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Age, growth and reproduction of the sand smelt Atherina boyeri Risso, 1810 in the Gomishan wetland – southeast Caspian Sea
Estuarine, Coastal and Shelf Science 81 (2009) 457–462
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Age, growth and reproduction of the sand smelt Atherina boyeri Risso, 1810 in the Gomishan wetland – southeast Caspian Sea Rahman Patimar a, *, Morteza Yousefi b, Seyyed Morteza Hosieni c a
Department of Natural Sciences, Gonbad Institutes of Higher Education, Gorgan University of Agricultural Sciences and Natural Resources, Shahid Fallahy Street, Gonbad, Iran Department of Fisheries, Faculty of Natural Resources, Tarbiat Modarres University, Tehran, Iran c Department of Fisheries, Faculty of Fisheries and Environments, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 June 2008 Accepted 8 December 2008 Available online 14 December 2008
A total of 2256 specimens of Atherina boyeri caught in Gomishan wetland (a marsh lagoon located at the southeast Caspian Sea) during spawning season from February to August 2007 were examined for lifehistory attributes. The population has a 4-year life cycle. Length–weight relationship was estimated as W ¼ 0.0053TL3.0181 for males and W ¼ 0.0050TL3.063 for females, being allometrically positive for both sexes. The von Bertalanffy growth function fitted to back-calculated size at age data was: Lt ¼ 155.17 [1 exp 0.28(t þ 0.738)] and Lt ¼ 162.77[1 exp 0.27(t þ 0.727)] for males and females respectively. The sex ratio was 1:1.30 in favor of females. The reproductive season, evaluated from GSI, extended from March to July, with a peak in March. The average absolute and relative fecundities were 2976 eggs and 874 eggs g1 of body weight respectively. The diameter of oocytes ranged from 0.03 to 0.20 mm with a mean value of 0.68. The life-history patterns of A. boyeri in the population under study imply that the population of this species in the southeast Caspian Sea differs markedly from those of other localities of its range distribution. The differences were thought to be due to differences in geographical locations. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Atherina boyeri age growth reproduction spawning Gomishan wetland Caspian Sea
1. Introduction Atherina boyeri is a euryhaline teleost fish which commonly inhabits coastal and estuarine waters. Its distribution ranges from the western Atlantic coast of Spain to Mauritania and Madeira, being found throughout the Mediterranean and Black Sea. Some isolated populations have been reported from the coast of England and the Netherlands (Quignard and Pras, 1986). The fish were first translocated from the Black Sea to Caspian Sea in 1953 and 1954 by the Soviet authorities (Markevich, 1977). Within such a broad geographical distribution, sand smelt populations are subject to variety of climatic conditions, forming different local populations. The Caspian sand smelt has been previously described as the species Atherina mochon pontica, but it is now considered to be a phenotypic variant of A. boyeri (Kiener and Spillmann, 1972). In the south Caspian basin the fish, because of its high abundance and not being subject to commercial exploitation, is considered to be in the category of ‘‘least concern’’ of the IUCN categories (Kiabi et al., 1999a). The species is common in the coastal and estuarine waters of the Caspian Sea. During the spawning season, it is found in high abundance in the Gomishan wetland and Gorgan bay which are
* Corresponding author. E-mail address: [email protected] (R. Patimar). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.12.007
considered as the most important spawning grounds for this species in the southeast Caspian Sea (Kiabi et al., 1999a). Coastal wetlands of the south Caspian Sea are an essential habitat for a range of fauna, A. boyeri is one of this fauna, and accurate information on growth and reproduction of this species would be a useful guideline in conservation and management of fish populations and wetland ecosystem. We hypothesized that the south Caspian basin may contribute to habitat-specific variation in life-history traits of sand smelt. The aim of this study was to describe the age structure, growth and reproduction of the sand smelt population in the Gomishan wetland, which provides an insight into the life history of this species, and to test whether the south Caspian region has developed locally different life-history strategies of this species.
2. Material and methods The study was carried out in the Gomishan wetland which is situated at the southeast of Caspian Sea (latitude: from 37, 90 , 900 to 37, 200 , 200 ; longitude: from 53 , 540 , 3400 to 53 , 580 , 5400 ). It is a type of large shallow marsh lagoon with a surface area of 20,000 ha, average depth of 100 cm, and maximum depth of 250 cm (Scott, 1995; Kiabi et al., 1999b). The following measurements were taken at the wetland monthly, and for three times at each sampling effort: pH (Corning
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
3. Results In the Gomishan wetland, during this study, temperature ranged from 9.02 to 30.50 C, salinity from 20.07 to 24.12, and pH from 8.14 to 8.59.
Frequency (% of total number)
12 10 Female Male
8 6 4 2
-3 40 9 -4 45 4 -4 50 9 -5 55 4 -5 60 9 -6 65 4 -6 70 9 -7 75 4 -7 80 9 -8 85 4 -8 90 9 -9 95 4 10 -99 0 10 -10 5 4 11 -10 0 9 11 -11 5 4 12 -11 0 9 12 -12 5- 4 12 9
0 35
410 pH meter), temperature ( C), and salinity (using the Practical Salinity Scale) (water quality checker U-10). Sampling was carried out using a small beach seine (30 m long, 2 m depth and mesh size of 3 mm knot to knot) between early March and late August 2007. It was set out in such a way that the drag line of one wing remained fastened to the beach, while one wing, the net bag, and then the other wing with its drag line are taken out in a wide arc and then brought back to the beach. Beach seining was limited between March and August, because before March and after August, the sand smelt was very scarce. Additional specimens (n ¼ 32) were collected from a trawling survey in Gomishan lagoon during February 2007. In the laboratory, total length (TL) was measured to the nearest 1 mm for all fish sampled. Total weight, weight of gonads and its subsamples were recorded with an electronic analytical balance to the nearest 0.01 g. For the age determination scales and opercula were used. The relationship between the total length and total weight were determined by fitting the data to a potential relationship in the form of: W ¼ aLb, where W is the weight in grams, L the total length in centimeters, a and b are the parameters to be estimated, with b being the coefficient of allometry based on the test given by Pauly (1984). The lengths-at-age were back-calculated using the equation Li ¼ SiS1 c (Lc c) þ c, where Li is the total length of the fish at age i, Lc the total length of the fish at capture, Si the largest radius of the scale at age i, Sc the largest radius of the scale at capture and c intercept of the regression of body lengths on scale radii (Johal et al., 2001). Length-atage was modeled using three key parameters of von Bertalanffy growth model (Bertalanffy, 1938) described as Lt ¼ LN ½1 eKðtt0 Þ , where Lt is the length-at-age t, LN the maximum theoretical length, K is the body growth coefficient synonym to the rate at which LN is attained and t0 is the age of zero length fish (Ricker, 1975). Growth performance index (40 ) was computed from the equation: 40 ¼ ln k þ 2ln LN (Munro and Pauly, 1983). Sex was determined by examination of the gonads. Maturity stages were estimated according to the Nikolsky (1963) scale. Gonadosomatic index (GSI %) ¼ (gonad weight/total body weight) 100 was calculated for each fish and all values were averaged for each sampling date. Atherina boyeri is a batch spawner, its spawning takes place over a long period of 2–3 months (Creech, 1992). Therefore, in order to decrease the error due to multiple spawning, we used ovaries of 172 ripe specimens with IV maturity stage, from females caught in March in order to estimate absolute and relative fecundities. The gonads were removed, weighed and then placed in Gilson’s fluid for 3–4 weeks to harden eggs and dissolve ovarian membranes. The peritoneum was removed and individual eggs were released from the egg mass. The number of eggs was estimated by gravimetric method, using three pieces removed from the ovary. Relative fecundity index was calculated as RF ¼ AF/TW, where AF is absolute fecundity and TW total weight (Bagenal and Tesch, 1978). Egg diameter was examined by measuring 20–30 eggs taken randomly from pieces of the ovary of 399 ripe females caught in March–July. Measurements were made to the nearest 0.05 mm with an ocular micrometer microscope. Comparison of GSI between months was carried out by analysis of variance (ANOVA). An analysis of co-variance (ANCOVA) was performed to test significance differences in weight–length relationships and GSI values between the sexes. The overall sex ratio was assessed using Chi square test (Zar, 1984). Statistical analyses were performed with SPSS 11.5 software package and a significant level of 0.05 was accepted.
