Nursery origin of yellowfin tuna in the western Atlantic Ocean: significance of Caribbean Sea and trans-Atlantic migrants.

Natural geochemical markers in the otolith of yellowfin tuna (Thunnus albacares) were used to establish nursery-specific signatures for investigating the origin of fish captured in the western Atlantic Ocean (WAO). Two classes of chemical markers (trace elements, stable isotopes) were used to first establish nursery-specific signatures of age-0 yellowfin tuna from four primary production zones in the Atlantic Ocean: Gulf of Mexico, Caribbean Sea, Cape Verde, and Gulf of Guinea. Next, mixture and individual assignment methods were applied to predict the origin of sub-adult and adult yellowfin tuna from two regions in the WAO (Gulf of Mexico, Mid Atlantic Bight) by relating otolith core signatures (corresponding to age-0 period) to baseline signatures of age-0 fish from each nursery. Significant numbers of migrants from Caribbean Sea and eastern Atlantic Ocean (EAO) production zones (Gulf of Guinea, Cape Verde) were detected in the WAO, suggesting that fisheries in this region were subsidized by outside spawning/nursery areas. Contributions from local production (Gulf of Mexico) were also evident in samples from both WAO fisheries, but highly variable from year to year. High levels of mixing by yellowfin tuna from the different production zones and pronounced interannual trends in nursery-specific contribution rates in the WAO emphasize the complex and dynamic nature of this species' stock structure and population connectivity. Given that geographic shifts in distribution across national or political boundaries leads to governance and management challenges, this study highlights the need for temporally resolved estimates of nursery origin to refine assessment models and promote the sustainable harvest of this species.

The distribution of subarctic and boreal deep-sea demersal fish assemblages across environmental gradients of the northwest Atlantic.

The oceanography of the Labrador Sea is well studied because of its globally important deep-water convection that oxygenates the deep ocean and drives climate-regulating ocean currents. However, little is known about the fish communities that inhabit this area, particularly beyond the depths accessible to standard research surveys and commercial fishing activities. We used baited longline surveys to characterize important components of demersal fish communities across a depth gradient of 200-3000 m and compared these data to a similar dataset collected c. 1200 km to the south in the Flemish Cap Region. We found demersal fish communities in the Labrador Sea to be similar to those of the Flemish Cap Region despite unique oceanography and lower primary productivity in the Labrador Sea. Moreover, both areas had high abundance, biomass, and species richness at intermediate depths that suggests factors beyond depth drive community structure in the deep ocean. These data are important for identifying high-value areas for potential protective measures in the northwest Atlantic and provide necessary data with which to assess potential environmental impacts of extractive industries that are expanding north and to deeper waters.

Chemical signatures in fin spine edge of Atlantic bluefin tuna (Thunnus thynnus) can serve as habitat markers of geographically distinct marine environments.

Chemical fingerprints in otoliths are commonly used as natural habitat markers in fishes. Alternatively, the first dorsal fin spine can provide valuable chemical information and may be more suitable for studying (i) endangered fish species that cannot be sacrificed for their otoliths or (ii) fishes for which otoliths might not be available because of management or commercial reasons. Here, we studied multi-element chemistry of fin spine edges collected from Atlantic bluefin tuna (ABFT; Thunnus thynnus) (Linnaeus, 1758) to investigate the utility of the fin spine edge as a natural habitat marker. We determined stable isotopic δ18O and δ13C ratios, as well as concentrations of the tracer elements Mg, Mn, Li, Ba, and Sr, at the edge of ABFT fin spines, and then we used these measures to discriminate ABFT individuals among capture regions (i.e., the eastern Atlantic Ocean or Mediterranean Sea). Isotope ratios and tracer element concentrations, and especially a combined multi-element approach, were able to effectively discriminate individuals by capture region. The Mg, Mn, Li, and δ18O concentrations were the strongest variables driving this discrimination. Overall, our results demonstrate that chemical signatures are consistently retained in the ABFT fin spine edge and support the use of fin spine edges for discerning habitat use. The fin spine chemistry as a minimally invasive sampling method, combined with otolith chemistry, genetic markers, and tagging efforts can help us to reconstruct fish movements, providing a deeper understanding of the spatial population dynamics of this iconic fish species.

