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Estimation of Age Growth and Reproduction of Boarfish Capros aper in the South Aegean Sea.

Byline: Sercan Yapici and Halit Filiz

Abstract

The present study investigated the age growth reproduction of boarfish (Capros aper L. 1758) collected from the South Aegean Sea between December 2009 and November 2010. The length-weight relationship was W= 0.019 L2.93 (n=790; r2= 0.95). Age data based on otoliths were comprised from 0+ to 4+. The parameters of the fitted von Bertalanffy growth equation were L8 = 11.05 cm k = 0.447 year-1 t0 = -0.480. Macroscopic gonad examination and analysis of the monthly values of the GSI indicated that reproduction occurs between April and August. Individuals become sexually mature at around 6.69 cm total length (TL) (a size that can be reached on 1.84 years) for both sexes. Sex ratio (female:male) was found as 1.00:0.74.

Keywords: Growth and reproduction boarfish Capros aper.

INTRODUCTION

Members of the teleost family Caproidae (known as boarfish) are widely distributed throughout Atlantic Indian and Pacific Oceans (Nelson 2007). Caproids are generally small to medium sized coastal marine fishes that are abundant and by-catch species in demersal pelagic and crustacean-trawl fisheries (Sartor et al. 2001; Borges et al. 2005; Fonseca et al. 2005; Farrell et al. 2012). The family is characterized by having rhomboidical-shaped laterally compressed and small protractil mouth (Nelson 2007). There are 18 species within the Caproidae and one belongs to the genus Capros.

Until recently biological studies on this species have been limited in literature because Capros aper (Linnaeus 1758) has no commercial value especially in Mediterranean being a small size fish. The boarfish is distributed along the Eastern Atlantic (western Norway Skagerrak Shetlands and western Scotland to Senegal) and the Mediterranean (QuACopyrightro 1986) between 40-700 m (Mytilineou et al. 2005). This species spreads a wide range habitats including over rock or coral but also over sandy ground and feed mainly on crustaceans worms mollusks (QuACopyrightro 1986).

In last 30 years abundance of C. aper has been increased exponentially in most parts of Northeast Atlantic (Southwest Ireland Celtic Sea Biscay Bay) that represents the main existence region of species owing to climate change and/or variability of its distribution (Blanchard and Vandermeirsch 2005). Thus the boarfish have recently become newly target species in commercial fishery conducted in Northern Atlantic. The annual catch rates increased from 600 t to 21584 t in Celtic Sea (White et al. 2011) and from 18382 t to 100000 t in Celtic Sea and Southwest of Ireland (HA1/4ssy et al. 2012b).

Despite the increasing globally exploitation

and importance of this species in commercial fisheries no detailed information on its biology in Mediterranean is known. The aim of present study was therefore to determine biological parameters of C. aper.

MATERIALS AND METHODS

Study sites

Specimens of C. aper were collected

randomly between 30-225 meters depths via F/V AKYARLAR (crustacean trawl vessel) during sixty- eight hauling carried on from December 2009 to November 2010 in South Aegean Sea (37.5 to

37.0 N). In the sampling traditional bottom trawl nets (44 mm strecthed mesh size) locally called Ottoman nets were used. Towing duration was limited to 30 minutes and the average trawling speed was approximately 2.5 knots. Specimens were

identified on board and then stored on ice and carried in the laboratory.

For each fish total length (TL cm) to the

nearest 0.1 cm and wet weight (W g) to the nearest

0.01 g were measured in the laboratory. The sagittal otoliths from 600 fish were removed for age estimation.

Age and growth

Estimated age was accomplished by sectioned otoliths. Each pair of sagittal otoliths was embedded in polyester catalyst and cut through Buehler-Isomet precision saw. The section was mounted on glass microscope slide with Buehler Crystalbond Mounting Wax and observed on stereo microscope using reflected light against a dark background. Annuli were identified as translucent and opaque zones where formed around the sulcus. Sum of each translucent and opaque zone was accepted representing annual growth. Otoliths were read twice by two different readers (blind reading). When no agreement between the two readings was found the otolith was excluded.

To examine fish growth von Bertalanffy growth equation was calculated using the iterated least square method (Beverton and Holt 1957): Equation

where L8 is the asymptotic total length Lt the total length at age t k the growth curvature parameter and t0 is the theoretical age that fish would have been at zero length (Sparre and Venema 1992). Von Bertalanffy growth curves were fitted to each sex separately and to combined data. The differences between sexes were compared by F-test.

Growth performance index (f') that allows to compare the growth rates of populations living in different areas was calculated by the following formula (Pauly and Munro 1984) Equation

The logarithmic relationship between weight and length (LWR) was accomplished by the following formula (Sparre and Venema 1992): ln W = ln a + b ln TL.

