INTRODUCTION
Chub mackerel, Scomber colias Gmelin, 1789, is widely distributed in the warm waters of the Atlantic Ocean including the Mediterranean and Adriatic Seas. This medium-sized pelagic fish species occurs in deeper waters during the colder part of the year and schools are found in coastal waters during the warmer parts of the year, where they spawn and feed. Atlantic chub mackerel is one of the most important commercial fish throughout its habitat (Anonymous, 2011) and as a consequence of its wide distribution and broad commercial exploitation, biological information on the growth and mortality is required for stock assessment and management (Cadima, Reference Cadima2000). Despite the abundance and economic importance of S. colias in the Adriatic Sea, knowledge about its biology and population dynamics is still limited. Studies of the age, growth, mortality, and exploitation rates of S. colias have not been undertaken previously in the Adriatic Sea. Therefore, the exploitation status of this species' stock in the Adriatic Sea is unknown. The purpose of this study was to provide information on the age, growth, and length–weight relationship as well as estimates of mortality and exploitation rate in order to define the present state of the population in the Adriatic Sea.
MATERIALS AND METHODS
The studied specimens of S. colias were collected randomly from the commercial landings during the night with artificial lights and purse seines with a stretched mesh size of 10 mm. The purse seine with artificial light is the preferred fishing technique in the Adriatic Sea for capturing those fish species that school or aggregate close to the surface, including anchovies, sardines, mackerels, herrings and some tuna species.
A total of 4189 specimens were sampled between January 1998 and December 2007 in the eastern part of the Adriatic Sea (geographical range from 44°13.586′N 15°08.883′E to 42°48.523′N 17°51.109′E). Samples were collected once a month, with the exception of 13 months when sampling was limited by logistical problems or bad weather. The number of specimens sampled each month ranged from 20 (May 2002) to 177 (September 2007) individuals. All fish were analysed in the laboratory immediately after landing. For each specimen, fork length (FL) (±0.1 mm) and total body weight (W) (±0.01 g) were measured. Sex was determined macroscopically considering the shape, appearance and structure of the gonads. The total sample comprised 1085 males, 1611 females and 1493 specimens of undetermined sex. The latter included those specimens that were immature, in the resting phase of reproduction (i.e. the sex could not be determined by macroscopic examination), or due to the specimens not being preserved well enough.
The relationship between FL and W was calculated for each sex separately by geometric mean functional regression (Ricker, Reference Ricker1975) in exponential form W = aFLb, where b is the regression coefficient and a is the regression constant. Length–weight regressions were tested for differences in slopes between sexes using the Mann–Whitney U-test.
Random subsamples of S. colias (10 specimens from fresh fish commercial landings sampled randomly each month) were taken during the period January 2006–December 2007; sagittal otoliths were removed from the head, cleaned, dried and stored in plastic tubes. Otoliths were immersed in alcohol and aged on three separate occasions, approximately two months apart, to reduce subjectivity. Reading was done using reflected light on a black background and a magnification of 1.6. The otolith was considered to be unreadable when two readings from the same otolith resulted in different age estimates. One opaque and one hyaline ring were considered to represent one year of life.
The weights of the undamaged and cleaned otoliths (N = 100) were measured on a Mettler analytical balance (to the nearest 0.01 mg). The relationship between fork length, weight, and age of the fish and weight of the otolith were examined with the linear, exponential regression model by the method of least squares (Sokal & Rohlf, Reference Sokal and Rohlf1995). StatSoft 5.5 software was used for the statistical analysis.
Values of L∞ (the asymptotic length), K (the growth constant), and t0 (the age at which FL = 0) were calculated by the Ford–Walford graphic method (Ford, Reference Ford1933; Walford, Reference Walford1946). The von Bertalanffy growth equation L t = L ∞ [1−e −K(t=to)] was fitted to length-at-age data using non-linear least squares parameter estimation (Gulland, Reference Gulland1983). Separate analyses were carried out for males, females and both sexes pooled together with unsexed specimens.
The growth performance index phi-prime (Φ′) was estimated to compare the growth parameters obtained in the present work with those reported by other authors. This index was calculated by the equation of Munro & Pauly (Reference Munro and Pauly1983): Φ′ = log K + 2 log L ∞.
