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A study on the scales and age estimation of the grey golden , Liza aurata (Risso, 1810), in the lagoon of Messolonghi (W. Greece)

Article in Journal of Applied Ichthyology · July 2003 DOI: 10.1046/j.1439-0426.2003.00481.x

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The user has requested enhancement of the downloaded file. J. Appl. Ichthyol. 19 (2003), 220–228 Received: November 18, 2002 Ó 2003 Blackwell Verlag, Berlin Accepted: February 2, 2003 ISSN 0175–8659

A study on the scales and age estimation of the grey golden mullet, Liza aurata (Risso, 1810), in the lagoon of Messolonghi (W. Greece) By G. N. Hotos

Laboratory for Culture of Euryhaline Fish, Department of Aquaculture and Fisheries, Technological Educational Institution (T.E.I.)of Messolonghi, Messolonghi, Greece

Summary surface of their embedded part in the fish body. These A detailed study was made of the scales on the golden grey structures that are the boundaries between two successive mullet Liza aurata in the lagoon of Messolonghi (W. Greece), growth zones are interpreted as representing annual events in order to examine the suitability of scales for ageing. From a and, therefore, should collectively be called annuli. However, total of 1048 specimens of 9–59 cm total length (TL), the such a structure should be examined with caution and be estimated ages ranged from 0+ to 8+ years, with only females counted as an annulus only when certain criteria are satisfied. at ages 7+ and 8+. The scale reading was reliable, the annuli First, they are not to be confused with possible supernumerary recognizable and each annulus radius easily measured. There (accessory) annulus-like bands; secondly, they are to be formed was a great overlapping in the annulus radius between the ages during the cessation of growth that occurs during the cold 1+ and 4+, indicative of extended spawning time and season; and thirdly, only one annulus is to be formed and differences in growth of yearly recruits. The scale radius counted per year. Provided these criteria are satisfied, the age estimation is then a matter of selecting the proper area of the (Rmax) was strongly related with TL by the pooled equation: 0.77 body from which the scales are readable and reliable for age TL ¼ 1.5501Rmax , with no significant differences between the sexes. From examination of the monthly variation in the estimation. distance of the outermost annulus from the scale margin, it For fish stock assessment, the growth rate is a very was determined that the annulus is formed in February. No important study component as even small differences can annuli were detected in fish of less than 20 cm TL. have substantial effects on population assessment. However, for Mugilidae, age estimations are in most cases attempted without an adequate and thorough examination of the hard Introduction structures; thus, the validity of published results remains , Liza aurata (Risso, 1810), is one of the uncertain. The present study, which is part of a more species of the family Mugilidae that constitutes the target of comprehensive project on the biology of the golden grey fishery exploitation of lagoons in Greece and elsewhere. The mullet in the lagoon of Messolonghi, attempts to assess the biology of this species in its natural environment has been validity of age estimations for L. aurata using the scales investigated in Greece only to a limited degree, including some located just under the first dorsal fin. A sufficient number of growth parameters of a presumable sea population (Konides specimens were used to cover the range of undersized (9– et al., 1992), the recruitment of its fry (Katselis et al., 1994) 20 cm) and larger (20–59 cm) fish in order to represent a true and its reproduction biology (Hotos et al., 2000). population and amend the uncertainties created by previous Studies of other European waters (Andaloro, 1983; Modru- studies. Some elements proving the counted annuli are san et al., 1988; Arruda et al., 1991; Brusle and Cambrony, presented photographically and may serve for comparison 1992; Kraljevic´ and Dulcˇ ic´ , 1996) dealt with the biology of the with future studies of L. aurata as well as other mugilid species in Italy, the Adriatic, Portugal and France. However, fishes. when comparing data presented by the above and other older relevant studies which included ageing of fish (Table 1), many Materials and methods uncertainties became obvious: there were great differences among the length-at-age; in some cases, no attempts were A total of 1048 L. aurata specimens of over 9 cm total length made to estimate the length-at-age, and some age classes were (TL) were sampled in monthly intervals during the period missing. The maximum age of the species remains uncertain as 1992–1994, from the Messolonghi lagoon and its adjacent sea, well as the comparability of results among these studies, using lagoonal fixed traps and seine nets with a rough because the methods (use of scales, or otoliths or length selectivity for fish sizes over 8 cm. Additionally, fry and frequency) and the material (number of specimens and/or juveniles (1–10 cm TL) were collected by beach seine year- various length ranges, missing sex information, etc.) were round. Each fish was properly treated by recording the TL and different or inadequate. Method descriptions used for ageing the total weight (TW) with an accuracy of no less than the the specimens were in general not sufficiently comprehensive. nearest millimeter and hundredth of a gram, respectively. Sex Thus, a more thorough study is required. was determined by visual inspection and gonads were weighed The most frequently used method for ageing mugilids is (0.001 g) and preserved in 4% neutralized formaldehyde the examination of their scales, interpreting and counting the solution for further confirmation. The specimens without Ôgrowth bandsÕ or Ôstop growth annuliÕ which appear on the developed gonads were classified as immature.

