INTRODUCTION
The common guitarfish (Rhinobatos rhinobatos) inhabit the coastal waters (less than 100 m depth, including estuaries, the surf zone and enclosed bays) of the eastern Atlantic (southern Bay of Biscay to Angola) and the Mediterranean Sea (Froese & Pauly, Reference Froese and and Pauly2006). Maturity is reached at about 75 cm for males and 85 cm for females and maximum length observed is 150 cm (Fischer et al., Reference Fischer, Bauchot and Schneider1987; Golani et al., Reference Golani, Öztürk and Başusta2006). The common guitarfish exhibit ovoviparity (aplacental viviparity), and one or two litters per year and produce 4–10 embryos per litter (Serena, Reference Serena2005).
The common guitarfish was extremely vulnerable to capture by fisheries because the inshore areas where all pregnant females and adult males congregate for parturition and mating were so heavily fished in İskenderun Bay (Çiçek, Reference Çiçek2006). Immature fish, which remain inshore year-round, were also taken.
Generic categories were used for reporting landings of elasmobranchs species in Turkey (e.g. skates, rays and mantas nei). The common guitarfish is part of this group. In the absence of species-specific landing data, most traditional stock assessment methods cannot be used to determine their status (Musick et al., Reference Musick, Burgess, Calliet, Camhi and Fordham2000; Ellis et al., Reference Ellis, Dulvy, Jennings, Parker-Humphreys and Rogers2005).
Most elasmobranchs have slow growth rate, late maturity and low fecundity compared to the bony fish. This suite of life history characteristics results in low reproductive potential and low capacity for population increases (Stevens et al., Reference Stevens, Bonfil, Dulvy and Walker2000). There is increasing evidence that fishing exploitation affects their composition and biodiversity to a greater extent than most teleost fish in the Mediterranean (Stevens et al., Reference Stevens, Bonfil, Dulvy and Walker2000). In this case, if elasmobranch fishing is to be sustainable, management must be driven by their biological capacity. This will require better knowledge of the biology (e.g. growth rate and age structure), reproductive characteristics etc. (Camhi et al., Reference Camhi, Fowler, Musick, Brautigam and Fordham1998). The same situation is valid for the common guitarfish which is a member of the elasmobranchs group.
Despite that information for this species includes taxonomic descriptions (Fischer et. al., Reference Fischer, Bauchot and Schneider1987; Lloris & Rucobada, Reference Lloris and Rucobada1998; Serena, Reference Serena2005), distribution and occurrence (Basusta et al., Reference Basusta, Erdem and Çevik1998; Capapé et al., Reference Capapé, Zaouali and Ben Brahim1999a; Basusta & Erdem, Reference Basusta and Erdem2000; Patokian & Litvinov, Reference Patokian and Litvinov2005), reproduction (Capapé et. al., Reference Capapé, Gueye-N'Diaye and Seck1997, Reference Capapé, Gueye-N'Diaye and Seck1999b; Abdel-Aziz et al., Reference Abdel-Aziz, Khalil and Abdel-Maguid1993a; Karalar, Reference Karalar2005) and feeding habits (Capapé & Zaouali, Reference Capapé and Zaouali1979; Abdel-Aziz et al., Reference Abdel-Aziz, Khalil and Abdel-Maguid1993b; Basusta et al., Reference Basusta, Demirhan, Karalar and Çekiç2007; Enajjar et al., Reference Enajjar, Bradai and Bouain2007), nothing is known about age and growth of common guitarfish. Hoff & Musick (Reference Hoff, Musick, Pratt, Gruber and Taniuchi1990) pointed to the lack of age and growth information as a limiting factor in the development of elasmobranchs management plans.
The aim of this study is to provide some new information concerning the ageing technique, some relationships between morphometric measurements and growth parameters of common guitarfish from the eastern Mediterranean and to compare the data with that available from other areas.
