NEW DATA ON BLUEFIN TUNA MIGRATORY BEHAVIOR IN THE WESTERN AND CENTRAL MEDITERRANEAN SEA

SCRS/2011/159 Collect. Vol. Sci. Pap. ICCAT, 68(1): 151-162 (2012) NEW DATA ON BLUEFIN TUNA MIGRATORY BEHAVIOR IN THE WESTERN AND CENTRAL MEDITERRANEAN SEA Pablo Cermeño 1, Sergi Tudela 1,*, Gemma Quílez-Badia 1, Susana Sainz Trápaga 1, Esteban Graupera 2 SUMMARY During 2010, several tagging expeditions were carried out in the NW Mediterranean and the Adriatic Sea in order to determine Atlantic bluefin tuna trajectories and behavior, following the tagging work carried out in 2008 and 2009. Pop-up satellite archival tags and internal archival tags were used on adults and juveniles. In total, 8 pop-up and 2 archival tags were deployed, including 2 mini-pop up tags placed on juveniles. Tagged bluefin tuna weights ranged from 17 to 140 kg, and retention rates of pop-up tags ranged from 4 to 247 days. Additionally, a 2008 archival tag was recovered after 963 days at liberty. None of the tagged tunas left the Mediterranean Sea during the whole tracking period. Results reinforce available evidence for (1) a strong attachment of some fish to the western Mediterranean basin, including a long-term residence area for juveniles associated to the Algerian Current system, between the Balearic Islands and the Algerian coast, (2) a temporary residence area north of the Balearic Islands in late summer and autumn, and (3) a strong attachment of fish occurring in the Adriatic Sea to this sea, with preference for the deeper areas. RÉSUMÉ En 2010, plusieurs campagnes de marquage ont été menées dans le Nord-Ouest de la Méditerranée et dans la mer Adriatique dans le but de déterminer les trajectoires et le comportement du thon rouge de l'atlantique, suite aux travaux de marquage réalisés en 2008 et 2009. Des marques-archives pop-up reliées par satellite et des marques-archives internes ont été utilisées sur des adultes et des juvéniles. Au total, huit marques pop-up et deux marquesarchives ont été apposées, y compris deux mini marques pop-up apposées sur des juvéniles. Les poids des thons rouges marqués ont oscillé entre 17 et 140 kg, et les taux de rétention des marques pop-up se sont situés entre quatre et 247 jours. En outre, une marque-archive de 2008 a été récupérée après 963 jours en liberté. Aucun des thons marqués n a quitté la mer Méditerranée pendant toute la durée de la période de suivi. Les résultats renforcent les preuves disponibles faisant étant (1) d'un fort attachement de la part de certains poissons au bassin méditerranéen occidental, y compris une zone de résidence à long-terme pour les juvéniles associée au système des courants algériens, entre les îles Baléares et la côte algérienne, (2) d'une zone de résidence temporaire au Nord des îles Baléares à la fin de l'été et de l'automne, et (3) d'un fort attachement des poissons se trouvant dans la mer Adriatique à cette mer, avec une préférence pour les zones plus profondes. RESUMEN Durante 2010 se llevaron a cabo varias campañas de marcado en el Mediterráneo noroccidental y en el mar Adriático con el fin de determinar las trayectorias y el comportamiento del atún rojo del Atlántico, como continuación del trabajo de marcado llevado a cabo en 2008 y 2009. Se utilizaron marcas archivo pop-up por satélite y marcas archivo internas en adultos y juveniles. En total se colocaron 8 marcas pop-up y 2 marcas archivo, lo que incluye 2 mini marcas pop-up colocadas en juveniles. Los pesos de los atunes rojos marcados oscilaban entre 17 y 140 kg y las tasas de retención de las marcas pop-up oscilaron entre 4 y 247 días. Además, se recuperó una marca archivo de 2008 tras 963 días en libertad. Ninguno de los atunes rojos marcados abandonó el Mediterráneo en todo el periodo de seguimiento. Los resultados refuerzan las evidencias disponibles de (1) una fuerte preferencia 1 WWF Mediterranean Programme Office, C/ Canuda 37 3 er, 08002 Barcelona, Spain. 2 Confederación Española de Pesca Recreativa Responsable, C/ Molinets 6, 07320 Mallorca, Spain. * Corresponding author: studela@atw-wwf.org 151