U.S. Copyright Clearance Centre Code Statement: 0175–8659/2003/1904–0220$15.00/0 www.blackwell.de/synergy 1 td ntesae n g siaino h rygle mullet golden grey the of estimation age and scales the on Study

Table 1 Data on mean lengths at ages of Liza aurata from the literature (all studies marked with an asterisk (*) are quoted in Quignard and Farrugio, 1981)

Length No. of fish Area Author Method Length range (cm) and sex L1 L2 L3 L4 L5 L6 L7 L8

Sea Ionian coast (from Messolonghi Konides et al. (1992) Length frequency FL 6–26 645 – – – – – – – – lagoon to Amvrakikos Gulf) N. Adriatic (Mirna Bay) Kraljevic´ and Dulcˇ ic´ (1996) Scales TL 20–42 1073 – – 23.2 27.1 29.0 31.1 32.6 35.1 France (Bay of Marseille) Albertini-Berhaut (1978) Length frequency SL 1–19 4800 – – – – – – – – Great Britain Hickling (1970) Scales, length frequency TL 20–41 – 5 10.7 18.7 24.2 26.5 34.3 – – (Devon, Wales, Scilly) – – – – – – 25.8 29 30 – – France (Brittany) Thong (1969) Scales FL 6.8–33.8 86 9.1 16.2 22.3 25.7 29.3 32.6 35.9 – TL 8.1–41.4 – 10.9 19.7 27.2 31.4 35.8 39.9 43.9 7 France (Morbihan) Thong (1971)* Scales FL 17.2–36.1 127 8.0 17.2 21.5 25.6 28.2 31.3 – – TL 20.9–44.2 9.6 20.9 26.2 31.3 34.5 38.3 – – 8 France (Bay of Biscay) Arne (1938)* Scales TL – – 11.2 17.3 27.1 31.1 34.9 – – – 9 Italy (Adriatic) Serbetis (1939)* Scales TL 7.3–30 71 11.3 18.3 30 – – – – – Black Sea Nikolskii (1954)* ? TL – – 12 21 26 30 36 – – – Caspian Sea Nikolskii (1954)* ? TL – – 21 28 33 36 41 43 46 47 Caspian Sea Alexandrova (1964) ? TL – – 13 24 32.7 37.5 41.5 45 48 – Internal waters (lakes–lagoons) Portugal (Ria de Aveiro lagoon) Arruda et al. (1991) Scales TL 2–29 3689 10.5 16.5 21.9 26.8 – – – – Italy (Marsala lagoon) Andaloro (1983) Scales – otoliths TL 10–25 ? 423 10.6 17.35 19.82 21.7 22.62 24.0 – – Southern Spain Drake et al. (1984) Length frequency TL 16–44 3012 26.2 30.7 34.5 – – – – – (wetlands, Cadiz) Adriatic (Krka estuary) Modrusan et al. (1988) – TL – – – 23.0 27.5 – 34.5 – – – Spain (Cadiz) Sancho (1975) Length frequency FL – 144 17 24 – – – – – – TL – – 20.7 29.3 – – – – – – Spain (Int. salt waters) Sancho (1975) Length frequency FL – – 21 26 – – – – – – TL – – 25.6 35 – – – – – – 10 France (Thau lagoon) Coutelan (1953)* Scales TL – – 12.5 17.6 21.6 31.9 – – – – 11 France (Berre lagoon) Ezzat (1965)* Scales Females 13.1 20.1 26.6 32.5 36.9 41 – – TL 9–42 1055 (M + F) Males 12.7 18.8 25.4 30.3 34 – – – France (Berre lag., Ezzat (1964) Scales TL – – 14 19.4 24 31.5 – – – – Port de Bouc) Tunisia (Tunis) Heldt (1948) Scales TL – – 18.8 27 32 – – – – – Italy (near Rome) Serbetis (1939)* Scales TL 14–43 40 13.5 25 33.5 39.2 – – – – 221 222 G. N. Hotos

