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AGE AND GROWTH, REPRODUCTION AND DIET OF THE BLACK GOBY, (GOBIUS NIGER) FROM AEGEAN SEA, TURKEY

Halit Filiz1*, Melahat Toğulga2

1Mugla University, Faculty of Fisheries, Department of Hydrobiology, Kotekli, Mugla, Turkey

2Ege University, Faculty of Fisheries, Department of Hydrobiology, Bornova, Izmir, Turkey

Corresponding Author:
Halit FİLİZ
Mugla University, Faculty of Fisheries
Department of Hydrobiology, 48000 Kotekli-Mugla-–TURKEY
Tel: (+ 90 252) 211 18 95
Fax: (+ 90 252) 223 8475
E-mail: [email protected]
 
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Abstract

Black gobies, Gobius niger L., 1758, were sampled monthly between March 2003 and February 2004 in Izmir Bay involving 1149 specimens. Length distribution varied between 5.1 and 15.2 cm total length. Age determined from direct reading on otoliths was comprised from zero to five years. There were significant differences in mean lengths at age group for the two sexes, which did not allow the use of combined data. The parameters of the fitted Von Bertalanffy growth equation (with seasonal component, birth date on the 1st of January) were L∞= 16.69 cm, k= 0.301 yr-1, t0= -2.205 for males, and L∞= 14.84 cm, k= 0.321 yr-1, t0= -1.459 for females. Macroscopic examination of the gonads, and analysis of the monthly values of the gonadosomatic index, indicated that reproduction starts in March and lasts during October, with a maximum in March, followed by August and October. Individuals become sexually mature around 7.80 cm TL (a size that can be reached in less than 1 year) for females. In this population, the sex ratio (male:female) was 3.6:1. Stomach contents were mainly Mollusca (%IRI= 47.53), Crustacea (%IRI= 42.94), Polychaeta (%IRI= 8.26), Foreminifera (%IRI= 1.14) and Teleostei (%IRI= 0.13).

Key words

Age and growth; reproduction; feeding; black goby; Gobius niger; Aegean Sea

Introduction

The black goby is widely distributed in Eastern Atlantic and Mediterranean Sea (include Black Sea), throughout North Africa from Cape Blanc, Mauritania north and eastwards to the Suez Canal; also along the eastern Atlantic coast northwards to Trondheim (Norway) and Baltic Sea (Miller, 1986). It can be found on sandy and muddy bottoms, in depth between 2 and 70 m (Hureau & Monod, 1973, Vesey & Langford, 1985). Also, it is able to live in brackish water down to %o 6 S (Vaas et al., 1975). This species is distributed on all coasts of Turkey (Bilecenoglu et al., 2002).

There are numerous studies about its abundance, distribution and habitat selection (Claridge et al., 1986; Wiederholm, 1987; Costello, 1992; Koutrakis et al., 2000; Gordo & Cabral, 2001; Letourneur et al., 2001; Malavasi et al., 2005), biology (Vaas et al., 1975; Fabi & Froglia, 1984; Vesey & Langford, 1985; Doornbos & Twisk, 1987; Arruda et al., 1993; Silva & Gordo, 1997; Bouchereau & Guelorget, 1998), growth (Fabi & Giannetti, 1985), feeding ecology and behavior (Casabianca & Kiener, 1969; McGrath, 1974; Fabi & Froglia, 1983; Magnhagen, 1988; Fernandez et al., 1995; Labropoulou & Markakis, 1998; Labropoulou & Papadopoulou-Smith, 1999), reproductive biology (Bonnin, 1971a, 1971b, 1975, 1977, 1981, 1984, 1989; Bonnin & Croizet, 1972, 1973; Holt & Byrne, 1988; Magnhagen, 1990, 1991; Joyeux et al., 1991b, 1992; Marconato et al., 1996; Pampoulie et al., 1999; Locatello et al., 2002; Mazzoldi & Rasotto, 2002; Pilastro et al., 2002; Rasotto & Mazzoldi, 2002; Immler et al., 2004; Mazzoldi et al., 2005; Scaggiante et al., 2005), genetic (Colombera & Rasotto, 1982; Vitturi & Catalano, 1989; Hoeglund & Thomas, 1992; Zander & Kesting, 1998; Sorice & Caputo, 1999; Mandrioli et al., 2001), parasites (Leiro et al., 1984; Loubes et al., 1984; Dezfuli et al., 1992; Zander, 2003; Kvach, 2005), and environmental effects and pollution (Bouchereau, 1997; Cunha & Antunes, 1999; Pampoulie et al., 2001; Antunes & Cunha, 2002; Arcos et al., 2002; Katalay & Parlak, 2002, 2004a, 2004b; Carnevali & Maradonna, 2003; Maradonna et al., 2004; Katalay et al., 2005; Migliarini et al., 2005). Also, length-weight relationships were given by Abdallah (2002), Cicek et al. (2006), and Verdiell- Cubedo et al. (2006).

