SCRS/2011/029 Collect. Vol. Sci. Pap. ICCAT, 67(1): 331-343 (2012)

STUDY ON THE EASTERN ATLANTIC AND MEDITERRANEAN BLUEFIN TUNA STOCK USING THE SPANISH TRAPS AS SCIENTIFIC OBSERVATORIES

J.M. de la Serna1, D. Macías, J.M. Ortiz de Urbina, E. Rodriguez-Marín, Francisco Abascal

SUMMARY

The aim of this paper is to describe the preliminary results of the study on bluefin tuna, using the traps as a scientific observatory that the “Secretaría General del Mar” (SGM) entrusted to the IEO in collaboration with the “Organización de Productores Pesqueros de Almadrabas” (OPP/51).

RÉSUMÉ

Le présent document a pour objet de décrire les résultats préliminaires de l’étude portant sur le thon rouge, en ayant recours aux madragues en tant qu’observatoire scientifique, que le Secretaría General del Mar (SGM) a confiée à l’IEO en collaboration avec l'Organización de Productores Pesqueros de Almadrabas (OPP/51).

RESUMEN

El objetivo de este documento es describir los resultados preliminares del estudio sobre atún rojo, utilizando las almadrabas como observatorio científico, que la Secretaría General del Mar encargó al IEO en colaboración con la “Organización de Productores Pesqueros de Almadrabas” (OPP/51).

KEY WORDS

Bluefin tuna, abundance index, trap fishery

1. Introduction

Bluefin tuna have been historically exploited in a sustainable way in the eastern Atlantic and Mediterranean Sea. Trap is the most traditional fishing gear targeting bluefin tuna, with catches declining since the second half of 20th century. The assessment of eastern bluefin tuna stock indicates high levels of overexploitation. In order to improve this situation, ICCAT recommended a 15-year recovery plan starting in 2007 and continuing through 2022.

Traps are the source for one of the relative abundance indexes used during stock assessment and could supply information on the effect of the ICCAT recovery plan on the reproductive fraction of the population.

The “Secretaria General del Mar” (SGM) entrusted a study on bluefin tuna, using the traps as a scientific observatory, to the IEO in collaboration with the “Organización de Productores Pesqueros de Almadrabas” (OPP/51). The main objective of this study was obtaining the relative abundance index of breeding stock in the same view that in the years previous to the implementation of the bluefin tuna recovery plan, and monitoring the catches in order to detect any trends in the abundance of bluefin tuna. Other particular objectives include studies on stock structure and migratory behaviour, age and growth, reproduction, feeding, biometric relationships, associated species and by-catch, historical data collecting (data mining), comparative studies with bluefin tuna caught from other areas- fleets and trap technical description.

1 Instituto Español de Oceanografía. C.O. Málaga. Pto Pesquero s/n, 29640, Fuengirola, España. E-mail: [email protected] 331 2. Material and methods

Catch and effort data for traps fisheries were collected by the Spanish Oceanographic Institute (IEO) on-board observers. In addition, data on number and size of fish released alive were recorded in order to estimate the bluefin tuna and by-catch species abundance indexes.

For each fishing operation, data were recorded on location, time, environmental data (sea surface temperature, distance to the coast, depth and weather conditions, moon phase, etc.), species composition; and corresponding biological information (size/weight). Data on marine mammals and sea birds sighting were also recorded.

Biological sampling consisted of: gonads, muscle, heart, spines, otoliths, gills and stomachs. Conservation and processing of each type of biological samples were made following conventional protocols.

General lineal models (GLM) were used to estimate the relative abundance index, assuming a negative binomial error distribution.

Historical information was recovered from trap companies’ archives.

3. Results and discussion

During 2010, a total of 49 fishing operations with 5218 bluefin tuna were observed. In addition, 9550 individuals were released.

3.1 Stock structure

− Tagging

Fifteen (15) pop-up were deployed. In addition, 100 bluefin tuna were tagged with ICCAT conventional tags. To date, data on pop-up have not been finished, and recapture of conventional tags have not been yet reported.

