Age, Growth, and Otolith Morphometrics of Trachinus draco (L., 1758) and Trachinus radiatus (Cuvier, 1829) in the Eastern Mediterranean

Abstract

Trachinus draco and Trachinus radiatus are two bycatch species of low commercial value and no sufficient knowledge on their biological features. In the present study, the weight–length relationship, age, growth, and ten otolith morphometric variables of these species were investigated in the southwestern Aegean Sea for the first time. Positive allometric and isometric growth in the weight were defined in T. draco and T. radiatus. The weight–length relationship was described by the parameters α = 0.002415 and b = 3.35745 in T. draco and α = 0.007582 and b = 3.09452 in T. radiatus. The von Bertalanffy growth function parameters were L_∞ = 44.51 cm, k = 0.15 year⁻¹, and t₀ = −1.31 years for T. draco and L_∞ = 58.47 cm, k = 0.16 year⁻¹, and t₀ = −0.78 years for T. radiatus. Ten otolith variables (radius, length, width, area, perimeter, roundness, circularity, form factor, rectangularity, and ellipticity) showed a significant relationship with size for both species, except the ellipticity in T. radiatus. The mean values of all the otolith variables were higher in T. radiatus than in T. draco. The otolith of T. radiatus was found to become more rectangular with size as compared to the otolith of T. radiatus. The results of this work can support further research on the behavioral and ecological features of the two species.

1. Introduction

Age and growth are essential for biology, population dynamics, stock assessment, and fisheries management. Moreover, by examining the structural, functional, and phenotypic variability of otoliths, researchers can acquire major knowledge on stock identification, species interactions, and interactions with their environment [1]. Their biological variables may be affected by a variety of environmental parameters, which may lead to differences in the biological parameters of a species among different regions, even over small geographical ranges [2]. This kind of information is also necessary for less commercial species [3], which contribute to the world’s biodiversity and the stability of ecosystems, and for which scientific knowledge is generally scarce. Therefore, improving our knowledge of their life history traits is very important.

The greater weever, Trachinus draco (Linnaeus, 1758), and the starry weever, Trachinus radiatus (Cuvier, 1829), are demersal species that belong to the family Trachinidae. They occur in the Eastern Atlantic, Mediterranean, and Black Sea. These species inhabit mainly sandy and muddy bottoms ranging from a few meters to 150 m in depth [4]. Both species are oviparous with pelagic eggs and larval stages [5]. The spawning period of T. draco is from June to August [6], while in T. radiatus, this period begins in May and extends till October [7]. Both species are carnivorous and feed on small fish, invertebrates, and crustaceans [8]. Moreover, they are well known for their venomous dorsal spines [9]. In the Mediterranean Sea, weevers are considered as fish of low commercial value, and are mainly caught as bycatch by bottom trawl and gill nets [10,11]. Although these two species are widely distributed and their ecological role is important [8], published information on their biological characteristics is limited, especially for T. radiatus.

Some of the studies have been focused on the weight–length relationship (WLR), age, growth, or otolith morphometrics of T. draco in the Mediterranean Sea [12,13,14,15,16,17,18,19,20,21,22,23,24]. Regarding T. radiatus, there are a few studies that have been conducted on the WLR for the species in the Mediterranean [14,24,25,26], while only one has been performed on its age and growth [9].

The objectives of the present work include the study of the age, growth, and otolith morphometrics of T. draco and T. radiatus in the southwestern Aegean Sea for first time. The aim is to improve the scientific knowledge on the life history traits of these two species and provide information that is necessary in population dynamics.

2. Material and Methods

2.1. Study Area and Data Collection

Samples of T. draco (89 individuals) and T. radiatus (76 individuals) were collected during experimental bottom trawl surveys conducted at depths ranging between 69 and 127 m in 37 sampling stations of the SW Aegean Sea (Figure 1) during May and June 2015.

The total length (TL) and total weight (TW) of each specimen were recorded to the nearest mm and g, respectively. Gonads were examined under a microscope to determine their sexual identity. The sagittal otoliths were extracted, cleaned in water to remove the organic matter, and then preserved dry. Each left otolith was placed proximal side down on a glass Petri dish filled with water and then imaged using Image-Pro Plus software (Version 4.5.0.29) under transmitted light against a black backdrop at 6.3× magnification.