de algunos peces por la cuenca mediterránea occidental, lo que incluye una zona de residencia a largo plazo para los juveniles asociados al sistema de la corriente argelina, entre las Islas Baleares y la costa argelina, (2) una zona de residencia temporal al Norte de las Islas Baleares a finales de verano y otoño y (3) una fuerte preferencia de los peces que se encuentran en el Adriático por este mar, especialmente por las zonas más profundas. KEYWORDS Thunnus thynnus, pop-up tags, archival tags, tagging, Western Mediterranean, Adriatic, migration 1. Introduction The Atlantic bluefin tuna inhabits the North Atlantic Ocean and its adjacent seas and has been fished since ancient times (Fromentin and Powers 2005, Rooker et al. 2007). Stocks of this species have been at critical levels in recent decades, including a high risk of collapse in the eastern Atlantic and the Mediterranean (Anon., 2009). Such figures urgently call for a clearer understanding of bluefin tuna biology to enable the implementation of the most effective management measures. During 2010, WWF collaborated with Confederación Española de Pesca Recreativa Responsable and Big Game Italia (which are two associations of recreational anglers from Spain and Italy, respectively, that promote the catch and release practice), and C.N. Sambenedettese and Barricata Fishing Club (in Italy) to deploy pop-up satellite tags on wild bluefin tuna in the western Mediterranean and Adriatic Sea. Here we report some preliminary results on the trajectories of the fish tagged with pop-ups in 2010. In addition we also present the preliminary results from an archival tag deployed in 2008 off Roses (NE Spain) which was recovered 2 years and 8 months later. This paper updates the results in Tudela et al. (2011) relative to tagging activities during the years 2008 and 2009. 2. Methods In 2010, five expeditions were carried out in August and September. Larger tunas were fished with rod and reel using the brumeo technique (chumming the water with sardines while anchored or drifting). Tunas were embarked and the total fork length of each fish was measured to the nearest 0.5 cm. On-board pop-up tagging (with either Wildlife Computers MK10 or MiniPAT) of BFT was done by means of two anchorages, using titanium darts. Juveniles were captured by trolling lures and taken on-board to have an archival tag surgicallyimplanted (Wildlife Computers MK9). The tracks were estimated by CLS (Collecte Localisation Satellites), applying the Kalman filtering of the lightbased geolocations and using satellite-obtained sea surface temperature and bathymetry as constraints (Sibert et al. 2003, Royer et al. 2005, Nielsen et al. 2006, Nielsen and Sibert 2007). The geolocation error within the Mediterranean was estimated to be of one to two degrees (F. Royer pers. comm.). The 2010 tags were programmed to register pressure, light level and water temperature at 60 second intervals. Depth layers were set at 0, 0-10, 10-20, 20-50, 50-100, 100-150, 150-200, then at 100 m intervals until 800, and over 800 m. Compared to the two previous years, tagging during 2010 was particularly unsuccessful (in terms of rough weather and poor catches) and we were only able to deploy a total of 10 tags (8 pop-up and 2 archival ones). 3. Results All the pop-up tags but one transmitted their pop-off location to the satellite, and tracks were estimated for those tunas that yielded information for over 30 days at liberty (5 individuals). Since the initially programmed recording period was 300 to 365 days after the tagging date it can be considered that premature releases occurred in all cases (Table 1). Due to the well-known transmission problems in the Mediterranean, data were not always 152