Scales from the second and third row just under the base of was taken as the month when the distance of the outermost the first dorsal fin from both sides of the body were removed annulus to the scale’s margin was minimal. The measurements and preserved in labelled envelopes for future treatment. Liza were repeated twice by one reader. Only when the two readings aurata scales from this body area are uniform and well were in agreement were the counts recorded. readable. In the laboratory the scales were put in Petri dishes with distilled water for 20–30 min; the epidermis was then removed by finger rubbing. The scales were thereafter rinsed Results several times in 10% NaOH and distilled water in order to From a total of 1048 golden grey mullets examined, the sex clean them of any tissue remains, and then fixed between was determined in 705 specimens. The scales of this species are labelled glass plates for microscopical examination. The scales of the percoid type and ctenoid. Those from the body area just were measured under transmitted light using a Nicon SMZ-U under the first dorsal fin are bilaterally symmetrical and highly binocular microscope equipped with an ocular graduated readable for detection of annuli. Their central area that micrometer. Measurements were taken by counting the contains the scale’s nucleus is clear and easily delineated in the corresponding subdivision lines (named hereafter as micros- early ontogenetic stages, slightly darkening at the later stages copy units) on the micrometer. The micrometer was then but nevertheless permitting the appropriate measurements to calibrated with a special microscopy plate with an imprinted be taken. The wavy circuli (the growth lines) on its front area scale of known distance. After calibration, the measured (embedded in the body part) are well shaped perimetrically, microscopy units multiplied by 0.095 can be converted to creating a general appearance of wide homogeneous growth millimetre. All scales acceptable for analyses were examined, areas consisting of evenly spaced circuli. However, the density and results were averaged for each individual fish. of the circuli in the front area is higher when compared with The measurements concerned the total scale radius (Rmax), the sides, where some of them fade. This condition becomes which is the distance from the scale nucleus to the scale margin progressively prominent at stages corresponding to total of the front side (embedded in the body part) of the scale in lengths over 3 cm (Fig. 4). vertical position, the radius from the scale nucleus to each The annulus is recognized as a condensation of a group of annulus (Rn), and the distance from the last (outermost) circuli (usually two or three), evenly delineated and recogniz- annulus to the margin of the scale (Rmarg.). Scales without able around the front and the lateral area of the scale. False annuli were assigned as 0+ age, those with one as 1+, with annuli were characterized by incomplete delineation, especially two as 2+ and so on in order to build a size-age key for the in the lateral areas of the scale. The age analysis (Table 2) estimated ages. The time period of the creation of the annuli revealed nine age classes, including the 0+ group that is

Table 2 Mean measured total length (TL) for Liza aurata with 95% confidence interval (CI) and respective TL estimated from the histograms of Figure 1

Range Modes in TL obtained Assigned age No. of specimens Mean TL (cm) SD ±95% CI of samples (TL) from histogram

All specimens 0+ 267 17.26 3.48 0.42 9.7–24 10, 17 1+ 371 25.72 2.26 0.23 20–31.5 23 2+ 187 27.72 1.61 0.23 20.5–34.3 27 3+ 90 31.20 1.61 0.34 27.3–36.5 32 4+ 79 34.65 1.71 0.38 29.3–38.1 35 5+ 18 39.72 2.14 1.06 35–42.5 41 6+ 28 44.63 2.96 1.15 37.3–49.3 46 7+ 7 50.71 1.71 1.58 48–52.8 50 8+ 1 59 59 Sum 1048 Females 0+ – – 1+ 142 26.11 2.04 0.34 20–31.5 27 2+ 115 27.82 1.55 0.29 24.7–34.3 29 3+ 59 31.31 1.65 0.43 28.6–36.5 32 4+ 42 34.72 1.95 0.61 29.3–38.1 35 5+ 10 39.75 2.3 1.64 35–42.5 42 6+ 17 44.04 3.4 1.75 37.3–49.3 46 7+ 7 50.71 1.71 1.58 48–52.8 50 8+ 1 59 59 Sum 393 Males 0+ – – 1+ 154 25.77 2.24 0.36 20.6–31.1 23 2+ 71 27.68 1.76 0.42 20.5–32.3 27 3+ 31 31 1.56 0.57 27.3–34.9 33 4+ 37 34.57 1.42 0.47 32.4–37.8 35 5+ 8 39.69 2.0 1.68 35.7–42.1 39 6+ 11 45.54 1.89 1.27 42.9–48.8 45 7+ – 8+ – Sum 312 1 Study on the scales and age estimation of the grey golden mullet 223

10 2+ 40 All samples 35 All samples 8 30 6 25 1+ 20 0+ 4 15 0+ 3+ 10 2 4+ 6+ 5 5+ 7+ 8+ 0 0 0 5 10 15 20 25 30 35 40 45 50 55 60 0+ 1+ 2+ 3+ 4+ 5+ 6+ 7+ 8+

15 Females 1+ 40 Females 12 35 2+ 30 9 25 20 6 3+ 15

Percentage 3 4+ 5+ 6+ 10 7+ 8+ 5 0 0 5 10 15 20 25 30 35 40 45 50 55 60 0 1+ 2+ 3+ 4+ 5+ 6+ 7+ 8+