Counting the annual growth rings, defined as alternating opaque and translucent zones along the left sagittal otolith axis from the core to the post-rostrum edge, served as the basis for age reading by three independent readers. A second reading was conducted when readings differed to reach an agreement or to exclude an otolith in the case of disagreement. Otoliths that were broken or damaged were not used in the age determination or the examination of the morphometric parameters. The final number of otoliths that were used for age determination and otolith morphometrics were 86 and 68 for T. draco and T. radiatus, respectively. Regardless of the species’ spawning season, the date of birth was established on 1 January, in accordance with standards used by the great majority of fish age determination laboratories worldwide [27,28].

Based on the observations of the left sagittal otolith, the following otolith morphometric variables were recorded from the otoliths of both studied species: otolith area (OA, mm²); otolith length (OL, mm); otolith width (OW, mm); radius (RA, mm); perimeter (PE, mm) (Figure 2); roundness (RD) (the ratio between the actual area and the area of a circle of the same diameter; factor is larger if and when the shape of the otolith is more circular) [29] taking a minimum value of 1 [30]; circularity (CI) (provides information on the complexity of the otolith contour) [31] taking a minimum value of 4π [30]. Additionally, the following shape factors were calculated: form factor (FF) = ([4 × OA/PE²]) (a dimensionless value that indicates the similarity of the otolith contour to a circle, taking values from 0 to 1, with a value of 1 corresponding to a perfect circle); rectangularity (RC) = (OA/[OL × OW]) (which gives information about the approximation to a rectangular or square shape, indicating a perfect rectangle or square if it has a value of 1); and ellipticity (EL) = (OL − OW/OL + OW) (reflects the similarity to an ellipse, with values close to 0 indicating a tendency towards circularity) [31].

2.2. Data Analysis

2.2.1. Growth

Length (TL) frequency distribution per species was calculated based on classes of 1 cm intervals. The weight–length relationship (WLR) was estimated according to the equation TW = αTL^b, where TW is the total weight in g, TL is the total length in cm, α is the intercept, and b is the slope of the log-linear regression. The WLR relationship was studied for both sexes and combined since no differences were detected between them [32]. Student’s t-test was used to examine the isometric growth null hypothesis (H₀: b = 3) for each species.

An age–length key was constructed by species based on the otolith age readings. The von Bertalanffy growth parameters [33] were determined through the equation: L_t = L_∞ (1 − e^{−k(t−t₀)}) where L_t is the predicted length at age t in cm, L_∞ is the mean theoretical asymptotic length in cm, k is the rate at which L_∞ is approached in year⁻¹, and t₀ is the theoretical age at zero length in years. The growth performance index Φ′ (Φ′ = logk + 2logL_∞) [34] was also used to compare the growth parameters of the two species with those available in the published literature.

2.2.2. Otolith Morphometrics

The mean (±standard error), minimum, and maximum values of the studied otolith morphometric variables were calculated by species. ANOVA was performed to investigate the between-species differences in otolith morphometric variables (significance level a = 0.05).

For each species, the relationship between each otolith morphometric variable and TL was examined based on the exponential regression y = Ax^B (where y is the otolith morphometric variable in mm, x is the total length in mm, A is the intercept, and B is the regression slope). For the regressions presenting statistically significant relationship (p-value < 0.05), comparison of slope b between the two species was performed using ANCOVA analysis (significance level a = 0.05).

3. Results

3.1. Growth

3.1.1. Length Distribution

In total, 165 individuals were examined for this study, including 89 samples of T. draco and 76 of T. radiatus. The size of T. draco varied from 13.3 to 30.7 cm TL, while that of T. radiatus varied from 16.0 to 43.2 cm TL (Figure 3). T. radiatus presented greater sizes than T. draco as a result of the different known somatic types of the two species.

3.1.2. Weight–Length Relationship

The total weight (TW) values varied from 16.0 to 244 g in T. draco and from 45.0 to 1042.0 g in T. radiatus. WLR for each species was as follows: TW = 0.00242 × TL^3.357 (R² = 98%) for T. draco; TW = 0.00758 × TL^3.095 (R² = 98%) for T. radiatus. The WLR showed that b was statistically significantly higher than three in T. draco (t-test = 6.62, p-value < 0.01), while no statistically significant difference was found in T. radiatus (t-test = 1.73, p-value = 0.09).

