm.
Otolith shape analysis
The obtained images of the otoliths were processed using Adobe Photoshop CS6 software, which transforms the original picture of the otolith into a binary image. Subsequently, the binary images of the otoliths' shapes were analysed using software SHAPE Ver. 1.3 (Iwata and Ukai, Reference Iwata and Ukai2002). The outlines of the contour shape of each otolith were evaluated by EFA as previously described by Ben Labidi et al. (Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b) and Khedher et al. (Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021) following the procedures suggested by Kuhl and Giardina (Reference Kuhl and Giardina1982).
Statistical data analysis and variable normalization
First, an analysis of variance (ANOVA) was performed to evaluate the significance of differences in the mean values of the SL and the TW among individuals of the two stations or populations in Tunisia and Mauritania and values were tested for the homogeneity (equality) and the normal distribution using Levene's and Shapiro–Wilks' λ tests, respectively. Second, the differences in the contour shape of otoliths from individuals of the two populations were analysed by discriminant function analysis (DFA). The effect of locations on the elliptical Fourier descriptors (EFDs) was first verified by multivariate analysis of variance (MANOVA); subsequently, all shape variable values were checked for normality; if the values did not follow the normal distribution, a transformation of Box–Cox (Box and Cox, Reference Box and Cox1964) was performed. Finally, Levene's and Shapiro–Wilks' λ tests were used to evaluate the homogeneity (equality) and the normal distribution of the variance in the values of the variables for the shape of otoliths, respectively. DFA was performed with the normalized elliptical Fourier descriptor coefficients (77 coefficients per otolith) to illustrate the similarities and differences among individuals in the same population or both populations. DFA was used to investigate the integrity of pre-defined groups of individuals belonging to the given geographic population or locality and the percentage of their correct classification by finding linear combinations of descriptors that maximize the value of Wilks' λ. The performance of DFA was verified using Wilks' λ test, which is the ratio between the intra-population variance and the total variance and provides an objective method for calculating the corrected percentage chance for agreement. Moreover, Fisher's (Reference Fisher1936) distance was also calculated to characterize the similarity (symmetry) and variability (asymmetry) between the left (L) and right (R) otoliths and between the left–left (L–L) and right–right (R–R) otoliths from the same side within and among males and females of the two populations. The results were interpreted using Wilk's λ test data, and the barycentre projections of the left and right otoliths for both males and females for both populations were displayed on graphs. In addition, MANOVA was used to test the significance of the left and right otoliths' shape values within and between populations. All analyses were performed by using XLSTAT 2010.
Otolith morphometric analysis
Analysis of morphometric parameters of the otoliths, including length (Lo), width (Wo), perimeter (Po), and area (Ao), was performed by ImageJ software (Figure 2A, B). Before statistical analyses, a one-way ANOVA was used to determine whether there were any significant differences between the mean values of Lo, Wo, Po, and Ao for the left and right sides of otoliths within and among males and females of the two populations. In addition, a two-way ANOVA was used to check whether there was a correlation between the otolith's morphometric parameters and the geographic origin of the individuals. Moreover, the Student's t-test was used to analyse the differences in the four parameters between the left and right and L–L and R–R otoliths of males and females between the two populations.
Fluctuating asymmetry (FA) measurement and analysis
Statistically, the FA is characterized by a normal distribution of the Li–Ri, with a mean equal to 0, and the variance of |li − ri| represents a measure of development instability. As depicted by Palmer and Strobeck (Reference Palmer and Strobeck1986), FAs are exceedingly subtle in the order of 1% of the character size or less and thus require great care to be detected. The FA between the right and left sides of the otoliths was calculated among males and females of the two populations for each morphometric parameter per individual ‘i’ by applying the following formula given by Palmer and Strobeck (Reference Palmer and Strobeck1986) and was estimated as the FAi index:
where r and l are the values of the traits on the right and left sides, respectively.