15 2+ 50 Males 45 Males 12 40 35 9 30 1+ 25 6 20 Fig. 1. Total length and age frequency 3+ 15 distributions of golden grey mullet 3 4+ 10 Liza aurata sampled in the Messo- 5+ 6+ 5 longhi lagoon, 1992–1994. n ¼ 1048, 0 0 number of males ¼ 393, number of 0 5 10 15 20 25 30 35 40 45 50 55 60 1+ 2+ 3+ 4+ 5+ 6+ females ¼ 312 TL (cm) Age classes

assigned to fish with no annulus. The older ages recorded strong relationship between the two variables. Thus, a definite (7+ and 8+ years) were represented by only eight female relationship can be established between scale measurement and specimens, while those of the three younger ones (0+, 1+ and fish length that secures the back-calculation procedure. As the 2+ years) were the most numerous, represented by 267, 371 two sexes exhibited similar slope and intercept values at the and 187 specimens, respectively. All specimens of the 0+ group 90% and higher confidence level (Fb ¼ 2.23, P ¼ 0.135; were classified as immature because of the lack of developed Fa ¼ 5.38, P ¼ 0.02), the pooled (including also the immature gonads. Immature specimens were also present in the 1+ class fish) Rmax ) TL regression can be used by the power equation: 0.77 2 at a considerable percentage, but disappeared from the 2+ and TL ¼ 1.5501Rmax (r ¼ 0.95; N ¼ 1048; P < 0.001). The older classes. There was a wide overlap of length ranges exponent of this equation differs significantly from the value between the ages (Table 2; Fig. 1), especially in the first four 1 (P < 0.01), an indication of allometry between the two classes in an almost identical pattern for both sexes. variables. After logarithmic transformation of the scale and The length–frequency distribution (Fig. 1) can nevertheless length values, the power equation can become a linear one in support the age estimations from scale readings as there are the form: ln TL ¼ 0.438 + 0.77 lnRmax. The so fitted straight distinct modes in the histograms which can be allocated to age line (Fig. 2) intercepts the Y axis at 0.438, which corresponds classes, and the modal lengths are in good agreement with the to a TL of 1.55 cm that represents the size of the fish at which mean values of the lengths measured per age class. The 0+ class scales first appear. This is quite close to the relevant observa- exhibited two distinct peaks, probably because of multiple tions made on the collected fry. recruitment pulses within the same year, owing to the extended The time of formation of the annulus was examined using spawning period of the species in this area (Hotos et al., 2000). the specimens of both sexes of all months in order to eliminate The hatching dates of major recruitment cohorts and/or growth to the greatest possible degree the bias resulting from the condition appear to differ substantially among years, as the absence or the insufficient sampling that occurred in some mean values of the radii per annulus number show statistically months. The use of pooled data from both sexes appears to be significant differences among year classes (age groups of fish), acceptable as no significant statistical differences were found in except for annulus R7 which includes a too small sample size annulus radii between sexes (Table 3; P > 0.05). From Fig. 3 (Table 3, Kruskal–Wallis test). The radii per annulus number it is evident that the least distance (Rmarg.) between the do not indicate any general trend toward higher ages of the fish. outermost annulus and the scale’s margin (Rmax) was recorded No differences in the mean radii per annulus number were in February and, consequently, this month is accepted as the found among sexes (ANOVA, P > 0.05; Table 3). period in which the annulus is created. The relation between scale radius (Rmax) and TL was calculated for both sexes separately and combined, also including juveniles, using a power and a linear model Discussion (Table 4). Both models provided a good fit to the data, with As otoliths alone have been used in only a few studies for age a high degree of determination (r2 > 0.9), indicating a very estimation of Mugilidae because of ÔmisreadingÕ problems 224

Table 3 Mean values (in microscopy units) with ±95% confidence interval (CI) of the radii of successive annuli on the scales of Liza aurata caught at different ages. The mean values are tested for statistically significant differences among age classes within each annulus number by the Kruskal–Wallis test (upper part). Differences among both sexes are tested per annulus number by ANOVA (lower part)

Annulus number

Age class N R1 R2 R3 R4 R5 R6 R7 R8

1+ 371 25.72 ± 0.373 ––––––– 2+ 187 23.85 ± 0.436 36.15 ± 0.551 –––––– 3+ 90 20.22 ± 0.607 35.26 ± 0.864 45.08 ± 0.724 ––––– 4+ 79 23.48 ± 0.683 36.4 ± 0.688 43.86 ± 0.785 49.84 ± 0.785 –––– 5+ 18 24.16 ± 0.708 40.38 ± 1.646 52.27 ± 1.97 56.88 ± 2.163 60.22 ± 1.71 – – – 6+ 28 25.32 ± 0.651 35.67 ± 0.775 46.25 ± 0.672 51.71 ± 0.752 57.25 ± 0.848 60.71 ± 0.83 – – 7+ 7 24.71 ± 1.029 34.14 ± 0.638 44.14 ± 1.805 53.85 ± 1.55 60.28 ± 1.383 64.42 ± 1.048 67.42 ± 1.048 – 8+ 1 26 36.01 47.03 56.04 61.99 65.98 69.02 72 N 781 781 410 223 133 54 36 8 1 Mean value ±95% CI 24.34 ± 0.258 36.12 ± 0.362 45.35 ± 0.522 51.45 ± 0.699 58.72 ± 0.815 61.58 ± 0.864 67.62 ± 0.992 72 Kruskal–Wallis Tstat. 167.5 31.4 46.3 44.05 22.81 15 1.84 P-value <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 >0.05 Annuli R1 R2 R3 R4 R5 R6 R7 R8 Females (±95% CI) 24.07 ± 0.362 36.22 ± 0.481 45.59 ± 0.657 51.78 ± 0.9 58.48 ± 1.06 61.56 ± 1.19 67.62 ± 0.99 72 N 393 251 136 77 35 25 8 1 Males (±95% CI) 24.45 ± 0.384 35.97 ± 0.55 45 ± 0.866 51 ± 1.13 59.15 ± 1.356 61.63 ± 1.125 – – N 312 158 87 56 19 11 – – Fratio 1.99 0.48 1.22 1.18 0.62 0.01 – – P-value >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 – – Sum 705 410 223 133 54 36 8 1 .N Hotos N. G. 1 Study on the scales and age estimation of the grey golden mullet 225