3.1.3. Age and Growth

Based on the otolith readings, 6 (from 1 to 6) and 7 (from 1 to 7) age groups were identified from 86 T. draco and 68 T. radiatus, respectively. The first visible ring around the nucleus of the otoliths of both species was considered a false ring (Figure 4 and Figure 5).

Table 1. Age–length key of Trachinus draco and Trachinus radiatus from SW Aegean Sea [TL: total length (cm); N: total number of individuals].

Trachinus draco							Trachinus radiatus
Length Classes (TL, cm)	Age Classes
	1	2	3	4	5	6	1	2	3	4	5	6	7
13.0–13.9	2
14.0–14.9	2	1
15.0–15.9		3
16.0–16.9		5					1
17.0–17.9		4
18.0–18.9		10
19.0–19.9		8	2					1
20.0–20.9			7
21.0–21.9			7					2
22.0–22.9			9
23.0–23.9				1					1
24.0–24.9				6					2
25.0–25.9				5					2
26.0–26.9				5	1				4
27.0–27.9					2				4
28.0–28.9					2
29.0–29.9						3				5
30.0–30.9						1				4
31.0–31.9										6
32.0–32.9										1	2
33.0–33.9										1	3
34.0–34.9											2
35.0–35.9										3	7
36.0–36.9										1	1	1
37.0–37.9											2	5
38.0–38.9											1	1
39.0–39.9												1
40.0–40.9												2
41.0–41.9												1
42.0–42.9
43.0–43.9													1
N	4	31	25	17	5	4	1	3	13	21	18	11	1

displays the relevant age–length keys for T. draco and T. radiatus. The majority of T. draco belonged to age group two; T. radiatus to age group four. The von Bertalanffy parameters and the growth performance index Φ′ for each species are shown in

Table 2. The von Bertalanffy growth parameters of Trachinus draco and Trachinus radiatus in the SW Aegean Sea (N: total number of individuals; L_∞: the mean theoretical asymptotic length in cm; k: a growth rate parameter in year⁻¹; t₀: the theoretical age at zero length in years; S.E: standard error; Φ′: the growth performance index).

Species	N	L∞ ± S.E (cm)	k ± S.E (Year−1)	t0 ± S.E (Year)	Φ′
Trachinus draco	86	44.51 ± 5.48	0.15 ± 0.04	−1.31 ± 0.37	2.47
Trachinus radiatus	68	58.47 ± 10.22	0.16 ± 0.06	−0.78 ± 0.63	2.74

and the von Bertalanffy growth curves per species are presented in Figure 6.

3.2. Otolith Morphometrics

The mean (±standard error) as well as the maximum and minimum values of the RA (radius), OL (otolith length), OW (otolith width), OA (otolith area), PE (perimeter), RD (roundness), CI (circularity), FF (form factor), RC (rectangularity), and EL (ellipticity) of the left otolith for each species are given in

Table 3. Mean (±standard error), minimum, and maximum (in parenthesis) values of the otolith morphometric variables: RA (radius, mm), OL (otolith length, mm), OW (otolith width, mm), OA (otolith area, mm²), PE (perimeter, mm), RD (roundness), CI (circularity), FF (form factor), RC (rectangularity), and EL (ellipticity) of Trachinus draco and Trachinus radiatus from the SW Aegean Sea. The p-values for the comparison of the otolith morphometric variables between the two species (ANOVA) are also shown.