Results
Total weight (TW) and total length (SL) variation
As shown in online Table S, the TW and SL ranged from 106.98 to 234.65 g and 130 to 273 mm in males and from 150.20 to 281.78 g and 173 to 278 mm in females for the Ghar El Melh population (Tunisia). However, the TW and SL varied from 160.10 to 450.90 g and 219 to 298 mm in males and from 208.04 to 425.86 g and 231 to 289 mm in females for the Etoile Bay population (Mauritania).
Otolith shape variation
Generally, Shapiro–Wilks' λ test confirmed that all shape variance values were almost distributed normally among individuals in each population with a P value > 0.05. At the intrapopulation level, the Wilks' λ test of the otolith shape values showed that there was a bilateral significant difference (P < 0.0001), i.e. there was asymmetry, between the left and right otoliths, as well as between the L–L and R–R otoliths, among males and females of the Ghar El Melh population (Tunisia) (Table 1). However, on the contrary, a significant bilateral similarity (P > 0.05), i.e. there was symmetry, was observed between the left and right otoliths and between the L–L and R–R otoliths among males and females of the Etoile Bay population (Mauritania). Similarly, Fisher's (Reference Fisher1936) distance matrix of the shape variance also revealed a significant bilateral asymmetry (P < 0.0001) between the left and right otoliths within and among males and females of the Ghar El Melh population (Tunisia). However, a significant bilateral symmetry (P > 0.05) was found between the left and right otoliths and between the L–L and R–R otoliths among males and females of the Etoile Bay population (Mauritania) (Table 2).
Table 1. Wilk's λ test of the left and right otoliths' shape variance distance approximation values between males and females of C. auratus samples collected from the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) stations, as well as between males and females from the two populations
The value marked in bold is statistically not significant (P > 0.05).
Table 2. Combined pairwise Fisher's (Reference Fisher1936) distance (D) mean values (above diagonal) and their corresponding P values (below diagonal) of the left (L) and right (R) otoliths within and between males (M) and females (F) of C. auratus samples collected from the Ghar El Melh (GM) (Tunisia) and Etoile Bay (EB) (Mauritania) stations
GMLM, Ghar El Melh left otolith of male; GMRM, Ghar El Melh right otolith of male; GMLF, Ghar El Melh left otolith of female; GMRF, Ghar El Melh right otolith of female; EBLM, Etoile Bay left otolith of male; EBRM, Etoile Bay right otolith of male; EBLF, Etoile Bay left otolith of female; EBRF, Etoile Bay right otolith of female.
At the interpopulation level, a combined analysis of the left and right otolith shape values between males and females from the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) populations using the Wilks' λ test revealed a significant bilateral asymmetry (P < 0.0001) in the left and right otoliths (Table 1). Also, Fisher's (Reference Fisher1936) distance matrix demonstrated a significant asymmetry (P < 0.0001) in the left and right otoliths, as well as in the L–L and R–R otoliths, among males and females of the two populations (Table 2).
In addition, the barycentre projection based on elliptical Fourier descriptors (EFDs) of the contour shape of the left and right otoliths between and within individuals of the Ghar El Melh population (Tunisia) on the first axes F1 and F2 of the DFA revealed that the two axes explained 78.69 and 12.13% of the total variation, respectively (Figure 3A). Therefore, the left and right otolith shapes of males and females were separated in the positive and negative parts of the two axes. The two axes accounted for 90.82% of the total shape variance, supporting a significant effect on the variability, and showed the segregation of the left otoliths, as well as the right otoliths, from both males and females either in the positive or negative parts of F1 or F2. However, in the Etoile Bay population (Mauritania), the first axes F1 and F2 of the DFA revealed that the two axes explained 54.82 and 31.67% of the total variation, respectively (Figure 3B). The two axes accounted for 86.48% of the total shape variance, and showed as well the segregation of the left otoliths, as well as the right otoliths, from both males and females either in the positive or negative parts of F1 or F2.