Length class (mm) Fig. 1. Total length (mm) frequency of males and females of sand smelt, A. boyeri in the Gomishan wetland – Southeast Caspian Sea (number of specimens ¼ 2256).
The sand smelt caught ranged in size from 37 to 128 mm TL and in total weight from 0.26 to 11.69 g. Of the 2256 specimens collected, 979 (43.40%) were identified as males, ranging from 37 to 120 mm and 0.26 to 9.01 g, while 1277 (56.60%) were females ranging from 44 to 128 mm and 0.40 to 11.69 g. Females were slightly longer and heavier than males. Dominant length class was 60–64 mm for both sexes (Fig. 1). Age was determined from 921 specimens (40.82% of total specimens). Four age groups (1þ–4þ) were identified in both sexes. The percentage occurrence of the age groups (1þ, 2þ, 3þ, and 4þ) was 43.75, 47.80, 6.04 and 2.41% in males and 18.55, 67.21, 11.21 and 3.03% in females respectively. Significant differences were obtained from the statistical comparison of length–weight relationships between males and females (ANCOVA, F ¼ 203.171, p < 0.05). The b-values of the relationships imply that the body shape of both sexes displays positive allometric form, with 95% confidence interval for b-value of 2.991–3.055 for males and of 3.030–3.096 for females (t-test, tmale ¼ 8.595, tfemale ¼ 2.889, p < 0.05) (Fig. 2). The mean back-calculated total lengths of each group were smaller than the observed lengths (Table 1). The back-calculations showed rapid growth during the first year of life and a steady, less rapid decline in the relative length increments occurred during
15
Female: W = 0.005TL3.0628 R2 = 0.96 N=1278
12
Total weight (g)
458
9
Male: W = 0.0053TL3.0181 R2 = 0.96 N=980
6
3
0
0
3
6
9
12
15
Total length (cm) Fig. 2. Relative growth curves (Total length–Total weight) for A. boyeri in the Gomishan wetland – southeast Caspian Sea.
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462 Table 1 Mean back-calculated lengths (mm) for age (S.D.) of A. boyeri during spawning period in the Gomishan wetland – southeast Caspian Sea. 1þ
3þ
10
4þ
Female
8 64.22 11.01 86.45 12.08 103.50 11.50 114.58 18.05 61.03 6.12
82.99 7.17
Male
6
102.67 10.08 113.75 11.17
Fig. 4. Variation of mean gonadosomatic index (GSI %) of male and female of A. boyeri in the Gomishan wetland – southeast Caspian Sea.
4. Discussion This study has established key population parameters of A. boyeri in the southeast Caspian Sea. Variation in life-history parameters of species could be explained on the basis of the different exploitation patterns and/or ecological conditions. The sand smelt is not subject to commercial exploitation in the south Caspian basin and therefore environmental conditions of this basin seem to be main factors affecting the life-history parameters of the fish. Henderson and Bamber (1987) showed that sand smelt populations vary greatly in longevity and maximum size attained with a trend to reduced growth along an oceanic-coastal–estuarinefreshwater habitat range. These attributes were related to habitat quality, such as salinity and temperature. The comparison of the population under consideration with other sand smelt populations (Henderson and Bamber, 1987) shows that the Caspian sand smelt is similar to the English channel populations, reaching a maximum length of 128 mm and an age of 4þ years. The largest age and size (length and weight) of A. boyeri in the southeast Caspian Sea are different from those of coastal populations in the Mediterranean Sea (Henderson and Bamber, 1987). Thus the majority of the specimens were between 1 and 2 ages indicates that the population was mostly young individuals. The low proportion of age 4þ specimens suggests that very few individuals survive to a maximum age, as is typical of most fishes (Matthews, 1998). This also concurs with the general patterns observed in most other populations of sand smelt throughout their distribution range (Henderson and Bamber, 1987). The exponents of total length–somatic weight relationship of A. boyeri, estimated in the wetland, showed that the somatic weight grows allometrically (Ricker, 1975) with the total length. Differences between males and females in the TL–W relationship are
Female
Lt=155.17[1-exp-0.28(t+0.738)]
0
1
2
3
Age (year)
4
Total length (mm)
Total length (mm)
Male L
5
us t
Month
subsequent years. The mean back-calculated length of individuals assigned to each age group was used to fit the von Bertalanffy growth model (Fig. 3). Males grew faster than females (kmale > kfemale), while asymptotic value of length was higher for females than for males. The 40 value for the females (8.87) was slightly higher than that of males (8.82). All individuals were sexed, the overall ratio of males to females was 1:1.30 and c2 analysis showed significant differences from the ratio 1:1 (c2 ¼ 39.36, p < 0.05). Considering the distribution of length classes according to the sex (Fig. 1), an unequal sex ratio was observed among the classes, females were dominant in the older size classes (60–64 mm), males in the younger (50–59 mm). Significant changes were obtained in the temporal variation of gonad activity (ANOVA, Ffemale ¼ 39.44, Fmale ¼ 3.51, p < 0.05). The GSI values of males were significantly lower than those of females using the size of the fish as covariate (ANCOVA, F ¼ 27.44, p < 0.05). The highest average values of GSI were 3.61 and 7.12 in March for males and females respectively. The GSI of both sexes followed almost the same pattern (Fig. 4). The reproductive period for this species in the wetland is thus from March to July when GSI is considerably higher. It thereafter decreases in August showing start of the resting period. Different kinds of eggs were found in the ovary during the spawning period from March to July (Fig. 5). In this period, the diameter of oocytes ranged from 0.03 to 0.20 mm with a mean value of 0.6773 0.3147 (Fig. 5). Absolute fecundity increased with age; a minimum value of 492 eggs was from a 1þ year old female weighing 2.50 g and a maximum value of 10,188 eggs was from 4þ year old fish weighing 8.12 g (Table 2). The mean value of absolute fecundity was 2796.73 1900.36 (S.D.) eggs/female. The regression between egg number and fish size (total length and weight) was statistically significant (p < 0.05) (Fig. 6). Fecundity relative to total weight fluctuated from 195 to 1726 eggs g1, with a mean value of 784.09 272.84 (S.D.). The relationship of relative fecundity with fish size (total length and total weight) was found to be statistically significant (Fig. 7).
180 160 140 120 100 80 60 40 20 0
Au g
y
e
Ju l
M
Fe
br
ar
ry
117.01 12.04
Ju n
0
105.86 8.97
M ay
61.48 5.45 83.25 8.02
il
2
Ap r
64.88 12.21 87.89 11.50 104.45 10.22 116.02 18.42
ch
4
ua
Males Mean observed TL, mm Mean backcalculated TL, mm Females Mean observed TL, mm Mean backcalculated TL, mm
2þ
12
GSI
Age (year)
459
180 160 140 120 100 80 60 40 20 0
Lt=162.77[1-exp-0.27(t+0.727)]
L
0
1
2
3
4
5
Age (year)
Fig. 3. von Bertalanffy length-at-age growth curves for males and females A. boyeri in the Gomishan wetland – southeast Caspian Sea.
