Des relations trophiques à l'état de santé : allocation d'énergie chez les thons tropicaux – Cas de l'Ouest de l'océan Indien

Tropical tunas (yellowfin, bigeye and skipjack tuna) are exploited worldwide with a quarter of the catches coming from Indian Ocean. Caught by purse seine in mixed schools, these top predators displayed a specific physiology (e.g. partial endothermy, ram-ventilators) but various life history traits (e.g. maximal size, reproduction batches). The objective of this work is to contribute to a better understanding of energy allocation in these species. For this purpose, a monthly sampling was carry out throughout 2013 in Seychelles, to collect tunas on a large range size and environmental conditions. In a first methodological step, we studied the lipids influence on isotopic values in tropical tunas and showed that using mathematical correction of lipids content requires a specific adjustment. Then, using ecological tracers (stable isotope of carbon and nitrogen and fatty acids), a trophic comparison of the three species showed that they do not exploited exactly the same energetic resources, especially due to an ontogenic diet shift. This shift was illustrated by an increasing assimilation of mono-unsaturated fatty acids over 100 cm FL. Study of lipid and protein content in four tissues presenting different physiological function (white and red muscles, liver, gonads) showed these species make little energetic reserves, only in liver and red muscle. In addition, males invest less energy for germinal cells production than females. Furthermore, only the gonado-somatic index brought information concerning energetic variations, the others tested indices (Le Cren condition factor, hepato-somatic index, girth) were bad proxies of energetic content in tissues. Finally, study of membrane fatty acids indicates a specific incorporation of 20:4ω6 and 22:6ω3 that varies with ontogeny. A great intra-specific variability was also observed and could suggest a specific physiological plasticity in these species.Les thons tropicaux (thon jaune, thon obèse et bonite à ventre rayé) sont des espèces largement exploitées dont un quart des prises mondiales provient de l'océan Indien. Capturés en bancs mixtes à la senne, ces prédateurs de haut niveau trophique présentent une physiologie particulière (e.g. thermorégulation partielle, nage obligatoire) mais différents traits de vie (e.g. taille maximale, stratégie de reproduction). L’objectif est ici de contribuer à une meilleure compréhension de l'allocation d'énergie chez ces espèces. Pour cela un échantillonnage mensuel a été mis en place en 2013 aux Seychelles, de manière à collecter des thons sur une large gamme de taille et de conditions environnementales. Un premier travail méthodologique nous a conduit à étudier l'effet de la teneur en lipides sur les valeurs isotopiques, et nous avons montré que l'utilisation d'équation de correction du taux de lipides lors des analyses isotopiques nécessite un ajustement spécifique. Au travers de traceurs écologiques (isotopes stables du carbone et de l'azote et acides gras), une comparaison trophique des trois espèces a montré qu'elles n'exploitent pas exactement les mêmes ressources énergétiques, notamment grâce à un changement alimentaire au cours de l'ontogénie. Ce changement se traduit par l'assimilation de proies plus riches en acides gras mono-insaturés pour les individus supérieurs à 100 cm FL. L'étude des contenus en lipides et protéines de quatre tissus aux fonctions physiologiques différentes (muscles blanc et rouge, foie et gonades) a montré que ces espèces font peu de réserves énergétiques et uniquement dans le foie et le muscle rouge. Les mâles consacrent également moins d'énergie que les femelles à la synthèse de cellules germinales. D'autre part, seul l'indice gonado-somatique permet de rendre compte de variations énergétiques, les autres indices testés (facteur de condition de Le Cren, indice hépato-somatique et circonférence) sont de mauvais proxies du contenu énergétique des tissus. Enfin, l'étude des acides gras membranaires indique une incorporation particulière du 20:4ω6 et du 22:6ω3, dont le niveau varie avec l'ontogénie et selon les tissus. Une grande variabilité intra-spécifique est cependant observée et suggère une certaine plasticité physiologique chez ces espèces

From trophic relationships to health status : energy allocation in tropical tunas - case study of the Western Indian Ocean