Seventy years of tunas, billfishes, and sharks as sentinels of global ocean health.

Fishing activity is closely monitored to an increasing degree, but its effects on biodiversity have not received such attention. Using iconic and well-studied fish species such as tunas, billfishes, and sharks, we calculate a continuous Red List Index of yearly changes in extinction risk over 70 years to track progress toward global sustainability and biodiversity targets. We show that this well-established biodiversity indicator is highly sensitive and responsive to fishing mortality. After ~58 years of increasing risk of extinction, effective fisheries management has shifted the biodiversity loss curve for tunas and billfishes, whereas the curve continues to worsen for sharks, which are highly undermanaged. While populations of highly valuable commercial species are being rebuilt, the next management challenge is to halt and reverse the harm afflicted by these same fisheries to broad oceanic biodiversity.

A review of the fisheries, life history and stock structure of tropical tuna (skipjack Katsuwonus pelamis, yellowfin Thunnus albacares and bigeye Thunnus obesus) in the Indian Ocean.

Skipjack (Katsuwonus pelamis), yellowfin (Thunnus albacares) and bigeye (Thunnus obesus) tuna are the target species of tropical tuna fisheries in the Indian Ocean, with high commercial value in the international market. High fishing pressure over the past three decades has raised concerns about their sustainability. Understanding life history strategies and stock structure is essential to determine species resilience and how they might respond to exploitation. Here we provide a comprehensive review of available knowledge on the biology, ecology, and stock structure of tropical tuna species in the Indian Ocean. We describe the characteristics of Indian Ocean tropical tuna fisheries and synthesize skipjack, yellowfin, and bigeye tuna key life history attributes such as biogeography, trophic ecology, growth, and reproductive biology. In addition, we evaluate the available literature about their stock structure using different approaches such as analysis of fisheries data, genetic markers, otolith microchemistry and tagging, among others. Based on this review, we conclude that there is a clear lack of ocean basin-scale studies on skipjack, yellowfin and bigeye tuna life history, and that regional stock structure studies indicate that the panmictic population assumption of these stocks should be investigated further. Finally, we identify specific knowledge gaps that should be addressed with priority to ensure a sustainable and effective management of these species.

Otolith chemical fingerprints of skipjack tuna (Katsuwonus pelamis) in the Indian Ocean: First insights into stock structure delineation.

The chemical composition of otoliths (earbones) can provide valuable information about stock structure and connectivity patterns among marine fish. For that, chemical signatures must be sufficiently distinct to allow accurate classification of an unknown fish to their area of origin. Here we have examined the suitability of otolith microchemistry as a tool to better understand the spatial dynamics of skipjack tuna (Katsuwonus pelamis), a highly valuable commercial species for which uncertainties remain regarding its stock structure in the Indian Ocean. For this aim, we have compared the early life otolith chemical composition of young-of-the-year (<6 months) skipjack tuna captured from the three main nursery areas of the equatorial Indian Ocean (West, Central and East). Elemental (Li:Ca, Sr:Ca, Ba:Ca, Mg:Ca and Mn:Ca) and stable isotopic (δ13C, δ18O) signatures were used, from individuals captured in 2018 and 2019. Otolith Sr:Ca, Ba:Ca, Mg:Ca and δ18O significantly differed among fish from different nurseries, but, in general, the chemical signatures of the three nursery areas largely overlapped. Multivariate analyses of otolith chemical signatures revealed low geographic separation among Central and Eastern nurseries, achieving a maximum overall random forest cross validated classification success of 51%. Cohort effect on otolith trace element signatures was also detected, indicating that variations in chemical signatures associated with seasonal changes in oceanographic conditions must be well understood, particularly for species with several reproductive peaks throughout the year. Otolith microchemistry in conjunction with other techniques (e.g., genetics, particle tracking) should be further investigated to resolve skipjack stock structure, which will ultimately contribute to the sustainable management of this stock in the Indian Ocean.

Using a Bayesian modelling approach (INLA-SPDE) to predict the occurrence of the Spinetail Devil Ray (Mobular mobular).