Parameter a and b were calculated by least-

squares regression as was the coefficient of determination (r2). Standard error was calculated for the slope (b): significant difference of b values from

3 which represents isometric growth was tested by the t-test (Pauly and Munro 1984) with values of P

less than 0.05 considered significant. Upon the statistical approach differences on LWR between sexes were tested by analysis of covariance (ANCOVA).

Reproductive biology

Sex of specimens was assessed by the existence of ovaries or testes. Stage of reproduction was assigned by macroscopic observation based on Holden and Raitt (1974). Fish were classed as being either mature (stage 3 or greater were accepted as capable of spawning during current spawning period) or immature (stage 2 or less). The gonads were then weighed to the nearest 0.01 g and a gonadosomatic index (GSI) (gonad weight expressed as a percentage of bodyweight without gonad) was calculated (Wootton 1991). The parameters length (L50) and age (A50) at first maturity for combined sexes were obtained by fitting logistic ogives to the proportion of sexually mature individuals by non-linear least squares analysis (King 1995). Difference of maturity curves between sexes were determined by chi-square test.

RESULTS

A total of 790 specimens of C. aper were collected during the surveys. The collected fish ranged in total length from 3.50 to 10.50 cm (mean

S.D = 7.190.27 cm) and in weight from 2.5325.82 g (mean S.D = 7.423.44 g).

The otolith core region of boarfish was slightly opaque followed by a narrower translucent zones. Counts of opaque zones were made for 600 boarfish otoliths. Counts ranged from 1 to 4. There was 94% agreement between all readings then 36 otoliths were not considered. Thus 199 (35.3%) males 325 (57.6%) females and 40 (0.7%) undetermined individuals (n = 564) were used for direct reading on otoliths. In terms of appropriate age readings maximum age was found as 4 years for both sexes. Percentage of age groups belonging

to population were 0+ (6%) 1+ (6%) 2+ (61%) 3+ (22%) and 4+ (5%) (Fig. 1). As a result 0+ and 1+ years old individuals were poorly observed while 2+ years old ones were dominant.

The estimated von Bertalanffy growth parameters fitted from data were as follows: L8 = 11.05 cm k = 0.45 year-1 and t0 = -0.480 year for the total sample. The differences between sexes were not statistically significant in F-test (Pgreater than 0.05).

However females reached a greater asymptotic length value than males (Table I). The growth performance index (f') was estimated as 1.74 for the total sample.

Table I.- Estimated von Bertalanffy growth parameters of C. aper.

Sex###n###L###k###t0###'

###318###11.12###0.415###-0.520###1.71

###432###11.35###0.432###-0.346###1.75

Total###790###11.05###0.447###-0.480###1.74

Comparison of LWRs between sexes did not represent statistical significance (ANCOVA: F = 2.175 P = 0.344) and the values of b suggest a

negative allometry growth (t-test P less than 0.05) (b = 2.94 for female and b = 2.93 for male and for the total sample). The high value of r2 indicated a strong relationship between length and weight (Table II).

As a result of 790 fish that were dissected there were significantly more females (432) than males (318) (2 = 17.328 P less than 0.05) and overall sex ratio was found as 1:0.74 (f:m). The number of males was higher than females only in February while the females were more abundants during the rest of the sampling period (Table III).

By the analysis of GSI C. aper displayed spring/summer spawning period between April and August (Fig. 2). Females and males had peak of GSIs during June and May respectively (Fig. 2)

however males displayed a similar seasonal pattern in mean GSI values. Additionally the average maximum GSI values of females was 4.95 compared to 1.1 for males. There were no significant differences between maturity curves for female and male C. aper (2 = 0.945 P greater than 0.05). The data were therefore combined and showed that C. aper matured at 6.69 cm TL and 1.84 years (Figs. 3 and 4).

Table II.- Length-weight relationships of C. aper.

###W = aLb

Sex###n###Lmin Lmax (cm)###Wmin Wmax (g)###Growth type

###a###b S.D###r2

###318###5.00 9.20###2.45 15.19###0.0198###2.934 0.05###0.93###A(-)

###432###5.20 10.50###2.53 25.82###0.0193###2.937 0.05###0.95###A(-)

Total###790###3.50 10.50###1.20 25.82###0.0194###2.934 0.04###0.95###A(-)

Table III.- Sex ratio of C. aper by months.