Les thons tropicaux (thon jaune, thon obèse et bonite à ventre rayé) sont des espèces largement exploitées dont un quart des prises mondiales provient de l'océan Indien. Capturés en bancs mixtes à la senne, ces prédateurs de haut niveau trophique présentent une physiologie particulière (e.g. thermorégulation partielle, nage obligatoire) mais différents traits de vie (e.g. taille maximale, stratégie de reproduction). L’objectif est ici de contribuer à une meilleure compréhension de l'allocation d'énergie chez ces espèces. Pour cela un échantillonnage mensuel a été mis en place en 2013 aux Seychelles, de manière à collecter des thons sur une large gamme de taille et de conditions environnementales. Un premier travail méthodologique nous a conduit à étudier l'effet de la teneur en lipides sur les valeurs isotopiques, et nous avons montré que l'utilisation d'équation de correction du taux de lipides lors des analyses isotopiques nécessite un ajustement spécifique. Au travers de traceurs écologiques (isotopes stables du carbone et de l'azote et acides gras), une comparaison trophique des trois espèces a montré qu'elles n'exploitent pas exactement les mêmes ressources énergétiques, notamment grâce à un changement alimentaire au cours de l'ontogénie. Ce changement se traduit par l'assimilation de proies plus riches en acides gras mono-insaturés pour les individus supérieurs à 100 cm FL. L'étude des contenus en lipides et protéines de quatre tissus aux fonctions physiologiques différentes (muscles blanc et rouge, foie et gonades) a montré que ces espèces font peu de réserves énergétiques et uniquement dans le foie et le muscle rouge. Les mâles consacrent également moins d'énergie que les femelles à la synthèse de cellules germinales. D'autre part, seul l'indice gonado-somatique permet de rendre compte de variations énergétiques, les autres indices testés (facteur de condition de Le Cren, indice hépato-somatique et circonférence) sont de mauvais proxies du contenu énergétique des tissus. Enfin, l'étude des acides gras membranaires indique une incorporation particulière du 20:4n-6 et du 22:6n-3, dont le niveau varie avec l'ontogénie et selon les tissus. Une grande variabilité intra-spécifique est cependant observée et suggère une certaine plasticité physiologique chez ces espèces.Tropical tunas (yellowfin, bigeye and skipjack tuna) are exploited worldwide with a quarter of the catches coming from Indian Ocean. Caught by purse seine in mixed schools, these top predators displayed a specific physiology (e.g. partial endothermy, ram-ventilators) but various life history traits (e.g. maximal size, reproduction batches). The objective of this work is to contribute to a better understanding of energy allocation in these species. For this purpose, a monthly sampling was carry out throughout 2013 in Seychelles, to collect tunas on a large range size and environmental conditions. In a first methodological step, we studied the lipids influence on isotopic values in tropical tunas and showed that using mathematical correction of lipids content requires a specific adjustment. Then, using ecological tracers (stable isotope of carbon and nitrogen and fatty acids), a trophic comparison of the three species showed that they do not exploited exactly the same energetic resources, especially due to an ontogenic diet shift. This shift was illustrated by an increasing assimilation of mono-unsaturated fatty acids over 100 cm FL. Study of lipid and protein content in four tissues presenting different physiological function (white and red muscles, liver, gonads) showed these species make little energetic reserves, only in liver and red muscle. In addition, males invest less energy for germinal cells production than females. Furthermore, only the gonado-somatic index brought information concerning energetic variations, the others tested indices (Le Cren condition factor, hepato-somatic index, girth) were bad proxies of energetic content in tissues. Finally, study of membrane fatty acids indicates a specific incorporation of 20:4n-6 and 22:6n-3 that varies with ontogeny. A great intra-specific variability was also observed and could suggest a specific physiological plasticity in these species

The key role of the Northern Mozambique Channel for Indian Ocean tropical tuna fisheries