To protect the most vulnerable marine species it is essential to have an understanding of their spatiotemporal distributions. In recent decades, Bayesian statistics have been successfully used to quantify uncertainty surrounding identified areas of interest for bycatch species. However, conventional simulation-based approaches are often computationally intensive. To address this issue, in this study, an alternative Bayesian approach (Integrated Nested Laplace Approximation with Stochastic Partial Differential Equation, INLA-SPDE) is used to predict the occurrence of Mobula mobular species in the eastern Pacific Ocean (EPO). Specifically, a Generalized Additive Model is implemented to analyze data from the Inter-American Tropical Tuna Commission's (IATTC) tropical tuna purse-seine fishery observer bycatch database (2005-2015). The INLA-SPDE approach had the potential to predict both the areas of importance in the EPO, that are already known for this species, and the more marginal hotspots, such as the Gulf of California and the Equatorial area which are not identified using other habitat models. Some drawbacks were identified with the INLA-SPDE database, including the difficulties of dealing with categorical variables and triangulating effectively to analyze spatial data. Despite these challenges, we conclude that INLA approach method is an useful complementary and/or alternative approach to traditional ones when modeling bycatch data to inform accurately management decisions.

Environmental characteristics associated with the presence of the Spinetail devil ray (Mobula mobular) in the eastern tropical Pacific.

In the eastern Pacific Ocean, the tropical tuna purse-seine fishery incidentally captures high numbers of five mobulid bycatch species; all of which are classified as mortalities by the Inter-American Tropical Tuna Commission due to uncertainties in post-release mortality rates. To date, the factors (operational or environmental) leading to the capture of these species by the fishery have not been well studied. Here, we developed Generalized Additive Models for fisheries observer data to analyze the relationships between the presence/absence of Mobula mobular bycatch and oceanographic conditions, the spatial and temporal variability in fishing location, and the set type (associated with dolphins, free-swimming tuna schools or floating objects). Our results suggest that chlorophyll concentration and sea surface height are the most important variables to describe the presence of M. mobular in conjunction with geographic location (latitude and longitude) and set type. Presence of the species was predicted in waters with chlorophyll concentrations between 0.5-1 mg·m-3 and with sea surface height values close to 0; which indicates direct relationships with productive upwelling systems. Seasonally, M. mobular was observed more frequently during December-January and August-September. We also found the highest probability of presence observed in School sets, followed by Dolphin sets. Three areas were observed as important hotspots: the area close to the coastal upwelling of northern Peru, the area west to Islands Colon Archipelago (Galapagos) and the area close to the Costa Rica Dome. This information is crucial to identify the mobulids habitat and hotspots that could be managed and protected under dynamic spatial management measures to reduce the mortality of mobulid rays in the eastern Pacific purse-seine fishery and, hence, ensure the sustainability of the populations of these iconic species.

Characterization of carbonate fraction of the Atlantic bluefin tuna fin spine bone matrix for stable isotope analysis.

The mineral component of fish otoliths (ear bones), which is aragonitic calcium carbonate (CaCO3), makes this structure the preferred sample choice for measuring biological carbon and oxygen-stable isotopes in order to address fundamental questions in fish ecology and fisheries science. The main drawback is that the removal of otoliths requires sacrificing the specimen, which is particularly impractical for endangered and commercially valuable species such as Atlantic bluefin tuna (Thunnus thynnus) (ABFT). This study explores the suitability of using the first dorsal fin spine bone of ABFT as a non-lethal alternative to otolith analysis or as a complementary hard structure. The fin spines of freshly caught ABFT were collected to identify carbonate ions within the mineral matrix (i.e., hydroxyapatite) and to determine the nature of the carbonate substitution within the crystal lattice, knowledge which is crucial for correct measurement and ecological interpretation of oxygen and carbon stable isotopes of carbonates. Fin spine sections were analyzed via X-ray Photoelectron Spectroscopy (XPS), Raman Spectroscopy, and Fourier Transform InfraRed (FTIR). The XPS survey analysis showed signals of Ca, O, and P (three compositional elements that comprise hydroxyapatite). The Raman and FTIR techniques showed evidence of carbonate ions within the hydroxyapatite matrix, with the IR spectra being the most powerful for identifying the type B carbonate substitution as shown by the carbonate band in the v 2 CO3 2- domain at ∼872 cm-1. The results of this study confirmed the presence of carbonate ions within the mineral matrix of the fin spine bone of ABFT, showing the feasibility of using this calcified structure for analysis of stable isotopes. Overall, our findings will facilitate new approaches to safeguarding commercially valuable and endangered/protected fish species and will open new research avenues to improve fisheries management and species conservation strategies.

