ADVANCES IN RESEARCH OF LARVAL BLUEFIN ECOLOGY: WORKSHOP PROPOSAL TOWARDS ESTABLISHING FUTURE RESEARCH ACTIONS

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SCRS/2013/168 Collect. Vol. Sci. Pap. ICCAT, 70(2): 511-517 (2014) ADVANCES IN RESEARCH OF LARVAL BLUEFIN ECOLOGY: WORKSHOP PROPOSAL TOWARDS ESTABLISHING FUTURE RESEARCH ACTIONS A. Garcia 1 and J. Lamkin 2 SUMMARY Responding to the SCRS recommendation of 2000 requesting exploratory research sampling of bluefin larvae and its associated oceanographic condition in the Central Atlantic and in the Mediterranean, oceanographic institutions as the Spanish Institute of Oceanography, the Southeast Fisheries Center of Miami (NOAA), and international projects, as CLIOTOP (CLimate Impact on Top Predators) have endeavoured to promote research in the field of early life ecology of tunas and associated species. The TUNIBAL project undertaken during 2001-2005, and its continuing successor projects (ATAME, BLUEFIN) have developed research in a wide suite of fields related to their early life biology, as growth, condition, and trophic ecology linked to the predominating oceanographic/climatic conditions that impact bluefin larval distribution determining their spawning habitat in the Balearic Sea. Likewise, overseas institutions as those working in the bluefin spawning habitat off the Gulf of Mexico, and in Pacific Ocean regions have undertaken research actions towards understanding the dynamics of early life ecology of bluefin and associated species. In view of recent developments in relation to the transatlantic agreement between USA and Europe within the framework of a NOAA-JRC destined to promote cooperative science activities in the areas of climate, weather, oceans and coasts, the moment is considered adequate for holding a workshop for paving a roadmap towards future cooperative actions. RÉSUMÉ En réponse à la recommandation de 2000 du SCRS qui préconisait que soit réalisé un échantillonnage des larves de thon rouge et de ses conditions océanographiques associées dans l'atlantique central et la Méditerranée dans le cadre de la recherche exploratoire, l'institut espagnol d'océanographie (IEO), le Centre des Sciences Halieutiques du Sud-Est (NOAA) de Miami, ainsi que des projets internationaux, tels que CLIOTOP (Impacts climatiques sur les principaux prédateurs), s'appliquent à promouvoir la recherche dans le domaine des premiers stades du cycle vital des thonidés et des espèces associées. Le projet TUNIBAL réalisé entre 2001 et 2005 et les projets ultérieurs qui l'ont suivi (ATAME, BLUEFIN) ont développé la recherche dans une vaste gamme de domaines relatifs à la biologie des premiers stades de leur cycle vital, tels que la croissance, condition et l'écologie trophique liée aux conditions océanographiques/climatiques prédominantes qui affectent la distribution des larves de thon rouge en déterminant leur habitat de frai dans la mer des Baléares. Pareillement, des institutions étrangères, comme celles qui travaillent sur l'habitat de frai du thon rouge au large du golfe du Mexique et dans les régions de l'océan Pacifique, ont entrepris des programmes de recherche en vue d'appréhender la dynamique de l'écologie des premiers stades du cycle vital du thon rouge et des espèces associées. Compte tenu des faits nouveaux récemment survenus en ce qui concerne l'accord transatlantique conclu entre les États-Unis et l'europe (NOAA-Centre de recherche conjointe de la Commission européenne) afin de promouvoir les activités scientifiques coopératives dans les domaines ayant trait au climat, à la météorologie, aux océans et au littoral, le moment semble opportun pour tenir un atelier destiné à préparer la voie vers des actions coopératives futures. RESUMEN Desde que el SCRS recomendó, en su reunión de 2000, que se realizasen muestreos exploratorios de investigación de larvas marinas de atún rojo y de sus condiciones oceanográficas asociadas en el Atlántico central y en el Mediterráneo, las instituciones oceanográficas como el Instituto Español de Oceanografía (IEO), el Southeast Fisheries Center of Miami (NOAA), así como proyectos internacionales como CLIOTOP (Climate Impact on Top 1 Instituto Español de Oceanografía, Centro Oceanográfico de Málaga, 29640 Fuengirola (Spain); agarcia@ma.ieo.es 2 Southeast Fisheries Science Center (NOAA), 75 Virginia Beach Drive, Miami, Fla. 33149 USA 511