− Parasites as biological tags

Preliminary results in terms of species composition and their locations are given in Table 1. Figure 1 shows the various species of parasites found.

For the first time, trematodes of the subfamily didimozoidos Nematobothriinae were found in the eye socket of bluefin tuna. This species is probably unknown to date due to host specificity and habitat. Our early results indicate that there is less diversity and prevalence of parasitological fauna in adult bluefin tuna caught by traps, in comparison to juvenile tuna caught in the Bay of Biscay, in spite of size differences found.

Stomach contents showed two types of parasites: (i) trematodes of the genus Hirudinella (21% of the stomachs analyzed); and (ii) nematodes anisakids (8% of the stomachs analyzed).

3.2 Age and growth

Our results show that most of the catches of the Spanish Atlantic traps consist of ages 7 to 10 years (Figure 2). These results are consistent with previous annual demographic composition of the traps, which shows that ages 7 and up are well represented in the capture and that from the age 10 are fully recruited to the gear.

Figure 3 shows that the Tarifa trap caught the older specimens, mostly ages 9 to 10 years. However, the trap of Conil caught younger specimens of 6 to 7 years.

3.3 Reproduction

Of the 61 females examined, all were classified as inactive mature. Only pre-vitellogenic or early vitellogenic oocytes (with little yolk) plus alpha and/or beta atresic follicles (Figure 4) were observed in their ovaries.

The size at first maturity estimated from the data was 108,004 cm. The L50 estimated from the bootstrap was slightly lower: 107,928 cm. The estimated L50 corresponds with tuna for 3-4 years and an estimated average

332 weight of 26 kg. Nevertheless and due to the low number of samples around the size at first maturity used in the study this value could be underestimating the size at first maturity (Figure 5).

3.4 Feeding

− Stomach contents

Ninety-one (91) stomachs of bluefin tunas caught in the traps of , Conil and Zahara were analysed. 100% of the stomachs were empty, although 10% of the stomachs had some species consumed inside the trap and 9% presented skeletal remains from the digestion of their prey (fish otoliths, cephalopod beaks and pincers of crustaceans).

− Isotopic analysis

Our preliminary results indicate that the relative abundances of Delta N (15N/14N) and Delta C (13C/12C) of the samples from the traps do not differ from samples from other sampling sites, as Larache (traps) and Balearic Islands (Purse seine). These results indicate that the prey species are very similar. Table 2 shows the main results in terms of prey composition from the isotopic analysis.

3.5 Biometric relationships

Size composition is shown in Figure 6. Our data showed average values of LH of 223.37 cm for males and 204.16 cm for females. With regard to the total weight, the average values were, 199.88kg for males and for females 152.20kg. Biometric values were found higher for males than for females. We estimated length-weight relationships for round weigh-fork length, and round weigh-first dorsal fin length (LD1).

Round Weight = 0.00029 x FL2.48515 Round Weight = 1.9655 x LD12.784

3.6 Comparative studies with other fleets

In general, most of the gear targets the adult fraction of the stock, except for the baitboat fishery which that part of the year targets the juvenile fraction. The largest average catch size corresponded to the hand line fishery of the Strait of , followed by traps, surface longline and purse seine.

3.7 Standardized index of relative abundance

Forty-nine (49) fishing operations with 5218 bluefin tuna were recorded. In addition, 9550 individuals were released. A total of 14 768 individuals were caught, which is a value higher than the average catch for the last decade.

As for the relative abundance index used in stock assessment, it is observed a stable trend for the last years, with some variability between years (Figure 7).

3.8 Environmental factors

Sea surface temperature was in the range 16ºC- 20ºC (Figure 8). Sea surface temperature was variable throughout the fishing period and across traps. Turbidity was in the range 2.5m- 28m, depending on the bottom of the trap (Figure 9). Wind: 51 % W, 37 % E y 22 % other and/or variable and/or calm (Figure 10).

