Mar Biol (2008) 154:623–630

DOI 10.1007/s00227-008-0955-6

RESEARCH ARTICLE

Spatial–temporal pattern of blueWn tuna (Thunnus thynnus L. 1758) gonad maturation across the Mediterranean Sea

Gilad Heinisch · Aldo Corriero · Antonio Medina · Francisco J. Abascal · Jose-Miguel de la Serna · Robert Vassallo-Agius · Antonio Belmonte Ríos · Antonio García · Fernando de la Gándara · Christian Fauvel · Christopher R. Bridges · Constantinos C. Mylonas · Saadet F. Karakulak · Isik Oray · Gregorio De Metrio · Hanna Rosenfeld · Hillel Gordin

Received: 24 January 2007 / Accepted: 4 March 2008 / Published online: 18 March 2008© Springer-Verlag 2008

Abstract Atlantic blueWn tuna (BFT; Thunnus thynnus) isa migrating species straddling the North Atlantic Ocean andMediterranean Sea. It is assumed that this species is dividedinto a western and an eastern stock, which spawn in theGulf of Mexico and the Mediterranean Sea, respectively.To learn more about the reproductive behavior of the east-ern BFT stock, we tracked gonadal development in adultWsh that were sampled between April and July during threeconsecutive years (2003–2005). Sampling campaigns werecarried out using common Wshing methods at selected loca-

tions within the Mediterranean Sea, namely Levantine Sea,Malta, and Balearic Islands. An additional sampling point,Barbate, was situated northwest of the Straits of Gibraltaralong the Atlantic coast. Morphometric parameters such asthe total body mass (MB) and the weights of the gonads(MG) were recorded, and the respective gonadosomaticindex (GSI) values were calculated. The data collectedrevealed two important trends: (1) GSI values are higher inWsh caught in the eastern rather than the western locationsacross the Mediterranean Sea, and (2) the GSI reaches max-

Communicated by A. Mclachlan.

G. Heinisch (&) · H. Rosenfeld · H. GordinIsrael Oceanographic and Limnological Research, National Center for Mariculture, P.O. Box 1212, 88112 Eilat, Israele-mail: giladh@ocean.org.il

A. Corriero · G. De MetrioDepartment of Animal Health and Well-being, University of Bari, Str. Prov. per Casamassima Km 3, 70010 Valenzano, BA, Italy

A. MedinaDepartment of Biology, Faculty of Marine and Environmental Sciences, University of Cadiz, Av República Saharaui, 11510 Puerto Real, Cádiz, Spain

F. J. AbascalIstituto Español de OceanograWa, C.O. Canarias, Ap. 1373, Santa Cruz de Tenerife, Spain

J.-M. de la SernaIstituto Español de OceanograWa, Centro OceanográWco de Malaga, Apartado 285, 29640 Fuengirola, 4 IEO, Malaga, Spain

R. Vassallo-AgiusMalta Centre for Fisheries Sciences, Fort San Lucjan, Marsaxlokk BBG06, Malta

A. B. RíosTuna Graso, S.A., Carretera de la Palma Km 7, Paraje la Estrella, 30593 Cartagena (Murcia), Spain

A. García · F. de la GándaraIstituto Español de OceanograWa, Centro OceanográWco de Murcia, Ctra. de la Azohía s/n, 30860 Puerto de Mazarrón (Murcia), Spain

C. FauvelStation Expérimentale d’Aquaculture, Chemin de Maguelone, Institut Français de Recherche pour l’Exploitation de la Mer, 34250 Palavas les Flots, France

C. R. BridgesHeinrich-Heine Universität, Institut für Zoophysiologie, 40225 Düsseldorf, Germany

C. C. MylonasInstitute of Aquaculture, Hellenic Center for Marine Research, P.O. Box 2214, 71003 Heraklion, Crete, Greece

S. F. Karakulak · I. OrayFaculty of Fisheries, Istanbul University, Ordu cad. No. 200, TR-Laleli-Istanbul, Turkey

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imum values between late May and early June in LevantineSea (eastern Mediterranean Sea), and only 2 and 4 weekslater in the central (Malta) and western (Balearic Islands)locations, respectively. The advanced gonadal developmentin BFT correlates well with higher sea surface tempera-tures. Our Wndings also distinguish the northern LevantineSea BFT population (mean MB 78.41 § 4.13 kg), and theBarbate BFT population with the greatest MB (all Wshsampled > 100 kg). These data reXect a situation in whichthe eastern Mediterranean basin may function as a habitatfor young BFT, until they gain a larger MB and are able tomove to the Atlantic Ocean. However, the existence ofgenetically discrete BFT populations in the MediterraneanSea cannot be ruled out.