Predators) se han esforzado en fomentar la investigación en el campo de la ecología de las primeras fases del ciclo vital de los túnidos y especies asociadas. El proyecto TUNIBAL, que se desarrolló de 2001 a 2005, y sus sucesores (ATAME y BLUEFIN) han desarrollado trabajos de investigación en un amplia gama de campos relacionados con la biología en las primeras fases del ciclo vital, como crecimiento, condición y ecología trófica vinculándolos con las condiciones oceanográficas y metereológicas predominantes que afectan a la distribución de larvas de atún rojo determinando su hábitat reproductor en el mar Balear. Además, las instituciones extranjeras como las que trabajan en el hábitat reproductor del atún rojo en aguas del golfo de México y en las regiones del océano Pacífico han emprendido trabajos de investigación encaminados a conocer la dinámica de la ecología de las primeras fases del ciclo vital del atún rojo y de especies asociadas. Dados los desarrollos recientes, en relación con el acuerdo transatlántico entre Estados Unidos y Europa en el marco de un NOAA-JRC concebido para fomentar las actividades científicas en régimen de cooperación en campos de clima, meteorología, océanos y costas, se considera que el momento actual es el adecuado para celebrar unas jornadas de trabajo para diseñar una hoja de ruta para futuras acciones de cooperación. KEYWORDS Early life ecology, Larval surveys, Bluefin 1. Introduction Historical perspective From the historical point of view, bluefin (Thunnus thynnus) tuna has been a main target species of Mediterranean fisheries, dating as far back as 7000 years B.C. (Desse and Desse-Berset, 1994; Doumenge, 1998). Due to the economic relevance of the fishery, mostly undertaken in the past with fish traps, it has been possible to track to the 17th century the fluctuations of the bluefin catches in several fish traps in the Mediterranean till the beginning of the 20th century (Fromentin and Powers, 2005). Such long historical records has allowed to undertake studies focusing long term climatic variability and bluefin fluctuations (Fromentin and Powers, 2005; Ravier C. and J.-M. Fromentin, 2001; 2004). Despite the economic importance of the bluefin fishery and the recognized role of the influence of early life survival on recruitment variability (Houde, 2008), considerably scarce attention has been paid to the biological aspects in the early life history of this species in the Mediterranean area. Recognizing the merit of the pioneer studies carried out in the Anton Dorn Zoological Station of Naples, renowned Italian researchers as Sella (1924) and Sanzo (1931) were the first scientists to do a taxonomic description of the eggs and larvae of the species. But it is not until the mid-seventies and early nineties when renewed interest rose with the prime objective of localizing bluefin spawning areas in the Mediterranean. A series of bluefin tuna larval surveys were carried out mainly in the W Mediterranean, off the Balearic Sea, the Tyrrhenian Sea, Ionian and S Adriatic (Duclerc et al., 1973; Dicenta et al., 1975; Piccinetti et al., 1976, 1977a; Piccinetti et al., 1977b; Rodriguez-Roda 1975; Piccinetti and Piccinetti-Manfrin, 1978; Rodriguez-Roda and Dicenta, 1981; Dicenta, 1983). This period of exploratory bluefin surveys relapsed until signs of an important decrease of the bluefin stock showed in the Mediterranean. This distressing situation led ICCAT to create the International Bluefin Year Program (BYP) in an effort to impart research guidelines and recommendations for analyzing the bluefin decline, or under a collapsed status for some scientists (McKenzie et al., 2009). Aware of the importance of emphasizing research in the early life history aspects, Japan undertook in 1994 a world-wide bluefin larval survey which sampled the main recognized bluefin spawning grounds located in the Gulf of Mexico and the Mediterranean on board the R/V Shoyo Maru. Tsuji et al. (1997) reported bluefin larval catches off the Baleares Sea and in the Sicilian Channel region. 512