MATERIALS AND METHODS
Material collection
This study was conducted on the north-eastern Mediterranean coast of Turkey (36°10′00″–36°55′00″E; 35°46′00″–36°10′00″N) between April 2004 and December 2005 (Table 1). Samples were collected by using commercial gill-net (44 mm mesh size), trawling (44 mm stretch length) and longline fishery. A total of 115 common guitarfish were examined, 66 females and 49 males. After the catching, the specimens were initially preserved in a plastic box with ice and they were kept in ice for approximately 6–8 h until they could be frozen at –20°C.
Age and morphological measurement of common guitarfish.
In the laboratory, each specimen was sexed by the examination of male claspers, and total weight (TW) was recorded to the nearest 0.1 g. Total length (TL) and disc width (DW) were measured to the nearest mm according to the method of Bongel & Abdallah (Reference Bongel and Abdallah2004), and vertebrae diameter (VD) was measured to the nearest 0.01 mm.
Processing of vertebrae and centra preparation
Eight to ten vertebrae were removed from the widest portion of the body, just behind the gill slits for each specimen (Türkmen et al., Reference Türkmen, Başusta, Demirhan and Karatas2005). Vertebrae were processed according to the method of Calliet et al. (Reference Musick, Burgess, Calliet, Camhi and Fordham1983). Remaining muscle tissue was removed from each centrum using a knife and to remove excess connective tissue, the centra were soaked in 5% sodium hydrochloride for one day and then rinsed in distilled water. The vertebrae were preserved in 70% ethanol until the examination.
The diameter of examined vertebrae was measured to the nearest 0.01 mm for each sample, using a manual caliper. Because of the concavity, a slice including the focus was sectioned sagittally (Cailliet et al., Reference Cailliet, Martin, Kusher, Wolf, Welden, Prince and Pulos1983) using a rotacraft variable speed (Yellow Shesto Limited) saw with cutting wheels (22 mm Ø, 0.5 mm thickness) and air-dried. The sections were mounted on microcope slides using transparent acrylic glue and were polished with sandpaper until approximately 0.5 mm in thickness (Figure 1).
Sectioning a vertebrae.
In this study alcian blue dying techniques were used to enhance the visibility of the band on vertebrae. The section was soaked in alcian blue solution (16 ml 100% ethanol, 2 mg alcian blue and 4 ml glacial acetic acid in 0.8 ml distilled water) for 12 h.
In order to determine the age (A), the sections were viewed in a stereo microscope (X10 magnification) with both transmitted and reflected light for identification of growth rings. Images of the vertebrae were captured with a digital camera (Kodak, 6.0 MP) and the images were examined using PhotoshopTM 7.0.
Analysis of growth and relationships
The relationships between DW–TL and VD–TL were determined using simple linear regression: L1 = a + bL2, where L1 and L2 are the two length measurements, a and b are the linear regression coefficients to be estimated.
A non linear regression was used to determine the relationship between TL–TW, DW–TW, DW–A, VD–TW, VD–A, TL–A and TW–A: x = a*yb, where x is dependent variable, y independent variable, a and b are the non-linear regression coefficients to be estimated.
Length–weight relationships were derived using the following power function. W = a*Lb where W and L presented weight and length respectively; a and b were regression parameters.
The von Bertalanffy growth function (VBGF) was fitted to back calculation and observed mean length-at-age data (von Bertalanffy, 1938). L t = L inf [1−e−k(t−t 0)]
where Lt, is the length of an individual at age (or time) t, L inf is the theoretical maximum attained length, k is the growth coefficient, and t 0 is the hypothetical age (or time) that individual is at length zero.
In order to analyse differences between the mean TL of females and males, the Z test was used (α = 0.005).
RESULTS
A total of 115 common guitarfish were sampled and 66 females and 49 males were sexed. Females made up 57.4% of the samples, which was not significantly different from a 1:1 sex ratio (χ2 test, P > 0.005).