Large-scale distribution of tuna species in a warming ocean.

Tuna are globally distributed species of major commercial importance and some tuna species are a major source of protein in many countries. Tuna are characterized by dynamic distribution patterns that respond to climate variability and long-term change. Here, we investigated the effect of environmental conditions on the worldwide distribution and relative abundance of six tuna species between 1958 and 2004 and estimated the expected end-of-the-century changes based on a high-greenhouse gas concentration scenario (RCP8.5). We created species distribution models using a long-term Japanese longline fishery dataset and two-step generalized additive models. Over the historical period, suitable habitats shifted poleward for 20 out of 22 tuna stocks, based on their gravity centre (GC) and/or one of their distribution limits. On average, tuna habitat distribution limits have shifted poleward 6.5 km per decade in the northern hemisphere and 5.5 km per decade in the southern hemisphere. Larger tuna distribution shifts and changes in abundance are expected in the future, especially by the end-of-the-century (2080-2099). Temperate tunas (albacore, Atlantic bluefin, and southern bluefin) and the tropical bigeye tuna are expected to decline in the tropics and shift poleward. In contrast, skipjack and yellowfin tunas are projected to become more abundant in tropical areas as well as in most coastal countries' exclusive economic zones (EEZ). These results provide global information on the potential effects of climate change in tuna populations and can assist countries seeking to minimize these effects via adaptive management.

Aggregation process of drifting fish aggregating devices (DFADs) in the Western Indian Ocean: Who arrives first, tuna or non-tuna species?

Floating objects drifting in the surface of tropical waters, also known as drifting fish aggregating devices (DFADs), attract hundreds of marine species, including tuna and non-tuna species. Industrial tropical purse seiners have been increasingly deploying artificial man-made DFADs equipped with satellite linked echo-sounder buoys, which provide fishers with information on the accurate geo-location of the object and rough estimates of the biomass aggregated underneath, to facilitate the catch of tuna. Although several hypotheses are under consideration to explain the aggregation and retention processes of pelagic species around DFADs, the reasons driving this associative behavior are uncertain. This study uses information from 962 echo-sounder buoys attached to virgin (i.e. newly deployed) DFADs deployed in the Western Indian Ocean between 2012 and 2015 by the Spanish fleet (42,322 days observations) to determine the first detection day of tuna and non-tuna species at DFAD and to model the aggregation processes of both species group using Generalize Additive Mixed Models. Moreover, different seasons, areas and depths of the DFAD underwater structure were considered in the analysis to account for potential spatio-temporal and structure differences. Results show that tuna species arrive at DFADs before non-tuna species (13.5±8.4 and 21.7±15.1 days, respectively), and provide evidence of the significant relationship between DFAD depth and detection time for tuna, suggesting faster tuna colonization in deeper objects. For non-tuna species, this relationship appeared to be not significant. The study also reveals both seasonal and spatial differences in the aggregation patterns for different species groups, suggesting that tuna and non-tuna species may have different aggregative behaviors depending on the spatio-temporal dynamic of DFADs. This work will contribute to the understanding of the fine and mesoscale ecology and behavior of target and non-target species around DFADs and will assist managers on the sustainability of exploited resources, helping to design spatio-temporal conservation management measures for tuna and non-tuna species.

Ecological data for western Indian Ocean tuna.