3.9 Associated species

The main associated species were small tuna and swordfish, as well as very low frequencies of other species. Table 3 shows the summary of the main associated species caught by the traps during 2010.

3.10 Data mining

Bluefin tuna catch series, in number of fish and weight by fishing operation for the period 1975- 2010, were collected for the four operative traps.

333 4. Acknowledgements

We are grateful to the skippers and crews of fishing vessels who worked in collaboration with the research team of the IEO, and to our colleagues of the Large Pelagic Fisheries Department in Malaga.

5. References

Alves, D.R., Luque, J.L. 2006, Ecologia das comunidades de metazoários parasitos de cinco espécies de escombrídeos (Perciformes: Scombridae) do litoral do estado do Rio de Janeiro, Brasil. Rev Bras Parasitol 15:167-181. Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W. 1997, Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575-583. Bussiéras, J., Baudin-Laurencin, F. 1973, Les helminthes parasites des thons tropicaux. Communication aux VIIIe journées médicales de Dakar du 9-14 Avril 1973. Rev Elev Med Veto Pays Trop 26:13-19. Cayré, P., Kothias, J.B.A., Stretta, J.M., Diouf, T. 1988, Biologie des thons. In Fonteneau A, Marcille J (Eds) Ressources, pêche et biologie des thonidés tropicaux de l’Atlantique centre-est. Rome. FAO Doc Tech Pêch 292:157-268. Cribb, T.H., Bray, R.A. 2010, Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Syst Parasitol 76:1-7. Dawes, B. 1946, The trematoda: with special reference to British and other European forms. University Press Cambridge. Dollfus, R.P. 1926, Sur l'état actuel de la classification des Didymozoonidae Monticelli, 1888 (Didymozoidae Franz Poche, 1907). Ann Parasit Hum Comp 4:148-161. Fromentin, J.M. 2006, Atlantic Bluefin Tuna, Chapter 2.1.5. ICCAT Manual. Guiart, J. 1938, Trematodes parasites provenant des campagnes scientifiques du prince Albert Ier de Monaco (1886-1912). Impr. de Monaco. Monaco. Justo, M.C.N., Kohn, A. 2005, Didymozoidae (Digenea) parasites of Scombridae (Actinopterygii) from Rio de Janeiro coast, Brazil. Revista Brasileira de Zoociências, 7:333-338. Kabata, Z. 1992, Copepods Parasitic on Fishes. Keys and notes for identification of the species. In: Kermack DM, Barnes RSK, Crothers JH (eds) Synopsys of the British fauna (new series). The Linnean Society of London and the Estuarine and Coastal Sciences Association, Oegstgeest, 47:1-264. Lester, R.J.G., MacKenzie, K. 2009, The use and abuse of parasites as stock markers for fish. Fish Res 97:1-2. Lo, C.M., Morand, S. 2001, Gill parasites of Cephalopholis argus (Teleostei: Serranidae) from Moorea (French Polynesia): site selection and coexistence. Folia Parasitol 48:30-36. MacKenzie, K., Abaunza, P. 1998, Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish Res 38:45-56. Mele, S., Garippa, G., Macías, D., Gómez, M.J., Alemany, F., Merella, P. 2010a, Didymozoid trematodes on gills of four tuna species (Osteichthyes: Scombridae:Thunnini) from the western Mediterranean Sea. XXVI Congresso nazionale della Società Italiana di Parassitologia. Perugia, 22-25 giugno 2010. Parassitologia 52: 358. Mele, S., Merella, P., Macias, D., Gómez, M.J., Garippa, G., Alemany, F. 2010b, Metazoan gill parasites of wild albacore, Thunnus alalunga (Bonaterre, 1788) from the Balearic Sea (western Mediterranean) and their use as biological tags. Fish Res 102:305-310. Nakamura, E.L., Yuen, H.S.H. 1961, Incidence of the giant trematode, Hirudinella marina Garcin, in skipjack tuna, Euthynnus pelamis (Linneaus), from Marquesan and Hawaiian waters. Trans Am Fish Soc 90:419- 423. Oliva, M.E., Valdivia, I.M., Costa, G., Freitas, N., Pinheiro de Carvalho, M.A., Sanchez, Z.L., Luque, J.L. 2008, What can metazoan parasites reveal about the taxonomy-554. Postel, E. 1963, Exposé synoptique des données biologiques sur la bonite â ventre rayé (Katsuwonus pelamis) (Linné, 1758). FAO Fish Rep 2: 515-37.

