Journal of Fisheries and Aquaculture Research JFAR Vol. 4(1), pp. 016-027, August, 2019. © www.premierpublishers.org, ISSN: 9901-8810

Research Article Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record

Sandra Agius Darmanin1*, F. Saadet Karakulak2, Adriana Vella3 1,3Conservation Biology Research Group, Department of Biology, University of Malta, Msida, MALTA 2Istanbul University, Faculty of Aquatic Sciences, Istanbul, TURKEY

Age, growth, length-weight relationship (LWR), condition factor (K) and relative condition factor (Kn) were investigated for the annular seabream Diplodus annularis collected from non- commercial catches around the Maltese Islands between July 2012 and December 2017 (N=1661). The age distribution of the specimens was found to range between 0+ and 17+ years with a positive allometric growth. Average Kn was found to be 1.03 in males and 0.99 in females. The -1 growth parameters of the von Bertalanffy equation were: L∞=21.38, K=0.123year and tₒ = - 5.40year for all individuals (males, females, hermaphrodites and unsexed). This study is the first reference for D. annularis on the length weight equation parameters, condition factor, relative condition factor and age around the Maltese Islands and establishes a new maximum of 17 years.

Keywords: Sparidae, Mediterranean, Malta, Length-weight relationship, relative condition factor, Fulton’s condition factor, maximum age.

INTRODUCTION

In the Maltese islands, fisheries are generally small scale Tsikliras, 2003). The body condition factor is affected by with most vessels under 10 m in length (NSO, 2018). The interactions among habitat characteristics. These include main species targeted by commercial fisheries include the food and habitat availability, competition, physical factors, horse mackerel (Trachurus sp.), dolphin fish (Coryphaena parasitic infections, pollution and fish physiology, hippurus), swordfish (Xiphias gladius), Bluefin tuna consequently supplying information about the (Thunnus thynnus) and demersal species (NSO, 2017). physiological state of the fish in relation to its welfare Recreational fishing is also very important, with both sport (Lizama and Ambrósio, 2002). and hobby fishing very popular amongst anglers (Agius Darmanin and Vella, 2018). D. annularis is listed as least concern (Russell et al., 2014). It is present in the Eastern Atlantic, Mediterranean, Black Information on parameters that associate weight to length Sea and Sea of Azov (Bauchot and Hureau (1986). It is a of fish is valuable in instituting standard results of fish demersal species with a preferred habitat of bottoms sampling programs (Morato et al., 2001) that are of great covered in seagrass beds in shallow waters extending significance for fish stock evaluation. The length-weight from 0 to 50 metres in depth (Bauchot, 1987). It is an relationship (LWR) is a frequently used tool in the calculation of the fish’s average weight per length class in addition to morphological comparisons between *Corresponding Author: Sandra Agius Darmanin; populations of the same species (Benedito-Cecilio et al., Conservation Biology Research Group, Department of 1997). These relationships are of use in calculating Biology, University of Malta, Msida, MALTA biomass when only length measurements are available. Email: [email protected]; Tel: +356 23401120 These parameters are valuable indications of fish body Co-Author 2E-mail: [email protected] condition (factor K) which permits comparisons of species Tel: +90 2124555700/16418 Fax: +90 212 5140379 growth rates between different regions (Koutrakis and 3E-mail: [email protected]; Tel: +356 2340 2790

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record Agius Darmanin et al. 017