Although this species is common in the Aegean Sea, surprisingly, there is no published study about its biology in Turkish waters. Since it has no commercial value in Turkey, probably, fisheries biologists did not give enough attention of its biology. However, this species has important ecologic values. Black goby is one of the species that used in monitoring pollution (as an indicator species) (Katalay & Parlak, 2002). Also, this species has an important role in the food chain in Izmir Bay (Bilecenoglu, 2003).

This paper provides the first information on the black goby, an important species of the Izmir Bay, in Aegean Sea, specifically on its age, growth, reproduction and feeding.

Material and Methods

Izmir Bay is situated at the western coast of the Anatolian peninsula, and is connected to the Aegean Sea. The bay is roughly ‘‘L’’ shaped. The leg of the ‘‘L’’ is about 20 km wide and 40 km long and the base of the ‘‘L’’ is about 5–7 km wide and 24 km long (Figure 1). The Izmir Bay has been divided into three areas according to their physical characteristics. These are Outer, Middle and Inner Bay (Sayin, 2003).

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Figure 1. Map showing the location of the Izmir Bay.

All kind of fisheries activity is prohibited in inner part of Izmir Bay because it has highly polluted by both domestic and industrial wastes. Also, southeast part of the line combined Ardıç Cape (38° 31' 58" N - 26° 37' 22" E) and Deveboynu (38° 39' 24" N - 26° 43' 42" E) is prohibited all kind of trawl by the Ministry of Agriculture and Rural Affairs (Anonymous, 2007). Therefore, purse seine, hook-and-line and gill net are important fisheries methods in the Izmir Bay (Bilecenoğlu, 2003). Because presence of economically important demersal fish species, it is known that illegal fisheries can be occurred (Metin et al., 2000). Main fisheries activity in the Bay rely on pelagic fish stocks (sardine, anchovy, mackerel, etc.) (Cihangir et al., 1999). There is no statistical data about caught fish amount in Izmir Bay (Bilecenoglu, 2003). Therefore, Kara & Gurbet (1999) reported that there is totally 2256 boat in the Bay and nearly 20000 tones fish caught yearly.

Izmir Bay was sampled monthly between March 2003 and February 2004. Specimens obtained via trawl (n= 78), and fishing line (n= 1071). Trawl specimens were sampled by R/V EGESUF (27 m length and 463 HP). A conventional bottom trawl net of 22 mm cod-end mesh size was used and three hauls in same day were carried out and haul durations stabilized 30 minutes. The vessel speed was maintained at 2.5 knots. Depth of the fishing ground was 30 m. fishing line sampling carried out in first, middle and last weeks of every month. A fishing line named “sinek oltasi” was used (no. 18 needle, 0.20 mm main body and 25 g lead weight). Fish were caught in the Izmir Bay (where they abundant) in three locations between 09:00 and 12:00 a.m. (Table 1). All the specimens were injected to abdomen region with 4% alcohol and frozen.