334 Priol, E.P. 1944, Observations sur les germons et les thons rouges capturés par les pêcheurs bretons. Rev Trav OSTPM 13: 394. Rodríguez-Marín, E., Barreiro, S., Montero, F.E., Carbonell, E. 2008, Looking for skin and gill parasites as biological tags for Atlantic bluefin tuna (Thunnus thynnus). Aquat Living Resour 21:365-371. Watertor, J.L. 1973, Incidence of Hirundinella marina Garcin, 1730 (Trematoda: Hirudinellidae) in Tunas from the . J Parasitol 59:207-208.

Table 1. Main parasites and their microhabitat on the bluefin tuna studied.

Metazoos parásitos Microhabitat

Copepoda Euryphorus brachypterus (Gerstaecker, 1853) Arcos branquiales, Pseudobranquia Pseudocycnus appendiculatus Heller, 1865 Arcos branquiales Monogenea Tristomella onchidiocotyle (Setti, 1899) Branquiespinas, narinas Hexostoma thynni (Delaroche, 1811) Arcos branquiales Digenea Copiatestes thyrsitae Crowcroft, 1948 Lavado arcos branquiales Didymocistis sp.1 Membrana branquioestegal Arcos branquiales, Bajo placas dentadas lengua, Membrana branquioestegal, Bajo Didymosulcus sp1, sp.2, sp3, sp4, sp5 placas dentadas pared opérculo, Cielo boca (paladar), Pseudobranquia Didymozoidae sp.1 Arcos branquiales Cardicola forsteri (Cribb, Daintith & Munday, 2000) Lavado cavidad orobranquial Nematobothrium sp . Ojo, cavidad orobranquial

Table 2. Diet composition of bluefin tuna caught in the Spanish traps estimated from Isotopic firms by means of SISUS software.

Prey mean±sd Polybiuns Henslowii sp (n=1) 0.48±0.06 Scomber scombrus (n=3) 0.14±0.04 Trachurus trachurus (n=3) 0.14±0.11 Capros aper (n=3) 0.09±0.07 Sardina pilchardus (n=3) 0.08±0.06 Engraulis encrasicolus (n=3) 0.07±0.05

335 Table 3. Associated species caught by the traps during 2010. CODE Common name Species AMB Pez limóm Seriola Dumerillii MOX Pez luna Mola mola MUF Lisa Múgil cephalus FLY Pez volador Exocoetidae YRS Barracuda Shyraena sp TTL Tortuga boba Caretta caretta LTA Bacoreta Euthynnus alleteratus SWO Pez espada Xiphias gladius BON Bonito del atlántico Sarda sarda BLT Melva Auxis MNZ Rape Lophius sp. RPG Pargo Pagrus pagrus SFS Sable Lepidopus caudatus PAX Besugo Pagellus spp SPN Pez martillo Sphyrna spp TTR Tembladera Torpedo marmorata PIL Sardina Sardina pilchardus

A B

C D E

Figure 1. Parasites observed on bluefin tuna studied: A. Euryphorus brachypterus (Gerstaecker, 1853); B. Pseudocycnus appendiculatus (Heller, 1865); C. Tristomella onchidiocotyle (Setti, 1899); D. Hexostoma thynni (Delaroche, 1811); and E. Copiatestes thyrsitae (Crowcroft, 1948).

336 Numero de atunes rojos atlánticos capturados por edad en las almadrabas atlánticas españolas en 2010

1200

1000

800

600

400 Numero de atunes de Numero

200

0 456789101112131415+ Edad

Figure 2. Demographic structure (age composition) shows by the bluefin tuna caught by the Spanish traps during 2010.