The Northern Mozambique Channel (NMC) is a tropical area of similar to 1 million km(2) where pelagic fisheries supply proteins to more than 9 million people living in Comoros, Mayotte, and along the coasts of Mozambique, Tanzania and Madagascar. Although uncertain, statistics suggest that about 20,000 mt of tropical tuna and other pelagic fish are annually caught by artisanal fisheries in the area. The NMC is also a major seasonal fishing ground for high-seas fleets that export an annual average catch of more than 20,000 mt to tuna can and sashimi markets of high-income countries for a value estimated to be more than 100 million USD. The fisheries productivity of the NMC appears to be highly variable in relation to strong annual and seasonal variability in oceanographic conditions. Our review shows that the NMC is a key feeding area for tropical tunas and a major spawning area for skipjack tuna thanks to warm waters and strong mesoscale activity that results in the enrichment of surface waters and efficient energy transfers enabled by short food chains. Projections of climate models under future warming scenarios predict some strong changes in the oceanographic conditions of the NMC which has already experienced substantial warming over the last decades. Changes in the pelagic ecosystem of the NMC could have dramatic consequences on the coastal populations that are expected to increase towards 100 million people by 2100. Improving monitoring systems and collecting information on the socio-economics of coastal fisheries is crucial to assess the dependence of NMC populations on tuna resources and empower the countries to more involvement in the management of tuna stocks

Estimating growth of tropical tunas in the Indian Ocean using tag-recapture data and otolith-based age estimates

International audienceA growth model from which the expected age of a fish can be estimated based on its length is a key component to most stock assessments. For the three tropical tuna species in the Indian Ocean – yellowfin (YFT; Thunnus albacares), bigeye (BET; T. obesus) and skipjack (SKJ; Katsuwonus pelamis) – information about growth has been very limited until recently, when data from a large-scale Indian Ocean tuna tagging program became available. In this paper, parametric growth models were fit to tag-recapture data for all three species using a maximum likelihood method that models the joint density of release and recapture lengths as a function of age by treating age at tagging as a random variable. The method allows for individual variability in growth by modelling the asymptotic length parameter as a random effect. Direct age and length data from otolith readings were also included in the analysis for YFT and BET. The results support two-stanza growth models for all three species; however, the growth patterns for YFT and BET differ from SKJ. YFT and BET exhibit a transition in growth between age 2 and 3, with faster growth in the second stanza than the first, whereas SKJ exhibit a transition in growth around age 1, with much faster growth in the first stanza than the second. Most likely, YFT and BET also experience a phase of rapid growth directly following hatching, but lack of data for fish less than 50 cm for these species precludes its estimation. Differences in growth between sexes were found for YFT and BET, with males growing to a larger size; information on sex was not available for SKJ

Are condition factors powerful proxies of energy content in wild tropical tunas?

The "condition" is used as an indicator of fish health and is generally equated with the quantity of energy reserves. Biometric condition factors have been widely used and preferred over costly and time-consuming biochemical condition. Here, we investigated the relevance of four common condition factors based on biometric measurements (Le Cren's index, girth -length index, gonado-somatic index and hepato-somatic index) and of size- and weight -based empirical models to describe the physiological condition of tropical tunas. Biometric condition factors of bigeye (Thunnus obesus), skipjack (Katsuwonus pelamis) and yellowfin (Thunnus albacares) tunas sampled throughout 2013 in the western Indian Ocean region were assessed against benchmark biochemical indices (lipid content, protein content, triacylglycerol:sterol ratio and energy density) estimated in tissues with different physiological functions, i.e. red muscle, white muscle, liver, and gonads. Our findings suggest that tropical tunas do not store lipids in white muscle and that protein content is less variable than lipid content, which largely varies with ontogeny and the seasons according to tissue and species. This variability induced inconsistency between biometric factors, including the empirically adjusted ones, and biochemical indices, with the exception of the gonado-somatic index that fitted well to the composition of the gonads in the three species, and especially in females. (C) 2016 Elsevier Ltd. All rights reserved

Trophic structures in tropical marine ecosystems: a comparative investigation using three different ecological tracers