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Table 1. Coordinates, depth and floor structure of stations where samples taken (M: muddy; S: sandy; St: Stony; G: grassy)

In the laboratory, the total length of all individuals was measured to the nearest millimeter below (later grouped in 1.0 cm length classes) and weighed to the nearest 0.01 g total weight. Sex was recorded and the gonads were weighed to the nearest 0.001 g (in the males, sperm-duct gland was not included in the gonadal weight). Sagittal otoliths were removed, cleaned, dried and stored in labeled plastic tubes.

For age determination, the otoliths of specimens were examined under a stereoscope microscope with a reflected light (x14 magnification). The otoliths were read by three readers and when there was no agreement among the three readings, the otolith was excluded. Age was expressed in years, the birthday of the fish being considered to be 1 January.

The mean lengths at age were analyzed separately per sex and were compared statistically using Student’s t test (p>0.05).

To examine fish growth, a von Bertalanffy growth equation (VBGE) was calculated using the iterated least square method (Sparre et al., 1989).

The relationship between weight and TL, W = aLb, was converted into logarithmic expression: ln W = ln a + b ln L. Parameters a and b were calculated by least-squares regression, as was the coefficient of determination (r2). Significant difference of b values from 3, which represent isometric growth, was tested with the t-test (Pauly, 1993).

To quantify the changes that occurred in the gonads during the annual sexual cycle and to determine the spawning season, the gonadosomatic index (GSI) (expressing gonadal weight as a percentage of total weight minus gonadal weight) (King, 1995) was calculated, between March 2003 and January 2004, monthly and per sex, their mean values being calculated from the individual ones. In order to determine first sexual maturation length and age, a logistic curve equation was used (King, 1995):

P = 1 / (1 + exp[ -r (L - Lm)])

here, P, proportion of mature individuals; r, slope of curve; L, total length, and Lm, mean length at maturity length or mean length of individuals where 50% of population is reproduced.

Sex ratio (males/females) was calculated by age.

Prey items in each stomach were identified to group level, measured, counted and weighed on an electronic balance (precision 0.0001 g). Diet composition was evaluated using three measures described by Hyslop (1980): the numerical index (%N); the gravimetric index (%W), and frequency of occurrence (%O). Based on Cortes' (1997) suggestion, the index of relative importance (IRI) was calculated and expressed as a percentage (%IRI). Subsequently, food items were grouped into categories of preference using the method proposed by Morato et al. (1998) and described by Sever et al. (2008). The categories were defined as follows:

IRI≥ 30*(0.15*Σ%O) main important prey (MIP)

30*(0.15*Σ%O)>IRI>10*(0.05*Σ%O) - secondary prey (SP)

IRI≤10*(0.05*Σ%O) occasional prey (OP)

Results and Discussion

Age and growth

The mean values of temperature recorded for the bay during the sampling period are shown in Figure 2. The lowest value of temperature (11.3°C) was found in February 2004 and the highest (27.8 °C) in August 2003.

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Figure 2. Mean values of temperature recorded in the Izmir Bay between March 2003 and February 2004.

Table 2 shows the descriptive statistics regarding length and weight data of all and sexed individuals.

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Table 2. Descriptive statistics of length and weight data of specimens obtained from Izmir Bay (Values given are the mean ± SD and range in parenthesis).

Among the 1149 black goby which were otolith’s taken, 49 individuals could not be aged since both there were undetermined specimens (n= 26) and there was no agreement between readers (n= 23). Thus, 865 (78.6%) males and 235 (21.4%) females were used for direct reading on otoliths (Table 3 and 4).

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Table 3. Results from direct reading on the otoliths of males G. niger from Izmir Bay. Age expressed in years.

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Table 4. Results from direct reading on the otoliths of females G. niger from Izmir Bay.