Natural, fishing, and total mortality were calculated for the total sample. Natural mortality (M) was defined as the mean value of three estimations using the general regression equations below:
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• log10M = −0.0066–0.279log10 L ∞ + 0.6543log10K + 0.4634 log10T (Pauly, Reference Pauly1980), where L∞ and K are the parameters of the von Bertalanffy growth equation (Gulland, Reference Gulland1983) and parameter T is the mean value of the water temperature (17.35°C) in the investigated area (Grbec et al., Reference Grbec, Vilibić, Bajić, Morović, Beg Paklar, Matić and Dadić2007);
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• M = 1.521/X0,72–0.155 (Rikhter & Efanov Reference Rikhter and Efanov1976), where X is the age at which most of the population has matured (four years for males, five years for females and overall: Čikes Keč, Reference Čikeš Keč2009);
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• M = 0.996/A0.95 (Taylor, Reference Taylor1959), where A 0.95 is the age at length of 95% L∞ (14.99 years).
The instantaneous total mortality rate (Z) was estimated using the linearized length-converted catch curve (Pauly, Reference Pauly1984) in the software FiSAT (Gayanilo et al., Reference Gaynilo, Sparre and Pauly1994). The natural logarithm of the ratio between the number of fish in each length-class and the time needed for the fish to grow through the length-class (lnNi/Δti) was plotted against their corresponding relative age (t) and the total mortality was estimated from the descending slope b. The Z value obtained was used to calculate the survival rate (S) by the formula S = e−Z (Ricker, Reference Ricker1975). The instantaneous rate of fishing mortality (F) was estimated from the difference between Z and M. The exploitation rate (E) was determined according to Gulland (Reference Gulland1983): E = F/Z. A defined limit reference point (LRP or Llimit) was calculated using the equation of Patterson (Reference Patterson1992): LRP = 2/3 M in order to define the present state of the S. colias resource.
RESULTS
Length–weight relationship
The fork lengths and weights of all analysed specimens (N = 4189) ranged from 10.1 to 39.1 cm (mean: 23.8 ± 4.68 cm) and from 8.90 to 804.50 g (mean: 164.49 ± 102.70 g), respectively. Females had both a wider length distribution (Figure 1) and a wider weight range than males (males ranged from 22.95 to 710.60 g and females from 16.51 to 701.66 g) and they also had lower mean values. The length frequencies of males, females, and the overall material were normally distributed (Kolmogorov–Smirnov test: d = 0.0505 males, d = 0.0375 females, and d = 0.0450 total; P < 0.05).
Length–frequency distribution of male and female chub mackerel specimens as well as sex-ratio by length, Adriatic Sea, 1998–2007.
The calculated length–weight relationships were W = 0.0061FL3.1836 (r2 = 0.922) for males, W = 0.0057FL3.1936 (r2 = 0.910) for females and W = 0.0052FL3.2238 (r2= 0.969) for all specimens. The hypothesis of isometric growth was discarded for males and females, as the obtained allometric index value (b) was significantly different from 3 (t = 0.713; t = 0.961; P < 0.05, respectively), but not for all the analysed material (t = 0.317; P > 0.05) of chub mackerel in the Adriatic Sea.
Interannual variations in the mean allometric index (b) of S. colias were noticed although its values stayed above the isometric value over the whole study period (Figure 2). Sharp decreases were noticed in 1998–1999 and 2007–2008. In both sexes, synchronous fluctuations of the allometric coefficient b by month were established (Figure 3). Namely, both males and females had lower b values during the colder part of the year (minimum in February, with an exception in January), while the peak was in June.
Mean annual allometric coefficient (b) and its standard deviations for each year together with the average allometric coefficient for the overall investigated period, Scomber colias, Adriatic Sea, 1998–2007.
Mean monthly allometric coefficient of males, females, and overall investigated specimens of Scomber colias, Adriatic Sea, 1998–2007.
Age and growth
Broader opaque and narrower hyaline zones of S. colias otoliths alternated outwards from the nucleus of the sagitta (Figure 4). A total of 280 otoliths were aged successfully. The fork lengths of aged specimens ranged from 14.1 to 39.0 cm (Table 1). The age-classes in the otolith sample ranged from 1+ to 9+ years, while the samples were dominated by the 2+ and 3+ age-classes (40.7% and 20.7% respectively). There appeared to be a difference between the age distributions of male and female fish, as most of the males were 6+ (30.4%) and 2+ (29.1%) years old, while females were mostly 3+ (38.9%) and 2+ (36.7%) years old. The mean lengths-at-age were more variable but generally larger for females (except in the 1+, 4+, and 9+ year olds) (Figure 5).
Scomber colias sagitta otolith (W = 140.29 g, FL = 23.6 cm, age 3+, magnification 1.6 × 40), 20 April 2007, Adriatic Sea.
Age structure of males, females and overall material, Scomber colias, Adriatic Sea, 2006–2008.
Age–length key for chub mackerel with mean fork length and standard deviation ( x ± SD), 2006–2008, Adriatic Sea.
