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specimens of swordfish (Xiphias gladius) tagged and recaptured in the Atlantic, ... Mediterranean and Atlantic populations of the swordfish, Xiphias gladius.
SCRS/2017/211

Collect. Vol. Sci. Pap. ICCAT, 74(3): 1354-1361 (2017)

NOTES ABOUT A TAGGED/RECAPTURED SWORDFISH IN THE LIGURIAN SEA (WESTERN MEDITERRANEAN) Garibaldi F.1, Lanteri L.1

SUMMARY This paper presents the observations carried out on a swordfish specimen tagged with pop up and traditional tags in August 2005 in the Ligurian Sea and recaptured in the same area in September 2016, after more than 11 years at liberty. The analysis of the anal fin sections allowed to determine the age and the pattern of annual rings formation. A summary of the tagged/recaptured swordfish known to date in the Mediterranean Sea is also given, suggesting the need to increase both conventional and satellite tagging activities in the area.

RÉSUMÉ Ce document présente les observations concernant un spécimen d'espadon porteur de marques de type pop-up et traditionnelle en août 2005 dans la mer de Ligure et recapturé dans la même zone en septembre 2016, après avoir passé plus de 11 ans en liberté. L'analyse des sections de la nageoire anale a permis de déterminer l'âge et la structure de la formation des anneaux annuels. Un résumé des espadons marqués/récupérés connus à ce jour dans la mer Méditerranée est également présenté et donne à penser qu’il s’avère nécessaire d'augmenter les activités de marquage conventionnel et par satellite dans la région.

RESUMEN Este documento presenta las observaciones realizadas en un ejemplar de pez espada marcado con marcas pop-up y tradicionales en agosto de 2005 en el mar de Liguria y recapturado en la misma zona en septiembre de 2016, tras más de 11 años en libertad. El análisis de las secciones de la aleta anal permitió determinar la edad y el patrón de la formación de los anillos anuales. Se facilita también un resumen de los peces espada marcados y recapturados conocidos hasta la fecha en el Mediterráneo, sugiriendo la necesidad de aumentar las actividades de marcado convencional y por satélite en la zona.

KEYWORDS Swordfish, tagging, recapture, growth, Ligurian Sea, Mediterranean

1

Dip.di Scienze della Terra, Ambiente e Vita – Università di Genova – C. so Europa, 26 – 16132 Genova, Italy, E-mail: [email protected]

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1. Introduction Tagging of large pelagic fish, tunas and billfishes, has always been used to try to better understand aspects of their biology and behavior. Among all these species, swordfish has always been a particularly difficult one for tagging, due to its extreme fragility and pugnacity. Several different techniques and protocols have been applied for conventional tagging, mainly in order to avoid shedding of the tag and damage to the fish during tagging operations, but the recovery rate has always been very low, generally less than 5% (Jones, 1997; Garcia Cortes et al., 2003; Sperling et al., 2005), which is probably due to the high mortality after tagging. Despite this, the traditional tagging activities have continued in the North Atlantic and other areas for decades, from the mid1950s (Anonymous, 2003), while in the Mediterranean is a more recent activity. Originally, some countries and research institutes carried out tagging campaigns independently, especially on YOY and juveniles; after that in the mid-2000s a very extensive campaign was promoted by the EU (Planning Group on Tuna Tagging, PGTT), coordinated by several research institutes, both in the Atlantic and the Mediterranean. Along the continuous use of “spaghetti tags”, satellite tagging was then introduced all over the world in order to obtain more detailed information on swordfish biology and behavior (Neilson et al, 2014). This was also done in the Mediterranean (Canese et al., 2008; MADE Project, 2008-2012), where the effort made is still very low. Satellite tagging has provided interesting and reliable data regarding habitat preferences and both vertical and horizontal displacements of individuals, but it is generally limited in time and moreover, expensive. Conventional tagging is less expensive, but as we have seen it has always given low recapture rate. In addition, due to the difficulty in reporting of recaptured animals, swordfish that have been tagged and recaptured are rarely analyzed in terms of their hard parts (otoliths, spines, etc.). Kasapidis et al (2008) reported the data on age and genetics of six tagged/recaptured swordfish in the Atlantic, Pacific and Indian Ocean, as well as Garibaldi et al (1998) for the first recaptured swordfish in the Ligurian Sea, Western Mediterranean. The present paper reports the observations carried out on one swordfish tagged and recaptured in the Ligurian Sea from which samples of its spine for growth analyzes were taken, with some consideration about tagging in the Mediterranean. 2. Material and methods One tagged swordfish was recaptured by commercial mesopelagic longline vessel in the Western Ligurian Sea; length, weight, gonads and anal fin were sampled for subsequent analysis. The second anal fin spine was extracted for ageing purposes, following the standardized protocols applied in many other studies (Berkeley and Houde (1983), Ehrhardt et al. (1996); Tserpes and Tsimenides (1995); Valeiras et al., 2008). It was immersed briefly in hot water in order to facilitate the cleaning operations. Soft tissues were removed carefully, without damaging the surface of the bone and finally the spine was left to dry completely. Cross sections of 0.5 mm thick were cut using an ISOMET Low Speed Saw, at two well defined points: 1) the first one located at a distance from the spine base equivalent to the maximum width of the condyle base 2) the second one located at half of this distance. In each cut location of the spine, four consecutive sections were made in order to choose the best one for readings. The sections were washed in deionized water and briefly in 70% ethanol solution. Pictures were taken using both reflected and transmitted light. Sections were preserved dried.