received with success. Table 1 shows the number of days during which light, depth and temperature data were successfully received, and the percentage and number of days for which at least one of the three types of data were received by the satellite. Five juvenile and adult tunas (estimated weight between 17 and 140 kg) were tagged with pop-up tags (Wildlife Computers Mk10 or MiniPAT) off the northern coast of Mallorca and in Roses, NE Spain, in August 2010 (Table 1), while 3 adult tunas (between 60 and 70 kg) were tagged with MK10 pop-up tags in the Adriatic Sea (Table 1). Two further archival tags were deployed in Roses, NE Spain, at the end of August beginning of September 2010 (Table 2) in the same area as the ones tagged during the 2008 and 2009 expeditions (Tudela et al. 2011). Two out of the eight pop-up tags deployed in 2010 detached from the fish within 11 days (one from the Balearic Islands and one from the coast of Roses), providing little information about the behavior of the fish (Table 1). Of the remaining six pop-up tags, one failed to pop-off and the other five detached from the fish and transmitted data via satellite after 48 to 247 days (Figures 1 and 2). The two archival tags deployed in 2010 have not been retrieved yet. An accurate analysis of the tracks corresponding to the five detached tags (over 30 days), including the temporal dimension (as shown by the daily dots on the trajectories from Figures 1 and 2), was conducted. The track from the Balearic Islands tuna (08A0403 in Figure 1) shows that it stayed north of Mallorca until September 11 2010, then migrated south-eastwards until its tag detached at the end of September 2010 (after 48 days at liberty) in the waters between Sardinia and Algeria. The two juvenile tunas tagged off Roses in early September traveled south-eastwards, in both cases also including a period of residence in the waters north of the Balearic Islands. One of them (10P0049 in Figure 1) travelled through the waters between the Balearic Islands and Corsica and Sardinia, where its tag popped-off in early November (after 71 days at liberty); the other one (10P0052) popped-off in early November (after 58 days at liberty) off the northern coast of Tunisia, although preliminary analyses suggest the animal (and the tag) was likely preyed upon by an unknown predator (possibly a shark) during its stay north of the Balearic Islands on 11 th October 2010. Of the pop-up tags deployed in the Adriatic Sea, two remained attached to the tuna for over 30 days (Table 1 and Figure 2). The one that was tagged off Venice and remained attached for 177 days (08A0396 in Figure 2) showed that the fish had stayed in the Adriatic Sea for the entire period, seemingly spending most of the time (from the end of October to the beginning of March) in the deeper areas around Jabuka Pit/Fossa di Pomo. It was in front of Biševo Island (Croatia) when its tag detached in late March 2011. The second tuna, tagged off the coast of San Benedetto del Tronto, central-eastern Italy (08A0390 in Figure 2), migrated for a month southeastwards, reaching the South Adriatic Pit in mid-october and remaining there until mid-november. Afterwards it started travelling north-westwards, reaching Jabuka Pit in mid-december and staying there until early January. From there it migrated steadily north-westwards arriving at the northern part of the Adriatic Sea on 31 January, just to resume the south-eastwards trajectory, reaching the waters off the Peloponnese (Greece) in the Ionian Sea at the end of April. From there it migrated again north-westwards and arrived to Manfredonia where its tag detached on May 5 2011, 281 days after its deployment. In May 2011 one of the archival tags deployed on a young tuna in August 2008 (Tudela et al. 2011) was recovered by an Italian fishmonger who bought in the Venice fishmarket a fresh tuna that had reportedly been caught around the Strait of Sicily (Table 3, Figures 3-6). This tag, which lasted for 963 days (some 2 years and 8 months) in the fish at liberty, is a twin of the one that was recovered in 2009 after 391 days, as they were deployed during the same tagging expedition off Roses, NE Spain (Tudela et al., 2011). During the period the animal remained tagged, it increased its weight from 13.5 kg at the moment of tagging to approximately 35-40 kg (as informed by the fishmonger). The detailed analysis of the data recorded by the tag conclusively shows that the animal spent the next two years and eight months after being tagged within the Algerian Basin, in the waters associated to the Algerian Current system between the Balearic Islands and the coast of Algeria. A more detailed analysis of Figures 3-6 reveals that the animal stayed closer to the Algerian coast in winter, whereas in summer it tended to remain farther from the African coast and closer to southern Balearic waters. 153

