Maternal Effects and Trophodynamics Drive Interannual Larval Growth Variability of Atlantic Bluefin Tuna (Thunnus thynnus) from the Gulf of Mexico.

Two cohorts of Atlantic bluefin tuna (Thunnus thynnus) larvae were sampled in 2017 and 2018 during the peak of spawning in the Gulf of Mexico (GOM). We examined environmental variables, daily growth, otolith biometry and stable isotopes and found that the GOM18 cohort grew at faster rates, with larger and wider otoliths. Inter and intra-population analyses (deficient vs. optimal growth groups) were carried out for pre- and post-flexion developmental stages to determine maternal and trophodynamic influences on larval growth variability based on larval isotopic signatures, trophic niche sizes and their overlaps. For the pre-flexion stages in both years, the optimal growth groups had significantly lower δ15N, implying a direct relationship between growth potential and maternal inheritance. Optimal growth groups and stages for both years showed lower C:N ratios, reflecting a greater energy investment in growth. The results of this study illustrate the interannual transgenerational trophic plasticity of a spawning stock and its linkages to growth potential of their offsprings in the GOM.

Evidence of isotopic maternal transmission influence on bluefin tuna (Thunnus thynnus) larval growth.

Pre-flexion stages of Atlantic bluefin tuna (Thunnus thynnus) larvae were collected in 2014 during the peak of spawning in the two main spawning areas: Gulf of Mexico (GOM) and Mediterranean Sea (MED). We examined daily growth, otolith biometry, and stable isotopes and found that the GOM grew at a faster rate, had larger otoliths, wider daily increments, and significantly lower values of δ15N when compared to the MED. In addition, an intra-population comparative analysis between slow- and fast-growing individuals (deficient vs. optimal growth groups, respectively) showed that optimal growth groups had significantly lower δ15N within each spawning area, implying a direct relationship between growth potential, development, and maternal transmission of isotopic signatures. A third pre-flexion larval group that was aquaculture-reared also exhibited the same pattern to the wild larval groups. In addition, for the first time, we estimated the maternal trophic niches using models developed with field-captured pre-flexion larvae. The estimated maternal trophic niches for the GOM were narrower than the MED, implying differences in the maternal trophodynamics from each nursery area. Overall, the inter-population (GOM vs. MED) and intra-population growth groups (deficient vs. optimal) grew faster and had narrower maternal niches. This study shows the advantages that larval SIA research can aid in the understanding of the trophodynamics of their breeders by examining the trophic relationship of a spawning stock jointly with the development of growth potential in offspring within the same breeding season.

Low levels of sibship encourage use of larvae in western Atlantic bluefin tuna abundance estimation by close-kin mark-recapture.

Globally, tunas are among the most valuable fish stocks, but are also inherently difficult to monitor and assess. Samples of larvae of Western Atlantic bluefin tuna Thunnus thynnus (Linnaeus, 1758) from standardized annual surveys in the northern Gulf of Mexico provide a potential source of "offspring" for close-kin mark-recapture (CKMR) estimates of abundance. However, the spatial patchiness and highly skewed numbers of larvae per tow suggest sampled larvae may come from a small number of parents, compromising the precision of CKMR. We used high throughput genomic profiling to study sibship within and among larval tows from the 2016 standardized Gulf-wide survey compared to targeted sampling carried out in 2017. Full- and half-siblings were found within both years, with 12% of 156 samples in 2016 and 56% of 317 samples in 2017 having at least one sibling. There were also two pairs of cross cohort half-siblings. Targeted sampling increased the number of larvae collected per sampling event but resulted in a higher proportion of siblings. The combined effective sample size across both years was about 75% of the nominal size, indicating that Gulf of Mexico larval collections could be a suitable source of juveniles for CKMR in Western Atlantic bluefin tuna.

Plankton food webs in the oligotrophic Gulf of Mexico spawning grounds of Atlantic bluefin tuna.

We used linear inverse ecosystem modeling techniques to assimilate data from extensive Lagrangian field experiments into a mass-balance constrained food web for the Gulf of Mexico open-ocean ecosystem. This region is highly oligotrophic, yet Atlantic bluefin tuna (ABT) travel long distances from feeding grounds in the North Atlantic to spawn there. Our results show extensive nutrient regeneration fueling primary productivity (mostly by cyanobacteria and other picophytoplankton) in the upper euphotic zone. The food web is dominated by the microbial loop (>70% of net primary productivity is respired by heterotrophic bacteria and protists that feed on them). By contrast, herbivorous food web pathways from phytoplankton to metazoan zooplankton process <10% of the net primary production in the mixed layer. Nevertheless, ABT larvae feed preferentially on podonid cladocerans and other suspension-feeding zooplankton, which in turn derive much of their nutrition from nano- and micro-phytoplankton (mixotrophic flagellates, and to a lesser extent, diatoms). This allows ABT larvae to maintain a comparatively low trophic level (~4.2 for preflexion and postflexion larvae), which increases trophic transfer from phytoplankton to larval fish.