3. Results 3.a Tag-recapture data The specimen was tagged in the Ligurian Sea with satellite tag (Wildlfe Computers MK10) in the framework of a project carried out in the period 2003-2006 in the Mediterranean Sea (Canese et al., 2008). The pop-up tag was deployed on 6 August 2005, directly at sea, without pulling the fish out of the water on the deck of the boat, avoiding possible damages to the fish. The size of the specimen was estimated to be 18 kilos in weight, which corresponds to a size of about 115 cm LJFL. The implantation was made using a dart steel tag (Floytag) identified with a progressive number (ICRAM 070), which remained on the fish once the satellite tag was detached. the satellite tag popped up after 60 days, as expected, on 5 October 2005 in the Gulf of Lion. The swordfish was recaptured on 23 September 2016, after more than 11 years at liberty; it was a male, measuring 173 cm LJFL and weighing 55 kg (GW). A map with the tag/recapture geographical positions and pictures of the fish and the tag are shown in Figure 1 and Figure 2 respectively. A summary of the main data of the fish is reported in Table 1.

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3.b Age reading and validation Given that the fish was tagged on August and it was estimated to be 18 kg in weight, we can presume it was likely 2 years old at the time of tagging: this actually means that at the time of recapture it was 13 years old. In Figure 2 the section of the second anal fin spine is shown, reporting the counting made by three different readers (colored dots). The three “blind” readings were all different, resulting respectively in 10, 11 and 13 years of estimated age. Given that growth bands corresponding to the first three years of life are clearly visible in the innermost portion of the section, the major difficulties and differences in the readings derive from the correct interpretation of bands in the outer portion of the section.