The weights of the otoliths were from 0.889 to 11.456 mg, with a mean of 4.252 ± 2.429 mg. The relationship between fork length and otolith weight was exponential and highly correlated (r = 0.901; Figure 6). Also, a high linear correlation was obtained between the weight of the fish and the weight of the otolith (r = 0.951). Age estimations correlated exponentially with otolith weight, as well (r = 0.907) (Figure 6).
Correlations between otolith weight (Wo) and total body weight (W), fork length (FL), and age, Scomber colias, Adriatic Sea, 2006–2008.
Length-at-age data for both sexes and the total sample were very well fitted by the von Bertalanffy growth curve (r2 > 0.957) (Figure 7). Overall, the relationship between age and length was described by the growth parameters L∞ = 45.31 cm, K = 0.180 year−1, t0 = −1.649 year. Slight variations between sexes were established. Namely, for males the relationship was L∞ = 41.31 cm, K = 0.237 year−1, t0 = −1.052 year and for females it was L∞ = 48.64 cm, K = 0.151 year−1, t0 = −1.943 year. The estimated growth performance index (Φ′) was 2.57 for the whole material, while for males and females the indices were 2.61 and 2.55, respectively.
Von Bertalanffy growth equations for (a) males, (b) females and (c) overall specimens, Scomber colias, Adriatic Sea, 2006–2008 (I t is the length at time t).
Mortality
The natural mortality (M), total mortality rate (Z) (Figure 8), fishing mortality coefficient (F), exploitation (E), and survivor (S) rate were estimated (Table 2). The value of the M/K ratio was 1.94, while the limit reference point (LRP) for S. colias was estimated as 0.23.
Total mortality coefficients (Z) for (a) males, (b) females and (c) overall specimens, Scomber colias, Adriatic Sea, 1998–2007.
Mortality coefficients of Scomber colias for males, females and overall material (total) in the eastern Adriatic Sea during the investigation period from January 2006 to December 2008.
DISCUSSION
The length–weight relationship is a key biological parameter (Martin, Reference Martin1949; Bagenal & Tech, Reference Bagenal, Tesch and Bagenal1978; Ricker, Reference Ricker, Hoar, Randall and Brett1978) and data from this and earlier studies are presented in Table 3. Isometric growth of S. colias determined in this study was in accordance with results reported in earlier studies (Stergiou & Moutopoluos, Reference Stergiou and Moutopoulos2001; Sinovčić et al., Reference Sinovčić, Franičević, Zorica and Čikeš Keč2004) and elsewhere in its range. Length–weight investigations of S. colias throughout its habitat revealed allometric coefficients (b) ranging from 3.227 (Portuguese coast: Goncalves et al., Reference Goncalves, Bentes, Lino, Ribeiro, Canario and Erzini1997) to 3.704 (Aegean Sea: Moutopoulos & Stergiou, Reference Moutopoulos and Stergiou2002). Negative allometry was recorded in the northern part of the Atlantic (Magnusson & Magnusson, Reference Magnusson and Magnusson1987: b = 2.880). As previously recorded by other researchers (Huxley, Reference Huxley1932; Frost, Reference Frost1945; Martin, Reference Martin1949; Bagenal & Tesch, Reference Bagenal, Tesch and Bagenal1978; Ricker, Reference Ricker, Hoar, Randall and Brett1978), changes in the length–weight relationship by year and by sex were noted during this investigation as well. Namely, positive allometry was established for males and females, and intra- and inter-annual variations of the mentioned allometric coefficient were noted; higher values of b were observed during the warmer part of the year. Therefore, the deviations between the results obtained in this study and those from other areas are probably due to differences in the time/area of investigations, sample size and/or sex-ratios.
Results of previously reported length–weight relationship parameters (regression coefficient b, regression constant a) of Scomber colias in different areas of habitat together with results for chub mackerel in the eastern Adriatic Sea during the investigation period from January 2006 to December 2008.
In natural populations the younger age-classes are expected to be more abundant than the older ones. The absence of 0+ age-class specimens as well as the rather poorly presented age-class 1+ might be explained by the selectivity of the fishing gear and ability of the smaller fish to escape the net and/or a different spatial distribution of young fish. Regarding the age-class proportions in the investigated sample, it seemed that specimens of age-class 2+ were fully fished while the rest of the age-classes in this area followed the expected fishing pattern (Figure 8). The same underrepresentation of the younger ages was also noticed in the Hellenic Seas (Kiparissis et al., Reference Kiparissis, Tsarpes and Tsimenidis2000).
The results of otolith weight in comparision with length, weight and age of the fish indicate that otolith weight could be an accurate indicator of somatic growth. This could be explained by the fact that otolith weight is the most sensitive to variations in growth rates and best related to changes in fish metabolism (Boehlert, Reference Boehlert1985; Reznik et al., Reference Reznick, Lindbeck and Bryga1989; Secor & Dean, Reference Secor and Dean1989; Pawson, Reference Pawson1990; Fletcher, Reference Fletcher1991).