Introduction

The Atlantic blueWn tuna (Thunnus thynnus Linnaeus,1758) (BFT) is a commercially valuable species in the EastAtlantic Ocean and the Mediterranean Sea (Ottolenghiet al. 2004). Fish are caught by long-lines, hand-lines or tra-ditional traps, and shipped mainly to the Japanese market(Bjørndal and Brasão 2004), or caught alive by purse sein-ers, transferred into towing cages and then on to Xoatingcages, where they are fattened for approximately 6 monthsbefore being slaughtered (Ottolenghi et al. 2004). AlthoughWshing quotas are regulated by the International Commis-sion for the Conservation of Atlantic Tunas (ICCAT), thetwo recognized Atlantic BFT stocks (i.e., western and east-ern Atlantic BFT) are subjected to severe Wshing pressure(Fromentin and Powers 2005, and references therein). Theeastern stock is intensely Wshed, especially upon itsentrance into the Mediterranean Sea through the Straits ofGibraltar and its aggregation in schools around the spawn-ing grounds. It is estimated that since the 1970s, the BFTspawning stock biomass (SSB) declined by 81 and 52% inthe western and eastern Atlantic populations, respectively(ICCAT 2007).

Over the years, BFT have attracted many research eVortsthat expanded the knowledge of the general biology andWsheries management of this species (reviewed by Matheret al. 1995; Fromentin and Powers 2005; Rooker et al.2007). Most of the data referring to the BFT spawning sea-son and spawning areas are largely based on two basic cri-teria: the presence of individuals with ready-to-spawngonads, and/or the presence of eggs and larvae in the saidarea. The earliest recognition of BFT larvae in the Mediter-ranean Sea dates back to the investigations of Sella (1924,1929) and Sanzo (1932) who found BFT larvae in theSicilian waters. More information regarding BFT spawningwas obtained later by using macroscopic scales of gonadmaturation (Rodríguez-Roda 1964a, b, 1967), biometric

indices like the index of maturity (Sarà 1963, 1973) orgonadosomatic index (GSI; de la Serna and Alot 1992), andhistological analysis of the gonads (Baglin 1982; Corrieroet al. 2003; Karakulak et al. 2004) as well as quantitativeanalysis of the reproductive steroid hormones and vitello-genin (i.e., a glycolipophosphoprotein precursor of the yolkproteins), whose concentrations in plasma or muscle varyaccording to the reproductive state of the Wsh (Bridges et al.2001; Susca et al. 2001). The above-mentioned studiesindicate that BFT reproduce during the spring–summerperiods. The western stock spawning season is from Aprilto July in the Gulf of Mexico and along the Florida Straits(Richards 1976; Montolio and Juarez 1977; Rivas 1978;Baglin 1982). The eastern stock reproduces in the Mediter-ranean Sea during the months of May to July (Corrieroet al. 2003; Abascal et al. 2004; Karakulak et al. 2004; Fro-mentin and Powers 2005). Furthermore, the possible exis-tence of spawning grounds in the mid-west Atlantic is still aquestion of debate (Lutcavage et al. 1999).

Besides the historically known Mediterranean spawninggrounds in the waters around the Balearic Islands in thewest, and the central waters around Malta and AeolianIslands (Sella 1924, 1929; Sanzo 1932; Rodríguez-Roda1967; Dicenta 1975; Nishida et al. 1997; Susca et al. 2001;Medina et al. 2002; Corriero et al. 2003), the presence of aspawning area in the eastern Mediterranean, i.e., LevantineSea, has only recently been demonstrated (Karakulak et al.2004; Oray and Karakulak 2005). However, the aforemen-tioned studies refer to only a few zones within the Mediter-ranean Sea, are based on limited sampling data, and fallshort of covering the inclusive seasonal reproductive cycleof the eastern BFT stocks.

In light of the above, this study has adopted a compara-tive approach, aiming at understanding the gonadal matura-tion patterns of BFT by verifying the spatial and temporalpatterns of this species’ gonadal development across theMediterranean Sea.