Figure 3. C. auratus Risso, 1810: DFA showing the barycentre projection of the left (L) and right (R) shape values of the sagittal otoliths of males (M) and females (F) collected from the (A) Ghar El Melh (Tunisia) (
) and (B) Etoile Bay (Mauritania) (
) stations, as well as the two populations combined (
). GMLM, Ghar El Melh left otolith of male; GMRM, Ghar El Melh right otolith of male; GMLF, Ghar El Melh left otolith of female; GMRF, Ghar El Melh right otolith of female; EBLM, Etoile Bay left otolith of male; EBRM, Etoile Bay right otolith of male; EBLF, Etoile Bay left otolith of female; EBRF, Etoile Bay right otolith of female.
Moreover, the combined barycentre projection of the contour shape of the left and right otoliths between males and females of the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) populations on the first axes F1 and F2 of the DFA revealed that the two axes explained 68.78 and 13.09% of the total variation, respectively (Figure 3C). The two axes accounted for 81.86% of the total shape variance, supporting also a significant effect on the variability, and showed the separation of the left and right otoliths of both males and females from the Etoile Bay population (Mauritania) on the positive part and those from the Ghar El Melh population (Tunisia) on the negative part of F1. However, the F2 axis showed segregation of the left otoliths of males and females from the Ghar El Melh population (Tunisia) with the left and right otoliths of females, alongside the right otoliths of half of the males, from the Etoile Bay population (Mauritania) on the positive part. But the right otoliths of males and females from the Ghar El Melh population (Tunisia) were segregated, alongside the right otoliths of half of the males, with the left otoliths of males from the Etoile Bay population (Mauritania) on the negative part of F2 axis.
Otolith morphometric variation
At the intrapopulation level, results of the one-way ANOVA and Student's t-test of the Lo, Wo, Po, and Ao showed significant differences, i.e. asymmetry, in Wo and Po between the left and right otoliths among males, females, and both sexes combined in the Ghar El Melh (Tunisia) population (Tables 3 and 4). In addition, the Student's t-test revealed a significant asymmetry in Lo between the left and right otoliths only among females (Table 4). Nevertheless, the paired samples Student's t-test indicated a significant asymmetry between the left and right otoliths in Lo only among females and Wo and Po among males, females, and both sexes combined (Table 5). In the Etoile Bay (Mauritania) population, one-way ANOVA detected significant differences (P < 0.05), i.e. asymmetry, in Wo between the left and right otoliths among females and both sexes combined (Table 3) and the Student's t-test also revealed a significant asymmetry in Lo between the left and right otoliths among males, females, and both sexes combined (Table 4). Besides, the paired samples Student's t-test designated a significant asymmetry between the left and right otoliths only in Wo among males, females, and both sexes combined (Table 6).
Table 3. One-way ANOVA of biometric parameters of the left and right otoliths between males and females of C. auratus collected from the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) stations
SD, standard deviation.
The values marked in bold are statistically significant (P < 0.05).
Table 4. Student's t-test of biometric parameters of the left and right otoliths between males and females of C. auratus collected from the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) stations
SD, standard deviation.
The values marked in bold are statistically significant (P < 0.05).
Table 5. Paired samples Student's t-test analysis of biometric parameters of the left (L) and right (R) otoliths within and among males and females of C. auratus collected from the Gar El Melh station (Tunisia)
SD, standard deviation; N, number of samples.
The values marked in bold are statistically significant (P < 0.05).
Table 6. Paired samples Student's t-test analysis of biometric parameters of the left (L) and right (R) otoliths within and among males and females of C. auratus collected from the Etoile Bay station (Mauritania)
SD, standard deviation; N, number of samples.
The value marked in bold is statistically significant (P < 0.05).
At the interpopulation level, the combined analysis of the morphometric measurements of the left and right otoliths between males and females from the Ghar El Melh (Tunisia) and the Etoile Bay (Mauritania) populations using the one-way ANOVA indicated that there were significant differences, i.e. there was asymmetry in the Lo only among females, in Wo among males, females, and both sexes combined, and in Po and Ao among males and females between the left and right sides of otoliths (Table 3). However, the Student's t-test showed a significant asymmetry between the left and right sides of otoliths in Lo only among females, in Wo among females and both sexes combined, and in Po only among both sexes combined (Table 4). Besides, the combined analysis between males and females from the two populations, using the paired samples’ Student's t-test, demonstrated a significant asymmetry in the left and right sides of otoliths in Lo only among females, in Wo among females and both sexes combined, and in Po only among both sexes combined (Table 7).