4. Discussion and conclusions Recapture of fish tagged with conventional tags has been used for several purposes (stock assessment, migration patterns, growth studies validation), but in highly migratory species and especially in swordfish, the main bias was given by the low recapture rate; this is mainly due to extreme fragility and sensitivity to the tagging operations of the swordfish and the fact that the reporting of the tags are strictly dependent on fishery activities and collaboration with fishermen. As a consequence, also the possibility to sample and analyze hard parts for age determination is really low. This is particularly true for the Mediterranean Sea, where in the last decades only a few swordfish recaptures were obtained, despite about 1,800 swordfish were tagged with conventional tags in the past. Analyzing the literature and the ICCAT database (updated to 22 September 2016), a summary of the tagged/recaptured swordfish is reported in Table 2. As far as we know, including the present specimen, in the Mediterranean only 11 swordfish have been recaptured after tagging with conventional tags, four in the Eastern Mediterranean (AAVV, 2008; P. Peristeraki, personal communication) and seven in the Western Mediterranean; the recovery rate is really low (< 1%), much lower than that recorded in other areas (Sperling et al., 2005). The times at liberty show a great variability, from few days to several years; the present specimen, remaining at liberty for over 11 years (4068 days, Table 1) represents unprecedented record for the Mediterranean and one of the longest periods at large also taking into account swordfish tagged in the Atlantic (Restrepo, 1990; Garcia-Cortes et al., 2003). Only for two specimens (the present one and the number 1 in Table 2), both tagged/recaptured in the Ligurian Sea, it was possible to sample and analyze the second spine of the anal fin for age validation. There are several studies published on age and growth of swordfish sampled in different areas, from eastern Mediterranean (Tserpes and Tsimenides, 1995), Ionian and Sicilian waters (Megalofonou et al., 1995; Cavallaro et al., 1998), Ligurian Sea (Orsi Relini et al., 1999) and Western Mediterranean (Valeiras et al., 2008). The VBGF parameters obtained by Tserpes and Tsimenides (1995) are used as reference growth parameters for the stock assessment of the Mediterranean swordfish. Since both fish recaptured and sampled for anal fin were male, their age/length data were compared to some different male growth curves calculated for the Mediterranean (Figure 4). It can be seen that while for the youngest one (3 years old at the time of recapture) all the curves seem to fit well, for the oldest one (13 years old at the time of recapture) the best fitting is that of Valeiras et al., (2008). It is easy to understand that these two individuals are not sufficient to validate a growth curve, but they can contribute to improve the knowledge of some aspects of swordfish biology. Moreover, the present specimen, 173 cm LJFL, weighted 55 kg GW, well below the average estimated weight (64.9 kg GW) derived from the new length/weight relationship published by Tserpes et al. (SCRS 2017/209) for the Mediterranean swordfish. This could be due to many reason (sex, old age, non-healthy conditions), but it is an example of great individual variability in swordfish. However, on the basis of these data and taking into account that larger males are present in the Mediterranean population, we can suspect that the longevity of swordfish could be greater than commonly estimated and expected so far. Analyzing the tagging/recapture positions it can be observe that all the swordfish tagged in the Eastern Mediterranean remained in that basin, as well as for the specimens tagged in the Western Mediterranean, except one that moved to the Atlantic through the Gibraltar Strait, identified in Table 2 with number 6 (De la Serna et al., 2008). Moreover, except for two individuals, the distances travelled are not so great and the recaptures occurred generally in the same area of tagging (i.e. the two specimens in the Ligurian Sea were recaptured after three and eleven years at liberty at a very short distance from the tagging locations). This may be due to the strong homing behavior of swordfish, described also in much larger basins such as Atlantic and Pacific Ocean (Sedberry and Loefer, 2001; Muths et al., 2009). These results are confirmed by satellite tagging that was carried

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out in the past in different areas of the Mediterranean (Canese et al., 2008; Afonso et al., 2012; Koutsikopoulos et al., 2012) (Table 3). As well as for conventional tagging, all fish tagged moved around in the same area, even if we have to consider that pop-up tags remained for short periods (less than120 days) on the fish and in many cases these individuals were juveniles. It is clear that the data and numbers of recaptured swordfish are not suitable for a deeper analysis or exhaustive conclusions, but this could make it possible to think of a low level of mixing not only between Mediterranean and Atlantic, but also between Western and Eastern Mediterranean. Genetic studies have shown presence of three stocks of swordfish (North Atlantic, South Atlantic, Mediterranean) (Kotoulas et al., 2007); Viñas et al. (2007) not only clearly indicate that Mediterranean swordfish stock is separated from the Atlantic one, but also that some differences could be present between Western and Eastern Mediterranean. However, possible mixing occurs between the western Mediterranean and north Atlantic through Gibraltar Straits; this was proved by finding Mediterranean swordfish in Atlantic area (Magoulas et al., 1993; Kotoulas et al., 2003 and 2007; Abid et al., 2015). This uncertainty about the migratory routes of the swordfish between western Mediterranean and Atlantic and inside the Mediterranean itself makes more evident the need to carry out tagging campaigns with both conventional and satellite tags to better understand the mixing rate (if any) with the Atlantic and clarify the possible presence of meta-populations in the Mediterranean.

