Coastal upwelling influences population structure of dusky grouper Epinephelus marginatus: An integrative approach based on otolith chemistry and muscle stable isotopes.

The dusky grouper (Epinephelus marginatus) is an overfished and threatened fish species with coastal distribution. In the Southwestern Atlantic, it occurs across a broad region influenced by two major oceanographic features: the Cabo Frio (23°S) and the Cabo Santa Marta (28°S) upwelling systems. Along the Brazilian coast, the species may present continuous or discrete populations, depending on the methodological approach used. In this study we combined otolith chemistry and muscle stable isotope analyses to examine the population structure of dusky groupers and its association with the two upwelling systems. Fish were collected in shallow coastal waters of the Southwest Atlantic Ocean, covering the southeastern and southern Brazilian coasts, among Macaé (22°S), Santos (24°S), Florianópolis (27°S), and in Rio Grande (32°S). The results show three statistically well-separated population groups along the region. We named these population groups as North (north of Cabo Frio); Center (between upwelling regions); and South (south of the Cabo Santa Marta system). Our findings allow to suggest that the upwelling systems may influence the distribution of E. marginatus stocks along the Brazilian south-western coast, even though a causal effect may not be attributed at this point. Overall, this combined approach, leveraging information from distinct natural tags, and reflecting variability of water chemistry and food webs with latitude, allowed us to enhance our understanding on how major upwelling systems influence the structuring of fish populations along the southwestern Atlantic Ocean.

Complex interactions of ENSO and local conditions buffer the poleward shift of migratory fish in a subtropical seascape.

Ocean warming is associated with the tropicalization of fish towards higher latitudes. However, the influence of global climatic phenomena like the El Niño Southern Oscillation (ENSO) and its warm (El Niño) and cold (La Niña) phases on tropicalization has been overlooked. Understanding the combined effects of global climatic forces together with local variability on the distribution and abundance of tropical fish is essential for building more accurate predictive models of species on the move. This is particularly important in regions where ENSO-related impacts are known to be major drivers of ecosystem change, and is compounded by predictions that El Niño is becoming more frequent and intense under current ocean warming. In this study, we used long-term time series of monthly standardized sampling (August 1996 to February 2020) to investigate how ocean warming, ENSO and local environmental variability influence the abundance of an estuarine dependent tropical fish species (white mullet Mugil curema) at subtropical latitudes in the southwestern Atlantic Ocean. Our work revealed a significant increasing trend in surface water temperature in shallow waters (<1.5 m) at estuarine and marine sites. However, against our initial expectation, we did not observe an increasing trend in the abundance of this tropical mullet species. Generalized Additive Models revealed complex, non-linear relationships between species abundance and environmental factors operating at large (ENSO's warm and cold phases), regional (freshwater discharge in the coastal lagoon's drainage basin) and local (temperature and salinity) scales across the estuarine marine gradient. These results demonstrate that fish responses to global climate change can be complex and multifaceted. More specifically, our findings suggested that the interaction among global and local driving forces dampen the expected effect of tropicalization for this mullet species in a subtropical seascape.

Elemental and spectral chemometric analyses of Octopus vulgaris beaks as reliable markers of capture location.

The high demand and economic relevance of cephalopods make them prone to food fraud, including related to harvest location. Therefore, there is a growing need to develop tools to unequivocally confirm their capture location. Cephalopod beaks are nonedible, making this material ideal for traceability studies as it can also be removed without a loss of commodity economic value. Within this context, common octopus (Octopus vulgaris) specimens were captured in five fishing areas along the Portuguese coast. Untargeted multi-elemental total X-ray fluorescence analysis of the octopus beaks revealed a high abundance of Ca, Cl, K, Na, S, and P, concomitant with the keratin and calcium phosphate nature of the material. We tested a suite of discrimination models on both elemental and spectral data, where the elements contributing most to discriminate capture location were typically associated with diet (As), human-related pressures (Zn, Se, and Mn), or geological features (P, S, Mn, and Zn). Among the six different chemometrics approaches used to classify individuals to their capture location according to their beaks' element concentration, classification trees attained a classification accuracy of 76.7%, whilst reducing the number of explanatory variables for sample classification and highlighting variable importance for group discrimination. However, using X-ray spectral features of the octopus beaks further improved classification accuracy, with the highest classification of 87.3% found with partial least-squares discriminant analysis. Ultimately, element and spectral analyses of nonedible structures such as octopus beaks can provide an important, complementary, and easily accessible means to support seafood provenance and traceability, whilst integrating anthropogenic and/or geological gradients.