Table 7. Combined paired samples Student's t-test analysis of biometric parameters of the left (L) and right (R) otoliths between males and females of C. auratus collected from the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) stations
SD, standard deviation; N, number of samples.
The values marked in bold are statistically significant (P < 0.05).
FA variation
Estimates of the mean FA values of Lo, Wo, Ao, and Po between the right and left otoliths within and among males and females are given in Table 8. At the intrapopulation level, a significant FA (P < 0.05) was observed only in Lo between the right and left otoliths among males, as well as between males and females, i.e. there was a sexual dimorphism, and in Ao among females of the Ghar El Melh (Tunisia). Similarly, significant FA differences (P < 0.05) were observed between the right and left otoliths in Lo among males, as well as between males and females, and in Po between males and females of the Etoile Bay (Mauritania), i.e. there was a sexual dimorphism. However, at the interpopulation level, only significant FA differences were found in Lo and Wo between the right and left otoliths among males and females. In addition, a box plot chart showing the distribution of the mean values and signs of skewness among males and females of the two populations is given in Figure 4.
Table 8. Estimates of the mean values of FA between the left (L) and right (R) sagittal otoliths' length (Lo), width (Wo), perimeter (Po), and area (Ao) of C. ramada males and females collected from the Ghar El Melh (GM) and Etoile Bay (EB) stations
P values marked in bold are significant (P < 0.05).
Figure 4. Box plots showing the distribution and signs of skewness of the mean values of FA of the right (R) and left (L) length (Lo), width (Wo), perimeter (Po), and area (Ao) of the otoliths between the Ghar El Melh (GM) (Tunisia) and Etoile Bay (EB) (Mauritania) populations. The central line is the median, the boxes indicate the first and third quartiles, and the whiskers indicate two standard deviations. Outliers are those outside the median ± 0.3–0.6 SD.
Discussion
Both EFA and Fisher's (Reference Fisher1936) distance analysis of the otolith contour shape revealed a bilateral significant difference (P < 0.0001), i.e. asymmetry, in the left and right otoliths and between the L–L and R–R otoliths only among males and females of the Ghar El Melh population (Tunisia). This asymmetry in the otolith shape is consistent with that found in a range of species inhabiting the Tunisian waters, including Scorpaena porcus (Trojette et al., Reference Trojette, Fatnassi, Ben Alaya, Mahouachi, Chalh, Quignard and Trabelsi2014), Diplodus annularis (Trojette et al., Reference Trojette, Ben-Falah, Fatnassi, Marsaoui, Mahouachi, Chalh, Quignard and Trabelsi2015), Liza ramada (Rebaya et al., Reference Rebaya, Ben-Faleh, Allaya, Khedher, Marsaoui, Chalh, Quignard and Trabelsi2016), Oblada melanura (Barhoumi et al., Reference Barhoumi, Khoufi, Kalai, Ouerhani, Essayed, Zaier, Jaziri, Ben Meriem and Fehri-Bedoui2018), Pagellus erythrinus (Mejri et al., Reference Mejri, Trojette, Jmil, Ben Faleh, Chalh, Quignard and Trabelsi2020, Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a), Boops boops (Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b), and Diplodus vulgaris (Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021). Similarly, this asymmetry in the shape of otoliths has also been observed in other species occurring elsewhere outside the Tunisian waters (for details of these species, see Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b; Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021; Mejri et al., Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a; Ben Mohamed et al., Reference Ben Mohamed, Mejri, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2023).
