Unsupervised estimation of the age at sea departure of Atlantic salmon using magnesium, manganese, and zinc otolith chemistry.

Investigating the age at sea departure of returning Atlantic salmon is critical to better understand the role of emigration timing in survival. Among the methods available, the use of otolith chemistry can be challenging in anadromous fish, as the elements frequently used (i.e., magnesium, manganese, and zinc) can jointly reflect individual metabolism and environmental conditions. Here, we present a new unsupervised and robust method for successfully estimating the outmigration age of Atlantic salmon in the Bay of Biscay, based on otolith zinc concentrations.

Heterogeneity of otolith chemical composition from two-dimensional mapping: Relationship with biomineralization mechanisms and implications for microchemistry analyses.

Although otoliths are widely used as archives to infer life-history traits and habitat use in fishes, their biomineralization process remains poorly understood. This lack of knowledge is problematic as it can lead to misinterpretation of the different types of signals (e.g., optical or chemical) that provide basic data for research in fish ecology, fisheries management, and species conservation. Otolith calcification relies on a complex system involving a pericrystalline fluid, the endolymph, whose organic and inorganic compositions are spatially heterogeneous for some constituents. This property stems from the particular structure of the calcifying saccular epithelium. In this study, we explored the spatial heterogeneity of elemental incorporation in otoliths for two species of high economic interest, European hake Merluccius merluccius (L. 1758) and European sea bass Dicentrarchus labrax (L. 1758). Two-dimensional mappings of chemical elements were obtained using UV high-repetition-rate femtosecond laser ablation (fs-LA) system coupled to a high-resolution inductively coupled plasma sector field mass spectrometer analyses on transverse sections of sagittae. Results highlighted a clear asymmetry between proximal (sulcus) and distal (antisulcus) concentrations for elements such as magnesium (Mg), phosphorus (P), manganese (Mn), and potassium (K) with concentration gradient directions that varied depending on the element. Strontium (Sr) and barium (Ba) did not show a proximo-distal gradient. These results are discussed in light of current knowledge on the endolymph composition and the mechanisms that lead to its compartmentalization, highlighting the need for further research on otolith biomineralization. Operational implications for studies based on otolith chemical composition are also discussed with emphasis on advice for sampling strategies to avoid analytical biases and the need for in-depth analyses of analytical settings before comparing otolith signatures between species or geographical areas.

Juvenile downstream migration patterns of an anadromous fish, allis shad (Alosa alosa), before and after the population collapse in the Gironde system, France.

Diadromous fish have exhibited a dramatic decline since the end of the 20th century. The allis shad (Alosa alosa) population in the Gironde-Garonne-Dordogne (GGD) system, once considered as a reference in Europe, remains low despite a fishing ban in 2008. One hypothesis to explain this decline is that the downstream migration and growth dynamics of young stages have changed due to environmental modifications in the rivers and estuary. We retrospectively analysed juvenile growth and migration patterns using otoliths from adults caught in the GGD system 30 years apart during their spawning migration, in 1987 and 2016. We coupled otolith daily growth increments and laser ablation inductively-coupled plasma mass spectrometry measurements of Sr:Ca, Ba:Ca, and Mn:Ca ratios along the longest growth axis from hatching to an age of 100 days (i.e., during the juvenile stage). A back-calculation allowed us to estimate the size of juveniles at the entrance into the brackish estuary. Based on the geochemistry data, we distinguished four different zones that juveniles encountered during their downstream migration: freshwater, fluvial estuary, brackish estuary, and lower estuary. We identified three migration patterns during the first 100 days of their life: (a) Individuals that reached the lower estuary zone, (b) individuals that reached the brackish estuary zone, and (c) individuals that reached the fluvial estuary zone. On average, juveniles from the 1987 subsample stayed slightly longer in freshwater than juveniles from the 2016 subsample. In addition, juveniles from the 2016 subsample entered the brackish estuary at a smaller size. This result suggests that juveniles from the 2016 subsample might have encountered more difficult conditions during their downstream migration, which we attribute to a longer exposure to the turbid maximum zone. This assumption is supported by the microchemical analyses of the otoliths, which suggests based on wider Mn:Ca peaks that juveniles in 2010s experienced a longer period of physiological stress during their downstream migration than juveniles in 1980s. Finally, juveniles from the 2016 subsample took longer than 100 days to exit the lower estuary than we would have expected from previous studies. Adding a new marker (i.e., Ba:Ca) helped us refine the interpretation of the downstream migration for each individual.

Effect of metabolic rate on time-lag changes in otolith microchemistry: an experimental approach using Salmo trutta.

Ecologists have long been interested in relevant techniques to track the field movement patterns of fish. The elemental composition of otoliths represents a permanent record of the growing habitats experienced by a fish throughout its lifetime and is increasingly used in the literature. The lack of a predictive and mechanistic understanding of the individual kinematics underlying ion incorporation/depletion limits our fine-scale temporal interpretation of the chemical signal recorded in the otolith. In particular, the rate at which elements are incorporated into otoliths is hypothesized to depend on fish physiology. However, to date, time lags have mostly been quantified on a population scale. Here, we report results from controlled experiments (translocation and artificially enriched environment) on individual trace element incorporation/depletion rates in Salmo trutta (Salmonidae). We reported significant lags (i.e. weeks to months) between changes in water chemistry and the subsequent change in otolith composition and highlighted substantial inter-individual variations in the timing and magnitude of Sr/Ca and Ba/Ca responses. These differences are partially linked to the energetic status (i.e. metabolic rate) of the individuals. It therefore appears that individuals with the highest metabolic rate are more likely to record detailed (i.e. brief) temporal changes than individuals having lower metabolic values. The time taken for environmental changes to be reflected in the growing otolith thus can no longer be assumed to remain a constant within populations. Results from the current study are a step towards the fine reconstruction of environmental histories in dynamic environments.