In the Gulf of Mexico, NOAA s Southeast Fisheries Science Center began larval survey cruises beginning in 1982, and continuing to the present (Richards, 1976; Richards and Potthoff, 1980; Richards et al., 1981) these surveys encompassed the northern Gulf of Mexico in the US EEZ (Kelley et al., 1990). These surveys were the basis of the spawning stock biomass estimates for the western Atlantic stock, and until recent work described above were the only fisheries independent assessment of bluefin (McGowan and Richards, 1986; Ingram et al., 2010). State of the art in larval bluefin research At the 2000 SCRS meeting of ICCAT, there were several activities viewed as essential to the future of the BYP. The SCRS endorsed the concept of the proposed exploratory research sampling of larvae and spawning-sized bluefin tuna and the associated oceanographic conditions in the central Atlantic as outlined in SCRS/00/125, extensible to the area around the Balearic Islands (Anon., 2000) as outlined in the research proposal developed by Spain (García et al., 2001), initiating the TUNIBAL project carried out by the Spanish Institute of Oceanography. Prior to the series of TUNIBAL yearly surveys that began in 2001 and lasted till 2005, bluefin larval catches were very sparse, providing very few larval samples to adequately undertake any sort of ecological or biological study on the early life stages of the species. The TUNIBAL surveys modified the sampling strategy, sampling gears and methods with the objective increasing sample size and collecting ample numbers of larvae that would enable to undertake biological studies with important ecological implications. The surveys were highly multidisciplinary, collecting information on the hydrographic conditions and related mesoscale structures, allowing the postulation of hypotheses, mainly to determine the environmental preferences that characterize the bluefin spawning habitat (García et al., 2003). The success of TUNIBAL surveys promoted other bluefin larval exploratory surveys, particularly in the area off northern Cyprus and in the Sicilian channels (García et al., 2004). TUNIBAL s international projection was substantiated by its integration in the CLIOTOP (CLimate Impact on Top Predators), an international project included in GLOBEC project framework. The first report of the Working Group of Early Life History of Top Predators addressed the key focal questions that determine survival at early life stages of top predator species, as tunas (García, Bakun and Margulies, 2007). These questions posed scientific challenges related with studies defining bluefin tuna spawning habitat and the associated hydrographic and climatic processes that condition the timing and reproduction of the species. Accordingly, it motivated early life history research of bluefin larval ecology from different scientific perspectives. The amount of samples throughout the consecutive five years of surveys from 2001-2005 allowed to characterize the spawning preferences of bluefin in the Balearic Sea (Alemany et al., 2010), as well as, the climatic-induced hydrographic scenarios prevailing during the summers of 2001-2005 that influence the bluefin spawning habitat by the formation of fronts and gyres (Balbín et al., in press) and its association with the ichthyoplanktonic assemblages (Rodríguez et al, 2013). From the biological standpoint, the larval samples acquired allowed to define the bluefin larval growth model and its co-ocurring congeneric species, albacore (T. alalunga) (García et al., 2006), together with an assessment on the 2003-2005 bluefin larval growth variability resulting from a climatic heating anomaly (García et al., 2013). Furthermore, studies on the trophic ecology of the species (Catalán et al., 2011) as well as, the influence of cannibalism at early life stages (Reglero et al., 2011) have shed light on the sources of larval survival. In 2006, NOAA undertook an effort funded in part by NASA to use remote sensing products to develop a habitat model for larval bluefin with the goal of reducing the variance of the larval bluefin tuna index in the Gulf of Mexico. This effort led to a series of advances and was instrumental in providing a timely estimate of potential damage to the 2010 bluefin larvae by the Deep Water Horizon oil spill (Muhling et al., 2010, 2011). Recent efforts to explore the boundaries of bluefin larval spawning habitat have led to the collection of bluefin larvae from the Yucatan coast of Mexico (Muhling et al., 2011), and the recent identification of small numbers of larvae northwest of the Bahamas in 2013. Common research goals with the TUNIBAL project led to the establishment of collaborative efforts with the Southeast Fisheries Center of Miami, USA. Exchange of scientific personnel and expertise have been undertaken in recent years leading to the implementation of the comparative approaches which has been exemplified in the comparison of the bluefin spawning habitats from the Gulf of Mexico and the Balearic Sea (Muhling et al., 2013). 513