omnivorous diurnal feeder with preference for Mollusks, magnification using reflected light against a dark Teleosts and small Crustaceans (Pita et al., 2002; background (Mendoza, 2006; Abecasis et al., 2008). Sánchez-Jerez et al., 2002; Chaouch, 2014). It was Larger otoliths were embedded in resin and sectioned at a previously considered a protandric species, but recent thickness of 1mm using an Accutom precision cutter, then findings by Alonso-Fernández et al. (2011) indicate non- sanded and polished manually. Sections were mounted on functional hermaphroditism. Spawning time varies across a slide using DPX medium. The annual increments were regions with the earliest starting in the Canary Islands in counted under a stereo microscope by passing light January (Pajuelo and Lorenzo, 2001) and ending latest in through the section. In both methods, when the two August in the central Aegean Sea (İlkyaz et al 2018). readings of the same otolith differed, a third reading was conducted. The otolith was discarded and considered In the Maltese Islands, D. annularis is an important species unreadable if this third reading was not conclusive in the recreational fishery and comprises the second most (Lorenzo et al., 2002). A subsample was used to determine frequently caught (10.1%) species during sport shore the percentage of otoliths with opaque margin for each fishing competitions held on a regular basis around the month using otoliths sampled in 2016 (largest sample Maltese Islands and is also very popular with recreational year). This method allowed the annual formation of the fishers (Agius Darmanin and Vella, 2019). It is however of rings to be determined (Pajuelo and Lorenzo, 2001; low commercial interest. Despite this, stock assessment Lorenzo et al., 2002; Méndez Villamil et al., 2002; Brouwer studies in Maltese waters are lacking therefore the aim of and Griffiths, 2004). Each fish was then aged and allotted this study was to investigate the aspects of age, growth to a year class with reference to the date of capture once and condition of D. annularis from around the Maltese the annual ring formation was confirmed (Pajuelo and coast and provide essential knowledge for the Lorenzo, 2003). development of a management strategy for this species. Length-to-weight relationship was estimated for all the fish sampled and separately for males and females using the MATERIALS AND METHODS exponential regression equation:

A total of 1661 fish specimens were collected from July W= aLb (Le Cren, 1951) (1) 2012 till December 2017 during 132 shore sport fishing where L is the total length (cm) and W is the total weight competitions taking place in 46 coastal locations around (g), a is a coefficient related to body form while b is an Malta, Gozo and Comino (Agius Darmanin and Vella, exponent that indicates isometric growth when equal to 3. 2019) together with 35 recreational fishing observations The parameters of a and b were estimated by linear and 33 target sampling sessions and specimens donated regression on the transformed equation: by recreational and sport fishermen (Figure 1; see supplementary data for list of locations with GPS co- Log10 (W) = log10 (a) + b log10 (L) (2) ordinates). Sampling was carried out continuously, several The null hypothesis of the isometric growth (H0: b =3) was times monthly throughout the sampling period. To tested using t-test at the 0.05 significance using the minimize the impact of the study on fish populations, most equation: of the fish collected had perished in keep-nets during fishing competitions. Upon collection, samples were t = b - 3/S.E(b) (3) placed immediately in ice with a subsample analyzed fresh where t is t statistic, S.E (b) Standard error of b was while the rest were frozen for subsequent processing. obtained from linear regression for testing significant differences among slopes (b) between two regressions for Lengths (total length (TL) and fork length (FL)) and weights the same species (Morey et al., 2003). were recorded to the nearest 0.1cm and 0.01g respectively. Sexes were confirmed by macroscopic and The linear regression model was used to examine the microscopic examination of the gonads. Sagittal otoliths relationship between the total fish’s length and weight and were removed, cleaned, dried and kept for further analysis. the otolith’s length and weight. The relationship between Prior to the age reading process all the otoliths were otolith length and weight and fish length (TL) and weight weighed (Otolith weight OW; to 10-2mg) and their length were determined using the equation: (Otolith length OL) measured along the longest dimension between the anterior and posterior edges of the otolith Y = a + bx (4) using digital Vernier callipers (0.1mm) prior to storing. where, y is the otolith length/weight, x is the fish length Otoliths under 0.0090g which were small enough to be (TL)/fish weight (TW) a is the intercept value and b is the used for whole otolith annual increment reading were coefficient value (slope). The strength of each of the immersed in glycerine as a clearing agent. Age estimates relationships was evaluated from the determination were obtained by counting the number of opaque bands coefficient (r2) (Zar, 1984). All data was tested and the from the nucleus to the margin. The annual increments outliers removed prior to each linear regression analysis were counted under a compound microscope at x10 for best model fit.

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record J. Fish. Aquacul. Res. 018

Figure 1: Map showing sampling locations. 1=Malta Freeport, 2=Boilers Wharf, 3=Deep Water Quay, 4=Laboratory Wharf