We looked at how three ecological tracers may influence the characterization and interpretation of trophic structures in a tropical marine system, with a view to informing tracer(s) selection in future trophic ecology studies. We compared the trophic structures described by stable isotope compositions (carbon and nitrogen), the total mercury concentration (THg) and levels of essential fatty acids (EFA) at both the individual and species level. Analyses were undertaken on muscle tissue samples from fish and crustacean species caught in the waters surrounding the Seychelles. The carbon isotope composition (delta C-13) correlated to the proportion of arachidonic acid (ARA), whereas the nitrogen isotope composition (delta N-15) correlated to the proportion of docosahexaenoic acid (DHA) and THg. At the individual level, trophic position obtained with these three last tracers are similar. In ' contrast, the eicosapentaenoic acid (EPA) was not clearly correlated to any of the tracers. At the species level, the use of EFA (ARA and DHA), as compared to stable isotopes, resulted in slight structural modifications, mainly in the middle trophic levels. For example, the EFA overestimated the trophic positions of Thunnus alalunga and Etelis coruscans but underestimated the trophic positions of other snappers and groupers. While ARA mainly originates from coastal/benthic areas, DHA is conserved throughout the food web and may be used as a proxy indicator of trophic position. However, metabolic disparities can affect ecological tracers and in turn, distort the trophic structures derived from their results. This is especially true for species with close trophic ecologies. Despite these caveats, we think that analysing at the individual level the wealth of ARA, DHA and THg data that has already been obtained through earlier nutrition or food security studies would enhance our understanding of trophic structures

Biological and environmental influence on tissue fatty acid compositions in wild tropical tunas

International audienceThis study examined the fatty acid composition of three sympatric tropical tuna species (bigeye Thunnus obesus, yellowfin T. albacares and skipjack tuna Kastuwonus pelamis) sampled in the Western Indian Ocean in 2013. The fatty acid compositions of neutral and polar lipids, respectively involved in energy storage and cell membrane structure, were explored and compared in four tissues (red and white muscles, liver and gonads), according to biological (size, sex and maturity) and environmental (season and area) factors. The liver and the red muscle were the fattest tissues (i.e., higher levels of storage lipids) in all species and polar lipids were the lowest in the white muscle. Species and tissue types explained most differences in fatty acid compositions, while environmental factors had limited effects, except in the hepatic cell membrane where fatty acid composition varied with monsoons. Docosahexaenoic acid (22:6n-3) was the major fatty acid in both polar and neutral lipid fractions, especially in muscles. Eicosapentaenoic acid (20:5n-3) and oleic acid (18:1n-9) were in higher proportion in neutral than in polar lipids. Arachidonic acid (20:4n-6) and 22:6n-3, together with docosapentaenoic acid (22:5n-6) and stearic acid (18:0), showed preferential accumulation in polar lipids. 20:4n-6 was particularly involved in cell membranes of ovary and white muscle. Overall, an important inter-individual variability in fatty acid compositions of structural lipids was found within tissue types despite considering biological factors that are most likely to influence this type of lipids. It suggests that fatty acid profiles are influenced by individual-specific behaviors

An integrated Bayesian modeling approach for the growth of Indian Ocean yellowfin tuna

The Indian Ocean Tuna Tagging Program provided a unique opportunity to collect demographic data on the key commercially targeted tropical tuna species in the Indian Ocean. In this paper, we focused on estimating growth rates for one of these species, yellowfin (Thunnus albacares). Whilst most growth studies only draw on one data source, in this study we use a range of data sources: individual growth rates derived from yellowfin that were tagged and recaptured, direct age estimates obtained through otolith readings, and length-frequency data collected from the purse seine fishery between 2000 and 2010. To combine these data sources, we used an integrated Bayesian model that allowed us to account for the process and measurement errors associated with each data set. Our results indicate that the gradual addition of each data type improved the model's parameter estimations. The Bayesian framework was useful, as it allowed us to account for uncertainties associated with age estimates and to provide additional information on some parameters (e.g., asymptotic length). Our results support the existence of a complex growth pattern for Indian Ocean yellowfin, with two distinct growth phases between the immature and mature life stages. Such complex growth patterns, however, require additional information on absolute age of fish and transition rates between growth stanzas. This type of information is not available from the data. We suggest that bioenergetic models may address this current data gap. This modeling approach explicitly considers the allocation of metabolic energy in tuna and may offer a way to understand the underlying mechanisms that drive the observed growth patterns