Fig. 1 Sampling locations at the entry of and within the Mediterra-nean Sea: 1 Barbate, East Atlantic Ocean, near the Spanish coast line;2 Balearic Islands; 3 Malta; 4 Northern Levantine Sea between Cyprusand Turkey. Samples were collected in 2003–2005. Circles indicatingthe sampling location are not to scale

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Materials and methods

Specimen collection

The study took advantage of the commercial BFT catch.Adult BFT, numbering 649 in total, were caught at fourdiVerent locations at the entrance of, and within the Medi-terranean Sea (Fig. 1). Sampling campaigns were con-ducted from May throughout July in three consecutiveyears (2003–2005). The number of specimens and the spe-ciWc Wshing method by which Wsh were caught at each loca-tion are listed in Table 1. Biometric parameters, includingfork length (FL, cm), total body mass (MB, kg) and gonadmass (MG, g) were measured for each Wsh. The relativegonad mass (GSI) was calculated as: 100 MG MB

¡1.

Histological analysis of the gonads

Soon after capture, slices of BFT gonads were Wxed inBouin’s Wxative or 10% buVered neutral formalin, dehy-drated in increasing ethanol concentrations, clariWed inxylene and embedded in paraYn wax. Thick sections of5 �m were cut and stained with haematoxylin-eosin. Forthe classiWcation of the reproductive state of females, themost advanced oocyte stage was recorded for each speci-men, according to the classiWcation of Corriero et al.(2003). The presence of atretic and postovulatory follicleswas also recorded. Vitellogenic atretic follicles were classi-Wed as � or � stage according to Hunter et al. (1986). Forthe classiWcation of the reproductive state of males, the typeof spermatogenic cysts was recorded and the quantity of

Table 1 Morphometric data of blueWn tuna sampled at the diVerent locations during the years 2003–2005

The percentages of females within a given sampled population are in parentheses. The MB and FL values represent mean § SE

Mean body mass is signiWcantly diVerent between the locations (P < 0.0001, Kruskal–Wallis nonparametric test)

No. Location Fishing method Sample size [no. of specimens (%)]

Body mass (MB; kg)

Fork length (FL; cm)

1 Barbate Traps 80 (60) 200.78 § 7.07 220.96 § 3.77

2 Balearic Islands Long-lines (max. 1,200 hooks baited with squid) 154 (43) 205.06 § 4.60 211.84 § 2.24

Purse seines 76 (61) 182.32 § 6.55 205.01 § 3.19

3 Malta Long-lines (max. 2,500 hooks baited with Atlantic mackerel/Japanese squid)

104 (62) 167.94 § 6.21 220.44 § 3.31

4 Levantine Sea Purse seines 235 (54) 78.41 § 4.13 151.81 § 2.20

Fig. 2 Total body mass (MB) distribution at the diVerent sam-pling locations. The upper limit of each weight class is reported on the x-axis. The MB distribu-tion is signiWcantly (P < 0.0001) diVerent between the four sam-pling locations

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spermatozoa in the lumen of seminiferous lobules was sub-jectively evaluated.

Statistical analysis

Data were analyzed using JMP IN® 5.1 statistical software(SAS Institute Inc., Cary, NC, USA). Normal distributionswere conWrmed using Shapiro–Wilk W test for the Good-ness of Wt. Analysis for signiWcant diVerence between themeans (one-way ANOVA followed by Tukey–KramerHSD, � = 0.05) was tested on the arcsine transformation ofthe GSI value. Kruskal–Wallis nonparametric test was usedto determine signiWcant diVerence between mean bodymass, since the data were not normal-distributed. G-statis-tics for goodness of Wt was applied to test diVerencesbetween body mass distributions. Parameters in Wgures andtext are presented as mean § SE (Sokal and Rohlf 1995).