To summarise the age composition D. annularis, age- estimated weight calculated from the length-weight length keys with 1 cm intervals were constructed. The relationship. The difference between Kn and K is that the Bertalanffy (VB) growth equation: former is measuring the divergence of an individual from the average weight for length, while the latter is measuring (-k(t-t )) Lt = L∞ (1 - e 0 ) (5) the divergence from a hypothetical ideal fish (Le Cren, which has been widely used to describe the growth pattern 1951). in fish stocks e.g., Gordoa and Molí (1997), Pajuelo et al. (2003), Mati Skoko et al. (2007) and Alós et al. (2010), was The growth performance was determined using the growth used to describe the growth of D. annularis. Where Lt = index (Ф’) through the equation: total length at age t, k is a rate constant with units of reciprocal time, L∞ represents the asymptotic length (mean Ф’ = lnK + 2lnL∞ (8) maximum length), t0 represents the theoretical age at to average the growth parameters and compare the results length 0. The Ford-Walford plot and Chapman’s method obtained in this study with published results from other were used to estimate the parameters (Sparre and regions (Sparre and Venema, 1998). All statistical Venema, 1998). analyses were performed using SPSS software package version 24 and a significance level of 0.05 was accepted. Fulton’s condition factor was determined by using the expression: RESULTS K = 100W/Lb (6) where, W is the weight in grams, L is in cm and b is Length-weight relationship exponent of the length-weight relationship (Torcu Koc et al., 2002; Nash et al., 2006). The relative condition factor Of the 1661 fish examined, 369 were males, 759 females, (Kn) was calculated using the equation: 30 hermaphrodites, 357 immature fish and 146 had decomposed gonads so could not be sexed. The total Kn= Wt/We (7) length ranged from 6.5 and 22.3cm (mean 13.8 ±2.5cm) as suggested by Le Cren (1951) and used in other studies (Figure 2) while weight ranged from 4.5g to 238.8g (mean in the Mediterranean (Torcu Koc et al., 2002). Where Wt is 51.0 ±31.4g) the observed body weight and We is the theoretically

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record Agius Darmanin et al. 019

(B)

Figure 2: Length frequency graph by sex (1=Male, 2=Female, 3=Unsexed juvenile, 4 = Bisexual, 5=Unsexed (C) (decomposed gonads)). Figure 3: D. annularis length weight relationship. A) All population, B) Females, C) Males. Linear regressions fitted to estimate the WLR were significant for males, females and the whole sample Condition factor (K) and relative condition (Kn) (p<0.001) (Figure 3). Student t-test showed that the ‘b’ values obtained for males (M) and females (F) and all the The condition factor was determined from the observed individuals were significantly different (M, t=3.00, t(2)0.05, 363 body weights and calculated separately for males and =1.96; F, t=4.091, t(2)0.05, 745 = 1.96; all individuals (t=8.308, females. The mean condition factor (K) was found to be t(2)0.05, 1628=1.96) indicating a positive allometric growth 1.44 (±0.05) in males and 1.39(±0.04) in females. Relative which implies that the fish becomes relatively deeper- condition factor (Kn) values were also calculated bodied as it increases in length (b>3.0). The slope (b- separately for males and females and the monthly values value) of the total length-total weight regression did not are presented in Figure 4. The Kn values were the lowest differ significantly between the males and females in June and July. The mean Kn values for males was (ANCOVA: F (2, 1105) =2.031. p=0.154). 1.03(±0.04) and 0.99(±0.03) for females.

(A) Figure 4: Monthly changes in relative mean condition (Kn) for D. annularis.

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record J. Fish. Aquacul. Res. 020

Otolith relationship with fish length and weight

1614 fish had their otoliths successfully extracted. Linear regression analysis showed strong relationships between the total length (TL) and otolith length (OL), total length and otolith weight (OW), total weight (TW) and otolith weight and total weight and otolith length (Table 1).

Age

A concentric pattern of translucent and opaque zones was readily distinguishable in the otoliths allowing age interpretation. Of the 1614 otoliths examined, 1406 were used for age estimation. 208 were discarded as their age readability was not optimal. The highest percentages of Figure 7: Diplodus annularis length at age data with fitted 0.123 2 otoliths with opaque rings at the margin were observed VBGF curve: Lt = 21.38 [1-e- (t + 5.396)]. r =0.99 between May and September (Figure 5). The ages of D. annularis ranged from 0+ to 17+ years (Table 3). The oldest female was 12+ years while the oldest male was DISCUSSION 17+ years old (Figure 6). The mean total lengths of individuals allocated to each group were used to fit the von There is no published data on length and age structure of Bertalanffy growth function presented in Figure 7 (Ages 12 D. annularis, from the Maltese Islands and few other and 17 years were excluded from the calculations due to studies in the Mediterranean that have considered such low sample size). Asymptotic values of total length (L∞) large sample size and sampling effort through the years were higher for males than for females. The growth (Table 4). Considering the importance of this species for performance index Ф’ was estimated at 1.744, 1.704 and the sport and recreational fishery, biodiversity and food 1.750 for males, females and all the sample respectively value, basic information on the LWRs and relative and the results compared with those of previous studies condition (Kn) of this species can be very helpful in (Table 4). studying its population dynamics and devise appropriate management measures for sustainable management, conservation and responsible utilization of such resources (Koushlesh et al., 2018). The condition factor (K) and relative condition factor Kn in this research, although indicating good condition, were lower than values from the Eastern Mediterranean (Torcu Koc et al., 2002). These may be the result of different environmental conditions such as nutritional condition, sea temperature (Froese, 2006) and fishing pressure (Götz et al., 2008) in the different areas. Other causes may be the potential bias introduced by the methodology used such as ageing and length composition of the samples (Mouine et al., 2010). The lowest Kn values observed in June and July in both Figure 5: Monthly percentages of otoliths with opaque males and females may also be linked to the spawning edge for D. annularis of the Maltese Islands (N = 377) period as observed by Mouine et al. (2012).