IO Tuna tagging

The Indian Ocean Tuna Tagging Program (IOTTP) provided a unique opportunity to assess the viability of estimating the age of tropical tunas from the micro-structural features of otoliths. Here, we analyzed the length measurements and micro-increment counts collected for 506 sagittal otoliths, of which 343 were chemically marked with oxytetracycline, for bigeye (Thunnus obesus), skipjack (Katsuwonus pelamis), and yellowfin tuna (Thunnus albacares). Our results show that the otoliths of tropical tunas grow more slowly than the rest of the body. Our findings confirm that both yellowfin and juvenile bigeye deposit daily increments in their otoliths, though ages are underestimated for large bigeye (>100 cm) when derived from micro-increment counts. Our results also indicate that skipjack otoliths are not suitable for age estimations during the adult phase, as evidenced by the poor agreement between micro-increment counts and days-at-liberty. We hypothesize that the income breeding strategy of skipjack could explain the variability observed in the deposition rates. Due to their complex micro-structural patterns, the reading of tropical tuna otoliths requires a degree of interpretation that can result in poor count precision and large variability in micro-increment counts, both among and within teams of readers. Age estimates were found to vary between readers, a factor which can eventually affect growth estimates and ultimately, impact on fisheries management decisions and outcomes. To address this, we recommend that reference collections of otoliths are developed, with a view to standardizing the reading process. Further, alternative methods, such as annual age estimations (as opposed to daily), and alternative structures, such as dorsal spines for skipjack, should be used to improve the accuracy of age estimations and the speed with which they can be made

How membrane fatty acids influence sardine size across diverse marine environments

Differences in diet quality and quantity may influence trophodynamic processes in small pelagic fish. Yet, we currently lack direct and comprehensive information on how large-scale areas differ in dietary resources and the degree to which these differences influence fish physiological performances (i.e., growth), ultimately influencing entire fish stocks. Fatty acid composition is one of the bioindicator that can provide insights on how dietary provisions of essential lipids influence the structure of the membrane fatty acids and subsequently fish growth among contrasted habitats. To address this issue, we conducted a large-scale sampling of European sardine (Sardina pilchardus) a species with major socio-economic importance that plays a key role as an energy pathway linking lower and upper trophic levels in pelagic ecosystems. We sampled individuals from the Gulf of Lions (Mediterranean Sea), the Bay of Biscay, and the English Channel (Atlantic Ocean) of age-0 to -3+and found clear spatial differences in the quantity and quality of dietary lipids. Sardines from the Gulf of Lions fed on trophic food web based on dinoflagellates, with greater proportions of DHA (22:6n-3; docosahexaenoic acid) in reserve lipids. Sardines’ reserve lipids had important proportions of zooplankton biomarkers in the English Channel (e.g., 20:1n-9 and 20:1n-11), and diatoms biomarkers such as 16C fatty acids and EPA (20:5n-3; eicosapentaenoic acid) in the Bay of Biscay. The relationship between sardines’ membrane fatty acid composition and individuals’ length changed progressively with individuals’ age, a result consistent across areas, indicating ontogenetic abilities between largest and smallest individuals. Before maturity, largest sardines had higher DHA proportions, followed after maturity by higher proportions of ARA (20:4n-6; arachidonic acid), EPA and DPA (22:5n-3; docosapentaenoic acid). Finally, the study highlights the importance of considering the quality and diversity of dietary resources to better understand how individuals cope with their physiological needs. It is thus important to consider combined aspects (e.g., diet quality and diversity, influence of particular nutrients on length) to better understand the underlying mechanistic processes influencing fish physiology, likely cascading to different expression of their life history traits and affecting fisheries stocks