Proporción por edad y por almadraba de las capturas de atún rojo atlántico en 2010

30 Tarifa 25 Barbate Zahara 20 Conil

15

10

5 Proporcion en numero de atunes numero en Proporcion

0 4 5 6 7 8 9 10 11 12 13 14 15+ Edad

Figure 3. Age composition of the bluefin tuna caught in each Spanish tuna trap during 2010.

337

Figure 4. A and B. Microphotographs of bluefin tuna ovaries caught in Spanish traps during 2010. The ovaries were in mature inactive stage.

Predicción Original Predicción Bootstrap Proporción Madurez Proporción 0.0 0.2 0.4 0.6 0.8 1.0

50 100 150 200 250 Talla ( cm )

Figure 5. Size at maturity (L50) estimated from bluefin tuna caught in Spanish traps.

338 14

12

10

8 %

6

4

2

0 115 125 130 135 140 145 150 155 160 165 170 175 180 185 190 195 200 205 210 215 220 225 230 235 240 245 250 255 260 265 270 275 280 Clases de talla

Porcentaje Hembras Porcentaje Machos

Figure 6. Size composition of bluefin tuna caught in Spanish traps during 2010: red = % of male and blue = % female.

339

Figure 7. The graphic shows the standardized relative abundance index and its corresponding confidence intervals (95%, based in normal approach). Atlantic bluefin tuna (ABFT), annual catches in number of specimens (1981-2010).

340 Temperaturas durante la primera parte de la temporada de pesca de A Almadrabas Españolas 2010

20

19

18 Tarifa Zahara TºC 17 Barbate Conil 16

15

14 19 20 21 22 23 24 25 26 27 28 29 30 Días

B Temperaturas durante la segunda parte de la temporada de pesca de Almadrabas Españolas 2010

20

19

18 Tarifa Zahara TºC 17 Barbate Conil 16

15

14 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 Días

Temperaturas durante la tercera parte de la temporada de pesca de C Almadrabas Españolas 2010

21

20

19 Tarifa 18 Zahara TºC Barbate 17 Conil 16

15

14 1 2 3 4 5 6 7 8 9 101112131415161718192021222324252627282930 Días

Figure 8. Daily Sea surface temperature (SST) data in each Spanish tuna trap during 2010. A: SST in April; B: SST in May; C: SST in June.

341 Turbidez durante el primer periodo de la temporada de pesca de A Almadrabas Españolas 2010

20

15 Tarifa Zahara metros Barbate 10 Conil

5

0 20 21 22 23 24 25 26 27 28 29 30 Días

Turbidez durante el segundo periodo de la temporada de pesca de B Almadrabas Españolas 2010

20

15 Tarifa Zahara metros 10 Barbate Conil

5

0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 Días

Turbidez durante el tercer periodo de la temporada de pesca de C Almadrabas Españolas 2010

20

15 Tarifa Zahara metros 10 Barbate Conil 5

0

1 3 5 7 9 3 9 5 11 1 15 17 1 21 23 2 27 29 Días

Figure 9. Daily turbidity (TB) data in each Spanish tuna trap during 2010. A: TB in April; B: TB in May; C: TB in June.

342 A B Viento en la Almadraba de Tarifa (%) Viento en la Almadraba de Zahara (%) Año 2010 Año 2010

6,09 13,72

40,5 56,41 29,41 56,86

Viento W Viento W Viento E Viento E Viento Calma-otros Viento Calma-otros

C D Viento en la Almadraba de Barbate (%) Viento en la Almadraba de Conil (%) Año 2010 Año 2010

7,81 4,83

40,32 53,14 39,06 54,83

Viento W Viento W Viento E Viento E Viento Calma-otros Viento Calma-otros

Figure 10. Percentage of daily dominant wind direction (W=dark blue, E= clear Blue y Otros= red) observed in the Spanish tuna traps during 2010. A: Tarifa trap; B: Zahara trap; C: Barbate trap; and D: Conil trap.

343