4. Discussion and conclusion Our preliminary results show that none of the tunas tagged in 2010 left the Mediterranean during 48 to 247 days after the tagging event, consistently with the results from the 2008 and 2009 expeditions (Tudela et al., 2011). A phase of temporary residence (over 30 days) during late summer/early autumn in the north of the Balearic Islands was found in 2010 (Figure 1). This fits the pattern reported for the tuna tagged in 2008 and 2009 in Mallorca and Roses (Tudela et al., 2011) and confirms its remarkable inter-annual stability. The resulting tracks obtained for the three tags deployed in 2010 on two juvenile tunas off Roses (NE Spain) and one adult off Mallorca showed a south-eastern migratory pattern (Figure 1). This result is consistent with the behavior of the adults tagged in 2009 in the same area, which remained in the waters between the Balearic Islands and Corsica and Sardinia, and one of them migrated south-eastwards crossing the Tyrrhenian Sea and reaching the north of Sicily where its tag detached (Tudela et al., 2011). A link between the Balearic Sea and the Tyrrhenian Sea was also observed for the juvenile tuna tagged with an archival tag in 2008 and recovered in 2009, which overwintered in the Tyrrhenian Sea and the Strait of Sicily (Tudela et al., 2011). Similarly to the four adult tunas tagged off Roses in 2009 (Tudela et al., 2011), the three bluefin tunas tagged in 2010 in the Balearic Islands and off Roses remained in the Mediterranean Sea and stayed far away from the Strait of Gibraltar during the period analyzed (Figure 1). The results from the archival tag recovered in 2011 are consistent with those obtained from its twin tag recovered in 2009, which showed a long residence of the fish south of the Balearic Islands and a temporary migration towards the southern Tyrrhenian Sea and the Strait of Sicily (Tudela et al., 2011). In the case of the 2011 tag, however, the long confinement of the fish to the waters of the Algerian Current system is outstanding as it uninterruptedly lasted for some two years and eight months, before the fish was captured near Sicily. This result further reinforces the idea of the strong attachment of some of the fish occurring in the Western Mediterranean to this basin. Moreover, the combined data from the two archival tags recovered so far (covering nearly 4 full years in the life of juvenile tunas) suggest an increased use of the waters south of the Balearic Islands for the species: besides hosting a well-known breeding area they may also constitute a long-term residence area for juveniles, particularly the waters associated to the Algerian Current. Overall, the results presented here for the year 2010, added to those from Tudela et al. (2011) for 2008 and 2009, strongly suggest that an important part of the bluefin tuna population occurring in the western Mediterranean (including both juveniles and adults) does not seem to engage in an annual Atlantic migration and remains strongly attached to the western Mediterranean basin. This thesis is further reinforced by the inter-annual persistency of the seasonal residence area described for the NW Mediterranean, as supported by our data from 2008, 2009 and 2010 and the parallel work by de la Serna et al. (2011). This situation, however, is compatible with the fast migration of some post-spawning adults from the western Mediterranean to the Atlantic, as recently confirmed by Medina et al. (2011) based on electronic tagging. The demographic balance in the W Mediterranean in an average year between Mediterranean-resident fish and Atlantic migrators, and the influence of biological, hydrological and ecological factors thereon, though, remains unknown. Likewise to 2009 (Tudela et al., 2011), the 2010 Adriatic tags also suggest a preference of the fish for deeper areas (like Jabuka Pit/Fossa di Pomo), probably linked to more biologically productive hydrological features. Again, the fish tagged in the Adriatic show a strong attachment to this sub-basin. WWF s tagging activities are still on-going and will continue in the next years. More in-depth analyses on the data set gathered from 2008, 2009, 2010 and 2011 tags are also under way, and are integrating hydrological data to help understanding vertical and horizontal patterns. Salat et al. (2011), for example, have recently found that there may be a relationship between autumnal storms in the NW Mediterranean and the start of tuna migration to either the SW or SE. The aforementioned authors have observed that out of 12 tunas (from our 2008-2010 expeditions) that were presumably feeding in the NW Mediterranean at the end of summer, 9 started migrating above 10 nautical miles/day when the SST started decreasing more than 1ºC/day, which happened immediately after the autumnal storms. Regarding the premature release of the pop-ups detected in 2008 and 2009 (Tudela et al., 2011), its rate was decreased in 2010 thanks to the use of a double anchor point (Table 1), which was inserted with a short-handle applicator (and not a pole). Moreover, the longest time at liberty was also increased from 172 days in the 154