As regards the causes of asymmetry in the otolith shape, it has been reported that the feeding habits, including food availability (quantity and quality), shifts in diet during ontogenetic development (Cardinale et al., Reference Cardinale, Doerin-Arjes, Kastowsky and Mosegaard2004; Mahé et al., Reference Mahé, Ider, Massaro, Hamed, Alba, Patricia, Aiketerini, Angelique, Chryssi, Romain, Zohir, Mahmoud, Rachid, Hélène and Bruno2019) and the depth at which the fish lives (Fashandi et al., Reference Fashandi, Valinassab, Kaymaram and Fatemi2019), physiology (e.g. hearing abilities associated with acoustic communication) (Schulz-Mirbach et al., Reference Schulz-Mirbach, Ladich, Plath and Heß2019), phylogeny (Torres et al., Reference Torres, Lombarte and Morales-Nin2000), sex, growth, and maturity (Cardinale et al., Reference Cardinale, Doerin-Arjes, Kastowsky and Mosegaard2004), and spatial isolation between demographic populations (Turan et al., Reference Turan, Oral, Öztürk and Düzgüneş2006) are among the factors driving differences in otolith shape. Also, Simoneau et al. (Reference Simoneau, Casselman and Fortin2000) and Vaux et al. (Reference Vaux, Rasmuson, Kautzi, Rankin, Blume, Lawrence, Bohn and O'Malley2019) declared that the differences in age and sex among species may lead to a notable difference in the shape of the otolith. Adding to these factors, the asymmetry in the otolith shape has also been attributed to other factors, such as ontogenetic (Capoccioni et al., Reference Capoccioni, Costa, Aguzzi, Menesatti, Lombarte and Ciccotti2011), genetic (Jawad et al., Reference Jawad, Gnohossou and Tossou2020), and environmental factors, including water temperature, salinity and depth, substrate, light regime and pollution (Panfili et al., Reference Panfili, Durand, Diop, Gourène and Simier2005; Al-Mamry et al., Reference Al-Mamry, Jawad and Ambuali2011; Jawad et al., Reference Jawad, Sadighzadeh and Al-Mamary2012a, Reference Jawad, Al-Mamry and Al-Mamary2012b, Reference Jawad, Gnohossou and Tossou2020; El-Regal et al., Reference El-Regal, Jawad, Mehanna and Ahmad2016; Ferri et al., Reference Ferri, Bartulin and Škeljo2018; Kontaş et al., Reference Kontaş, Bostanci, Yedіer, Kurucu and Polat2018; Yedier et al., Reference Yedier, Bostancı, Kontaş, Kurucu and Polat2018; Mahé et al., Reference Mahé, Ider, Massaro, Hamed, Alba, Patricia, Aiketerini, Angelique, Chryssi, Romain, Zohir, Mahmoud, Rachid, Hélène and Bruno2019; Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b; Geladakis et al., Reference Geladakis, Somarakis and Koumoundouros2021; Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021; Mejri et al., Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a, Reference Mejri, Bakkari, Allagui, Rebaya, Jmil, Mili, Shahin, Quignard, Trabelsi and Ben Faleh2022b; Ben Mohamed et al., Reference Ben Mohamed, Mejri, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2023; Bouriga et al., Reference Bouriga, Bahri, Bejaoui, Adjibayo Houeto, Shahin, Quignard, Trabelsi and Ben Faleh2023; Adjibayo Houeto et al., Reference Adjibayo Houeto, Mejri, Bakkari, Bouriga, Chalh, Shahin, Quiganrd, Trabelsi and Ben Faleh2024). Besides, Jawad and Al-Sadighzadeh (Reference Jawad and Al-Sadighzadeh2013) ascribed the asymmetry between the left and right otoliths to exposure of individuals to environmental stress conditions resulting from changes in some environmental factors, including pollution, severe physical conditions, and habitat quality (Al-Rasady et al., Reference Al-Rasady, Jawad, Al-Mamry, Al-Mamari, Al-Yarubi and Al-Mamary2010). In addition, Popper et al. (Reference Popper, Ramcharitar and Campana2005) stated that the complex shape of otoliths may provide richer information for hearing or balance, whereas Deng et al. (Reference Deng, Wagner and Popper2013) suggested that the complex shape of otoliths may alter the dynamics of otolith responses to sounds. Moreover, Gauldie and Crampton (Reference Gauldie and Crampton2002) noted that saccular otoliths with more complex shapes are found in hearing-dependent species more often than non-hearing-dependent species.