Morphometric Variable	Trachinus draco	Trachinus radiatus	ANOVA (p-Value)
RA (mm)	3.60 ± 0.06 (2.75–4.97)	5.61 ± 0.09 (3.75–6.84)	<0.05 *
OL (mm)	7.87 ± 0.14 (5.78–10.83)	11.73 ± 0.19 (7.53–14.81)	<0.05 *
OW (mm)	3.62 ± 0.05 (2.61–4.52)	4.89 ± 0.08 (3.14–6.24)	<0.05 *
OA (mm2)	20.85 ± 8.42 (11.28–39.48)	44.70 ± 1.36 (16.95–67.42)	<0.05 *
PE (mm)	18.62 ± 0.33 (13.54–26.15)	28.06 ± 0.48 (17.16–34.95)	<0.05 *
RD	1.29 ± 0.00 (1.21–1.43)	1.42 ± 0.01 (1.30–1.56)	<0.05 *
CI	16.23 ± 0.06 (15.18–17.92)	17.90 ± 0.10 (16.34–19.84)	<0.05 *
FF	0.25 ± 0.00 (0.22–0.26)	0.22 ± 0.00 (0.20–0.24)	<0.05 *
RC	0.75 ± 0.03 (0.69–0.83)	0.77 ± 0.00 (0.71–0.83)	<0.05 *
EL	0.37 ± 0.00 (0.31–0.44)	0.41 ± 0.00 (0.33–0.47)	<0.05 *

* Significance level a = 0.05.

. Statistically significant differences were defined in all the otolith morphometric variables between the two species (ANOVA, p-value < 0.05) (Table 3).

In both species, TL presented a statistically significant correlation (p-value < 0.05) with all otolith characteristics that were studied, except for the EL in T. radiatus (

Table 4. Parameters of the exponential regression of the total length (TL) of Trachinus draco and Trachinus radiatus with the otolith morphometric variables: RA, radius (mm); OL, otolith length (mm); OW, otolith width (mm); OA, otolith area (mm²); PE, perimeter (mm); RD, roundness; CI, circularity; FF, form factor; RC, rectangularity; and EL, ellipticity of T. draco and T. radiatus. A, intercept; B, slope; R², coefficient of determination; r, correlation coefficient. The p-value of the regressions and the p-values of the comparison of slope b of the regression lines between the two species (ANCOVA) are also shown.

Variables	Species	A	B	R2	r	Regression p-Value	ANCOVA p-Value for b
TL/RA	T. draco	0.11	0.66	0.82	0.90	<0.01 *	0.88
	T. radiatus	0.14	0.65	0.82	0.91	<0.01 *
TL/OL	T. draco	0.14	0.76	0.92	0.96	<0.01 *	0.14
	T. radiatus	0.21	0.70	0.89	0.94	<0.01 *
TL/OW	T. draco	0.13	0.63	0.84	0.92	<0.01 *	0.59
	T. radiatus	0.11	0.66	0.80	0.89	<0.01 *
TL/OA	T. draco	0.01	1.49	0.93	0.97	<0.01 *	0.22
	T. radiatus	0.01	1.40	0.92	0.96	<0.01 *
TL/PE	T. draco	0.29	0.78	0.94	0.97	<0.01 *	0.37
	T. radiatus	0.38	0.75	0.92	0.96	<0.01 *
TL/RD	T. draco	0.90	0.07	0.18	0.42	<0.01 *	0.48
	T. radiatus	0.85	0.09	0.18	0.43	<0.01 *
TL/CI	T. draco	11.26	0.07	0.18	0.42	<0.01 *	0.37
	T. radiatus	10.34	0.10	0.19	0.43	<0.01 *
TL/FF	T. draco	0.36	− 0.07	0.18	−0.42	<0.01 *	0.37
	T. radiatus	0.39	−0.10	0.19	−0.43	<0.01 *
TL/RC	T. draco	0.43	0.10	0.35	0.59	<0.01 *	0.04 *
	T. radiatus	0.59	0.05	0.08	0.28	0.03 *
TL/EL	T. draco	0.17	0.15	0.19	0.44	<0.01 *	-
	T. radiatus	0.34	0.03	0.01	0.10	0.44

* Significance level a = 0.05.

, Figures S1 and S2). No significant differences (ANCOVA, p-value > 0.05) were found for slope b between the two species in terms of the otolith variables (RA, OL, OW, OA, PE, RD, CI and FF) except for RC (ANCOVA, p-value < 0.05) (Table 4).

4. Discussion

T. draco and T. radiatus are two widely distributed species, but little is known about their biology and ecology, especially for T. radiatus. Although little historical data on the WLR for both species from the study area [14] are available, no data exist on their age, growth, and otolith morphometrics. The results of this study produced updated information on the WLR of both species. New knowledge on the age and growth of T. draco and T. radiatus is provided for the southwestern Aegean Sea for the first time. The novelty of this work includes mainly the detailed study on the otolith morphometrics of the two species in the whole Mediterranean Sea.