Quantifying larval dispersal portfolio in seabass nurseries using otolith chemical signatures.

The temporal asynchronies in larvae production from different spawning areas are fundamental components for ensuring stability and resilience of marine metapopulations. Such a concept, named portfolio effect, supposes that diversifying larval dispersal histories should minimize the risk of recruitment failure by increasing the probability that at least some larvae successfully settle in nursery. Here, we used a reconstructive approach based on otolith chemistry to quantify the larval dispersal portfolio of the European seabass, Dicentrarchus labrax, across six estuarine nursery areas of the northeast Atlantic Ocean. The analysis of natal and trajectory signatures indicated that larvae hatch in distinct environments and then dispersed in water masses featured by contrasting chemical signatures. While some trace elements appeared affected by temporal changes (Mn and Sr), others varied spatially during the larval stage but remained poorly affected by temporal fluctuation and fish physiology (Ba, Cu, Rb and Zn). We then proposed two diversity metrics based on richness and variations of chemical signatures among populations to reflect spatio-temporal diversity in natal origins and larval trajectories (i.e., estimates of dispersal portfolio). Along the French coast, the diversity estimates were maximum in nurseries located at proximity of offshore spawning sites and featured by complex offshore hydrodynamic contexts, such as the Mont St-Michel bay. Finally, our findings indicate that the dispersal portfolio was positively related with the local abundance of seabass juveniles, supporting the assumption that heterogeneity in dispersal history contributes to promote recruitment success in nurseries.

Metal localisation in gastropod shells: New insights from mass spectrometry techniques.

Gastropod shells are calcified structures made of several crystal layers. They grow throughout the lifecycle of mollusks by integrating some of the chemical elements present in their environment, including metals. This characteristic means mollusks can be useful bioindicators of metal exposure. The present study aimed to better understand the role of layer composition on metal accumulation. To that end, the gastropods Radix balthica were collected in a French river adjacent to a municipal wastewater treatment plant. Microchemical metal analyses in the different shell layers were performed by Femtosecond-Laser Ablation Inductively Coupled Plasma Mass Spectrometry (Fs-LA-ICP-MS) and analyses of the molecular environment of the metals were performed by Time-of-Flight Secondary Ion Mass Spectrometry (TOF-SIMS). Strontium, Ba and Mn were well distributed within the whole shell and the high concentrations of these elements were found to be related to the aragonite structure of the shell. Copper, Ni, Pb and Zn were mostly present at the outer surfaces of the shell where the organic constituents were more concentrated. The analysis of metal distribution in shell layers could improve our understanding of the relationships between metal exposure and accumulation in mollusks, therefore providing evidences of their use as powerful integrated bioindicator of metal contamination.

European flounder foraging movements in an estuarine nursery seascape inferred from otolith microchemistry and stable isotopes.

Despite the importance of estuarine nurseries in the regulation of many fish stocks, temporal and spatial movements and habitat use patterns of juvenile fish remain poorly understood. Overall, combining several movement metrics allowed us to characterize dispersal patterns of juvenile flounder, Platichthys flesus, along an estuarine seascape. Specifically, we investigated otolith microchemistry signatures (Sr:Ca and Ba:Ca ratios) and stable isotope ratios (δ13C and δ15N) in muscles of these juveniles, during three consecutive years to assess inter-annual fluctuations in their home range and isotopic niches. The morphological condition and lipid content of individuals were lower in years of high as compared to low dispersal along the estuarine gradient. We discuss these results in relation to the ecosystem productivity and intra- and inter-specific competition level, which in turn affects movements and foraging behaviors of juvenile flounders.

Specific pathways for the incorporation of dissolved barium and molybdenum into the bivalve shell: an isotopic tracer approach in the juvenile Great Scallop (Pecten maximus).

Dissolved barium and molybdenum incorporation in the calcite shell was investigated in the Great Scallop Pecten maximus. Sixty six individuals were exposed for 16 days to two successive dissolved Ba and Mo concentrations accurately differentiated by two different isotopic enrichments (97Mo, 95Mo; ¹³5Ba, ¹³7Ba). Soft tissue and shell isotopic composition were determined respectively by quantitative ICP-MS (Inductively Coupled Plasma Mass Spectrometer) and laser ablation--ICP-MS. Results from Ba enrichment indicate the direct incorporation of dissolved Ba into the shell in proportion to the levels in the water in which they grew with a 6-8 day delay. The low spike contributions and the low partition coefficient (D(Mo) = 0.0049 ± 0.0013), show that neither the soft tissue nor the shell were significantly sensitive to Mo enrichment. These results eliminate direct Mo shell enrichment by the dissolved phase, and favour a trophic uptake that will be investigated using the successive isotopic enrichment approach developed in this study.