The maximum observed length (22.3cm) found for D. annularis in this study was similar to results reported by Matić Skoko et al. (2007) (23cm) and Pajuelo and Lorenzo (2001) (20.9cm). This study provides useful information on the length-weight relationships of D. annularis in Maltese waters which are also very useful tools in fisheries research. They allow the conversion of growth-in-length to growth-in weight that is used in fisheries management. The b value for this species was found to be consistent with the expected range of 2.5-3.5 (Froese, 2006). The results can be considered as mean values for the species since the fish samples were collected during different seasons throughout the sampling period. Figure 6: Example of sectioned otolith showing 17year-old D. annularis

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record Agius Darmanin et al. 021

D. annularis showed positive allometric growth which tends to be very rapid in the juvenile stages and slows matches with the results for the Aegean and Levantine down substantially in the adult stages (Kallianiotis et al., seas, the Adriatic and Ionian seas and the western and 2005). Changes in the environmental conditions between south western Mediterranean (Table 2) with the other habitat of juveniles and adults may be responsible for the studies indicating isometric growth. These inter-regional differences recorded between juveniles and adult growth differences in b-values may be attributed to: Seasonality; pattern. Diet regime may also be important indicating that Effects of different areas; Differences in number of the food required during sub adult and adult stage may be specimens examined; Differences in observed length more limiting since diet shifts towards larger prey as the ranges of the species caught; Area/season effect; Food fish increase in size (Rodríguez-Ruiz et al., 2002). A study availability; Feeding rate; Gonadal development or by Sánchez-Jerez et al. (2002) indeed observed significant spawning period (Weatherley et al., 1987; Wootton, 1999; differences in diet between habitat type and among Moutopoulos and Stergiou, 2002; Froese, 2006; different sized fish. It is therefore important to study the Moutopoulos et al, 2011). growth of juvenile stages in more detail in future studies (Kallianiotis et al., 2005). The phi-prime test (Ф’) estimations present an indication of the reliability of estimations since it is intimated that phi- The maximum published age till now was 13 years (Matić prime values are analogous for the same species and Skoko et al., 2007). The maximum age of 17 years found genera (Bellido et al., 2000). The calculated asymptotic in this study is the oldest recorded in published literature. length for the whole population shows similarity with other This may indicate a higher longevity of this species research especially for the population in the Adriatic Sea population around the Maltese Islands or better sampling (Matić‐Skoko et al., 2007). Lower asymptotic lengths are strategy allowing for larger coverage of different aged presented for the population in the Balearic Sea (Alós et specimens in relatively shallower waters. The fact that only al. 2010) and Aegean Sea (Torcu Koc et al. 2002) (Table one 17-year-old specimen was collected may indicate that 4). However, in the latter, the maximum age was only 9+ such old specimens are very rare. Older specimens years with the authors stating that the calculated sampled in this study were caught from the Malta Freeport asymptotic length was dramatically underestimated, with quay where fishing is not allowed all along the quay and the older individuals displaying a lower asymptotic length carried out by permission granted only for this research. than the observed total length at the moment of catch Other fishing restricted sites such as Boilers wharf, (Torcu Koc et al., 2002). While the majority of research Laboratory Wharf and Deep Water quay (Figure 1), which indicated a higher asymptotic length for females, in the are all ship berthing sites found within the Grand Harbour present study, males had a higher asymptotic length than also accounted for most of the older specimens sampled. females. This is similar to the research carried out in the This indicates that reduced fishing pressure may result in Aegean Sea (Torcu Koc et al., 2002). higher longevity for this species and that such sites are contributing to its survival. Restrictions are in place for Such differences between regions may be the caused by these sites due to heavy shipping activity and berthing and differences in age reading methodologies and in the size not for the conservation of fish species. The current range of sampled fish (Mouine et al., 2010). A lower k was minimum legal size for D. annularis in European Union observed in this study indicating a slower growth rate. The countries is 12 centimetres and is largely unenforced in the calculated values for Ф’ were similar and are therefore Maltese Islands. No other restrictions such as bag limits characteristic of the species (Mouine et al., 2010). and temporary fishing closure are in place for this species. Differences in parameters with other regions may also be Thus, based on the findings of this study, where older due to segregation of the local stock from other regions. specimens were caught in sites with limited access to Vella and Vella (2011) had found that the Maltese fishing, the D. annularis population would benefit from population lacked genetic diversity indicating that it is a fishing restrictions such as in marine protected areas. localised and inbred population rather than being a population in expansion with random mating within a large regional population. CONCLUSIONS