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
May
1.80-1.89
1.90-1.99
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
June
Egg diameter size group (mm)
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
0.10-0.19
Frequency (%)
Number of specimens=31 Number of eggs=694 Mean egg diameter mm (S.D.): 0.6178mm (0.2642)
20 18 16 14 12 10 8 6 4 2 0
1.90-1.99
1.80-1.89
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
0.10-0.19
1.90-1.99
April
Frequency (%)
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
Egg diameter size group (mm)
Number of specimes=101 Number of eggs=2105 Mean egg diameter mm (S.D.):0.6908mm (0.3169)
20 18 16 14 12 10 8 6 4 2 0
1.80-1.89
Egg diameter size group (mm)
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
Number of specimens=60 Number of eggs=1514 Mean egg diameter mm (S.D.): 0.6283mm (0.2671)
0.10-0.19
Frequency (%)
20 18 16 14 12 10 8 6 4 2 0
1.90-1.99
1.80-1.89
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
Number of specimens:172 Number of eggs:4177 Mean of egg diameter mm (S.D.): 0.7147mm (0.3583)
0.10-0.19
Frequency (%)
March 20 18 16 14 12 10 8 6 4 2 0
1.30-1.39
460
Egg diameter size group (mm)
1.90-1.99
1.80-1.89
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0.10-0.19
20 18 16 14 12 10 8 6 4 2 0 0-0.09
Frequency (%)
July Number of specimens=35 Number of eggs=912 Mean egg diameter mm (S.D.): 0.6121mm (0.2640)
Egg diameter size group (mm) Fig. 5. Size frequency distribution of oocytes diameters of A. boyeri during spawning period in the Gomishan wetland – southeast Caspian Sea.
explained by the differences in size distribution of the two sexes as a consequence of inter-sexual differences in growth, suggesting the convenience of using the appropriate estimate from those proposed for each group when calculating weight by sex. The ‘‘b’’ values estimated in the studied population are different from those Table 2 Total number of oocytes for each month of reproductive season of A. boyeri population in the Gomishan wetland – southeast Caspian Sea. X: mean total number of oocytes, S.D.: standard deviation. Age
n
Minimum
Maximum
X S:D:
1þ 2þ 3þ 4þ
58 112 49 16
508 880 1358 2170
3780 7666 7900 10,188
1440.69 2682.32 3989.14 6374.58
695.97 1566.53 1852.77 2775.89
found in European regions (Palmer and Culley, 1983; FernandezDelgado et al., 1988; Creech, 1992; Leonardos and Sinis, 2000; Leonardos, 2001; Andreu-Soler et al., 2003; Bartulovic et al., 2004; Koutrakis et al., 2004); all estimated positive allometric growth. Gon and Ben-Tuvia (1983) reported a negative allometric growth (bsexes combined ¼ 2.93) for a sand smelt population in the Bardawil lagoon on the Mediterranean coast of Sinai where the water is hyper-saline (40–110). It seems that geographic location and associated environmental conditions can significantly affect the value of ‘‘b’’ in A. boyeri populations; therefore, the variations in the ‘‘b’’ exponent between populations can be attributable to species responses to different habitats. Fitting the von Bertalanffy growth formula to back-calculated lengths resulted in the estimation of higher values of maximum theoretical length than the maximum observed total lengths.
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
12000
AF= 81.99TL - 3870.9 R2 = 0.3928 F=109.34 N=172
10000 8000
Absolute fecundity
Absolute Fecundity
12000
6000 4000 2000 0
461
AF = 639.34TW + 495.77 R2 = 0.4335 F=129.32 N=172
10000 8000 6000 4000 2000 0
0
20
40
60
80
100
120
140
0
2
4
Total length (mm)
6
8
10
12
Total weight (g)
Fig. 6. Relationship between egg number and fish total length (mm) and total weight (g) of female A. boyeri in the Gomishan wetland – southeast Caspian Sea.
2000 1800 1600 1400 1200 1000 800 600 400 200 0
RF = -8.3983TL + 1460.6 R2 = 0.1945 F=31.21 N=172
0
30
60
90
Total length (mm)
120
150
populations of this species; 1:1.24 in the Mesolongi and Etolikon lagoons – western Greece (Leonardos and Sinis, 2000), 1:1.30 in the estuary of the Mala Neretva River – middle-eastern Adriatic, Croatia (Bartulovic et al., 2004) and 1:2.5 in an estuarine system of northern Greece (Koutrakis et al., 2004). Sex ratio is thus significantly different between populations of this species throughout its range distribution. From the maximum recorded GSI values it is evident that the reproductive season of the A. boyeri extends from March to July. Nikolsky (1963) pointed out that the spawning characteristics of a fish vary in respect to their species and ecological characteristics of water system in which they live. In comparison with other fish species inhabiting south Caspian Sea, A. boyeri has an extended spawning season (w4 months). This extended spawning of population appears to be a feature of the biology of this species and may be interpreted as an increase of reproductive effort (Fernandez-Delgado et al., 1988; Creech, 1992). The observed size range of eggs 0.03–2.00 mm was different from that of 0.08–2.08 mm reported by Creech (1992) in Aberthaw lagoon in south Wales and that of 0.1–1.80 mm found by Palmer and Culley (1983) at Oldbury-on Severn in England. The great heterogeneity in egg size of A. boyeri is indicative of a batch spawner. Even though a number of problems come from invalid estimates of fecundity in batch spawners that are derived from either the total number of eggs of batch sizes including incomplete ovulation (Yamamoto and Yamazaki, 1961), discontinuous addition of recruitment stock eggs to the spawning egg stock (Hunter and Goldburg, 1979) and atresia (Macer, 1974), we made an attempt to estimate absolute fecundity in the present study. For Caspian sand smelt absolute fecundity was positively correlated to fish size (length or weight) and this positive correlation remains consistent even when considering absolute fecundity and fish size relationships separately for each age groups. While a negative effect of fish size on relative fecundity was observed for the fish, an increase in female size (total length or/and weight) implied a decrease of
Relative fecundity
Relative fecundity
Considering an LN value 30% higher than the maximum lengths observed (Garcia-Rodriguez et al., 2005), the obtained results are reliable values for both sexes. The LN value of female was calculated to be higher than that of males. The higher coefficient (k) for males emphasizes that they grow rapidly initially and approach their asymptotic length (LN) earlier in the life. Comparison of k and LN from different populations in the range distribution of the sand smelt shows that the growth patterns vary greatly in the estimated parameters (Table 3). These differences may be regarded as biological feature of the A. boyeri in different habitats, as a trade-off between growth rate (k) and maximum size (LN) is often found. Optimum ecological conditions cause a shift towards larger maximum size. The study area in the southeast Caspian Sea is an isohaline coastal wetland with almost stable conditions which seems to be an optimum habitat for this species resulting greater longevity and maximum size being attained. The index of growth performance (40 ) is to be considered a useful tool for comparing the growth curves of different populations of the same species and/or of different species belonging to the same family (Sparre and Venema, 1998). In general, the values of the growth performance index from different geographical areas show that growth patterns are different for the different stocks, but similar for the stocks of neighboring localities. By calculation from published data of k and LN, in different populations of the sand smelt (Table 3), the index ranges from 8.23 to 9.50, and the value obtained of the index for the present population occurs within this range. In the Gomishan wetlands, the overall sex ratio is unbalanced in favor of females, probably as a consequence of higher survival rate and greater longevity of females, or the greater endurance of females to environmental variability. Even though Fernandez-Delgado et al. (1988) and Creech (1992) reported no significant deviation from parity in the ratio of males to females of this species in the Guadalquivir river (Spain) and Bristol channel (south Wales) respectively, dominance of females has been reported in some
2000 1800 1600 1400 1200 1000 800 600 400 200 0
RF = -55.812TW + 979.39 R2 = 0.1559 F=40.81 N=172
0
3
6
9
12
Total weight (g)
Fig. 7. Relationship between relative fecundity and fish total length (mm) and total weight (g) of female A. boyeri in the Gomishan wetland – southeast Caspian Sea.