The length range by age group for both males and females was different. Application of the Student’s t-test to the mean lengths and standard deviations per age groups showed that there was significant difference between sexes (Table 5). The test was not applied to both males and females of age V because there was no female in this age. So, results from direct reading on the otoliths were not pooled, and calculations were made by sex separately.

fisheriessciences-lengths-per-age

Table 5. Results of the application of the Student’s t test to the mean lengths per age group for males and females G. niger from Izmir Bay.

To describe the growth of the black goby population found in Izmir Bay, a VBGE, based on the males and females data, was established (Table 6).

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Table 6. Growth parameters of G. niger in Izmir Bay.

The length-weight relationships were calculated for each sex (Table 7).

fisheriessciences-Descriptive-statistics

Table 7. Descriptive statistics and estimated parameters of the length–weight relationship for G. niger collected from Izmir Bay of the eastern Aegean Sea, Turkey. Lmin – Lmax = minimum and maximum lengths (cm); Wmin – Wmax = minimum and maximum weights (g); C.I = confidence intervals; a = intercept of the relationship; b = slope of the relationship; r2= coefficient of determination; n = sample size.

Reproduction

Monthly changes in gonadosomatic index (GSI) for females are shown in Figure 3. GSI values remain similar between November and February, and then show a marked increase in March. Therefore, this month seems to be the beginning of the spawning season which lasts until November.

fisheriessciences-gonadosomatic-index

Figure 3. Variation in gonadosomatic index, GSI for female G. niger in the Izmir Bay.

Comparing the GSI values attained by females it can be noticed that, during the reproduction period, females reach GSI values of about 18.2%.

The sex ratio was found as 3.3:1 males were dominant in all ages (Table 8), as in all months and seasons.

fisheriessciences-sex-composition

Table 8. Age and sex composition of G. niger from Izmir Bay.

Females reached sexual maturity at 7.80 cm TL and before I year old (0.86 year) (Figure 4 and 5). The smallest female had well developed gonad was 7.50 cm TL.

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Figure 4. Length of first maturity of females in Izmir Bay.

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Figure 5. Age of first maturity of females in Izmir Bay

Food

Of the 508 black goby stomachs examined, 489 had food (96.3%) and 19 were empty (3.7%). Mollusca, Crustacea and Polychaeta were found to be most important prey group (MIP; IRI≥561) in the diet. Foraminifera constituted the secondary prey group (SP; 561>IRI>63), whereas Teleost fishes were an occasional prey group (OP; IRI≤63). Mollusca, Crustacea and Polychaeta constituted of 98.73% of the diet. Foraminifera and Teleostei comprised 1.14 and 0.13% of the diet, respectively (Table 9).

fisheriessciences-food-items

Table 9. General food items found for G. niger in Izmir Bay

In order to determine whether any difference between seasons, stomach contents were examined for each season (Table 10-13). Generally, Crustacea and Mollusca were found as important prey items in all seasons. Teleosts never consumed in spring, while they eaten occasionally in other seasons (Table 14).

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Table 10. Food items found for G. niger in Izmir Bay in spring.

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Table 11. Food items found for G. niger in Izmir Bay in summer.

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Table 12. Food items found for G. niger in Izmir Bay in autumn.

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Table 13. Food items found for G. niger in Izmir Bay in winter.

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Table 14. Comparison of food preferences of G. niger in Izmir Bay according to seasons.

In order to determine whether any difference between ages, stomach contents are examined for each age group (Table 15-20). Generally, Crustacea and Mollusca were found as important prey items in all ages. While Teleosts were consumed as occasianlly by 1 year old specimens, they became secondary in 3 and important in 4 years old (Table 21).

fisheriessciences-0-year-old

Table 15. Food of “0” year old individuals in Izmir Bay.

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Table 16. Food of “1” year old individuals in Izmir Bay.

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Table 17. Food of “II” years old individuals in Izmir Bay.

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Table 18. Food of “III” years old individuals in Izmir Bay.

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Table 19. Food of “IV” years old individuals in Izmir Bay.