Table 4 Descriptive parameters of the relation between the total length (TL, cm) and the scale radius (Rmax, in microscopy units) by using the multiplicative and linear equations for the different categories of Liza aurata samples

Equation N abr2 SE(a) SE(b)t(b) P-value

b Males TL ¼ a* Rmax 312 1.1525 0.8515 0.90 0.0579 0.0154 9.64 <0.01 Males TL ¼ a + bRmax 312 3.2116 0.584 0.91 0.4306 0.0097 b Females TL ¼ a* Rmax 393 1.032 0.8831 0.90 0.0542 0.0143 8.17 <0.01 Females TL ¼ a + bRmax 393 1.9083 0.6192 0.92 0.413 0.009 b Females + males TL ¼ a* Rmax 705 1.0738 0.8716 0.90 0.039 0.01 12.84 <0.01 Females + males TL ¼ a + bRmax 705 2.384 0.6061 0.91 0.299 0.0066 b All specimens TL ¼ a* Rmax 1048 1.5501 0.7751 0.95 0.018 0.005 44.07 <0.01 All specimens TL ¼ a + bRmax 1048 4.1776 0.5685 0.95 0.1587 0.0039

12 The P-value checks for statistical difference of (superscript b) from the value of 1.

4.2 working with L. ramada and cephalus, respectively, observed either annulus-like formations on the scales of the 3.8 fry, or two supposed annuli per year on the scales of adult fish. Contrary to that, in the present study in which a sufficiently 3.4 large sample with a wide range of fish lengths was used, no annulus was observed on scales of specimens under 20 cm TL, lnTL 3 which form the first two modes in the length frequency distribution and are considered as 0+ group (Fig. 1). It is 2.6 quite possible that the specimens represented by the second mode were erroneously assigned as being of older age in other studies of the species (Table 1), especially in those that relied 2.2 2.3 2.7 3.1 3.5 3.9 4.3 4.7 solely upon the length frequency analysis. Also, false annuli lnRmax may have been counted as true annuli. This cannot be clarified as not enough elements of proof, such as photos and scale Fig. 2. Total length (TL) ) scale radius (Rmax) relationship of golden grey mullet, Liza aurata (all specimens) sampled in the Messolonghi analysis data, were provided. lagoon. n ¼ 1048 (natural logarithms used, TL in cm, Rmax in Concerning the creation of the annuli, especially that of the microscopy units, multiplied by 0.095 converted to millimetre) first annulus (designated as age 1+), two facts should be clarified: the month at which the annulus is formed, and the true age of the fish corresponding to the month of its 16 formation. Most references support the formation of only Pooled ages (1+) – (7+) +/– SE 14 one annulus per year during cold months in other mugilid species of temperate and subtropical regions (Thomson, 1951; 12 Erman, 1959; Farrugio and Quignard, 1974; Libosvarsky, 10 1976; Cambrony, 1984; Koutrakis et al., 1994), although there 8 are cases where the time period of formation is protracted or

6 variable while the fish are growing (Kesteven, 1953; Kennedy and Fitzmaurice, 1969). For L. aurata in the literature, there is 4 no information about the exact period of creation of the Rmarg. ( × 0.095 = mm) = Rmarg. ( × 0.095 2 annuli, but in the present study in the Messolonghi 0 lagoon, annuli undoubtedly are formed during February (Figs 3 and 6). DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV Months The true age at the time of the annulus formation can vary from less than or more than a year. The first case means that Fig. 3. Mean monthly distances (R ) between the outermost marg. the fish formed the annulus very early in life. Such was annulus and the scale’s margin (Rmax) pooled from all age classes of golden grey mullet, Liza aurata sampled in the Messolonghi lagoon reported for M. cephalus in N. Australia (Grant and Spain, 1975) ageing 0.5 years at first annulus formation, 1.5 years at (Thong, 1969), the scales that are highly readable were chosen the second, and so forth. Under such conditions, accepting as in this study in order to facilitate comparison with most of the correct the above findings introduces an error in the usual available studies that used the same method (Thomson, 1966; assignment of the ichthyological ages of 1+, 2+, and Arruda et al., 1991; Kraljevic´ and Dulcˇ ic´ , 1996; among would not represent the true age of this fish. In another others). The age estimation and age validation of Mugilidae example of M. cephalus in the Salton Sea (USA), the annulus is based on the assumption that only one annulus is formed per formed 12 months after hatching; in this case the biological 3year on their scales (Kesteven, 1942; Farrugio and Quignard, age of the fish coincides with the ichthyological age (Hend- 21974; Koutrakis et al., 1994) should be considered with some ricks, 1961). precautions. One is the recognition of the annuli and the other Contrary to M. cephalus above, L. aurata does not form an is the correct estimation of the time that the annulus is formed. annulus during its first winter in the Messolonghi lagoon. This El Maghraby et al. (1973) and Cech and Wohlschlag (1975) is probably attributable to some kind of difference in the 226 G. N. Hotos