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R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
Table 3 The growth parameters (LN, k, t0) of the A. boyeri in this study and in studies by other authors. Study area
Sex
LN (mm)
k (year1)
t0 (years)
40
Henderson and Bamber (1987)
English Channel
Sexes combined
138
0.7
–
9.49
Gon and Ben-Tuvia (1983),b
Bardawil lagoon-Sinai
Sexes combined
42
2.93
–
8.55
Author ,a
Creech (1992)
,b
Aberthaw lagoon, S. Wales
Sexes combined
92
–
–
–
Leonardos and Sinis (2000),a
Mesolongi and Etolikon lagoons, W. Greece
Male Female
74.97 84.58
0.67 0.81
0.46 0.65
8.23 8.66
Leonardos (2001),a
Trichonis lake, W. Greece
Sexes combined
112.40
0.42
0.40
8.58
Andreu-Soler et al. (2003),a
Mar Menor coastal lagoon, SE Iberia Peninsula
Male Female
81.90 84.58
0.91 0.81
0.45 0.65
8.72 8.66
Bartulovic et al. (2004),a
Estuary of the Mala Neretva River (Middle-eastern Adriatic – Croatia
Male Female
99.14 105.77
0.97 1.19
0.19 0.006
9.16 9.50
Koutrakis et al. (2004),a
Vistonis estuarine system, N. Greece
Male Female
128.09 166.54
0.26 0.16
1.64 1.90
9.36 8.40
Present studya
Gomishan wetland, SE Caspian Sea
Male Female
155.17 162.77
0.28 0.27
0.738 0.727
8.82 8.87
a b
Using TL. Using SL.
relative fecundity. It can be hypothesized, however, that the largest spawner was not able to increase the quantity of eggs per unit somatic weight proportionally to the absolute number of eggs and thus, the egg quantity relative to fish size decreased. This means that total energetic investment in reproduction tends to be higher in the larger member of the fish, but proportional energetic investment in reproduction (as energy allocation per unit of fish size) tends to decrease with increasing in fish size. In conclusion, the life-history pattern of sand smelt in the Gomishan wetland as a representative of Caspian sand smelt differs markedly from those of many other populations of the species from European regions. This pattern is important with respect to the management of the species. It can be concluded that the life-history patterns of this species varied relatively to the habitat to which they exposed. The variations relating to growth and reproduction may be interpreted as phenotypic plasticity and adaptation to local selective pressure. References Andreu-Soler, A., Oliva-Paterna, F.J., Fernandez-Delgado, C., Torralva, M., 2003. Age and growth of the sand smelt, Atherina boyeri (Risso 1810), in the Mar Menor coastal lagoon (SE Iberian Peninsula). Journal of Applied Ichthyology 19, 202–208. Bagenal, T., Tesch, F., 1978. Methods for Assessment of Fish Production in Fresh Waters. IBP Handbook 3. Blackwell, Oxford. 365pp. Bartulovic, V., Glamuzina, B., Conides, A., Dulcic, D., Njire, D., Kozul, V., 2004. Age, growth, mortality and sex ratio of sand smelt, Atherina boyeri Risso, 1810 (Pisces: Atherinidae) in the estuary of the Mala Neretva River (middle-eastern Adraitic, Croatia). Journal of Applied Ichthyology 20, 427–430. Bertalanffy, L., 1938. A quantitative theory of organic growth (inquiries on growth laws II). Human Biology 10, 181–212. Creech, S., 1992. A study of the population of Atherina boyeri (Risso, 1810) in Aberthaw lagoon, on the Bristol Channel, in south Wales. Journal of Fish Biology 41, 277–286. Fernandez-Delgado, C., Hernando, J.A., Herrera, M., Bellido, M,, 1988. Life-history patterns of the sand smelt Atherina boyeri Risso, 1810 in the Estuary of the Guadalquiver river, Spain. Estuarine, Coastal and Shelf Science 27, 697–706. Garcia-Rodriguez, M., Pereda, P., Landa, J., Esteban, A., 2005. On the biology and growth of the anglerfish Lophiu budegassa Spinola, 1807 in the Spanish Mediterranean: a preliminary approach. Fisheries Research 71, 197–208. Gon, O.A., Ben-Tuvia, A., 1983. The biology of Boyer’s sand smelt, Atherina boyeri Risso, in the Bardawil lagoon on the Mediterranean coast of Sinai. Journal of Fish Biology 22, 537–547. Henderson, P.A., Bamber, R.N., 1987. On the reproductive biology of the sand smelt Atherina boyeri Risso (Pisces: Atherinidae) and its evolutionary potential. Biological Journal of the Linnean Society 32, 395–415.
Hunter, J.R., Goldburg, S.R., 1979. Spawning incidence and batch fecundity in the northern anchovy, Engraulis mordax. Fishery Bulletin 77, 641–652. Johal, M.S., Esmaeili, H.R., Tandon, K.K., 2001. A comparison of back-calculated lengths of silver carp derived from bony structures. Journal of Fish Biology 59, 1483–1493. Kiabi, B.H., Abdoli, A., Naderi, M., 1999a. Status of the fish fauna in the south Caspian Basin of Iran. Zoology in the Middle East 18, 57–65. Kiabi, H.B., Ghaemi, R.A., Abdoli, A., 1999b. Wetland and Riverian Ecosystems of Golestan Province. Department of the Environment, Gorgan. 182pp (in Persian). Kiener, A., Spillman, C.J., 1972. Note complementaire a l’etude systematique et ecologique d’Atherina boyeri Risso (Poissons, Cyprinidae) dan sa zone de dispersion actuella. Bulletin du National d’Histoire Naturelle Zoology 41 (55), 563–580. Koutrakis, E.T., Kamidis, N.I., Leonardos, I.D., 2004. Age, growth and mortality of a semi-isolated lagoon population of sand smelt, Atherina boyeri (Risso, 1810) (Pisces: Atherinidae) in an estuarine system of northern Greece. Journal of Applied Ichthyology 20, 382–388. Leonardos, I.D., 2001. Ecology and exploitation pattern of a landlocked population of sand smelt, Atherina boyeri (Risso, 1810), in Trichonis Lake (western Greece). Journal of Applied Ichthyology 17, 262–266. Leonardos, I., Sinis, A., 2000. Age, growth and mortality of Atherina boyeri Risso, 1810 (Pisces: Atherinidae) in the Mesolongi and Etolikon lagoons (W. Greece). Fisheries Research 45, 81–91. Macer, C.T., 1974. The reproductive biology of the hors mackerel Trachurus trachurus (L.) in the North Sea English Channel. Journal of Fish Biology 6, 415–438. Markevich, N.B., 1977. Some morphological indices of the silverside Atherina movhon pontica, in the Aral Sea in connection with age structure of its population. Journal of Ichthyolgia 17, 618–626. Matthews, W.J., 1998. Patterns in Freshwater Fish Ecology. Chapman and Hall, London. 756pp. Munro, J.L., Pauly, D., 1983. A simple method for comparing growth of fishes and invertebrates. ICLARM Fishbyte 1, 5–6. Nikolsky, G.V., 1963. The Ecology of Fishes (L. Birkett, Trans.). Academic Press, London. 352pp. Palmer, C.J., Culley, M.B., 1983. Aspects of the biology of the sand smelt Atherina boyeri Risso, 1810 (Teleostei: Atherindae) at Oldbury-on-Severn, Gloucestershire, England. Estuarine, Coastal and Shelf Science 16, 163–172. Pauly, D., 1984. Fish population dynamics in tropical waters: a manual for use for programmable calculators. ICLARM Studies and Reviews 8 325pp. Quignard, J.P., Pras, A., 1986. Atherinidae. In: Whitehead, P., Bauchot, M.L., Hureau, J.C., Nielsen, J., Tortonese, E. (Eds.), Fishes of the North-eastern Atlantic and Mediterranean. UNESCO, Paris, pp. 1207–1210. Ricker, W.E., 1975. Computation and interpretation of biological statistics of fish populations. Bulletin of Fisheries Research Board of Canada 191, 235–264. Scott, D.A., 1995. A Directory of Wetlands in the Middle East. IUCN, the World Conservation Union. 560pp. Sparre, P., Venema, S.C., 1998. Introduction to tropical fish stock assessment. Part 1, Manual FAO Fisheries Technical Papers No. 306, Rev. 2, 407pp. Yamamoto, K., Yamazaki, F., 1961. Rhythm of development in the oocyte of the goldfish, Carassius auratus. Bulletin of the Faculty of Fisheries Hokkaido University 12, 93–110. Zar, J.H., 1984. Biostatistical Analysis. Prentice Hall, Englewoods Cliffs, NJ. 717pp.