Tuna are marine apex predators that inhabit the tropical and sub-tropical waters of the Indian Ocean where they support socially and economically important fisheries. Key component of pelagic communities, tuna are bioindicator species of anthropogenic and climate-induced changes through modifications of the structure and related energy-flow of food webs and ecosystems. The IndianEcoTuna dataset provides a panel of ecological tracers measured in four soft tissues (white muscle, red muscle, liver, gonads) from 1,364 individuals of four species, i.e., the albacore (ALB, Thunnus alalunga), the bigeye (BET, T. obesus), the skipjack (SKJ, Katsuwomus pelamis), and the yellowfin (YFT, T. albacares), collected throughout the western Indian Ocean from 2009 to 2015. Sampling was carried out during routine monitoring programs, at sea by observers onboard professional vessels or at landing. For each record, the type of fishing gear, the conservation mode, as well as the fishing date and catch location are provided. Individuals were sampled to span a wide range of body sizes: 565 ALB with fork length from 58 to 118 cm, 155 BET from 29.5 to 173 cm, 304 SKJ from 30 to 74 cm, and 340 YFT from 29 to 171.5 cm. The IndianEcoTuna dataset combines: (1) 9,512 records of carbon and nitrogen stable isotopes (percent element weights, δ13 C and δ15 N values) in 1,185 fish, (2) 887 concentrations of total proteins in 242 fish, (3) 8,356 concentrations of total lipids and three lipid classes (triacylglycerols TAG; phospholipids PL; sterols ST) in 695 fish, and (4) 1,150 and 1,033 profiles of neutral and polar fatty acids in 397 and 342 fish, respectively. Information on sex and weights of the whole fish, gonads, liver and stomach is provided. Because of the essential trophic role and wide-ranging of tuna in marine systems, and the large panel of tropho-energetic tracers and derived-key quantitative parameters provided (e.g., niche width, trophic position, condition indices), the IndianEcoTuna dataset should be of high interest for global and regional research on marine trophic ecology and food web analysis, as well as on the impacts of anthropogenic changes on Indian Ocean marine ecosystems. There are no copyright restrictions for research and/or teaching purposes. Usage of the dataset must include citation of this Data Paper.

RAD-seq derived genome-wide nuclear markers resolve the phylogeny of tunas.

Although species from the genus Thunnus include some of the most commercially important and most severely overexploited fishes, the phylogeny of this genus is still unresolved, hampering evolutionary and traceability studies that could help improve conservation and management strategies for these species. Previous attempts based on mitochondrial and nuclear markers were unsuccessful in inferring a congruent and reliable phylogeny, probably due to mitochondrial introgression events and lack of enough phylogenetically informative markers. Here we infer the first genome-wide nuclear marker-based phylogeny of tunas using restriction site associated DNA sequencing (RAD-seq) data. Our results, derived from phylogenomic inferences obtained from 128 nucleotide matrices constructed using alternative data assembly procedures, support a single Thunnus evolutionary history that challenges previous assumptions based on morphological and molecular data.

Closely Related Fishes Inhabiting Different Ecosystems Exhibit the Same Oocyte Production and Recruitment Pattern.

Information on oocyte production and recruitment in phylogenetically related species can help in understanding the evolution of reproductive life-history traits in fish of indeterminate fecundity. The present study compared, for the first time, oocyte production and recruitment patterns between two closely related species: Stellifer brasiliensis and Stellifer rastrifer (Perciformes, Sciaenidae), in the southwestern Atlantic, Brazil. Specimens of S. brasiliensis were sampled from the coastal waters of Ubatuba, and samples of S. rastrifer were taken from the Cananéia Lagoon Estuarine System. Ovaries were investigated using histology and model-based stereology. The total number of oocytes per individual (N) and stage-specific oocyte packing density did not differ significantly between S. brasiliensis and S. rastrifer The number of pre-vitellogenic and vitellogenic oocytes were positively correlated with female total weight and length, and ovary weight in both species. Analysis of oocyte recruitment across their development stages revealed that approximately 5.9% of the standing stock oocytes larger than 50 µm in S. brasiliensis and 5.0% in S. rastrifer were recruited to form the next batches. Females of S. brasiliensis and S. rastrifer, in spawning-capable phase, exhibit the same oocyte production and recruitment patterns, showing no influences of the ecosystems on primary and secondary oocyte production.