An overlap was observed between the different age The present study gives a new maximum age of 17+ years groups (Table 3). This is a common occurrence in fishes for this species and provides the first reference on the due to the presence of differences in growth rates among length-weight relation, condition factor, relative condition individuals within the age groups (Mahmoud, 2010). In the factor and age structure of the population of D. annularis majority of the published works (Table 4) in which the von around coastal waters of the Maltese Islands. Although Bertalannfy growth model is applied, including this study, this population shows a good condition, local conservation the estimations of t0 are negative suggesting that this management is advised to safeguard and protect the local model does not accurately describe growth in the early stock from overexploitation. Future genetic studies that stages (Sparre and Venema, 1998; Gordoa and Molí, compare the local stock with different regions in the 1997; Kraljević et al., 2007) where growth in Sparid fish Mediterranean are recommended.

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record J. Fish. Aquacul. Res. 022

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Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record Agius Darmanin et al. 025

APPENDIX

Table 1 - Otolith dimensions and sizes of D. annularis. Dependent Independent Sample Equation r2 SE of Significance variables variables size estimate D. annularis TL OL 1558 TL=2.802(OL) – 1.262 0.795 0.945 p=<0.001 TL OW 1565 TL=8.648 + 243.903(OW) 0.892 1.116 p=<0.001 TW OL 1558 TW=29.543(OL) – 108.677 0.752 13.349 p=<0.001 TW OW 1559 TW=2679.400(OW) – 6.378 0.741 14.263 p=<0.001 OL=otolith length (mm), OW=otolith weight (g), TL=total length (cm) and TW= total weight(g). r2 = determination coefficient. All regressions were significant at p<0.001.

Table 2 - Parameters of length-weight relationship of D. annularis in the Maltese Islands and other regions. Species Authors Locality Length a b Sex r2 Growth type D. annularis Present study Maltese Islands TL 0.014 3.090 F 0.97 A+ 0.014 3.081 M 0.97 A+ 0.013 3.108 All 0.98 A+ Torcu Koc et al., 2002 Aegean Sea Turkey FL 0.037 2.798 F 0.93 A- 0.046 2.696 M 0.92 A- Bok et al., 2011 Sea of Marmara, Turkey TL 0.022 2.957 All 0.99 I İlkyaz, et al., , 2008 Central Aegean Sea, Turkey TL 0.012 3.130 F 0.96 - 0.013 3.090 M 0.95 - 0.011 3.160 All 0.96 - Cicek et al., , 2006 Mersin Bay, Levantine Sea, TL 0.011 3.147 All 0.96 A+ Turkey Karakulak et al., , 2006 Northern Aegean Sea, TL 0.007 3.315 All 0.97 A+ Turkey 0.008 3.271 F 0.98 A+ 0.007 3.305 M 0.98 A+ Keskin and Gaygusuz, 2010 Erdek bay, Sea of Marmara, TL 0.013 3.110 All 0.99 I Turkey Samsun et al., 2017 Central Black Sea, Turkey TL 0.031 2.840 All 0.92 - Morey et al., 2003 Balearic Islands and Iberian TL 0.012 3.167 All 0.97 A+ coast, Western Mediterranean Borges et al., 2003 Algarve, Atlantic Sea, TL 0.015 3.140 All 0.97 - Portugal Matić‐Skoko et al., 2007 Adriatic Sea, Croatia TL 0.014 3.073 All 0.98 I Maci et al., 2012 Adriatic Sea, Italy TL 0.017 3.304 All 0.99 A+ Moutopoulos et al., 2013 Korinthiakos Gulf, Ionian TL 0.011 3.114 All 0.98 A+ Sea, Greece Cherif et al., 2008 Gulf of Tunis, South West TL 0.010 2.86 F 0.92 A+ Mediterranean 0.056 2.72 M 0.92 A+ 0.012 2.90 All 0.93 A+ Moutopoulos et al., 2011 Klisova Lagoon, Greece FL 0.008 3.10 All 0.96 - Papas Lagoon, Greece FL 0.003 3.26 All 0.98 -