Acknowledgments The authors would like to thank the skippers and crew members of the Italian longline boat Ale&Miki for their help and collaboration.

References Abid N., Bakkali M., Tserpes G. and Idrissi M. 2015. Swordfish growth pattern in the Strait of Gibraltar; implications for mixing among Atlantic and Mediterranean stocks. Collect. Vol. Sci. Pap. ICCAT, 71(5): 2059-2072 Afonso P., Vandeperre F., McGinty N., Tserpes G., Peristeraki N., Koutsikopoulos C., Valastro M., di Natale A. 2012. Using tracking data to evaluate spatial protection measures for juvenile bycatch in longline fisheries. MADE Project – Abstract EBFMTuna conference, Montpellier (Fr), October 2012. Anonymous. 2003. Report of the 2002 Atlantic Swordfish Stock Assessment Session. Madrid, September 9 to 13. 2002. Collect. Vol. Sci. Pap. ICCAT, 55(4): 1289-1415. AAVV. Planning Group on Tuna Tagging. pgtt 2008, Report of the fourth and final meeting of the Planning Group on Tuna Tagging (PGTT) in the Atlantic and Mediterranean Sea. 44 pp. Berkeley, S. A. and E.D. Houde. 1983. Age determination of broadbill swordfish, Xiphias gladius, from the Straits of Florida, using anal fin spine sections. NOAA Technical Report NMFS, 8: 137-143. Canese S., Garibaldi F., Orsi Relini L., Greco S., 2007. Swordfish tagging with pop up satellite tags in the Mediterranean Sea. ICCAT, Coll. Vol. Sci. Pap. 62: 1052-1057 Cavallaro G., Cefali A., Potoschi A. 1998. Alcuni aspetti biologici e pesca di pescespada, tonno ed alalunga in studi eseguiti tra il 1984 ed il 1996 nel Tirreno Meridionale e nello Ionio. Biol. Mar. Mediterr., 5(3): 241251. Garcia-Cortes B., J. Mejuto, M. Quintans. 2003. Summary of the sworsfish (Xiphias gladius) recaptures carried out by the Spanish surface longline fleet in the Atlantic Ocean: 1984-2002. Col. Vol. Sci. Pap. ICCAT, 55(4): 1476-1484 Ehrhardt, N. M., R.J. Robbins and F. Arocha. 1996. Age validation and growth of swordfish, Xiphias gladius, in the northwest Atlantic. Collect. Vol. Sci. Pap. ICCAT, 45(2): 358-367. Garibaldi F., Palandri G., Orsi Relini L. 1999. The first Mediterranean recapture, useful for growth studies, of tagged swordfish. – ICCAT, Coll. Vol. Sci. Pap., 49 (1): 151-152. Jones, C.D. 1997. Cooperative Tagging Center release and recapture activities for swordfish (Xiphias gladius): 1961-1996. ICCAT, Coll. Vol. Sci. Pap., 46 (3): 379-382.