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Table 20. Food of “V” years old individuals in Izmir Bay.

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Table 21. Comparison of food preferences of G. niger in Izmir Bay according to ages.

In order to determine whether any difference between sexes, stomach contents were examined for each sex. Mollusca and Crustacea were found as important prey items in both sexes. Teleosts consumed occasionally (Table 22 and 23).

fisheriessciences-Food-males

Table 22. Food of males in Izmir Bay.

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Table 23. Food of females in Izmir Bay.

Age and growth

There are various studies providing information about maximum lengths of the species both in Mediterranean and Atlantic. These studies give us a chance to make a comparasion (Table 24). As it is seen, maximum length in Izmir Bay is a little higher than those obtained in other parts of Mediterranean (except central Adriatic) and quite higher than those obtained from Atlantic. It seems that Mediterranean populations can be attained much bigger lengths from Atlantic ones. Whereas, expected outcome is that individuals living in Atlantic must be bigger. Sampling methods used may affect to this situation. It can be difficult to obtain bigger individuals in Atlantic by trawls since black gobies possess nest in the sand or under some substratum like stone, rocks or shells. Therefore, we obtained a big part of samples via fishing line in the shallow zone. This allowed us be able to see individuals when fishing and bigger male individuals attacker bait. Additionally, if we consider that most of the Mediterranean studies are made in lagoon areas, temperature and food availability can affect in this outcome.

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Table 24. Comparison of the maximum lengths.

Age determination from direct observations on the otoliths resulted in the establishment of six age groups (0, I, II, III, IV and V) for the population. Among the 1100 specimen aged, 865 (78.6%) were males and 235 (21.4%) were females. Age group II and I included 46.6% and 26.0% of the population, respectively. Age group V was consisted of only males (Table 25).

fisheriessciences-sex-composition

Table 25. Age and sex composition of the G. niger in Izmir Bay.

The maximum age reached by specimens of black goby (5 years) from the Izmir Bay is within the longevity limits observed over the biogeographical distribution area (Table 26). Indeed, if black goby longevity (5 year) is similar on the Adriatic (Fabi & Giannetti, 1985) and Norwegian coasts (Nash, 1984), the life span seems to be shorter (2-3 years) in the Atlantic lagoons and estuaries. From these results, it can be concluded that the populations living in the Aegean and Adriatic Sea are the ones that reach the maximum age (5) and close to the maximum length ever recorded (16.5cm).

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Table 26. Comparison of maximum age and age at lengths records.

In terms of mean length per age group significant differences were found between the two sexes (Table 5). Males attain a bigger length than females. These differences between male and female growth rates and life span have already been noticed by Vaas et al. (1975), Fabi & Froglia (1984), Fabi & Giannetti (1985), Joyeoux et al. (1991a), Arruda et al. (1993), Silva & Gordo (1997) and Bouchereau & Guelorget (1998) (Table 26). Just about any factor that might possibly influence growth has been shown to have an effect, including temperature, food availability, nutrient availability, light regime, oxygen, salinity, pollutants, current speed, predator density, intraspecific social interactions and genetics (Helfman et al., 1997). These factors, often working in combination, create large variations in size of fishes of the same and different ages (Helfman et al., 1997).

In this study, growth rate of the population has been found relatively low. Since the earlier spawning fish has slower somatic (body) growth (Helfman et al., 1997), this finding was expected. However, the growth coefficient is highly variable among different studies (k= 0.19-0.91) (Table 27). The asymptotic length (L∞) estimated in this study was within the observed total length of males and females. When compared with the the previous studies made in Mediterranean (Table 27), calculated growth performance index (Φ) value for the Izmir Bay was higher than that found by Fabi & Giannetti (1985). Analyzing the same table for Atlantic, it can be seen that our Φ value was lower than those calculated by Vesey & Langford (1985) and Silva & Gordo (1997). Although there were observed differences, no significant differences were found among our Φ value and ones obtained for Mediterranean and Atlantic from previous studies (p> 0.05).

fisheriessciences-growth-parameters

Table 27. Comparisons of growth parameters.