Age and morphological measurements
A total of 115 common guitarfish specimens were measured. TL of females (N = 66) varied from 42.0 to 147.0 cm (all means presented ±SD, 99.7 ± 27.1 cm) and TW ranged from 174–13042 g (3844.0 ± 2922.9 g), whereas TL and TW of the males (N = 49) ranged from 39–124 cm (89.4 ± 23.2 cm) and 121–5586 g (2467.5 ± 1548.8 g) respectively. Mean TL and TW for combined sexes were calculated as 95.3 ± 25.9 cm and 3257.5 ± 2519.7 g, respectively (Table 1). Females of the sample were both longer and heavier than males.
The non-linear relationship between TL and TW is presented as TW = 0.0014*TL3.1672 (R2 = 0.985) for females, TW = 0.0012*TL3.1947 (R2 = 0.990) for males and TW = 0.0012*TL3.1915 (R2 = 0.987) for both sexes (Figure 2). There were no significant differences in the relationship between TL and TW for males and females (analysis of variance), and therefore the data were combined.
Length–weight relationship for common guitarfish (W, total weight, L, total length).
The relationships between morphological measurements are presented in Table 2. The regression analysis indicated that the morphometric measurements were all and significantly related according to the equation which is presented in Table 2.
The relationship between TL–TW, DW–TW, DW–TL, DW–A, VD–TW, VD–A, VD–TL, TL–A and TW–A for the common guitarfish.
TL, total length; TW, total weight; DW, disc width; VD, vertebrae diameter; A, age.
Growth in age
A total of 115 (66 females, 49 males) vertebrae were removed from the samples. However, age estimation was only possible from 56 female and 41 male vertebrae (total 97 vertebrae) because some of the vertebral rings were not visible to read accurately. Age–frequency distribution is presented in Figure 3. It can be seen in Figure 3 that age of the common guitarfish varied from 1 to 15 y for males and to 24 y for females. The most frequent age group was age group 3rd for males and age groups 2nd and 3rd for females.
Age–frequency distribution of common guitarfish.
Some age bands on the sectioned vertebrae were captured under the stereobinocular microscopy by using a digital camera (Figure 4). The growth bands on the vertebrae can be seen clearly.
Age marks on the vertebrae (total length of the specimens: A, 85 cm; B, 112 cm; C1 and C2, 123 cm).
The common guitarfish growth curve fits for the von Bertalanffy growth functions for each sex and pooled data in Table 3. On the other hand, the fitted von Bertalanffy growth curve observed length-at-age data for combined sexes (see Figure 5).
von Bertalanffy growth curve fitted from observed length-at-age for combined sexes.
von Bertalanffy growth parameters for the common guitarfish.
Mean back calculated length-at-age for both sexes for observed ages and mean observed length-at-age for same ages are shown in Table 4. It can be seen from the table, especially for young age, that there were very big differences between observed and back calculated length-at-age.
Mean observed and back calculated length-at-age data of females, males and pooled data for the common guitarfish.
OTL, observed total length in cm; BCTL, back calculated total length in cm.
DISCUSSION
Females of the sample were both longer and heavier than sampled males. The occurrence of sexual differences in growth is well documented in elasmobranchs, with females usually growing longer (Casey et al., Reference Casey, Pratt and Stillwell1985; Ismen, Reference Ismen2003; Skomal & Natanson, Reference Skomal and Natanson2003; Yamaguchi et al., Reference Yamaguchi, Kawahara and Ito2005). In this study mean total length of females and males are significantly different from each other; it can be hypothesized that females grow to an older age and reach larger size than males.