The continuity on larval bluefin research in the Mediterranean is at present being carried out through the cooperative project ATAME funded by the Spanish Research Council in which the Basque research institution, AZTI and the University of Cádiz are collaborating. The project also counts on the collaboration of a stakeholder, the Balfegó group which is dedicated to commercialization of bluefin food products. The project is focused on the development of fishery independent stock assessment methods related to bluefin reproduction parameters and egg production, as well as, to the development of larval production indices (Ingram et al., 2010). Final Considerations and Recommendations The scientific policies of the EU and USA are advocating in the past years for more transatlantic cooperative research. In fact, the 7 th Framework of the EU includes some EU-USA projects under the general topic of Food, Agriculture and Biotechnology (see Anon., 2009), a step ahead of the Horizon 2020 EU Framework Program which will further enhance and develop greater transatlantic scientific cooperation. Last year, the Joint Research Center of the EU and NOAA signed a cooperation agreement http://ec.europa.eu/dgs/jrc/index.cfm?id=1410&obj_id=14930&dt_code=nws&lang=en&ori=hpg) with the intention of enhancing cooperation on climate, weather, oceans and coasts. The Atlantic bluefin tuna spawning habitat was among the topics considered suitable for transatlantic scientific cooperation by the national delegations. In view of the recent research advances in the field of bluefin early life ecology and the success of bluefin reproduction in captivity that allows larval rearing for experimentation under controlled conditions, a workshop is recommended with the aim of discussing and integrating research efforts from different international institutions. The actual state of cooperative scientific ties between both sides of the Atlantic is considered adequate and timely to develop cooperative actions that could be the basis for the development of future projects. The proposed workshop is intended to encompass a wide suite of topics that define spawning habitat preferences, ranging from larval sampling methodologies to set standards to the implementation of new tools and technologies, as genetics and isotope analysis to define population distribution and species interactions (food web dynamics), growth and fecundity studies, including the environmental impact and climate change on these parameters. New tools based on satellite imagery to undertake spawning habitat studies as exemplified by the work of Druon (2010) will be explored, as well as, those relating the spatial pattern of larval distribution with mesoscale hydrographic features. The end-product of the implementation of these new tools will refer to the development modeling aspects that contribute to the further understanding of the bluefin spawning habitat by integrating the influence of hydrographic circulation and larval distribution and survival. The final objective is intended to foster the implementation state of the art methods and techniques to establish common scientific grounds for comparative research and promote scientific collaboration between research groups from different institutions. This implies sharing current research plans and efforts, the comparison of methods used in each research team and identify areas of potential collaboration for providing a joint research plan in areas of mutual interests. The attainment of these objectives is in line with providing some insight integrating the ecosystem-based approach into fisheries advice. Nonetheless, this workshop recommendation is in need of requiring some funding aid. It has been considered that bearing in mind that the GBYP program contemplated research efforts in different aspects related to early life ecology of bluefin, and that some of the foreseeable participants may be non-iccat participants, some GBYP funding is needed to guarantee the success of the workshop. References Alemany F., García A, Gonzalez-Pola C., Jansa J, Lopez Jurado J.L., Rodriguez J.M., Velez Belchi, P. (2010) Atlantic bluefin tuna and related species spawning habitat characterization: influence of environmental factors on larval abundance and distribution off Balearic archipelago (western Mediterranean). Prog. Oceanogr. 86: 21 38. Anon. (2001) Report of the BYP coordination meeting for sampling survey research in the central Atlantic and near the Balearic Islands (Miami, Florida, USA - April 25-26, 2001). Col.Vol.Sci.Pap. ICCAT, 54 (2): 432-464. 514

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