Month###Female###Male###Ratio (F:M)

January###18###17###1 : 0.94

February###22###23###1 : 1.04

March###19###13###1 : 0.68

April###33###18###1 : 0.55

May###81###64###1 : 0.79

June###52###31###1 : 0.60

July###71###50###1 : 0.70

August###39###31###1 : 0.79

September###28###19###1 : 0.68

October###23###20###1 : 0.87

November###26###23###1 : 0.88

December###20###9###1 : 0.45

Total###432###318###1 : 0.74

DISCUSSION

The reproduction cycle of boarfish was observed between April and August. Spawning period based on monthly changes in gonadosomatic index for females suggested in present study is similar to preliminary studies. Tortonese (1970) reported a spawning period for C. aper as March and August in Mediterranean. Kaya and Ozaydin (1996) stated that the collected specimens in July were mature and suggested that spawning period of C. aper occurs in spring and summer. In the Northern Atlantic Farrell et al. (2012) claimed that C. aper spawn between April-September.

Consequently this suggested that C. aper prefer warm waters to spawning. It may be related to oceanographic conditions that are suitable for improving successful recuitment. As it is known when water temperature begin to warm larvae may have high food availability (Wootton 1991). However without a understanding of the early life history of C. aper and oceanographic conditions in species distribution area possible link between spawning time and oceanographic these processes remain unknown.

According to t-test there was a significant difference in the mean GSI indices between males and females (P less than 0.05). The GSI patterns of C. aper are similar to most of marine fishes. As a known GSI values of males are commonly lower than those of females. The difference in male and female

gonadosomatic indices suggests that energy invested in gamete production by male is probably less than that invested by females. Difference on mean GSI values belonging to males and females of C. aper arised from this phenomenon.

Males and females of C. aper reached first maturity at 6.69 cm TL and 1.84 years from their growth rate. Results from reproduction data associated with age and length showed that females are considerably early maturing. In Atlantic Ocean White et al. (2011) found that the length and age at maturity were 8.05 cm (TL) and 4.60 years respectively. HA1/4ssy et al. (2012a) estimated these values as 9.72 cm (TL) and 3.4 years respectively. In the Mediterranean these values were found as

8.50 cm (TL) and 2 years by Kaya and Ozaydin (1996). Results of reaching maturing time in present study and previous studies conducted in Mediterranean show similarity. Besides northern populations of fish is known to reach sexual maturity later because of oceanographic conditions such as primarily water temperature. Sex ratio of C. aper was explicitly biased towards females. Males predominated only in February with females predominating through the year. In group spawners large amounts of sperm enable advantages for successfully fertilizing eggs and broadcast spawning which groups of fish congregate together with the potential for sperm from one male to fertilize the eggs of many females and the eggs from one female to be fertilized by many males and thus males must have gonads of equivalent sizes to females (Karleskint et al. 2010).

There is observed distinctly difference in GSI values between male and female C. aper however the monthly oscillations in GSI values show similarities for both sexes. Therefore it may be clue that boarfish are group spawners. Additionally the both sexes were observed in all months it is indication that females and males co-occur in continental shelf throughout the year.

Growth of boarfish show similarity with pelagic fishes in the Mediterranean based on results of age and growth characteristics. The boarfish spreading in the Mediterranean Sea grow rapidly attain maturation at early stage of life (~2 years) after which growth slowed considerably ranging of age-classes in population is narrow (from 0+ to 4+ years old) and show high colonisation or schooling rate (r-strategy). Males and females C. aper grow at similar rates. However females may attain slightly larger sizes than males after sexual maturation. Greater and faster growth trends in females than in males is recognised phenomenon in many marine fishes (Landa and PiAeiro 2000). The advantages of females reach larger sizes than males may be related to increase reproductive success (e.g. raising fecundity) since there is no observed sexual dimorphism or social interactions in members of this genus.

The exponential length of C. aper was estimated as 11.05 cm in Aegean Sea for present study. It may be accepted as realistic because the largest captured specimen was 10.5 cm. This value is different from results of studies from Atlantic

waters where asymptotic lengths were reported as 12.89 cm by White et al. (2011) and 15.47 cm (mean) by HA1/4ssy et al. (2012a). Many demersal fish stocks are much smaller in Mediterranean than Atlantic. This is the best known phenomenon called as dwarfism (Stergiou et al. 1997).

Results of ANCOVA showed that no significant difference was found between males and females in the length-weight relationships. The length-weight relationship based on 790 individuals represented negative allometric growth in accordance with the results reported by other authors (Kaya and Ozaydin 1996; Lamprakis et al.