The WLR analysis showed that the growth of T. draco was allometrically positive (b > 3), while that of T. radiatus was isometric (b = 3), which shows that the former species grows more in weight that the latter. In T. draco, the value of slope b of the WLR of the present study was quite similar with that of studies carried out in the Aegean Sea [14,15,16,17,35,36,37,38], but it was higher than that of other areas of the Mediterranean Sea (

Table 5. Weight–length relationship of Trachinus draco from different study areas (TL Range: minimum–maximum total length in cm; α: intercept; b: slope of the weight–length relationship).

Reference	Area	TL Range (cm)	α	b
[12]	Eastern Adriatic	9.2–26.8	0.00002	2.934
[13]	Balearic Islands	14.0–34.0	0.00740	2.930
[14]	Kyklades, Aegean Sea	14.5–32.0	0.00441	3.120
[44]	Alexandria, Egypt	10.0–23.0	0.01400	2.800
[25]	Balearic Islands and eastern coast of the Iberian Peninsula	6.2–26.5	0.01000	2.835
[45]	Gökceada Island, northern Aegean Sea (coastal waters of Turkey)	4.4–35.2	0.02430	2.578
[35]	Saros bay, northern Aegean Sea (Turkey waters)	15.0–37.0	0.00366	3.202
[15]	Izmir bay, Central Aegean Sea, (Turkey waters)	17.2–34.0	0.00400	3.178
[46]	North-Eastern Mediterranean Coast of Turkey	9.0–20.0	0.00520	3.090
[16]	Izmir Bay, Central Aegean Sea, (Turkey waters)	15.3–36.6	0.00520	3.100
[17]	North Aegean Sea	15.0–30.5	0.00540	3.062
[36]	Izmir Bay, Aegean Sea (Turkey waters)	15.3–36.6	0.00500	3.137
[47]	Eastern Black Sea	5.0–35.0	0.00400	3.433
[18]	Gulf of Castellammare (north-western Sicily)	16.0–29.5	0.00540	3.059
[19]	French Catalan coast	15.0–38.5	0.04300	3.070
[11]	Eastern Black Sea	5.0–25.8	0.00690	3.005
[20]	Mallorca, Spain	9.0–29.0	0.00500	3.075
[37]	Gökçeada Island, northern Aegean Sea, (Turkey waters)	2.4–29.3	0.00900	2.847
[22]	Iskenderun Bay, North-eastern Levantine Sea	13.5–32.0	0.00770	2.950
[38]	Gallipoli peninsula, northern Aegean Sea, (Turkey waters)	13.0–36.4	0.00800	2.972
[23]	Gulf of Tunis	10.0–32.0	0.00600	3.040
[24]	Eastern Adriatic Sea	10.4–32.2	0.00820	2.906
[48]	Western Black Sea	5.6–21.5	0.01740	2.657
[49]	Western Egyptian Mediterranean Sea	11.8–27.6	0.00680	2.963
[50]	Sea of Marmara	6.7–24.6	0.00760	2.971
This study	SW Aegean Sea, Eastern Mediterranean Sea	13.3–30.7	0.00242	3.357

). Variability in the b values of WLR was also found in T. radiatus among the study areas (

Table 6. Weight–length relationship of Trachinus radiatus from different study areas (TL Range: minimum–maximum total length in cm; α: intercept; b: slope of the weight–length relationship).

Reference	Area	TL Range (cm)	α	b
[14]	Kyklades, Aegean Sea	15.4–40.4	0.01271	2.897
[25]	Balearic Islands and eastern coast of the Iberian Peninsula	16.5–47.0	0.00520	3.206
[26]	Zakynthos Island, Ionian Sea	16.0–25.4	0.01600	2.923
[9]	Gulf of Tunis	11.0–50.7	0.00900	3.035
[24]	Eastern Adriatic Sea	13.8–33.5	0.00850	3.029
This study	SW Aegean Sea	16.0–43.2	0.00758	3.095

). Genetics, habitat, variations in the length composition, number of samples examined, preservation techniques, wellness, stomach conditions, dietary habits, sex, maturity stages, sampling period, rates of growth, and age are some of the factors that are typically attributed to the differences in the parameters of the WLR [39,40,41,42,43].