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Age, growth and reproduction of the sand smelt Atherina boyeri Risso, 1810 in the Gomishan wetland – southeast Caspian Sea Rahman Patimar a, *, Morteza Yousefi b, Seyyed Morteza Hosieni c a
Department of Natural Sciences, Gonbad Institutes of Higher Education, Gorgan University of Agricultural Sciences and Natural Resources, Shahid Fallahy Street, Gonbad, Iran Department of Fisheries, Faculty of Natural Resources, Tarbiat Modarres University, Tehran, Iran c Department of Fisheries, Faculty of Fisheries and Environments, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 June 2008 Accepted 8 December 2008 Available online 14 December 2008
A total of 2256 specimens of Atherina boyeri caught in Gomishan wetland (a marsh lagoon located at the southeast Caspian Sea) during spawning season from February to August 2007 were examined for lifehistory attributes. The population has a 4-year life cycle. Length–weight relationship was estimated as W ¼ 0.0053TL3.0181 for males and W ¼ 0.0050TL3.063 for females, being allometrically positive for both sexes. The von Bertalanffy growth function fitted to back-calculated size at age data was: Lt ¼ 155.17 [1 exp 0.28(t þ 0.738)] and Lt ¼ 162.77[1 exp 0.27(t þ 0.727)] for males and females respectively. The sex ratio was 1:1.30 in favor of females. The reproductive season, evaluated from GSI, extended from March to July, with a peak in March. The average absolute and relative fecundities were 2976 eggs and 874 eggs g1 of body weight respectively. The diameter of oocytes ranged from 0.03 to 0.20 mm with a mean value of 0.68. The life-history patterns of A. boyeri in the population under study imply that the population of this species in the southeast Caspian Sea differs markedly from those of other localities of its range distribution. The differences were thought to be due to differences in geographical locations. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Atherina boyeri age growth reproduction spawning Gomishan wetland Caspian Sea
1. Introduction Atherina boyeri is a euryhaline teleost fish which commonly inhabits coastal and estuarine waters. Its distribution ranges from the western Atlantic coast of Spain to Mauritania and Madeira, being found throughout the Mediterranean and Black Sea. Some isolated populations have been reported from the coast of England and the Netherlands (Quignard and Pras, 1986). The fish were first translocated from the Black Sea to Caspian Sea in 1953 and 1954 by the Soviet authorities (Markevich, 1977). Within such a broad geographical distribution, sand smelt populations are subject to variety of climatic conditions, forming different local populations. The Caspian sand smelt has been previously described as the species Atherina mochon pontica, but it is now considered to be a phenotypic variant of A. boyeri (Kiener and Spillmann, 1972). In the south Caspian basin the fish, because of its high abundance and not being subject to commercial exploitation, is considered to be in the category of ‘‘least concern’’ of the IUCN categories (Kiabi et al., 1999a). The species is common in the coastal and estuarine waters of the Caspian Sea. During the spawning season, it is found in high abundance in the Gomishan wetland and Gorgan bay which are
* Corresponding author. E-mail address: [email protected] (R. Patimar). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.12.007
considered as the most important spawning grounds for this species in the southeast Caspian Sea (Kiabi et al., 1999a). Coastal wetlands of the south Caspian Sea are an essential habitat for a range of fauna, A. boyeri is one of this fauna, and accurate information on growth and reproduction of this species would be a useful guideline in conservation and management of fish populations and wetland ecosystem. We hypothesized that the south Caspian basin may contribute to habitat-specific variation in life-history traits of sand smelt. The aim of this study was to describe the age structure, growth and reproduction of the sand smelt population in the Gomishan wetland, which provides an insight into the life history of this species, and to test whether the south Caspian region has developed locally different life-history strategies of this species.
2. Material and methods The study was carried out in the Gomishan wetland which is situated at the southeast of Caspian Sea (latitude: from 37, 90 , 900 to 37, 200 , 200 ; longitude: from 53 , 540 , 3400 to 53 , 580 , 5400 ). It is a type of large shallow marsh lagoon with a surface area of 20,000 ha, average depth of 100 cm, and maximum depth of 250 cm (Scott, 1995; Kiabi et al., 1999b). The following measurements were taken at the wetland monthly, and for three times at each sampling effort: pH (Corning
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
3. Results In the Gomishan wetland, during this study, temperature ranged from 9.02 to 30.50 C, salinity from 20.07 to 24.12, and pH from 8.14 to 8.59.