Bouchereau & Guelorget (1998) interpreted the differences in the growth rates: “G. niger growth is different in the Atlantic and the Mediterranean. Growth rate in the Mediterranean populations is, during the first year, clearly higher than of Atlantic populations. Afterwards, it decrases strongly in the Mediterranean but regulate itself in Atlantic. After the third year, differences in size are less evident, but final performances are better in the Mediterranean (136 mm) than in the Atlantic (130 mm).

A comparison of published length–weight relationships for the species is given in Table 28. The values of the slope (b) ranged from 2.86 to 3.39 and our results remained within the ranges given. Our b value (2.86) has constituted of lowest limit. Concerning growth type, the length-weight relationships revealed negative allometry. 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 of the specimen caught (Tesch, 1971; Wootton, 1998), which were not accounted for in the present study. Thus, differences in lengthweight relationships between this and other studies could potentially be attributed to the combination of one or more of the factors given above.

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Table 28. Comparision of the LW relationships.

Reproduction

The male:female ratios obtained both in Mediterranean and Atlantic have shown in Table 29. In all seasons, including reproduction period, males were found as dominant. In previous studies, a decrease in the availability of the males has been reported, especially in spring and summer months (reproduction period). According to Miller (1984), this fact is very common among gobioid fishes since during the breeding season, there is a marked reduction in the proportion of males due to the egg protection behaviour, because they guard eggs under shells or stones and so less easily cauhgt. This egg protection behaviour of males also has been observed in free divings, especially made in reproduction period. So, the dominancy of the males in Aegean Sea does not mean that they have no egg protection. The most important factor in this differency is probably sampling method. Altought, studies claimed a decrease in the availability of the males especially in the reproduction period used beach siene nets (Arruda et al., 1993; Silva & Gordo, 1997; Bouchereau & Guelorget 1998; Pampoulie et al., 1999) and trawl (Vaas et al., 1975; Fabi & Froglia, 1984; Fabi & Giannetti, 1985; Vesey & Langford, 1985), in this study most of specimens was caught by hand line.

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Table 29. Comparison of male:female ratios.

Monthly changes in gonadosomatic index for females are shown in Figure 3. A comparison between the spawning season of the black goby population living in Izmir Bay with those from other areas (Table 30) shows that there is a certain homogeneity in the spawning period, although the Northern populations have a shorter breeding season than the Southern ones. The longer spawning period of the latter can not be dissociated from the climatic conditions. In fact, the warmer temperature and longer day length have a large influence on gonadal development, favouring a longer spawning period (Joyeux et al., 1992; Silva & Gordo, 1997).

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Table 30. Comparison of the spawning season of G. niger obtained from different areas and according to several authors.+ = occurence of spawning season; ?= possible occurence of spaning season.

Most individuals of the Izmir Bay populations probably reproduce in their first year. Females reached sexual maturity at 7.80 cm TL and before I year old (0.86 year) (Figure 4 and 5). The smallest female had well developed gonad was 7.50 cm TL. Obtained first maturity ages and lengths from previous studies were compared in Table 31.

fisheriessciences-maturity-age

Table 31. Comparison of the maturity age (tm) and length (Lm) of G. niger obtained from different areas and according to several authors.

Vaas et al. (1975) reported that reproduction of the black goby starts when the water temperature exceeds 12 °C (in May in Veerse Meer). Measured water temperatures in Izmir Bay in March appeared to be support the relationship between reproduction and water temperature.

Food

In the Izmir Bay, the diet of black goby is based on small benthic invertebrates, generally similar to that of other populations (Table 32). Therefore, Foraminifera comprised 8.26% of the diet. We believed that those foraminiferans are ingested accidentally, together with the animal constituents of the diet.

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Table 32. Food items of different populations of G. niger. (M): Mediterranean; (A): Atlantic

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