Scomber colias growth rates rather similar to those revealed in this study have also been observed for both sexes in the other regions of this species distribution (Gagliardi & Cousseau, Reference Gagliardi and Cousseau1970; Perrotta & Forciniti, Reference Perrotta and Forcinitti1989). Growth parameters for all analysed material given in this paper were compared with the results of the other authors in other study areas (Table 4). It was obvious that S. colias grow differently in the different geographical areas. Generally, the growth coefficient (K) is considered a genetic feature of a species, whilst L∞ is phenotypic and can be limited by environmental conditions. Temperature is stated by many authors (Gunter, Reference Guntner1950; Bull, Reference Bull1952; Taylor, Reference Taylor1959) to be the most limiting factor as a higher temperature stimulates a premature onset of sexual maturity and therefore slower growth and smaller maximum length. Also, Beverton & Holt (Reference Beverton, Holt, Wolstenholme and O'Connor1959) considered that the changes in growth intensity are directly connected with fishing effort. As fishing effort increases, the abundance of a species decreaseas, which can lead to faster growth of the species. Nevertheless, there was a similarity between the results obtained in this study and those reported for S. colias populations in the Mediterranean (Kipparissis et al., Reference Kiparissis, Tsarpes and Tsimenidis2000). This was expected since genetic and morphological data revealed the clear existence of Mediterranean and Southern Atlantic chub mackerel groups (Scoles et al., Reference Scoles, Collette and Graves1998; Roldan et al., Reference Roldan, Perotta, Cortey and Carles2000). Furthermore, similarity was also found in the parameter Φ′ evaluation of errors in estimations of the fish growth parameters. Namely, Moreau et al. (Reference Moreau, Bambino, Pauly, Maclean, Dizon and Hosillos1986) established that species within the same family are expected to have similar Φ′ values. Hence, Φ′ values from this investigation were almost the same as that obtained in Greece (Kiparissis et al., Reference Kiparissis, Tsarpes and Tsimenidis2000).
Results of previously reported growth parameters (L∞, the asymptotic length; K, the growth constant; t0, the ‘age’ at which LT = 0; growth performance index phi-prime Φ′) of Scomber colias in different areas of habitat together with results for chub mackerel in the eastern Adriatic Sea during the investigation period from January 2006 to December 2008.
The ideal situation for a population is when the fishing mortality is equal to the natural mortality, meaning that fishing activities exploit the part of the population which is lost anyway by natural mortality. With knowledge of these parameters, one can control the population stock and determine the right exploitation rate which permits the optimum catch whilst saving the reproductive proportion of the population. Scomber colias males during this investigation had an ideal ratio of M = F = 0.46. On the contrary, females as well as the overall material did not (M = 0.32, F = 0.71 and M = 0.35, F = 0.56, respectively). This may indicate that the females are more harvested than the males in this area, which could lead to a reduction in the number of females which could threaten the reproductive advantage of the population (Murua et al., Reference Murua, Kraus, Saborido-Rey, Witthames, Thorsen and Junquera2003).
The natural mortality of 0.35 estimated in this study was not in agreement with the natural mortality of 0.19 found in the area of the Azores for the same species (Carvalho et al., Reference Carvalho, Perrotta and Isidro2002). Observed differences might be due to the fact that natural mortality varies with age, density, disease, parasites, food supply, predator abundance, water temperature, fishing pressure, sex and size (Vetter, Reference Vetter1988).
The limit reference point (LRP) for S. colias in this area of investigation was estimated to be 0.23, which indicated that only approximately 23% of the available stock of chub mackerel is harvested on an annual basis, and since this is lower than the threshold for pelagic fish species (0.4: Patterson, Reference Patterson1992), an increase in the fishing effort can be cautiously recommended for S. colias in this area.
The present data provide a necessary foundation for determining the growth and mortality of S. colias in the Adriatic Sea. However, this stock needs to be further investigated as S. colias is often caught as a by-catch of purse seiners targeting sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus). Since sardine and anchovy are the most commercially important fish species in the whole of the Mediterranean and Adriatic Seas, their exploitation could affect the chub mackerel population. So, management of these commercially important species should take into account its impact on the management of S. colias, which should be based on this species' population dynamics.
ACKNOWLEDGEMENTS
This study was supported by the Ministry of Science, Education and Sports of the Republic of Croatia, as part of the research project ‘Biodiversity and Management of Pelagic and Demersal Resources of the Adriatic Sea (001-0013077-0532)'. The referees' comments and suggestions are greatly appreciated.