Frequency (% of total number)
12 10 Female Male
8 6 4 2
-3 40 9 -4 45 4 -4 50 9 -5 55 4 -5 60 9 -6 65 4 -6 70 9 -7 75 4 -7 80 9 -8 85 4 -8 90 9 -9 95 4 10 -99 0 10 -10 5 4 11 -10 0 9 11 -11 5 4 12 -11 0 9 12 -12 5- 4 12 9
0 35
410 pH meter), temperature ( C), and salinity (using the Practical Salinity Scale) (water quality checker U-10). Sampling was carried out using a small beach seine (30 m long, 2 m depth and mesh size of 3 mm knot to knot) between early March and late August 2007. It was set out in such a way that the drag line of one wing remained fastened to the beach, while one wing, the net bag, and then the other wing with its drag line are taken out in a wide arc and then brought back to the beach. Beach seining was limited between March and August, because before March and after August, the sand smelt was very scarce. Additional specimens (n ¼ 32) were collected from a trawling survey in Gomishan lagoon during February 2007. In the laboratory, total length (TL) was measured to the nearest 1 mm for all fish sampled. Total weight, weight of gonads and its subsamples were recorded with an electronic analytical balance to the nearest 0.01 g. For the age determination scales and opercula were used. The relationship between the total length and total weight were determined by fitting the data to a potential relationship in the form of: W ¼ aLb, where W is the weight in grams, L the total length in centimeters, a and b are the parameters to be estimated, with b being the coefficient of allometry based on the test given by Pauly (1984). The lengths-at-age were back-calculated using the equation Li ¼ SiS1 c (Lc c) þ c, where Li is the total length of the fish at age i, Lc the total length of the fish at capture, Si the largest radius of the scale at age i, Sc the largest radius of the scale at capture and c intercept of the regression of body lengths on scale radii (Johal et al., 2001). Length-atage was modeled using three key parameters of von Bertalanffy growth model (Bertalanffy, 1938) described as Lt ¼ LN ½1 eKðtt0 Þ , where Lt is the length-at-age t, LN the maximum theoretical length, K is the body growth coefficient synonym to the rate at which LN is attained and t0 is the age of zero length fish (Ricker, 1975). Growth performance index (40 ) was computed from the equation: 40 ¼ ln k þ 2ln LN (Munro and Pauly, 1983). Sex was determined by examination of the gonads. Maturity stages were estimated according to the Nikolsky (1963) scale. Gonadosomatic index (GSI %) ¼ (gonad weight/total body weight) 100 was calculated for each fish and all values were averaged for each sampling date. Atherina boyeri is a batch spawner, its spawning takes place over a long period of 2–3 months (Creech, 1992). Therefore, in order to decrease the error due to multiple spawning, we used ovaries of 172 ripe specimens with IV maturity stage, from females caught in March in order to estimate absolute and relative fecundities. The gonads were removed, weighed and then placed in Gilson’s fluid for 3–4 weeks to harden eggs and dissolve ovarian membranes. The peritoneum was removed and individual eggs were released from the egg mass. The number of eggs was estimated by gravimetric method, using three pieces removed from the ovary. Relative fecundity index was calculated as RF ¼ AF/TW, where AF is absolute fecundity and TW total weight (Bagenal and Tesch, 1978). Egg diameter was examined by measuring 20–30 eggs taken randomly from pieces of the ovary of 399 ripe females caught in March–July. Measurements were made to the nearest 0.05 mm with an ocular micrometer microscope. Comparison of GSI between months was carried out by analysis of variance (ANOVA). An analysis of co-variance (ANCOVA) was performed to test significance differences in weight–length relationships and GSI values between the sexes. The overall sex ratio was assessed using Chi square test (Zar, 1984). Statistical analyses were performed with SPSS 11.5 software package and a significant level of 0.05 was accepted.
Length class (mm) Fig. 1. Total length (mm) frequency of males and females of sand smelt, A. boyeri in the Gomishan wetland – Southeast Caspian Sea (number of specimens ¼ 2256).
The sand smelt caught ranged in size from 37 to 128 mm TL and in total weight from 0.26 to 11.69 g. Of the 2256 specimens collected, 979 (43.40%) were identified as males, ranging from 37 to 120 mm and 0.26 to 9.01 g, while 1277 (56.60%) were females ranging from 44 to 128 mm and 0.40 to 11.69 g. Females were slightly longer and heavier than males. Dominant length class was 60–64 mm for both sexes (Fig. 1). Age was determined from 921 specimens (40.82% of total specimens). Four age groups (1þ–4þ) were identified in both sexes. The percentage occurrence of the age groups (1þ, 2þ, 3þ, and 4þ) was 43.75, 47.80, 6.04 and 2.41% in males and 18.55, 67.21, 11.21 and 3.03% in females respectively. Significant differences were obtained from the statistical comparison of length–weight relationships between males and females (ANCOVA, F ¼ 203.171, p < 0.05). The b-values of the relationships imply that the body shape of both sexes displays positive allometric form, with 95% confidence interval for b-value of 2.991–3.055 for males and of 3.030–3.096 for females (t-test, tmale ¼ 8.595, tfemale ¼ 2.889, p < 0.05) (Fig. 2). The mean back-calculated total lengths of each group were smaller than the observed lengths (Table 1). The back-calculations showed rapid growth during the first year of life and a steady, less rapid decline in the relative length increments occurred during
15
Female: W = 0.005TL3.0628 R2 = 0.96 N=1278
12
Total weight (g)
458
9
Male: W = 0.0053TL3.0181 R2 = 0.96 N=980
6
3
0
0
3
6
9
12
15
Total length (cm) Fig. 2. Relative growth curves (Total length–Total weight) for A. boyeri in the Gomishan wetland – southeast Caspian Sea.
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462 Table 1 Mean back-calculated lengths (mm) for age (S.D.) of A. boyeri during spawning period in the Gomishan wetland – southeast Caspian Sea. 1þ
3þ
10
4þ
Female
8 64.22 11.01 86.45 12.08 103.50 11.50 114.58 18.05 61.03 6.12
82.99 7.17
Male
6
102.67 10.08 113.75 11.17
Fig. 4. Variation of mean gonadosomatic index (GSI %) of male and female of A. boyeri in the Gomishan wetland – southeast Caspian Sea.
4. Discussion This study has established key population parameters of A. boyeri in the southeast Caspian Sea. Variation in life-history parameters of species could be explained on the basis of the different exploitation patterns and/or ecological conditions. The sand smelt is not subject to commercial exploitation in the south Caspian basin and therefore environmental conditions of this basin seem to be main factors affecting the life-history parameters of the fish. Henderson and Bamber (1987) showed that sand smelt populations vary greatly in longevity and maximum size attained with a trend to reduced growth along an oceanic-coastal–estuarinefreshwater habitat range. These attributes were related to habitat quality, such as salinity and temperature. The comparison of the population under consideration with other sand smelt populations (Henderson and Bamber, 1987) shows that the Caspian sand smelt is similar to the English channel populations, reaching a maximum length of 128 mm and an age of 4þ years. The largest age and size (length and weight) of A. boyeri in the southeast Caspian Sea are different from those of coastal populations in the Mediterranean Sea (Henderson and Bamber, 1987). Thus the majority of the specimens were between 1 and 2 ages indicates that the population was mostly young individuals. The low proportion of age 4þ specimens suggests that very few individuals survive to a maximum age, as is typical of most fishes (Matthews, 1998). This also concurs with the general patterns observed in most other populations of sand smelt throughout their distribution range (Henderson and Bamber, 1987). The exponents of total length–somatic weight relationship of A. boyeri, estimated in the wetland, showed that the somatic weight grows allometrically (Ricker, 1975) with the total length. Differences between males and females in the TL–W relationship are
Female
Lt=155.17[1-exp-0.28(t+0.738)]
0
1
2
3
Age (year)
4
Total length (mm)
Total length (mm)
Male L
5
us t
Month
subsequent years. The mean back-calculated length of individuals assigned to each age group was used to fit the von Bertalanffy growth model (Fig. 3). Males grew faster than females (kmale > kfemale), while asymptotic value of length was higher for females than for males. The 40 value for the females (8.87) was slightly higher than that of males (8.82). All individuals were sexed, the overall ratio of males to females was 1:1.30 and c2 analysis showed significant differences from the ratio 1:1 (c2 ¼ 39.36, p < 0.05). Considering the distribution of length classes according to the sex (Fig. 1), an unequal sex ratio was observed among the classes, females were dominant in the older size classes (60–64 mm), males in the younger (50–59 mm). Significant changes were obtained in the temporal variation of gonad activity (ANOVA, Ffemale ¼ 39.44, Fmale ¼ 3.51, p < 0.05). The GSI values of males were significantly lower than those of females using the size of the fish as covariate (ANCOVA, F ¼ 27.44, p < 0.05). The highest average values of GSI were 3.61 and 7.12 in March for males and females respectively. The GSI of both sexes followed almost the same pattern (Fig. 4). The reproductive period for this species in the wetland is thus from March to July when GSI is considerably higher. It thereafter decreases in August showing start of the resting period. Different kinds of eggs were found in the ovary during the spawning period from March to July (Fig. 5). In this period, the diameter of oocytes ranged from 0.03 to 0.20 mm with a mean value of 0.6773 0.3147 (Fig. 5). Absolute fecundity increased with age; a minimum value of 492 eggs was from a 1þ year old female weighing 2.50 g and a maximum value of 10,188 eggs was from 4þ year old fish weighing 8.12 g (Table 2). The mean value of absolute fecundity was 2796.73 1900.36 (S.D.) eggs/female. The regression between egg number and fish size (total length and weight) was statistically significant (p < 0.05) (Fig. 6). Fecundity relative to total weight fluctuated from 195 to 1726 eggs g1, with a mean value of 784.09 272.84 (S.D.). The relationship of relative fecundity with fish size (total length and total weight) was found to be statistically significant (Fig. 7).