previous work, to 247 days in the present work (with almost half the number of tunas tagged). Unfortunately, the challenge related to the poor transmission of data with the lowest percentage of data transmitted corresponding to the area close to Sicily -, still remains. Acknowledgments The authors want to express their gratitude particularly to the Prince Albert II of Monaco Foundation and the Project Oceans - United Postcode Lotteries, who gave the needed financial support for the project. The authors are also particularly indebted to Confederación Española de Pesca Recreativa Responsable and the crew of their tagging vessels, to BigGame Italia, C.N. Sambenedettese and Barricata Fishing Club, to the ports participating in the fishing and tagging events as well as to the collaboration of the WWF France vessel Columbus and its crew. All mentioned partnerships were essential to make this tagging initiative On the Med Tuna Trail possible. In addition we would like to acknowledge our collaborative work with Tag-A-Giant Foundation in the Adriatic Sea s tagging expedition. We would also like to thank the free availability of the Maptool program (seaturtle.org). References Anon, 2009, Report of the 2008 Atlantic Bluefin Tuna Stock Assessment Session. Collect. Vol. Sci. Pap. ICCAT 64, 1-352. de la Serna J.M., Abascal F., Godoy M.D., 2011, Resultados, J.M., Powers, J.E. 2011, Resultados preliminares de las actividades de marcado de atún rojo (Thunnus thynnus) realizadas por la Confederación Española de Pesca Marítima Recreativa Responsable (CEPRR) con la coordinación científica del Instituto Español de Oceanografía (IEO). Collect. Vol. Sci. Pap. ICCAT 66, 984-988. Fromentin J.M., Powers J.E., 2005, Atlantic bluefin tuna: Population dynamics, ecology, fisheries and management. Fish and Fisheries 6:281-306. Medina A., Cort J.L., Aranda G., Varela J.L., Aragón L., Abascal F.J., 2011, Summary of bluefin tuna tagging activities carried out between 2009 and 2010 in the East Atlantic and Mediterranean. Collect. Vol. Sci. Pap. ICCAT 66, 874-882. Nielsen A., Bigelow K.A., Musyl M.K., Sibert J.R., 2006, Improving light-based geolocation by including sea surface temperature. Fish. Oceanogr. 14, 314-325. Nielsen A., Sibert J.R., 2007, State-space model for light-based tracking of marine animals. Can. J. Fish. Aquat. Sci. 64, 1055-1068. Rooker J.R., Alvarado Bremer J.R., Block B.A., Dewar H., De Metrio G., Corriero A., Kraus R.T., Prince E.D., Rodriguez-Marin E., Secor D.H., 2007, Life history and stock structure of Atlantic bluefin tuna (Thunnus thynnus). Rev. in Fish. Sci. 15, 265-310. Royer F., Fromentin J.M., Gaspar P., 2005, A state-space model to derive bluefin tuna movement and habitat from archival tags. Oikos 109, 473-484. Salat J., Tudela S., Sainz-Trápaga S., Cermeño P., Quílez-Badia G., 2011, Are bluefin tuna fishes in the Mediterranean waiting from a sign from skies to start their migrations? 13 th Plinius Conference on Mediterranean Stroms, Plinius Conference Abstracts Vol. 13, Plinius 13-87. Sibert J., Musyl M., Brill R.W., 2003, Horizontal movements of bigeye tuna (Thunnus obesus) near Hawaii determined by Kalman filter analysis of archival tagging data. Fish. Oceanogr. 12, 141-151. Tudela S., Sainz-Trápaga S., Cermeño P., Hidas E., Graupera E., Quílez-Badia G., 2011, Bluefin tuna migratory behavior in the western and central Mediterranean Sea revealed by electronic tags. Collect. Vol. Sci. Pap. ICCAT 66, 1157-1169. 155