Six (1–6) and seven (1–7) age groups were identified in the current study for T. draco and T. radiatus, respectively. More age groups have been reported in the published literature. This can be related to the larger size range of samples examined in other studies (

Table 7. Growth parameters of Trachinus draco and Trahinus radiatus from different study areas (TL Range: minimum–maximum total length in cm; N: number of age groups; L_∞: mean theoretical asymptotic length in cm; k: growth rate in year⁻¹; t₀: theoretical age at zero length in years; Φ′: growth performance index).

Species	Reference	Area	TL Range (cm)	Age Groups N (Range)	L∞ (cm)	k (Year−1)	t0 (Year)	Φ′
Trachinus draco	[11]	Eastern Black Sea	5.0–25.8	6 (1–6)	28.62	0.28	−0.89	2.36
	[20]	Mallorca, Spain	9.0–29.0	10 (0–9)	42.3	0.10	−1.83	2.25
	[22]	Iskenderun Bay, North-eastern Levantine Sea	13.5–32.0	10 (2–11)	46.45	0.08	−3.29	2.24
	[49]	Western Egyptian Mediterranean Sea	11.8–27.6	5(1–5)	27.3	0.5	13.29	2.27
	This study	SW Aegean Sea, Eastern Mediterranean Sea	13.3–30.7	6 (1–6)	44.51	0.15	−1.31	2.47
Trachinus radiatus	[9]	Gulf of Tunis	11.0–50.7	15 (1–15)	41.54	0.26	-	2.65
	This study	SW Aegean Sea, Eastern Mediterranean Sea	16.0–43.2	7 (1–7)	58.47	0.16	−0.78	2.74

) or to differences in the growth pattern of the species between geographical areas because of different environmental conditions. The study of the microstructure of the otoliths and the daily ring readings could clarify these inconsistencies in the age identification of the studied species.

The growth parameters and Φ′ values for both species (Table 7) showed a variability among the different study areas, which can be attributed to variations in the studied samples’ size range, life history characteristics, methods of analysis, and the different environmental factors of each study area.

Differences between the values of the otolith morphometric variables (ANOVA, p-value < 0.05) of the two species showed that the otoliths of T. radiatus are larger than those of T. draco as expected.

A statistically significant correlation was found between TL and all the otolith morphometric variables studied in T. draco and T. radiatus except one (EL) in the latter species. Our findings agree with those presented by Başusta and Buz (2015), who also reported an important relationship between total length and otolith length and width in T. draco. No published information exists for the other otolith variables of T. draco. Otolith morphometry of T. radiatus has not been studied to date.

No significant differences (ANCOVA, p-value > 0.05) were detected for slope b of the regression lines of the otolith variables with TL, except for RC between the two studied species. However, in the case of RC, the statistically significant higher value found in T. draco showed that the otolith of this species becomes more rectangular as the size increases than the otolith of T. radiatus. This may indicate physiological and/or ecological differences between the two species. Otolith morphology is affected by the growth pattern, food availability, and environmental conditions (salinity, temperature, and depth) [51,52], and is used to identify fish species at the taxonomic, phylogenetic, geographic, and dietary levels [51,52,53,54,55]. It is also a source of information on several biological and ecological aspects of teleosts showing the interactions between fish species and their habitat [1].

In future, more research based on the microstructure of the otoliths could clarify the inconsistencies in the age groups identified for the two studied species among different geographical areas and relate them to the local environmental conditions.

5. Conclusions

This study has updated our knowledge of T. draco and T. radiatus age, growth, and otolith morphometrics. The weight–length relationship, age, growth and ten otolith morphometric variables of these species were investigated in the southwestern Aegean Sea for first time. Positive allometric and isometric growth in weight was defined in T. draco and T. radiatus, respectively. Six (1–6) and seven (1–7) age groups were identified in the current study for T. draco and T. radiatus, respectively. Ten otolith variables (radius, length, width, area, perimeter, roundness, circularity, form factor, rectangularity, and ellipticity) showed a significant relationship with the size for both species, except ellipticity in T. radiatus. The mean values of all the otolith variables were higher in T. radiatus than in T. draco. The results of this work can support further research on the behavioral and ecological features of the two species.