Fig. 4. Photos of Liza aurata scales at the fry stage, sampled in the Messo- longhi lagoon. No annulus present. Arrows at D, E and Findicate cycloid (D) and ctenoid (E and F) scales

Fig. 5. Photos of Liza aurata scales at 0+, 1+, 2+ and 4+ age classes sampled in the Messolonghi lagoon. Arrows indicate the relevant annuli 1 Study on the scales and age estimation of the grey golden mullet 227

If it occurs in L. aurata, it could jeopardize the entire age estimation that is attempted in the present study. However, from examination of the large sampling used, it was shown that the scales of L. aurata up to age 4+ possess a satisfactorily clear central part (Fig. 5) that does not negatively interfere with age estimation. The overlapping of the radius of the first four annuli that appears in the specimens should be attributed to variations in the hatching date and growth rather than to a possible hidden first annulus. This variation is a consequence of the extended reproductive period that charac- terizes Mugilidae (Farrugio and Quignard, 1974). For fish older than 4+, there is a possibility for the first annulus not to be detected, as the central part of their scale enlarges, begins to darken more, and possibly masks the annulus. However, from the examination of the recorded values of the radius of the 5th–8th annulus, it seems that these values are in accordance with the expected progressive increase relative to those previous (Table 3). Additionally from Table 3, the data for R1 derived from fish of higher ages exhibit no general increase in their values that could indicate that a hidden annulus has been omitted. The presence of an annulus in immature fish (Hotos et al., 2000) of age-class 1+ suggests that the formation of the annulus is rather related to seasonal growth patterns affected by physical parameters such as the water temperature, rather than to reproductive activity (Newman et al., 2000). There is great variation in the literature on the maximum 5recorded age (Table 1). Nikolskii (1954) for the Caspian Sea also reported age 8+ as the maximum age for that species. Thong (1969) and Alexandrova (1964) for Brittany and the Black Sea, respectively, recorded age 7+; in the remainder of the literature, age 6+ is considered maximum for L. aurata, Fig. 6. Photos of Liza aurata scales at 5+, 6+ and 7+ age classes with many studies recording ages up to 4+. On the contrary, sampled in the Messolonghi lagoon. Arrows indicate the relevant 6Kraljevic´ and Dulcˇ ic´ (1996) for the Adriatic and Reay (1987) annuli for Great Britain recorded L. aurata of 11 and 14 years old, respectively. Reay (1987) attributed the rareness of these ages in the samples to a preference of the bigger and very aged fish biology of the two species rather than to the difference between of this species for the open sea, with the consequence of their the environments. Liza aurata in this particular area exhibits a lack of appearance in the usual near shore sampling collec- protracted spawning period from September until January, tions. Although the information presented on the age analysis and probably February (Hotos et al., 2000). Consequently, its is not sufficiently detailed and the age of 14 years seems fry will appear in coastal waters about 2 months after questionable, the general hypothesis seems to be well founded, hatching, that is, from November until April. In the examined as in the present study the ages 7+ and 8+ were also sampled specimens of small fish, some of them are 4–5 months old in in the sea adjacent to the Messolonghi lagoon. Additionally, February; however, although February has been proven as the literature data indicate older maximum ages for specimens month of the annulus formation (Fig. 3), no annulus has been from the sea than for those from inland waters. In the present recorded on scales of the fry for that month, not even in study area the highest recorded age of L. aurata was 8+, adjacent months. Additionally, from examination of the bigger which seems to be the maximum age based on the fact that the specimens, no annulus has been recorded which could corres- only fish collected was very large (59 cm TL) and no bigger fish pond to the first February of their lives. Thus, the first annulus was ever recorded in the literature. Specimens of ages 6+ and is laid on the scales when their true age is somewhere between 7+ were adequately represented and of reasonable smaller 12 and 17 months. Such a case was also recorded for mugilids sizes. on the Mediterranean coast of France (Cambrony, 1984) and In conclusion, the present study findings based on the scale for Sparisoma cretence in the Aegean Sea (Petrakis and analyses of a sufficiently large and representative sample Papaconstantinou, 1990). Based on the above, the wide range including fry, young and adult fish of L. aurata allowed of the fish TL per age class (Table 2) in the present study can discussion and clarification given the uncertainties in annuli be adequately explained. recognition (Figs 4–6), the exact time of their formation Another possible problem in the examination of mugilid (Fig. 3), the reported doubts about the visibility of the first scales is related to the recognition of the first annulus (and annuli in older fish (Figs 5 and 6), the question of annulus probably of the second) in the older specimens, because of the formation in fry during the first winter (Fig. 4), and the opaque appearance of their scale’s central part as reported in maximum age for the species. A conclusive discussion of the literature. Such cases have been reported for M. cephalus possible differences between local stocks of this species requires 4(Pajet, 1923; Erman, 1959; Hendricks, 1961; Kennedy and information obtained with comparable methods. The present Fitzmaurice, 1969; Grant and Spain, 1975; Libosvarsky, 1976). approach attempts to provide a standard for comparison. 228 G. N. Hotos