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Kasapidis, P., X. Valeiras, A. B. García-Cortés and J. Mejuto, 2008. Genetic and growth profiles of several specimens of swordfish (Xiphias gladius) tagged and recaptured in the Atlantic, Indian and Pacific Oceans. Collect. Vol. Sci. Pap. ICCAT, 62(4): 1142-1151. Koutsikopoulos C., Afonso P., Peristeraki P., Valastro M., Di Natale A., Tserpes G. 2012. Vertical behavior of juvenile swordfish revealed by electronic tags. MADE Project – Abstract EBFMTuna conference, Montpellier (Fr), October 2012. Kotoulas, G., A. Magoulas, N. Tsimenides, E. Zouros. 1995. Marked mitochondrial DNA differences between Mediterranean and Atlantic populations of the swordfish, Xiphias gladius. Molecular Ecology 4: 473-481. Kotoulas, G., J. Mejuto, A. Antoniou, P. Kasapidis, G. Tserpes, C. Piccineti, P. Peristeraki, B. Garcia- Cortes, K. Oikonomaki, J.M. De la Serna, A. Magoulas. 2007. Global genetic structure of the swordfish Xiphias gladius, as revealed by microsatellite markers. ICCAT swordfish stock structure workshop (Crete, Greece, 13-15 March, 2006). Collect. Vol. Sci. Pap. ICCAT, 61: 79-88. Magoulas, A., G. Kotoulas, N. Tsimenides, E. Zouros, J.M. de la Serna and G. de Metrio. 1993. Genetic structure of swordfish (Xiphias gladius) populations of the Mediterranean and the eastern side of the Atlantic: analysis by mitochondrial DNA markers. Collect. Vol. Sci. Pap. ICCAT, 40(1): 126-136. Muths D., Grewe P., Jean C., Bourjea J. 2009. Genetic population structure of the Swordfish (Xiphias gladius) in the southwest Indian Ocean: Sex-biased differentiation, congruency between markers and its incidence in a way of stock assessment. Fisheries Research 97: 263–269 Neilson JD., Loefer J., Prince E.D. Royer F., Calmettes B., Gaspar P. Lopez R., Andrushchenko I. 2014. Seasonal Distributions and Migrations of Northwest Atlantic Swordfish: Inferences from Integration of Pop-Up Satellite Archival Tagging Studies. PLoS One. 2014; 9(11): e112736. Orsi Relini L., Palandri G., Garibaldi F., Cima C., Relini M., Torchia G. 1999. Biological parameters of the Mediterranean swordfish derived from observations in the Ligurian Sea – ICCAT, Coll. Vol. Sci. Pap., 49 (1): 397-406. Restrepo V. 1990. An update of swordfish tagging data for use in growth analysis. Col.Vol.Sci.Pap. ICCAT, 32 (2) : 360-370. Sedberry, G., Loefer, J., 2001. Satellite telemetry tracking of swordfish, Xiphias gladius, off the eastern United States. Mar. Biol. 139, 355–360. Sperling A., Neilson J.D., Carruthers E.H., Stone H.H. 2005. Compilation and analyses of Canadian conventional tagging data for swordfish (Xiphias gladius), 1961-2004. Collect. Vol. Sci. Pap. ICCAT, 58(4): 1483-1494. Tserpes, G. and N. Tsimenides, 1995. Determination of age and growth of swordfish, Xiphias gladius L., 1758, in the eastern Mediterranean using anal-fin spines. Fishery Bulletin, 93(3): 594-602. Tserpes G., Ortiz de Urbina j., Abid N., Ceyhan T., Garibaldi F., Peristeraki P., Di Natale A. 2017. Lengthweight relationships for the Mediterranean swordfish. SCRS 2017/2019. Valeiras, X., J.M. de la Serna, D. Macías, M. Ruiz, S. García-Barcelona, M.J. Gómez y J.M. Ortíz de Urbina, 2007. Age and growth of swordfish (Xiphias gladius) in western Mediterranean sea. Collect. Vol. Sci. Pap. ICCAT, 62(4):1112-1121. Vinas J., Perez-Serra A., Vidal O., Alvarado Bremer J., Pla C. (2010) - Genetic differentiation between eastern and western Mediterranean swordfish revealed by phylogeographic analysis of the mitochondrial DNA control region. ICES J. Mar. Sci., 67(6): 1222-1229.