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record J. Fish. Aquacul. Res. 026

Table 3 - Age-TL key for all individuals of D. annularis. TL (cm) 0+ 1+ 2+ 3+ 4+ 5+ 6+ 7+ 8+ 9+ 10+ 11+ 12+ 17+ Total 6.0-6.9 4 4 7.0-7.9 4 4 8.0-8.9 11 11 9.0-9.9 36 12 1 49 10.0-10.9 30 32 29 4 1 1 97 11.0-11.9 16 36 70 29 8 2 1 162 12.0-12.9 1 18 91 72 27 15 3 7 1 1 1 237 13.0-13.9 6 44 76 44 39 18 6 3 1 237 14.0-14.9 1 4 22 43 38 38 27 10 6 1 1 2 193 15.0-15.9 2 10 27 35 40 15 10 6 5 1 151 16.0-16.9 1 9 16 25 20 10 14 4 2 1 102 17.0-17.9 1 11 22 9 6 8 3 5 2 67 18.0-18.9 1 5 5 14 9 6 2 1 43 19.0-19.0 1 6 10 2 2 4 1 26 20.0-20.9 1 2 2 2 2 1 1 11 21.0-21.9 2 1 2 2 1 1 9 22.0-22.9 1 1 1 3 Total 103 111 267 261 186 191 115 71 49 21 14 11 5 1 1406 % 7.33 7.89 18.99 18.56 13.26 13.58 8.18 5.05 3.49 1.49 1.00 0.78 0.36 0.07 100 Mean TL 9.81 11.46 12.40 13.35 14.35 15.03 15.80 16.28 16.44 17.09 17.34 18.57 19.56 20.30 13.74

Table 4 - Von Bertalanffy growth parameters and growth performance indexes (Φ’) for D. annularis from this study and in different regions. Species Author Area Method Length Max N L∞ K t0 sex Ф’ type age (cm) (year-1) (year) (year) D. Present study Maltese Islands Otoliths TL 17 1406 24.63 0.091 -6.07 M 1.744 annularis Central Mediterranean 22.92 0.096 -6.96 F 1.704 21.38 0.123 -5.40 All 1.750 Alós et al., 2010 Balearic Sea, Mallorca Otoliths TL 9 2614 15.2 0.470 -0.07 M 2.036 15.9 0.450 -0.12 F 2.056 Gordoa and Molí, 1997 Catalan coast, Spain Otoliths TL 7 180 17.1 0.560 -0.02 All 2.214 Torcu Koc et al., 2002 Aegean Sea Turkey Otoliths FL 7 652 17.2 0.210 -1.73 F 1.794 18.4 0.140 -2.93 M 1.674 16.6 0.200 -1.96 All 1.742 Nouacer and Djebar, Golfe d' Annaba, Scales TL 6 648 19.5 0.460 - All 2.243 2007 Algeria Wurtz and Matricardi, Tyrrhenian Sea, Italy Length- TL - 21.1 0.386 - All 2.235 2002 frequency Matić‐Skoko et al., Adriatic Sea, Croatia Scales TL 13 768 21.9 0.125 -1.68 M 1.778 2007 22.1 0.126 -1.54 F 1.790 24.0 0.126 -1.66 All 1.859 Tosunoglu et al., , 1997 Aegean Sea, Turkey - FL - - 22.5 0.159 -2.39 All 1.906

Bradai et al., 2001 Gulf of Gabes, Tunisia Scales TL 6 - 22.6 0.160 -2.00 All 1.912

Pajuelo and Lorenzo, Atlantic Sea, Canary Otoliths TL 6 371 24.6 0.271 -0.88 M 2.215 2001 Islands 25.0 0.243 -0.90 F 2.181 L∞: asymptotic mean length; k: constant expressing the rate at which length reaches L∞; to: hypothetic age at zero length.