Growth portfolios buffer climate-linked environmental change in marine systems.

Large-scale, climate-induced synchrony in the productivity of fish populations is becoming more pronounced in the world's oceans. As synchrony increases, a population's "portfolio" of responses can be diminished, in turn reducing its resilience to strong perturbation. Here we argue that the costs and benefits of trait synchronization, such as the expression of growth rate, are context dependent. Contrary to prevailing views, synchrony among individuals could actually be beneficial for populations if growth synchrony increases during favorable conditions, and then declines under poor conditions when a broader portfolio of responses could be useful. Importantly, growth synchrony among individuals within populations has seldom been measured, despite well-documented evidence of synchrony across populations. Here, we used century-scale time series of annual otolith growth to test for changes in growth synchronization among individuals within multiple populations of a marine keystone species (Atlantic cod, Gadus morhua). On the basis of 74,662 annual growth increments recorded in 13,749 otoliths, we detected a rising conformity in long-term growth rates within five northeast Atlantic cod populations in response to both favorable growth conditions and a large-scale, multidecadal mode of climate variability similar to the East Atlantic Pattern. The within-population synchrony was distinct from the across-population synchrony commonly reported for large-scale environmental drivers. Climate-linked, among-individual growth synchrony was also identified in other Northeast Atlantic pelagic, deep-sea and bivalve species. We hypothesize that growth synchrony in good years and growth asynchrony in poorer years reflects adaptive trait optimization and bet hedging, respectively, that could confer an unexpected, but pervasive and stabilizing, impact on marine population productivity in response to large-scale environmental change.

Elemental Fingerprinting of Wild and Farmed Fish Muscle to Authenticate and Validate Production Method.

In the context of expanding fish production and complex distribution chains, traceability, provenance and food safety tools are becoming increasingly important. Here, we compare the elemental fingerprints of gilthead seabream (Sparus aurata) muscle from wild and different aquaculture productions (semi-intensive earth ponds and intensive sea cages from two locations) to confirm their origin and evaluate the concentrations of elements with regulatory thresholds (Cu, Hg, Pb and Zn). Using a chemometric approach based on multi-elemental signatures, the sample origin was determined with an overall accuracy of 90%. Furthermore, in a model built to replicate a real-case scenario where it would be necessary to trace the production method of S. aurata without reliable information about its harvesting location, 27 of the 30 samples were correctly allocated to their original production method (sea-cage aquaculture), despite being from another location. The concentrations of the regulated elements ranged as follows: Cu (0.140-1.139 mg/Kg), Hg (0-0.506 mg/Kg), Pb (0-2.703 mg/Kg) and Zn (6.502-18.807 mg/Kg), with only Pb presenting concentrations consistently above the recommended limit for human consumption. The present findings contribute to establishing elemental fingerprinting as a reliable tool to trace fish production methods and underpin seafood authentication.

Harnessing the Full Power of Chemometric-Based Analysis of Total Reflection X-ray Fluorescence Spectral Data to Boost the Identification of Seafood Provenance and Fishing Areas.

Provenance and traceability are crucial aspects of seafood safety, supporting managers and regulators, and allowing consumers to have clear information about the origin of the seafood products they consume. In the present study, we developed an innovative spectral approach based on total reflection X-ray fluorescence (TXRF) spectroscopy to identify the provenance of seafood and present a case study for five economically relevant marine species harvested in different areas of the Atlantic Portuguese coast: three bony fish-Merluccius merluccius, Scomber colias, and Sparus aurata; one elasmobranch-Raja clavata; one cephalopod-Octopus vulgaris. Applying a first-order Savitzky-Golay transformation to the TXRF spectra reduced the potential matrix physical effects on the light scattering of the X-ray beam while maintaining the spectral differences inherent to the chemical composition of the samples. Furthermore, a variable importance in projection partial least-squares discriminant analysis (VIP-PLS-DA), with k - 1 components (where k is the number of geographical origins of each seafood species), produced robust high-quality models of classification of samples according to their geographical origin, with several clusters well-evidenced in the dispersion plots of all species. Four of the five species displayed models with an overall classification above 80.0%, whereas the lowest classification accuracy for S. aurata was 74.2%. Notably, about 10% of the spectral features that significantly contribute to class differentiation are shared among all species. The results obtained suggest that TXRF spectra can be used for traceability purposes in seafood species (from bony and cartilaginous fishes to cephalopods) and that the presented chemometric approach has an added value for coupling with classic TXRF spectral peak deconvolution and elemental quantification, allowing characterization of the geographical origin of samples, providing a highly accurate and informative dataset in terms of food safety.