Despite some studies conducted on the taxonomic descriptions (Fischer et al., Reference Fischer, Bauchot and Schneider1987; Lloris & Rucobada, Reference Lloris and Rucobada1998; Serena, Reference Serena2005), distribution and occurrence (Basusta et al., Reference Basusta, Erdem and Çevik1998; Capapé et al., Reference Capapé, Zaouali and Ben Brahim1999a; Basusta & Erdem, Reference Basusta and Erdem2000; Patokian & Litvinov, Reference Patokian and Litvinov2005), reproduction (Capapé et al., Reference Capapé and Zaouali1981, Reference Capapé, Gueye-N'Diaye and Seck1997, Reference Capapé, Zaouali and Ben Brahim1999b; Abdel-Aziz et al., Reference Abdel-Aziz, Khalil and Abdel-Maguid1993a) feeding habits (Capapé & Zaouali, Reference Capapé and Zaouali1979; Abdel-Aziz et al., Reference Abdel-Aziz, Khalil and Abdel-Maguid1993b; Basusta et al., Reference Basusta, Demirhan, Karalar and Çekiç2007; Enajjar et al., Reference Enajjar, Bradai and Bouain2007), no information about age and growth were previously available for common guitarfish in the FishBase online version of January 2006 (Froese & Pauly, Reference Froese and and Pauly2006). Age and growth parameters were estimated for the first time with this study.
Numerous techniques have been used in the attempts to enhance the visibility of growth bands in vertebrae of elasmobranchs (Cailliet et al., Reference Cailliet, Martin, Kusher, Wolf, Welden, Prince and Pulos1983). All of these techniques show that the success of each technique is often species specific and that slight modifications in the technique may enhance the results. Alcian blue dying techniques were used to enhance the visibility of the cartilage skeleton of mouse embryos (Dingerkus & Uhler, Reference Dingerkus and Uhler1977) and cartilage and related tissues in the trunk and fins of teleosts (Benjamin et al., Reference Benjamin, Ralphs and Eberewariye1992). However, the techniques have been used for the first time on elasmobranchs vertebrae successfully in this study. A total of 97 vertebrae out of 115 had a visible vertebral band in this study. The percentage of readable vertebrae was 84% in this study. In the previous studies, the percentage was 19% with crystal violet dying techniques on Dasyatis pastinaca (Ismen, Reference Ismen2003) and 52% with X-ray techniques on Furgaleus macki (Simpfendorfer et al., Reference Simpfendorfer, Chidlow, McAuley and Unsworth2000). Therefore, it can be hypothesized that the alcian blue dying techniques can be used successfully for elasmobranchs vertebrae.
Previously verification of annual band periodicity for the common guitarfish has not been done. It is assumed that one growth ring is deposited each year for this species. But some previous studies showed that one year growth of some of the elasmobranchs fish consists of two bands. For example, on Atlantic mako sharks (Isurus oxyrinchus) two pairs of bands are deposited annually (Ribot-Carballal et al., Reference Ribot-Carballal, Galvan-Magana and Quinonez-Valezques2005). Therefore, a detailed study should be carried out to demonstrate whether band formation indicates one year growth or not for the common guitarfish.
The estimation of k (0.159), a growth parameter, implies that this species relatively is a higher growing species compared with other elasmobranch species. Thus, k values were reported by Ismen (Reference Ismen2003) for Dasyatis pastinaca (0.089), by Yamaguchi et al. (Reference Yamaguchi, Kawahara and Ito2005) for Aetobatus flagellum (0.111) and by McFarlane & King (Reference McFarlane and King2006) for Raja binoculata (0.04) and R. rhina (0.07).
There were very big differences between observed and back calculated length-at-age of the common guitarfish. It can be hypothesized that the differences were a lower value of L∞ and a slightly higher value for the K parameters (Lessa et al., Reference Lessa, Santana and Paglerani1999). It can be seen from Table 3, that maximum observed total length was low for females (147.0 cm) but high for males (123.0 cm) compared with calculated L∞ values (154.9 cm for females and 121.7 cm for males).
ACKNOWLEDGEMENTS
The authors thank Mustafa Çekiç and Murat Karalar for their asistance in obtaining the fish samples.