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record Agius Darmanin et al. 027

Supplementary data Marsa (Ras ħanzir) 35.883867, 14.505537 Marsa 3 35.882575, 14.503146 List of D. annularis sampling locations with corresponding Marsalforn (Gozo) 36.072255, 14.260253 GPS co-ordinates. Marsaskala 2 35.865221, 14.568492 Marsaxlokk 35.839084, 14.544018 Location GPS co-ordinates Marsaxlokk pontoons 35.840072, 14.546886 Bighi 35.893187, 14.523536 St Julians 35.919451, 14.491948 Valletta (Pixkerija) 35.893170, 14.511563 Valletta Breakwater 35.903128, 14.522490 Vittoriosa (Toqba) 35.890855, 14.520335 Baħar iċ-ċagħaq (1) 35.953951, 14.433027 Valletta (Foss) 35.901583, 14.515318 Birżebbuġia LC 35.829573, 14.530616 Valletta (Pitch) 35.900870, 14.510195 Cospicua (baċir) 35.881564, 14.520197 Valletta (waterfront) 35.889606, 14.508601 Deep water quay 35.886111, 14.501695 Senglea 35.889763, 14.516970 Gzira 35.902591, 14.495763 Laboratory wharf 35.881401, 14.515575 Mġarr ix-xini (Gozo) 36.019849, 14.271932 Boilers wharf 35.887568, 14.515418 Msida 35.895550, 14.492530 Sliema 35.907865, 14.506710 Valletta Ferry 35.895295, 14.513885 Manoel Island 35.904850, 14.506586 Valletta wine wharf 35.887941, 14.506117 Senglea Maċina 35.885542, 14.520082 Sa Maison terminal 35.894266, 14.498198 Xemxija Veċċja 35.946036, 14.387438 St Paul's Islands 35.966222, 14.405560 Xemxija 35.951017, 14.388767 Mistra 35.903667, 14.507737 St Paul's Bay Jetty 35.951883, 14.407799 Qawra 35.959023, 14.422587 Għadira 35.970044, 14.350550 St Maria Estate 35.968407, 14.368135 Aħrax Point 35.993285, 14.372004 White tower bay 35.994304, 14.362200 Armier 35.993982, 14.362488 Baћar iċ-ċagћaq 2 35.949922, 14.429036 Baћar iċ-ċagћaq 3 35.937085, 14.462789 Birzebbugia Al fresco 35.831728, 14.530550

Għar id-Dwieb 35.866650, 14.356310

Ft St Angelo Marina 35.891495, 14.517527

Manoel Island Yacht yard 35.905385, 14.499207

St George's Bay 35.926930, 14.488997 Pieta 35.896543, 14.495580 Shipbuilding 35.878661, 14.501236 Ta Xbiex 35.898981, 14.500728 Xagћjra 35.869526, 14.572224 Accepted 29 July 2019 Żonqor 35.869282, 14.572653 Marsaskala (Pitch) 35.866600, 14.568061 Citation: Agius Darmanin S, Karakulak FS, Vella A (2019). Marsaskala 35.865345, 14.563287 Population Dynamics of the Annular Seabream Diplodus Marsaskala (Jerma) 35.860574, 14.574421 annularis (Linnaeus, 1978) from the Maltese Islands Birżebbuġia 35.865345, 14.563287 Reveals a New Maximum Age Record. Journal of Comino 36.005496, 14.335479 Fisheries and Aquaculture Research, 4(1): 016-027. Ħondoq (Gozo) 36.028010, 14.322960 Dwejra 36.050750, 14.190290 Marsa 2 35.880226, 14.503437 Ft St Angelo 35.892903, 14.515758 St Paul’s bay Sirens 35.949929, 14.404040 Copyright: © 2019 Agius Darmanin et al. This is an open- Cirkewwa Quay 35.987880, 14.328441 access article distributed under the terms of the Creative Malta Freeport 35.818703, 14.546609 Commons Attribution License, which permits unrestricted Kalkara 35.889402, 14.526208 use, distribution, and reproduction in any medium, Manoel Island pontoons 35.902578, 14.500674 provided the original author and source are cited.

Population Dynamics of the Annular Seabream Diplodus annularis (Linnaeus, 1978) from the Maltese Islands Reveals a New Maximum Age Record