180 160 140 120 100 80 60 40 20 0
Au g
y
e
Ju l
M
Fe
br
ar
ry
117.01 12.04
Ju n
0
105.86 8.97
M ay
61.48 5.45 83.25 8.02
il
2
Ap r
64.88 12.21 87.89 11.50 104.45 10.22 116.02 18.42
ch
4
ua
Males Mean observed TL, mm Mean backcalculated TL, mm Females Mean observed TL, mm Mean backcalculated TL, mm
2þ
12
GSI
Age (year)
459
180 160 140 120 100 80 60 40 20 0
Lt=162.77[1-exp-0.27(t+0.727)]
L
0
1
2
3
4
5
Age (year)
Fig. 3. von Bertalanffy length-at-age growth curves for males and females A. boyeri in the Gomishan wetland – southeast Caspian Sea.
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
May
1.80-1.89
1.90-1.99
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
June
Egg diameter size group (mm)
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
0.10-0.19
Frequency (%)
Number of specimens=31 Number of eggs=694 Mean egg diameter mm (S.D.): 0.6178mm (0.2642)
20 18 16 14 12 10 8 6 4 2 0
1.90-1.99
1.80-1.89
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
0.10-0.19
1.90-1.99
April
Frequency (%)
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
Egg diameter size group (mm)
Number of specimes=101 Number of eggs=2105 Mean egg diameter mm (S.D.):0.6908mm (0.3169)
20 18 16 14 12 10 8 6 4 2 0
1.80-1.89
Egg diameter size group (mm)
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
Number of specimens=60 Number of eggs=1514 Mean egg diameter mm (S.D.): 0.6283mm (0.2671)
0.10-0.19
Frequency (%)
20 18 16 14 12 10 8 6 4 2 0
1.90-1.99
1.80-1.89
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0-0.09
Number of specimens:172 Number of eggs:4177 Mean of egg diameter mm (S.D.): 0.7147mm (0.3583)
0.10-0.19
Frequency (%)
March 20 18 16 14 12 10 8 6 4 2 0
1.30-1.39
460
Egg diameter size group (mm)
1.90-1.99
1.80-1.89
1.70-1.79
1.60-1.69
1.50-1.59
1.40-1.49
1.30-1.39
1.20-1.29
1.10-1.19
1.00-1.09
0.90-0.99
0.80-0.89
0.70-0.79
0.60-0.69
0.50-0.59
0.40-0.49
0.30-0.39
0.20-0.29
0.10-0.19
20 18 16 14 12 10 8 6 4 2 0 0-0.09
Frequency (%)
July Number of specimens=35 Number of eggs=912 Mean egg diameter mm (S.D.): 0.6121mm (0.2640)
Egg diameter size group (mm) Fig. 5. Size frequency distribution of oocytes diameters of A. boyeri during spawning period in the Gomishan wetland – southeast Caspian Sea.
explained by the differences in size distribution of the two sexes as a consequence of inter-sexual differences in growth, suggesting the convenience of using the appropriate estimate from those proposed for each group when calculating weight by sex. The ‘‘b’’ values estimated in the studied population are different from those Table 2 Total number of oocytes for each month of reproductive season of A. boyeri population in the Gomishan wetland – southeast Caspian Sea. X: mean total number of oocytes, S.D.: standard deviation. Age
n
Minimum
Maximum
X S:D:
1þ 2þ 3þ 4þ
58 112 49 16
508 880 1358 2170
3780 7666 7900 10,188
1440.69 2682.32 3989.14 6374.58
695.97 1566.53 1852.77 2775.89
found in European regions (Palmer and Culley, 1983; FernandezDelgado et al., 1988; Creech, 1992; Leonardos and Sinis, 2000; Leonardos, 2001; Andreu-Soler et al., 2003; Bartulovic et al., 2004; Koutrakis et al., 2004); all estimated positive allometric growth. Gon and Ben-Tuvia (1983) reported a negative allometric growth (bsexes combined ¼ 2.93) for a sand smelt population in the Bardawil lagoon on the Mediterranean coast of Sinai where the water is hyper-saline (40–110). It seems that geographic location and associated environmental conditions can significantly affect the value of ‘‘b’’ in A. boyeri populations; therefore, the variations in the ‘‘b’’ exponent between populations can be attributable to species responses to different habitats. Fitting the von Bertalanffy growth formula to back-calculated lengths resulted in the estimation of higher values of maximum theoretical length than the maximum observed total lengths.
R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
12000
AF= 81.99TL - 3870.9 R2 = 0.3928 F=109.34 N=172
10000 8000
Absolute fecundity
Absolute Fecundity
12000
6000 4000 2000 0
461
AF = 639.34TW + 495.77 R2 = 0.4335 F=129.32 N=172
10000 8000 6000 4000 2000 0
0
20
40
60
80
100
120
140
0
2
4
Total length (mm)
6
8
10
12
Total weight (g)
Fig. 6. Relationship between egg number and fish total length (mm) and total weight (g) of female A. boyeri in the Gomishan wetland – southeast Caspian Sea.