Elemental Chemometrics as Tools to Depict Stalked Barnacle (Pollicipes pollicipes) Harvest Locations and Food Safety.

The stalked barnacle Pollicipes pollicipes is an abundant species on the very exposed rocky shore habitats of the Spanish and Portuguese coasts, constituting also an important economical resource, as a seafood item with high commercial value. Twenty-four elements were measured by untargeted total reflection X-ray fluorescence spectroscopy (TXRF) in the edible peduncle of stalked barnacles sampled in six sites along the Portuguese western coast, comprising a total of 90 individuals. The elemental profile of 90 individuals originated from several geographical sites (N = 15 per site), were analysed using several chemometric multivariate approaches (variable in importance partial least square discriminant analysis (VIP-PLS-DA), stepwise linear discriminant analysis (S-LDA), linear discriminant analysis (LDA), random forests (RF) and canonical analysis of principal components (CAP)), to evaluate the ability of each approach to trace the geographical origin of the animals collected. As a suspension feeder, this species introduces a high degree of background noise, leading to a comparatively lower classification of the chemometric approaches based on the complete elemental profile of the peduncle (canonical analysis of principal components and linear discriminant analysis). The application of variable selection approaches such as the VIP-PLS-DA and S-LDA significantly increased the classification accuracy (77.8% and 84.4%, respectively) of the samples according to their harvesting area, while reducing the number of elements needed for this classification, and thus the background noise. Moreover, the selected elements are similar to those selected by other random and non-random approaches, reinforcing the reliability of this selection. This untargeted analytical procedure also allowed to depict the degree of risk, in terms of human consumption of these animals, highlighting the geographical areas where these delicacies presented lower values for critical elements compared to the standard thresholds for human consumption.

Extrinsic and intrinsic factors shape the ability of using otolith chemistry to characterize estuarine environmental histories.

Reconstructing habitat use and environmental histories of fish via otolith chemistry relies on linking otolith chemical composition to the surrounding environment, as well as disentangling the consequences of ontogenetic or physiological effects that may mask environmental signals. We used multiple linear and linear mixed models to analyse the importance of environmental (temperature, salinity, water chemistry) and individual based (fish size) factors on otolith chemical composition and incorporation (Li, Mg, Mn, Sr, and Ba) of juvenile Dicentrarchus labrax, over their time within an estuarine nursery area. Multi model inference highlighted the importance of ontogeny, as well as the influence of temperature and salinity on otolith chemistry and elemental incorporation, with results indicating that intrinsic effects may potentially outweigh environmental effects. Ultimately, understanding if otolith chemistry accurately reflects fine-scale environmental variation is key to reconstruct environmental histories of juvenile fishes in estuaries and will contribute to determining the impact changing estuarine conditions may have on growth and survival.

Reconciling differences in natural tags to infer demographic and genetic connectivity in marine fish populations.

Processes regulating population connectivity are complex, ranging from extrinsic environmental factors to intrinsic individual based features, and are a major force shaping the persistence of fish species and population responses to harvesting and environmental change. Here we developed an integrated assessment of demographic and genetic connectivity of European flounder Platichthys flesus in the northeast Atlantic (from the Norwegian to the Portuguese coast) and Baltic Sea. Specifically, we used a Bayesian infinite mixture model to infer the most likely number of natal sources of individuals based on otolith near core chemical composition. Simultaneously, we characterised genetic connectivity via microsatellite DNA markers, and evaluated how the combined use of natural tags informed individual movement and long-term population exchange rates. Individual markers provided different insights on movement, with otolith chemistry delineating Norwegian and Baltic Sea sources, whilst genetic markers showed a latitudinal pattern which distinguished southern peripheral populations along the Iberian coast. Overall, the integrated use of natural tags resulted in outcomes that were not readily anticipated by individual movement or gene flow markers alone. Our ecological and evolutionary approach provided a synergistic view on connectivity, which will be paramount to align biological and management units and safeguard species' biocomplexity.