Results

Biometric characteristics

Based on the size of the Wsh, two extreme groups werediscerned (P < 0.0001, Kruskal–Wallis). These includerelatively small Wsh (mean MB = 78.41 § 4.13 kg; FL =151.81 § 2.20 cm) in the northern Levantine Sea, and remark-ably large Wsh in Barbate (mean MB = 200.78 § 7.07 kg;FL = 220.96 § 3.77 cm) and the Balearic Islands (meanMB = 205.06 § 4.60 kg; FL = 211.84 § 2.24 cm: long line;MB = 182.32 § 6.55 kg; FL = 205.01 § 3.19 cm: purseseine). An intermediate body size group was found nearMalta (mean MB = 167.94 § 6.21 kg; FL = 220.44 §3.31 cm). A signiWcant diVerence (G2 = 216.1, P < 0.0001)in the MB distribution among these groups was alsoobserved (Fig. 2). Furthermore, the Barbate BFT sampleconsisted of over 95% large Wsh (150–250 kg) and lackedWsh smaller than 100 kg, whereas the Levantine Sea sampleconsisted of over 40% small Wsh whose MB ranged between25 and 100 kg.

Spatial–temporal pattern of gonad maturation and spawning

The average GSI values of male and female BFT did notvary signiWcantly (P > 0.05, student’s t test; arcsine trans-formation resulted in a normal distribution) from each other(checked temporally and spatially), and were thus pooledand analyzed together. Moreover, no “Wshing gear eVect”on GSI values was detected in Wsh caught at the BalearicIslands (P > 0.05, student’s t test). During May and Junesamplings, the GSI values were higher in Wsh caught inthe eastern Mediterranean locations compared to the GSI

values from Wsh caught in the central and western parts ofthe basin (Table 2). For example, during June maximum GSIvalues were recorded in the Levantine Sea (4.91 § 0.14;mean 2003–2005), whereas a gradual decrease wasobserved towards western locations (Malta, 4.23 § 0.22;Balearic Islands, 3.25 § 0.16; Barbate, 1.30 § 0.39). More-over, the maximum GSI values measured at the aforemen-tioned sampling locations showed temporal variations, withGSI values peaking during late May to early June in Wshcaught in the Levantine Sea, and only 2 and 4 weeks later inMalta and Balearic Islands, respectively (Fig. 3).

The histological analysis of the gonads (Fig. 4) showedthat during mid-May to early June, BFT caught in the Lev-antine Sea were reproductively active as indicated by thepresence of oocytes at late vitellogenesis stage in the ova-ries and seminiferous lobules Wlled with spermatozoa inthe testes. Most of the analyzed females also displayedoocytes in Wnal maturation, including hydrated oocytes, and

Table 2 GSI values of BFT sampled across the Mediterranean Sea

GSI values from Wsh sampled in the same location and year that are sig-niWcantly diVerent (P < 0.05) are indicated with a (*) (Student’s t-test),or with a diVerent lowercase letter (Tukey–Kramer HSD)

Year Location Month Sample size (no. of specimens)

GSI (mean § SE)

2003 Barbate May 12 0.61 § 0.44

June 17 1.29 § 0.48*

Balear May 21 2.44 § 0.33a

June 37 3.01 § 0.32a

July 14 2.14 § 0.30a

Malta May 5 4.05 § 0.68a

June 19 3.96 § 0.45a

July 8 1.52 § 0.40b

Levant May 17 5.93 § 0.37

June 26 5.45 § 0.38

2004 Barbate May 21 1.09 § 0.29

June 4 1.36 § 0.86

Balear May 14 2.00 § 0.35a

June 31 3.03 § 0.31b

July 6 4.00 § 0.53b

Malta May 25 2.14 § 0.26

June 27 4.51 § 0.33*

Levant May 63 4.17 § 0.17

June 70 5.16 § 0.20*

2005 Barbate May 26 0.78 § 0.19

Balear May 33 2.03 § 0.17a

June 58 3.52 § 0.22b

July 16 3.26 § 0.31b

Malta June 18 4.06 § 0.40

July 2 1.92 § 0.88

Levant June 59 4.37 § 0.22

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postovulatory follicles. In the waters around Malta, sampledWsh showed gonads with histological signs of recent orimminent spawning during mid-June to early July. Fishcaught in the waters around the Balearic Islands were stillin spawning condition during mid–late July.

The spatial–temporal pattern of BFT spawning in theMediterranean Sea during the sampling period is summa-rized in Fig. 5.

Discussion and conclusions

During three consecutive years (2003–2005), we studiedthe gonadal development in BFT populations sampled inthe East Atlantic before entering the Mediterranean Sea andin the Mediterranean Sea aggregating around allegedspawning grounds.