Table 1. Summary information on the deployment and pop-off of the pop-ups and mini pop-ups deployed in 2010 in the Western Mediterranean and Adriatic Sea. 'Days with all data' refers to the successful transmission of the three data sets (depth, light and temperature). 'D/L/T' means days when only one or two of the three data sets were received. Note: * tag did not pop-off when it was supposed to. Year Pop-up ID Area Release position Pop-off position Weight Deployment Pop-off Days at Days with all Perc (%) D/L/T Perc (%) Dart (kg) liberty data 2010 08A0404 Balearic Islands 40º 02 N 03º 10 E 40º36 N 04º27 E ~101 07/08/2010 18/08/2010 11 - - - - Metalx2 08A0403 Balearic Islands 40º 02 N 03º 10 E 38º16 N 07º01 E ~140 08/08/2010 25/09/2010 48 7 14,58 36 75,00 Metalx2 08A0402 Roses 42º20 N 03º 20 E 42º24 N 03º27 E ~69 03/09/2010 07/09/2010 4 - - - - Metalx2 08A0390 Adriatic 42º55 N 14º 14 E 41º34 N 15º57 E ~60 13/09/2010 18/05/2011 247 18 7,29 97 39,27 Metalx2 08A0396 Adriatic 44º 49 N 12º 51 E 42º34 N 15º49 E ~70 24/09/2010 20/03/2011 177 3 1,69 52 29,38 Metalx2 08A0392* Adriatic 44º 49 N 12º 50 E? ~62 28/09/2010 -? - - - - Metalx2 Year Mini popup Area Release position Pop-off position Weight Deployment Pop-off Days at Days with all Perc (%) D/L/T Perc (%) Dart ID (kg) liberty data 2010 10P0049 Roses 42º15 N 03º 40 E 39º52 N 6º 20 E ~17 01/09/2010 11/11/2010 71 16 22,54 52 73,24 Metalx2 10P0052 Roses 41º 51 N 03º 50 E 37º48 N 9º 27 E ~18 05/09/2010 02/11/2010 58 9 15,52 38 65,52 Metalx2 Table 2. Summary information on the archival tags deployed in 2010 off Roses (Catalonia, NE Spain). Year TagID Area Release position Pop-off position Weight Deployment Recapture Days at liberty (kg) 2010 890137 Roses 41º 56 N 03º 36 E - ~17 26/08/2010 - - 890141 Roses 42º 18 N 03º 34 E - ~18 01/09/2010 - - Table 3. Summary information on the archival tag deployed in 2008 off Roses and recovered in 2011 near Sicily. Year TagID Init. Weight Deployment Area Release position Recapture Recapture position Days at liberty (kg) 2008 890152 13,5 31/08/2008 Roses 31º 55 N 03º 50 E 21/04/2011 near Sicily 963 156

Figure 1. Estimated tracks for the three tunas tagged with pop-up tags (over 30 days) off Pollença (north of Mallorca Island) and Roses (NE Spain) in August and early September 2010. Note: the dots on the trajectories show the estimated daily position. 157

Figure 2. Estimated tracks of two of the three tunas tagged in the Adriatic Sea during September 2010. Note: the dots on the trajectories show the estimated daily position. 158

Figure 3. Complete estimated track of the juvenile tuna tagged with an archival tag on August 2008 in NE Spain (TagID 890152) and recovered near Sicily after 963 days at liberty. 159

Figure 4. Estimated track of juvenile tuna 890152: only positions pertaining to the period summer 2008 - spring 2009 are shown. 160

Figure 5. Estimated track of juvenile tuna 890152: only positions pertaining to the period summer 2009 - spring 2010 are shown. 161

Figure 6. Estimated track of juvenile tuna 890152: only positions pertaining to the period summer 2010 - spring 2011 are shown 162