As far as we know, C. auratus is a pelagic neritic species living at a depth of 10–20 m (Thomson, Reference Thomson, Quero, Hureau, Karrer, Post and Saldanha1990), and adults feed mainly on trivial benthic organisms and detritus (Bakhshalizadeh et al., Reference Bakhshalizadeh, Liyafoyi, Mora-Medina and Ayala-Soldado2023). Regarding age and sex, the samples studied are adult and sexually mature, with SL ranging from 130 to 273 mm in males and 173 to 278 mm in females in the Ghar El Melh population (Tunisia) to avoid the confounding effect of allometric growth (Cardinale et al., Reference Cardinale, Doerin-Arjes, Kastowsky and Mosegaard2004) and sexual maturity (Campana and Casselman, Reference Campana and Casselman1993) on the otolith shape. Therefore, we can assume that the bilateral asymmetry observed in the left and right and the L–L and R–R otolith shape between males and females can be attributed to the differences in their response to sounds and differences in degrees of hearing and balance, an assumption that needs further investigation. However, Wiff et al. (Reference Wiff, Flores, Segura, Barrientos and Ojeda2020) attributed this bilateral asymmetry to reproductive isolation between individuals that may lead to inter- or even intraindividual variations (Panfili et al., Reference Panfili, Durand, Diop, Gourène and Simier2005) or the possibility of within-individual stress that lead to developmental abnormalities of individuals or poor living conditions for larvae (Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a, Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b; Mejri et al., Reference Mejri, Trojette, Jmil, Ben Faleh, Chalh, Quignard and Trabelsi2020, Reference Mejri, Bakkari, Tazarki, Mili, Chalh, Shahin, Quignard, Trabelsi and Ben Faleh2022a, Reference Mejri, Bakkari, Allagui, Rebaya, Jmil, Mili, Shahin, Quignard, Trabelsi and Ben Faleh2022b; Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021).
Regarding the environmental characteristics of the Ghar El Melh station (Tunisia), the water temperature ranges from 11.2°C in winter to 24.7°C in summer (Feki et al., Reference Feki, Hamza, Frossard, Abdennadher, Hannachi, Jacquot, Bel Hassen and Aleya2013), the salinity mostly varies between 38 and 43‰ in winter (Sellem et al., Reference Sellem, Guetat, Enaceur, Ghorbel-Ouannes, Othman, Harki, Lakuireb and Rafrafi2019) and 42.19 and 53.3‰ in summer (Khedhri et al., Reference Khedhri, Djabou and Afli2015), and the pH fluctuates between 7.92 in winter and 8.31 in summer (Ben Aoun et al., Reference Ben Aoun, Farhat, Chouba and Hadjali2007). In addition, the station is polluted with organic discharges through harbour-related activities in its southern part (Guetat et al., Reference Guetat, Sellem, Akrout, Brahim, Atoui, Ben Romdhane and Daly Yahia2012), sewage resulting from the transportation of the surrounding ports, and the entry of seawater loaded with phosphorous from the Gulf of Gabes (Sellem et al., Reference Sellem, Guetat, Enaceur, Ghorbel-Ouannes, Othman, Harki, Lakuireb and Rafrafi2019). In this context, it is worth mentioning that the samples were collected during the period between June and October, and it has previously been confirmed that fish are more sensitive to a temperature change of about 0.03°C (Rebaya et al., Reference Rebaya, Ben Faleh, Allaya, Kheder, Trojette, Marsaoui, Fatnassi, Chalh, Quignard and Trabelsi2017). Therefore, we can attribute the significant asymmetry in the left and right sides, as well as the L–L and R–R sides, of otolith shape within and among males and females in the Ghar El Melh population (Tunisia) to differences in their susceptibility to differences in these environmental parameters.