2000 1800 1600 1400 1200 1000 800 600 400 200 0
RF = -8.3983TL + 1460.6 R2 = 0.1945 F=31.21 N=172
0
30
60
90
Total length (mm)
120
150
populations of this species; 1:1.24 in the Mesolongi and Etolikon lagoons – western Greece (Leonardos and Sinis, 2000), 1:1.30 in the estuary of the Mala Neretva River – middle-eastern Adriatic, Croatia (Bartulovic et al., 2004) and 1:2.5 in an estuarine system of northern Greece (Koutrakis et al., 2004). Sex ratio is thus significantly different between populations of this species throughout its range distribution. From the maximum recorded GSI values it is evident that the reproductive season of the A. boyeri extends from March to July. Nikolsky (1963) pointed out that the spawning characteristics of a fish vary in respect to their species and ecological characteristics of water system in which they live. In comparison with other fish species inhabiting south Caspian Sea, A. boyeri has an extended spawning season (w4 months). This extended spawning of population appears to be a feature of the biology of this species and may be interpreted as an increase of reproductive effort (Fernandez-Delgado et al., 1988; Creech, 1992). The observed size range of eggs 0.03–2.00 mm was different from that of 0.08–2.08 mm reported by Creech (1992) in Aberthaw lagoon in south Wales and that of 0.1–1.80 mm found by Palmer and Culley (1983) at Oldbury-on Severn in England. The great heterogeneity in egg size of A. boyeri is indicative of a batch spawner. Even though a number of problems come from invalid estimates of fecundity in batch spawners that are derived from either the total number of eggs of batch sizes including incomplete ovulation (Yamamoto and Yamazaki, 1961), discontinuous addition of recruitment stock eggs to the spawning egg stock (Hunter and Goldburg, 1979) and atresia (Macer, 1974), we made an attempt to estimate absolute fecundity in the present study. For Caspian sand smelt absolute fecundity was positively correlated to fish size (length or weight) and this positive correlation remains consistent even when considering absolute fecundity and fish size relationships separately for each age groups. While a negative effect of fish size on relative fecundity was observed for the fish, an increase in female size (total length or/and weight) implied a decrease of
Relative fecundity
Relative fecundity
Considering an LN value 30% higher than the maximum lengths observed (Garcia-Rodriguez et al., 2005), the obtained results are reliable values for both sexes. The LN value of female was calculated to be higher than that of males. The higher coefficient (k) for males emphasizes that they grow rapidly initially and approach their asymptotic length (LN) earlier in the life. Comparison of k and LN from different populations in the range distribution of the sand smelt shows that the growth patterns vary greatly in the estimated parameters (Table 3). These differences may be regarded as biological feature of the A. boyeri in different habitats, as a trade-off between growth rate (k) and maximum size (LN) is often found. Optimum ecological conditions cause a shift towards larger maximum size. The study area in the southeast Caspian Sea is an isohaline coastal wetland with almost stable conditions which seems to be an optimum habitat for this species resulting greater longevity and maximum size being attained. The index of growth performance (40 ) is to be considered a useful tool for comparing the growth curves of different populations of the same species and/or of different species belonging to the same family (Sparre and Venema, 1998). In general, the values of the growth performance index from different geographical areas show that growth patterns are different for the different stocks, but similar for the stocks of neighboring localities. By calculation from published data of k and LN, in different populations of the sand smelt (Table 3), the index ranges from 8.23 to 9.50, and the value obtained of the index for the present population occurs within this range. In the Gomishan wetlands, the overall sex ratio is unbalanced in favor of females, probably as a consequence of higher survival rate and greater longevity of females, or the greater endurance of females to environmental variability. Even though Fernandez-Delgado et al. (1988) and Creech (1992) reported no significant deviation from parity in the ratio of males to females of this species in the Guadalquivir river (Spain) and Bristol channel (south Wales) respectively, dominance of females has been reported in some
2000 1800 1600 1400 1200 1000 800 600 400 200 0
RF = -55.812TW + 979.39 R2 = 0.1559 F=40.81 N=172
0
3
6
9
12
Total weight (g)
Fig. 7. Relationship between relative fecundity and fish total length (mm) and total weight (g) of female A. boyeri in the Gomishan wetland – southeast Caspian Sea.
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R. Patimar et al. / Estuarine, Coastal and Shelf Science 81 (2009) 457–462
Table 3 The growth parameters (LN, k, t0) of the A. boyeri in this study and in studies by other authors. Study area
Sex
LN (mm)
k (year1)
t0 (years)
40
Henderson and Bamber (1987)
English Channel
Sexes combined
138
0.7
–
9.49
Gon and Ben-Tuvia (1983),b
Bardawil lagoon-Sinai
Sexes combined
42
2.93
–
8.55
Author ,a
Creech (1992)
,b
Aberthaw lagoon, S. Wales
Sexes combined
92
–
–
–
Leonardos and Sinis (2000),a
Mesolongi and Etolikon lagoons, W. Greece
Male Female
74.97 84.58
0.67 0.81
0.46 0.65
8.23 8.66
Leonardos (2001),a
Trichonis lake, W. Greece
Sexes combined
112.40
0.42
0.40
8.58
Andreu-Soler et al. (2003),a
Mar Menor coastal lagoon, SE Iberia Peninsula
Male Female
81.90 84.58
0.91 0.81
0.45 0.65
8.72 8.66
Bartulovic et al. (2004),a
Estuary of the Mala Neretva River (Middle-eastern Adriatic – Croatia
Male Female
99.14 105.77
0.97 1.19
0.19 0.006
9.16 9.50
Koutrakis et al. (2004),a
Vistonis estuarine system, N. Greece
Male Female
128.09 166.54
0.26 0.16
1.64 1.90
9.36 8.40
Present studya
Gomishan wetland, SE Caspian Sea
Male Female
155.17 162.77
0.28 0.27
0.738 0.727
8.82 8.87
a b
Using TL. Using SL.
relative fecundity. It can be hypothesized, however, that the largest spawner was not able to increase the quantity of eggs per unit somatic weight proportionally to the absolute number of eggs and thus, the egg quantity relative to fish size decreased. This means that total energetic investment in reproduction tends to be higher in the larger member of the fish, but proportional energetic investment in reproduction (as energy allocation per unit of fish size) tends to decrease with increasing in fish size. In conclusion, the life-history pattern of sand smelt in the Gomishan wetland as a representative of Caspian sand smelt differs markedly from those of many other populations of the species from European regions. This pattern is important with respect to the management of the species. It can be concluded that the life-history patterns of this species varied relatively to the habitat to which they exposed. The variations relating to growth and reproduction may be interpreted as phenotypic plasticity and adaptation to local selective pressure. References Andreu-Soler, A., Oliva-Paterna, F.J., Fernandez-Delgado, C., Torralva, M., 2003. Age and growth of the sand smelt, Atherina boyeri (Risso 1810), in the Mar Menor coastal lagoon (SE Iberian Peninsula). Journal of Applied Ichthyology 19, 202–208. Bagenal, T., Tesch, F., 1978. Methods for Assessment of Fish Production in Fresh Waters. IBP Handbook 3. Blackwell, Oxford. 365pp. Bartulovic, V., Glamuzina, B., Conides, A., Dulcic, D., Njire, D., Kozul, V., 2004. Age, growth, mortality and sex ratio of sand smelt, Atherina boyeri Risso, 1810 (Pisces: Atherinidae) in the estuary of the Mala Neretva River (middle-eastern Adraitic, Croatia). Journal of Applied Ichthyology 20, 427–430. Bertalanffy, L., 1938. A quantitative theory of organic growth (inquiries on growth laws II). Human Biology 10, 181–212. Creech, S., 1992. A study of the population of Atherina boyeri (Risso, 1810) in Aberthaw lagoon, on the Bristol Channel, in south Wales. Journal of Fish Biology 41, 277–286. Fernandez-Delgado, C., Hernando, J.A., Herrera, M., Bellido, M,, 1988. Life-history patterns of the sand smelt Atherina boyeri Risso, 1810 in the Estuary of the Guadalquiver river, Spain. Estuarine, Coastal and Shelf Science 27, 697–706. Garcia-Rodriguez, M., Pereda, P., Landa, J., Esteban, A., 2005. On the biology and growth of the anglerfish Lophiu budegassa Spinola, 1807 in the Spanish Mediterranean: a preliminary approach. Fisheries Research 71, 197–208. Gon, O.A., Ben-Tuvia, A., 1983. The biology of Boyer’s sand smelt, Atherina boyeri Risso, in the Bardawil lagoon on the Mediterranean coast of Sinai. Journal of Fish Biology 22, 537–547. Henderson, P.A., Bamber, R.N., 1987. On the reproductive biology of the sand smelt Atherina boyeri Risso (Pisces: Atherinidae) and its evolutionary potential. Biological Journal of the Linnean Society 32, 395–415.
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