Biometric parameters of BFT specimens, caught by Wsh-ermen operating under commercial quotas and gathered byscientists, provided a large data base, which enabled aphysiological insight into BFT reproduction season. Muchof these data are not reported to ICCAT by commercialWsheries, due to a lack of funding or proper management.

Our records show evidence of a particular characteristicof the eastern Atlantic BFT population caught around Bar-bate: this population consists mostly (>95%) of large Wshand lacks Wsh smaller than 100 kg. Similar Wndings basedon a larger sampling size (approximately 5,000 specimens)were demonstrated by de la Serna and Alot (1992). In con-trast, our Wndings show that the eastern Mediterranean BFTpopulation, caught by purse seines in the Levantine Searegion, consists of a large (»40) percent of small Wsh(<100 kg). The relatively small body size of the latter popu-lation was also reported by Karakulak et al. (2004). A pos-sible basis for a skewed size distribution within a sampledpopulation is the use of discriminatory Wshing methods,such as the long line by which larger Wsh tend to be caught(Bjørndal and Brasão 2004). On the other hand, our Barbateand Levantine Sea samples were obtained by trap andpurse-seine gears, respectively. Therefore, we tend to adoptSarà’s (1963) suggestion that the Mediterranean basin func-tions as a habitat for young BFT, until they gain a large MB

and are able to perform a trans-Atlantic migration. Matheret al. (1995) also suggest that BFT entering the MediterraneanSea from the Atlantic Ocean are relatively large (>100 kg)and head towards the Balearic Islands for spawning, while

Fig. 3 Gonadal development of blueWn tuna at selected sampling locations of the Mediterranean Sea from May throughout July. In Barbate BFT were sampled between 24 April and 08 June; Balearic Islands: 02 May–25 July; Malta: 02 May–09 July; Levantine Sea: 11 May–13 June. Identical lowercase letters repre-sent statistical non-signiWcance (P > 0.05, Tukey–Kramer HSD)

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other Wsh continue their eastern migration towards centralMediterranean locations. Studies carried out with taggedBFT monitored electronic signals along their migrationpath across the Atlantic Ocean and up to Malta (Block et al.2005). No electronic signals for the migrating BFT wererecorded east of Malta. Interestingly, our records indicatethat the BFT population around Malta exhibits a statisti-cally normal size distribution, which could suggest that thislocation is a mixing point for small BFT arriving from the

Levantine Sea and large BFT arriving from the AtlanticOcean.

In recent years the existence of discrete BFT populationswithin the Mediterranean basin has become a controversialissue. Genetic studies conducted with BFT caught aroundthe Ionian Sea, Tyrrhenian Sea and the Balearic Islandssuggest the presence of a genetically discrete BFT popula-tion at the eastern Mediterranean Sea (Carlsson et al. 2004;Carlsson et al. 2007). However, similar studies with Wshcaught near Libya and western Mediterranean reached con-tradicting conclusions (Viñas et al. 2001, 2003).

In the current study, we demonstrated a characteristicspatial–temporal pattern of BFT gonadal maturation acrossthe Mediterranean Sea, with an initial peak during mid-Mayat eastern locations, and during June and July at central andwestern Mediterranean locations, respectively. The sam-pling program carried out in the present work could not be

Fig. 4 Micrographs of the go-nads from blueWn tuna speci-mens caught in selected locations of the Mediterranean Sea. Haematoxylin–eosin stain-ing. a Ovary from an active non-spawning individual with oo-cytes at late vitellogenesis (bar 500 �m). b Ovary from a spawn-ing specimen with hydrated oo-cytes (bar 500 �m). c Ovary from a spawning specimen with both oocytes at Wnal maturation and postovulatory follicles (bar 500 �m). d Ovary from an inac-tive Wsh showing major � atresia of vitellogenic follicles (bar 500 �m). e Ovary from an inac-tive individual with unyolked oocytes and advanced stage of atresia of vitellogenic follicles (bar 100 �m). f Mature testis with seminiferous lobules Wlled with spermatozoa (bar 300 �m). Arrow postovulatory follicle, arrowhead advanced stage of atresia of vitellogenic follicle, af � atretic follicle, ev early vitello-genic oocyte, h hydrated oocyte, lv late vitellogenic oocyte, p perinucleolar stage oocyte, mn migratory nucleus stage oocyte