On the contrary, both EFA and Fisher's (Reference Fisher1936) distance analysis of the otolith contour shape indicated a significant bilateral similarity (P > 0.05), i.e. there was symmetry, between the left and right, as well as between the left and L–L and R–R sides, of otoliths shape among males and females of the Etoile Bay population (Mauritania). A similar finding of the bilateral symmetry between the right and left otoliths has been recorded in B. boops from the Kelibia station in Tunisian waters (Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020a). As previously reported, mullet species, including C. auratus, are highly euryhaline and eurythermal and tolerate broad salinities (González-Castro and Minos, Reference González-Castro, Minos, Crosetti and Blaber2015). Therefore, this apparent bilateral symmetry recognized here can be explained in terms of the increased developmental stability of individuals in response to environmental stress, resulting from the high water temperature (26.5°C), salinity (35.8‰), pH (8) (Legraa, Reference Legraa2019), and chronic pollution (Berque et al., Reference Berque, Ould Taleb, Ould Hamadi, M'bengue, Ould Abed and Diop2012), experienced by the individuals during the warm season (August–October).
In addition, Wilk's λ test of the shape variance between left and right otoliths revealed a significant asymmetry (P < 0.0001) between males and females of the two populations. Moreover, the DFA based on EFDs of the otoliths' contour shape noticeably separated between the left and right otoliths among males and females at both the intra- and interpopulation levels. Therefore, we can conclude that the spatial and environmental differences induced apparent effects on the otolith shape between males and females of C. auratus populations collected from the Ghar El Melh (Tunisia) and Etoile Bay (Mauritania) stations.
On the contrary, intrapopulation analysis of the Lo, Wo, Po, and Ao between the left and right otoliths using one-way ANOVA and Student's t-test showed an apparent asymmetry in Wo and Po between the left and right otoliths among males, females, and both sexes combined in the Ghar El Melh (Tunisia) population. In addition, the Student's t-test revealed a significant asymmetry in Lo between the left and right otoliths only among females. Besides, the Student's t-test of paired samples indicated a significant asymmetry between the left and right otoliths in Lo only among females and in Wo and Po among males, females, and both sexes combined. However, in the Etoile Bay (Mauritania) population, the one-way ANOVA detected a significant asymmetry in Wo between the left and right otoliths among females and both sexes combined, and Student's t-test revealed an asymmetry in Lo between the left and right otoliths among males, females, and both sexes combined. In addition, the paired samples Student's t-test demonstrated a significant asymmetry between the left and right otoliths only in Wo among males, females, and both sexes combined.
Nevertheless, at the interpopulation level, the combined analysis of the morphometric dimensions of the otoliths between males and females from the two populations produced a significant asymmetry in the left and right otoliths in Lo only among females, in Wo among males, females, and both sexes combined, and in Po and Ao among males and females. In addition, the Student's t-test showed a significant asymmetry between the left and right sides of otoliths in Lo only among females, in Wo among females and both sexes combined, and in Po only among both sexes combined. Moreover, the combined paired samples Student's t-test analysis scored a significant asymmetry in the left and right otoliths between males and females from the two populations in Lo only among females, in Wo among females and both sexes combined, and in Po only among both sexes combined. Similar results of asymmetry in Wo have also been found in P. erythrinus (Mejri et al., Reference Mejri, Trojette, Jmil, Ben Faleh, Chalh, Quignard and Trabelsi2020), B. boops (Ben Labidi et al., Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b), and D. vulgaris (Khedher et al., Reference Khedher, Mejri, Shahin, Quiganrd, Trabelsi and Ben Faleh2021) in Tunisian waters, as well as elsewhere in Lo and Wo in Rastrelliger kanagurta (Al-Mamry et al., Reference Al-Mamry, Jawad and Ambuali2011), Sardinella sindensis and Sillago sihama (Jawad et al., Reference Jawad, Sadighzadeh and Al-Mamary2012a), Lutjanus bengalensis (Jawad et al., Reference Jawad, Al-Mamry and Al-Mamary2012b), Chlorurus sordidus and Hipposcarus harid (El-Regal et al., Reference El-Regal, Jawad, Mehanna and Ahmad2016), Merlangius merlangus (Kontaş et al., Reference Kontaş, Bostanci, Yedіer, Kurucu and Polat2018), Trachurus mediterraneus (Yedier et al., Reference Yedier, Bostancı, Kontaş, Kurucu and Polat2018), and Sarotherodon melanotheron and Coptodon guineensis (Jawad et al., Reference Jawad, Gnohossou and Tossou2020). As is reported, this significant asymmetry in the morphometric dimensions of the otoliths can be interpreted as FA, which Jawad and Al-Sadighzadeh (Reference Jawad and Al-Sadighzadeh2013) attributed to the assumption that vulnerable individuals under stressful environmental conditions may develop asymmetry on either side of the otoliths. This assumption has also been confirmed by Ben Labidi et al. (Reference Ben Labidi, Mejri, Shahin, Quignard, Trabelsi and Ben Faleh2020b) and Mejri et al. (Reference Mejri, Trojette, Jmil, Ben Faleh, Chalh, Quignard and Trabelsi2020), who reported a direct correlation between environmental stress resulting from pollution and asymmetry in the otolith morphology in the species they examined. In addition, the bilateral asymmetry recorded in the otolith morphometric dimensions within and among males and females from the two populations can be explained in terms of abnormal swimming activity and interference with correct sound localization, which results in the incapability of the individuals to integrate with the environment where they live (Helling et al., Reference Helling, Hausmann, Clarke and Scherer2003; Lychakov and Rebane, Reference Lychakov and Rebane2005).