2003; Filiz and Bilge 2004; Leblebici et al. 2006; White et al. 2011; HA1/4ssy et al. 2012a). The length- weight relationship in fishes can be affected by a number of factors including season habitat gonad maturity sex diet and stomach fullness health and preservation techniques and differences in the length ranges considering the caught specimen (Tesch 1971; Wootton 1991). Furthermore comparison of length-weight relationships values belong to present and previous studies are also presented in Table IV.

Different longevity has been suggested for boarfish spreading on different seas and oceans. Age-reading results of present study indicated that age classes of C. aper varied between 0+ to 4+ years (Table V). The age composition of C. aper in commercial fishing area showed that typically between 2 and 3 years old fishes are exploited as a discard.

Regarding age and growth of boarfish there are considerable differences with data of previous studies. As mentioned by Campana (1984) age- reading from sectioned otoliths are observed higher ages than otoliths read whole. Despite that sectioned otoliths were used to increase precision of age- reading maximum age was found only 4 years. In the Mediterranean Kaya and Ozaydin (1996) reported maximum age as 4 years. White et al. (2011) claimed life span of C. aper as 26 years and HA1/4ssy et al. (2012b) found as 8 years in Northern Atlantic Ocean. Nevertheless sampling stations of these two studies (White et al. 2011 HA1/4ssy et al.

2012b) are closer surprisingly the authors have found extremely different results. It may be reason that White et al. (2011) collected samples from

closed area for fishing or role of differences in preparatory and viewing methods of otoliths. Presence of old fish was not surprising where is no over-exploitation fishing pressure or predation in the stock. However HA1/4ssy et al. (2012a) explained that C. aper has high abundance in trawl composition as a discard species and subject to predation mortality (diet of sharks rays and bony fishes) but then suggested that C. aper has high longevity. As is known drastic occurence of any species in trawl composition means exposed to overfishing. Overfishing negatively affects the existence of age classes especially older age groups in the population (King 1995). Consequently this hypothesis seems to be thought- provoking. Even so there may be an alternative hypotheses to support longevity of boarfish. For instance Lopes et al. (2006) mentioned about different morphotypes of C. aper which have presumably different growth rate and age features.

Those authors may have collected morphotype of C. aper has slowest growth rate. There are on the other hand species morphologically similar to C. aper in the North Atlantic (e.g. Genus: Antigonia). These species (Genus: Antigonia and Capros) may be share potentially the same distribution area. Therefore species identification should be more careful and sensitive. Nonetheless it should be noted that variation of maximum age length and longevity between studies may be influenced by especially mesh size sampling depth and sea- bottom characteristics.

In conclusion understanding the life history or population dynamics of non-commercial fishes is important because the existence and/or nonexistence of non-commercial fish populations may affect abundance of target species. Non-commercial fish resources are important not only in terms of biodiversity but also in terms of quantities harvested and even more in terms of future commercial harvests. Accordingly comprehensive studies on non-commercial fish populations are keystones to understand their biological aspects on marine food web and essential for sustainable fisheries management (Alverson et al. 1994). On the other hand economical benthopelagic fish families reported preying on C. aper such as Merluccidae Phycidae and Sparidae were abundant both in the

Table V.- Results of the mean lengths and percentage per age group for males females and undetermined C. aper specimens.

###Age###Undetermined

###Total###%

(Years)###n###Mean TL (cm)###n###Mean TL (cm)###n###Mean TL (cm)

0+###5###5.22 0.19###6###5.29 0.16###23###4.46 0.47###34###6.03

1+###18###5.40 0.44###6###5.50 0.34###10###5.59 0.11###34###6.03

2+###121###6.97 0.43###215###6.90 0.40###7###6.52 0.62###343###60.81

3+###47###8.50 0.46###77###8.60 0.51###-###-###124###21.98

4+###8###9.10 0.20###21###9.20 0.51###-###-###29###5.15

Total###199###325###40###564###100.00

Mediterranean and Aegean Sea (Gomes et al. 1998; Morato et al. 1999; Cabral and Murta 2002).

The present study will increase the knowledge on age growth reproduction biology of boarfish in the Aegean Sea. It may also put across role and importance of C. aper in the food chain of marine ecosystem. Thus the biology of commercial fish species that are main predators of C. aper may be understood better. Thereby enforce regulation related to commercial fisheries may make more sensitive and appropriate.

ACKNOWLEDGEMENTS

This research was supported by Mugla University Scientific Research Fund (BAP 09/31). We would like to thank the Republic of Turkey Ministry of Agriculture and Rural Affairs General Directorate of Protection and Control" and Turkish Coast Guard Command (TCGC)" and TCG Aegean Sea Area Command" for giving trawl permission in prohibited areas during the survey. Also the authors would like to thank the two anonymous reviewers for their suggestions and comment.

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