References Kesteven, G. L., 1942: Studies in the biology of Australian mullet. I. Account of the fishery and preliminary statement of the biology of Albertini-Berhaut, J., 1978: Croissance line´ aire et ponde´ rale de Mugil dobula. Bull. Austr. CSIRO Melb. 157, 1–99. M. auratus dans le Golfe de Marseille compare´ e a celle de Kesteven, G. L., 1953: Further results of tagging sea mullet, Mugil M. capito. Cybium, 3eme serie 4, 51–60. cephalus L. on the eastern Australian coast. Austr. J. Mar. Alexandrova, K., 1964: Peculiarities in the growth of Mugil auratus R. Freshwater Res. 4, 251–306. along the Bulgarian coast of the Black Sea. Izv. Tsentr. Nauch. Konides, A.; Anastasopoulou, K.; Photis, G.; Koussouris, T.; Izsl. Rib. Varna 4, 80–87. Diapoulis, A., 1992: Growth of four Mugilidae species in Western Andaloro, F., 1983: Contribution on the knowledge of the age and Greek lagoons. 27th European Mar. Biol. Symp. Trinity College, growth of the Marsala lagoon golden mullet, Liza aurata (Risso, Univ. Dublin, Ireland, 7–11 September 1992. 1810). Rapp. Comm. Int. Mer. Me´ dite´ rr. 28, 81–82. Koutrakis, E. T.; Sinis, A. I.; Economidis, P. S., 1994: Seasonal Arne, P., 1938: Contribution a` l’e´ tude de la biologie des muges du occurrence, abundance and size distribution of gray mullet fry Golfe de Gascogne. Rapp. P.-V. Comm. Int. Explor. Me´ diterr. 11, (pisces, Mugilidae) in the Porto-Lagos lagoon and Lake 77–115. Vistonis (Aegean Sea, Greece). Isr. J. Aquacult. Bamidegh 46, Arruda, L. M.; Azevedo, J. N.; Neto, A. I., 1991: Age and growth of 182–196. the grey mullet (Pisces, Mugilidae) in Ria de Aveiro (Portugal). Kraljevic´ , M.; Dulcˇ ic´ , J., 1996: Age, growth and mortality of the Sci. Mar. 55, 497–504. golden grey mullet Liza aurata (Risso, 1810) in the eastern Brusle, J.; Cambrony, M., 1992: Les lagunes Me´ diterrane´ e: Des Adriatic. Arch. Fish. Mar. Res. 44, 69–80. nurseries favorables aux juve´ niles de poissons euryhalins et/ou des Libosvarsky, J., 1976: Lepidological note on grey mullet (Mugil capito) pieges redoutables pour eux? Vie Milieu 42, 193–205. from Egypt. Zoologicke Listy 25, 73–79. Cambrony, M., 1984: Identification et pe´ riodicite´ du recrutement des Modrusan, Z.; Teskeredzic´ , E.; Jukic´ , S., 1988: Biology and ecology of juve´ niles de Mugilidae dans les e´ tangs littoraux du Languedoc- Mugilidae species on the Eastern Adriatic coast (Sibenik Bay). Roussillon. Vie Milieu 34, 221–227. FAO Fish. Rep. 394, 159–167. Cech, J. J.; Wohlschlag, P. E., 1975: Summer growth depression in the Newman, J. S.; Cappo, M.; Williams, McB. D., 2000: Age, growth striped mullet M. cephalus. Contrib. Mar. Sci. 19, 92–100. and mortality of the stripey, Lutjanus carponotatus (Richardson) Coutelan, R., 1953: Contribution a` l’e´ tude des muges de l’e´ tang de and the brown-stripe snapper, L. vitta (Quoy and Gaimard) Thau. DES Universite´ des Sciences et Techniques du Languedoc, from the central Great Barrier Reef, Australia. Fish. Res. 48, 263– Montpellier. 275. Drake, P.; Arias, A. M.; Rodriguez, R. B., 1984: Biology of mullets Nikolskii, G. V., 1954: Special Ichthyology. Translated from Russian (Osteichthyes, Mugilidae) in the esteros of San Fernando (Cadix). by J. I. Lengy & Z. Krauthamer. Israel Programme for Scientific I. Growth in length and weight. Invest. Pesquera 48, 139–156. Translation, IPST cat. no. 233. El Maghraby, A. M.; Hashem, M. J.; El-Sedfy, H. M., 1973: Some Pajet, G. W., 1923: The determination of the rate of growth of Bouri, biological characters of Mugil capito (Cuv.) in Lake Borollus. Mugil cephalus in Lake Mariyut. Rep. Fish. Serv. Egypt 1922, 43– Bull. Inst. Oceanog. Fish. 3, 55–88. 