In conclusion, according to our knowledge attained from earlier studies on the intra- and interspecific variations in the otolith shape, most of these studies have been carried out on species inhabiting local or inland waters. Therefore, the present study was conducted for the first time on C. auratus populations collected from inland and outland waters representing two ecologically different niches, the Gar El Melh (Tunisia) and Etoile Bay (Mauritania) stations, as an attempt to assess whether or not the variations in the environmental conditions between the two niches induce differences in the otolith shape and morphometry. At the intrapopulation level, analysis of the otoliths' contour shape revealed a significant asymmetry between the left and right sides, as well as the L–L and R–R sides, among males and females of the Ghar El Melh (Tunisia) population, and a significant symmetry among males and females of the Etoile Bay (Mauritania) population. At the interpopulation level, a significant asymmetry was also detected between the left and right otoliths' shape among males and females of the two populations. In addition, DFA based on EFDs of the otoliths' contour shape conspicuously separated between the left and right otoliths among males and females at both the intra- and interpopulation levels and also separated between those of the two populations. Moreover, analysis of the otolith morphometric dimensions showed a differential significant asymmetry in the Lo, Wo, Po, and Ao between the left and right otoliths among males and females at the intra- and interpopulation levels. These significant asymmetries observed at the intra- and interpopulation levels between the left and right otoliths in both contour shape and morphometry were interpreted as FA caused by environmental stress conditions resulting from variations in the water temperature, salinity, pH, and pollution between the two ecological niches. However, the significant symmetry detected between the left and right otoliths, particularly among males and females of the Etoile Bay (Mauritania), was attributed to the increased developmental stability of individuals in response to environmental stress experienced by the individuals during the warm season (August–October). Therefore, the geospatial variations in the environmental conditions between the two ecological niches effectually induced differences in the otolith morphology. The results of this investigation largely contribute to the knowledge of the otolith shape and morphometric data that have long been confirmed as perfect tools for discriminating between species and identifying new species.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315424000547.
Data
Data supporting the findings of this study are available from the corresponding author upon request.
Acknowledgements
The authors thank all the people and fishermen who helped collect the C. auratus individuals from the Gar El Melh (Tunisia) and Etoile Bay (Mauritania) stations.
Author contributions
All authors contributed to the conceptualization, discussion, and writing of this article. In addition, all authors read and approved the final version of the manuscript.
Financial support
The authors declare that they did not receive any specific grant from funding agents for this work.
Competing interests
None.
Ethical standards
The Laboratory of Ecology, Biology, and Physiology of Aquatic Organisms, and Laboratory of Biodiversity, Biotechnology, and Climate Change, Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia have approved this research. In addition, all procedures in this study were performed following the guidelines for the Proper Conduct of Animal Experiments outlined by the University of Tunis El Manar, Tunis, Tunisia (No. 1474 certificated on 14 August 1995), as well as all applicable international, national, and/or institutional guidelines for the care and use of animals in research.