Fig. 5 Spatial–temporal spawning activity of blueWn tuna across theMediterranean Sea (May throughout July). Gray cells indicate the esti-mated spawning season by week

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extended throughout the year because Wshing activity tar-geting this species is limited to the pre-spawning andspawning periods when BFT group in schools and swim insurface waters. The mean GSI value calculated in the cur-rent study in the Balearic Islands is in agreement with theone calculated by Medina et al. (2002) and conWrms theoccurrence of BFT spawning activity in that location andtime. The histological analysis of the gonads points out thatthe majority of Wsh were in spawning condition in the Lev-antine Sea in May, in the central Mediterranean in mid-June to early July, and in the western Mediterranean in lateJune–July. This pattern correlates well with the spatial–temporal warming-up patterns of the Mediterranean Seasurface (2003, 2004 and 2005 Mediterranean Sea surfacethermal maps; http://www.medspiration.org; http://www.meteomed.eu; http://oceancolor.gsfc.nasa.gov). Ear-lier studies indicated that the rise in sea surface temperature(>23°C) has a dominant role in promoting gonadal matura-tion in several tuna species (Schaefer 2001). In addition,other studies carried out either in eastern or western Medi-terranean locations indicate shifted spawning seasons, i.e.,May–June and June–July, respectively (Mather et al. 1995;Medina et al. 2002; Corriero et al. 2003; Abascal et al.2004; Karakulak et al. 2004; Fromentin and Powers 2005).These Wndings give further support to the hypothesis wepropose of successive spawning, ranging from Maythroughout July depending on the sea surface temperatureat the speciWc spawning ground. Interestingly, the results ofa recent study suggest multiple spawning grounds also forthe west Atlantic BFT stock (Goldstein et al. 2007).

The relatively low GSI values measured in Barbate con-form to those previously reported by Rodríguez-Roda(1964a) and Furnestin and Dardignac (1962), and appear torepresent Wsh migrating toward their spawning grounds, asdescribed by Medina et al. (2002) (and references therein).On the other hand, GSI values measured in the Mediterra-nean Sea during June are consistent with those measured inearlier BFT studies in this sea (de la Serna and Alot 1992;Karakulak et al. 2004), as well as those of the westernAtlantic BFT (reviewed by Mather et al. 1995). These val-ues are typical of asynchronous spawners (Elizur et al.1996). It is worth noting that the relatively small BFTcaught around the Levantine Sea exhibit the highest GSIvalues, contradicting the general assumption that the high-est GSI values positively correlate with large body size(Mather et al. 1995, Murua et al. 2003). Furthermore, thebody sizes of these Wsh (mean FL = 151.81 § 2.20 cm)conWrm their sexual maturity (Corriero et al. 2005; Medinaet al. 2002; Rodríguez-Roda 1967). Recent studies thatfocused on characterizing the reproductive status of the lat-ter population (Karakulak et al. 2004), as well as on larvalsurveys (Oray and Karakulak 2005) provide solid evidencethat the Levantine Sea is an active BFT spawning ground,

thus ruling out the possible occurrence of a “dummy-run”,i.e., incomplete reproductive cycle before reaching fullmaturity, as reported for juvenile striped bass, Moronesaxatilis (Holland et al. 2000). Moreover, the diVerences inmean body weight between the examined spawninggrounds resemble the Wndings of Itoh (2006) for T. orien-talis, where distribution, migration patterns and spawninggrounds change as adult BFT grow older, and may repre-sent a behavioral pattern for BFT species. These Wndingsalso question the recent conclusion made by Rooker et al.(2007) on natal spawning site Wdelity.

In conclusion, this study provides an expanded view ofthe spatial and temporal proWles of BFT gonadal develop-ment in the Mediterranean Sea between the months May–July. Our study also distinguishes two BFT populationsdiVering in their body size and temporal reproductive activ-ities, at the northern Levantine Sea and around Barbate.These populations appear to mix around Malta. As the exis-tence of genetically discrete BFT populations in the Medi-terranean Sea is still controversial, the northern LevantineSea and Barbate BFT populations could be good candidatesfor genetic analysis in future studies.

Acknowledgments This study was undertaken as part of the REP-RODOTT project (EU Q5RS-2002-01355). The research complieswith the current laws of the countries in which the study was con-ducted.

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