Methodological assessment of 2b-RAD genotyping technique for population structure inferences in yellowfin tuna (Thunnus albacares).

Global population genetic structure of yellowfin tuna (Thunnus albacares) is still poorly understood despite its relevance for the tuna fishery industry. Low levels of genetic differentiation among oceans speak in favour of the existence of a single panmictic population worldwide of this highly migratory fish. However, recent studies indicated genetic structuring at a much smaller geographic scales than previously considered, pointing out that YFT population genetic structure has not been properly assessed so far. In this study, we demonstrated for the first time, the utility of 2b-RAD genotyping technique for investigating population genetic diversity and differentiation in high gene-flow species. Running de novo pipeline in Stacks, a total of 6772 high-quality genome-wide SNPs were identified across Atlantic, Indian and Pacific population samples representing all major distribution areas. Preliminary analyses showed shallow but significant population structure among oceans (FST=0.0273; P-value<0.01). Discriminant Analysis of Principal Components endorsed the presence of genetically discrete yellowfin tuna populations among three oceanic pools. Although such evidence needs to be corroborated by increasing sample size, these results showed the efficiency of this genotyping technique in assessing genetic divergence in a marine fish with high dispersal potential.

Contrasting evolutionary demography induced by fishing: the role of adaptive phenotypic plasticity.

Mounting evidence now shows that fishing activity modifies both heritable life-history traits and ecological processes in harvested populations. However, ecological and evolutionary changes are intimately linked and can occur on the same time scale, and few studies have investigated their combined effect on fish population dynamics. Here, we contrast two population subunits of a harvested fish species in the Northeast Atlantic, the European hake (Merluccius merluccius), in the light of the emerging field of evolutionary demography, which considers the interacting processes between ecology and evolution. The two subunits experienced similar age/size truncation due to size-selective fishing, but displayed differences in key ecological processes (recruitment success) and phenotypic characteristics (maturation schedule). We investigate how temporal variation in maturation and recruitment success interactively shape the population dynamics of the two subunits. We document that the two subunits of European hake displayed different responses to fishing in maturation schedules, possibly because of the different level of adaptive phenotypic plasticity. Our results also suggest that high phenotypic plasticity can dampen the effects of fisheries-induced demographic truncation on population dynamics, whereas a population subunit characterized by low phenotypic plasticity may suffer from additive effects of ecological and life-history responses. Similar fishing pressure may thus trigger contrasting interactions between life history variation and ecological processes within the same population. The presented findings improve our understanding of how fishing impacts eco-evolutionary dynamics, which is a keystone for a more comprehensive management of harvested species.

The biology and fisheries of European hake, Merluccius merluccius, in the north-east Atlantic.

The aim of this chapter is to review the biology and fishery, including the management, of European hake in the north-east Atlantic. The European hake is widely distributed throughout the north-east Atlantic, from Norway in the north to the Guinea Gulf in the south, and throughout the Mediterranean and Black Sea, being more abundant from the British Isles to the south of Spain. In this area, ICES (International Council for the Exploration of the Sea) recognises the existence of two stocks: the northern stock and the southern stock. Both stocks have been extensively and intensively harvested and since the beginning of the 90s have been considered to be outside safe biological limits. The northern stock, however, is currently considered to lie within safe biological limits. In any case, recovery plans were implemented for the northern stock in 2004 and for the southern stock in 2006. Despite its commercial importance, knowledge of the biology and ecology of the European hake in the North Atlantic is still quite scarce. For example, recent investigations suggest that European hake grows much faster, by a factor of two, than was considered previously. This faster growth also affects the maturity-at-age pattern of hake and the agreed maturity-at-age ogive used in the assessments. European hake is a top predator in the demersal community in the north-east Atlantic area; mainly preying on blue whiting, horse mackerel and other cupleids. In relation to the reproductive biology, European hake is considered to be a batch spawner species with indeterminate fecundity and spawning activity all year round. All these characteristics could, in turn, be interpreted as European hake adopting a more opportunistic life strategy, which is unusual for a gadoid and demersal species, and raises several questions about hake biology and ecology that require further investigation.