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Table 1. Main data of the tagged/recaptured specimen in the Ligurian Sea. Sat Tag ID

Floy Tag N

Rel. date

Rel. position Pop-up date

Pop-up position

Rec. date

Rec. position

43°39'174 N 007°43'270 E

42°49N 004°45E

23/09/2016

43°11'672 N 008°14' 587 E

Argos 53169 ICRAM 070 06/08/2005

05/10/2005

Days at Size at release liberty 4068

~18 kg ~115cm LJFL

Size at release

Size at recovery

Size at recovery

Sex

173 cm LJFL 55 kg (GW)

Male

Table 2. List of the tagged/recaptured swordfish in the Mediterranean Sea. Tag Number

Area

Rel. date

Rel. position

Rec. date

1

HTN009484

Western Med Ligurian Sea

13/12/1994

43,750 7,883333

15/09/1997

43,0000 7,0000

1006

2

HES011857

Western Med North Balearics

23/11/2000

41,6333333333 2,96666667

21/07/2008

39,0883333 0,00

3

HTN006833

Eastern Med Aegean Sea

23/10/2004

36,857833 26,940833

20/05/2005

4

HCT010190

Eastern Med Aegean Sea

07/12/2005

37,06666667 26,96666667

5

HCT010187

Eastern Med Aegean Sea

07/12/2005

6

HCT 015605

Western Med Balearic Islands

02/12/2006

40 18 N 02 52 E

7

HCT013697

Eastern Med Aegean Sea

18/11/2006

8

HCT011021

Eastern Med Aegean Sea

9

HCT 011691

10

HCT015940

Rec. position

Days at liberty

Sex

Source

80 cm JJFL 134 cm LJFL

Male

Garibaldi et al. ,1999 ICCAT DB

2795

100 cm LJFL 124 cm LJFL

-

ICCAT DB

36,153533 26,132550

209

67 cm LJFL

-

AAVV 2008 ICCAT DB

16/02/2007

37,66667 26,81667

436

70 cm LJFL 110 cm LJFL

-

AAVV 2008 ICCAT DB

37,06666667 26/02/2008 26,9833333333

37, 16667 25,03333

811

70 cmLJFL 140cm LJFL

-

AAVV 2008 ICCAT DB

31/01/2007

36 00 N 14 26 W

60

-

76 cm LJFL

-

De la Serna et al ., 2008 *

37,4077 24,825

09/06/2010

37,786 15,87

1298

73cm LJFL

20 kg

-

P. Peristeraki pers. comm. *

13/08/2007

37,41666667 24,78333333

10/03/2010

37,65 24,83333

939

88 cm LJFL 120 cm LJFL

-

ICCAT DB

Western Med Balearic Islands

21/02/2008

39,3166667 2,05

12/08/2011

43,8885 9,57

1267

65 cm LJFL 30 kg (GW)

-

F. Garibaldi Unp. Data *

Western Med Balearic Isalnds

05/06/2012

39,5166666666 1,75

08/07/2014

38,7333333 3 3,55

763

70 cm CFL

-

ICCAT DB

-

20 kg

* These records shall be added to the ICCAT database. Table 3. Number and geographical areas of the swordfish tagged in the Mediterranean Sea by pop-up tags. N 7 12 6 4

Area Ligurian Sea Messina Strait Sicily Channel Aegean Sea

Years 2003-2006 2004-2006 2010-2011 2010-2011

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Data source Canese et al., 2008 Koutsikopoulos et al 2012

Figure 1. Map of the mark/recapture positions: tagging on 6 August 2005 (60 days) – Recapture on 23 September 2016 (4068 days).

sat tag pop-up on 5 October 2005

Figure 2. Pictures of the fish and the tag. a) the fish at the moment of recapture (tag is indicated by the white arrow) b) A detail of the tag implanted under the first dorsal fin. c) the tag with the progressive number visible.

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Figure 3. Section of the second anal fin ray. The dots of different colors are referred to the age readings performed by 3 different readers (yellow estimated age 10 – red 13 – light blue 11)

Figure 4. Different Mediterranean swordfish growth curves. The age-length data of the two specimens tagged and recaptured in the Ligurian Sea are superimposed (triangle and dot).

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