49. Erman, F., 1959: Observations on the biology of the common grey Petrakis, G.; Papaconstantinou, C., 1990: Biology of Sparisoma mullet (Mugil cephalus). Proc. Tech. Pap. Gen. Fish. Counc. cretense in the Dodecanese (Greece). J. Appl. Ichthyol. 6, 14–23. Mediterr. 16, 157–169. Quignard, J. P.; Farrugio, H., 1981: Age and growth of grey mullets. Ezzat, A., 1964: Contribution a` lÕe´ tude de la biologie des Mugilidae de In: Aquaculture of grey mullets. O. H. Oren (ed.). University la re´ gion de lÕe´ tang de Berre et de Port de Bouc. Rec. Trav. Stn. Press, IBP 26, Cambridge, pp. 155–184. Mar. Endoume 47, 187–202. Reay, P. J., 1987: A British population of the grey mullet, Liza aurata Ezzat, A., 1965: Contribution a` l’e´ tude de la biologie de quelques (Teleostei, Mugilidae). Mar. Biol. Assoc. UK 67, 1–10. Mugilidae de la re´ gion de l’e´ tang de Berre et de Port de Bouc. Sancho, J. M., 1975: Estudio comparativo del crecimiento del Albur, Thesis, Marseille. Mugil auratus, en tres esteros de la provincia de Cadiz y Farrugio, H.; Quignard, J. P., 1974: Biologie de Mugil (Liza)ramada parametros mas importantes obtenidos. Publ. Tec. Junta Est. Risso 1826 et de Mugil ()labrosus Risso, 1826 (Poissons, Pesca 11, 231–243. Teleoste´ ens, Mugilides) du Lac de Tunis. Age et croissance. Bull. Serbetis, C. D., 1939: L’eta` e l’accrescimento dei Mugilidi. Boll. Pesca Inst. Oceanogr. Peˆ che Salammboˆ 3, 139–152. Piscic. Idrobiol. 15(6), 628–707. Grant, C. J.; Spain, A. V., 1975: Reproduction, growth and size Thomson, J. M., 1951: Growth and habits of the sea mullet, Mugil allometry of Mugil cephalus L. (Pisces: Mugilidae) from North dobula Gunther, in western Australia. Aust. J. Mar. Freshw. Res. Queensland inshore waters. Aust. J. Zool. 23, 181–201. ¨ 1, 199–220. Heldt, H., 1948: Contribution a` lÕe´ tude de la biologie des muges des Thomson, J. M., 1966: The grey mullet. Oceanogr. Mar. Biol. 4, 301– lacs Tunisiens. Bull. Stn. Oceanogr. Salammboˆ 41, 1–35. 335. Hendricks, L. J., 1961: The striped mullet Mugil cephalus L. Fish. Bull. Thong, L. H., 1969: Contribution a lÕe´ tude de la biologie des Mugilides Calif. 113, 95–103. (Poissons, Teleoste´ ens) des cotes du Massif Armoricain. Trav. Hickling, C. F., 1970: A contribution to the natural history of the Fac. Sci. Rennes, Oceanogr. Biol. 2, 55–136. English grey mullet (Pisces, Mugilidae). J. Mar. Biol. Ass. UK 50, Thong, L. H., 1971: Notes sur la croissance du mullet Mugil (Liza) 609–633. auratus Risso, 1810 (Te´ leoste´ en, Mugilide´ ) dans la partie orientale Hotos, G.; Avramidou, D.; Ondrias, I., 2000: Reproduction biology of du Golfe du Morbihan. Trav. Lab. Biol. Halieutique. Univ. Liza aurata (Risso, 1810), (Pisces: Mugilidae), in Klisova lagoon Rennes 5, 3–27. (Messolonghi, W. Greece). Fish. Res. 47, 57–67. Katselis, G.; Minos, G.; Marmagas, A.; Hotos, G.; Ondrias, I., 1994: Author’s address: Dr George N. Hotos, Laboratory for Culture of Seasonal distribution of Mugilidae fry and juveniles in Messo- Euryhaline Fish, Department of Aquaculture and longhi coastal waters, Western Greece. Bios (Macedonia, Greece) Fisheries, Technological Educational Institution 2, 101–108. (T.E.I.) of Messolonghi, GR-30200 Messolonghi, Kennedy, M.; Fitzmaurice, P., 1969: Age and growth of thicklipped Greece. grey mullet labrosus in Irish waters. J. Mar. Biol. Ass. E-mail: [email protected] US 49, 683–699.

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