Trade-offs between risks of predation and starvation in larvae make the shelf break an optimal spawning location for Atlantic bluefin tuna.

Atlantic bluefin tuna (ABT) (Thunnus thynnus) travel long distances to spawn in oligotrophic regions of the Gulf of Mexico (GoM) which suggests these regions offer some unique benefit to offspring survival. To better understand how larval survival varies within the GoM a spatially explicit, Lagrangian, individual-based model was developed that simulates dispersal and mortality of ABT early life stages within realistic predator and prey fields during the spawning periods from 1993 to 2012. The model estimates that starvation is the largest cumulative source of mortality associated with an early critical period. However, elevated predation on older larvae is identified as the main factor limiting survival to late postflexion. As a result, first-feeding larvae have higher survival on the shelf where food is abundant, whereas older larvae have higher survival in the open ocean with fewer predators, making the shelf break an optimal spawning area. The modeling framework developed in this study explicitly simulates both physical and biological factors that impact larval survival and hence could be used to support ecosystem based management efforts for ABT under current and future climate conditions.

Genetic connectivity between Atlantic bluefin tuna larvae spawned in the Gulf of Mexico and in the Mediterranean Sea.

The highly migratory Atlantic bluefin tuna (ABFT) is currently managed as two distinct stocks, in accordance with natal homing behavior and population structuring despite the absence of barriers to gene flow. Larval fish are valuable biological material for tuna molecular ecology. However, they have hardly been used to decipher the ABFT population structure, although providing the genetic signal from successful breeders. For the first time, cooperative field collection of tuna larvae during 2014 in the main spawning area for each stock, the Gulf of Mexico (GOM) and the Mediterranean Sea (MED), enabled us to assess the ABFT genetic structure in a precise temporal and spatial frame exclusively through larvae. Partitioning of genetic diversity at nuclear microsatellite loci and in the mitochondrial control region in larvae spawned contemporarily resulted in low significant fixation indices supporting connectivity between spawners in the main reproduction area for each population. No structuring was detected within the GOM after segregating nuclear diversity in larvae spawned in two hydrographically distinct regions, the eastern GOM (eGOM) and the western GOM (wGOM), with the larvae from eGOM being more similar to those collected in the MED than the larvae from wGOM. We performed clustering of genetically characterized ABFT larvae through Bayesian analysis and by Discriminant Analysis of Principal Components (DAPC) supporting the existence of favorable areas for mixing of ABFT spawners from Western and Eastern stocks, leading to gene flow and apparent connectivity between weakly structured populations. Our findings suggest that the eastern GOM is more prone for the mixing of breeders from the two ABFT populations. Conservation of this valuable resource exploited for centuries calls for intensification of tuna ichthyoplankton research and standardization of genetic tools for monitoring population dynamics.

Early life ecology of the invasive lionfish (Pterois spp.) in the western Atlantic.

The invasion of the western Atlantic by the Indo-Pacific lionfish (Pterois volitans/miles) is a serious threat to the ecological stability of the region. The early life history of the lionfish remains poorly understood despite the important role that larval supply plays reef fish population dynamics. In this study, we characterized patterns in the horizontal and vertical distributions of larval lionfish collected in the western Caribbean, US Caribbean, and the Gulf of Mexico from 19 ichthyoplankton surveys conducted from 2009-2016. Using generalized additive models (GAMs), we assessed the relative effects of spatiotemporal and environmental variation on the distribution of lionfish larvae. We also examined otoliths to determine larval ages and report the first larval growth rate estimates for this species. Lionfish larvae were present at 7.8% of all stations sampled and our model suggests that lionfish presence is related to sea surface temperature and the lunar cycle. Year and location also strongly affected the larval distribution, likely reflecting the ongoing expansion of the species during our sampling timeframe. Much of the variation in larval lionfish presence remained unexplained, and future studies should incorporate additional environmental factors to improve model predictions. This study improves our understanding of the lionfish life cycle and accentuates the need for further research into the early life history of this invasive species. The design and implementation of effective long-term lionfish control mechanisms will require an understanding of their entire life history.

Trophic ecology of Atlantic Bluefin Tuna (Thunnus thynnus) [corrected] larvae from the Gulf of Mexico and NW Mediterranean spawning grounds: A Comparative Stable Isotope Study.

The present study uses stable isotopes of nitrogen and carbon (δ15Nandδ13C) as trophic indicators for Atlantic bluefin tuna larvae (BFT) (6-10 mm standard length) in the highly contrasting environmental conditions of the Gulf of Mexico (GOM) and the Balearic Sea (MED). These regions are differentiated by their temperature regime and relative productivity, with the GOM being significantly warmer and more productive. MED BFT larvae showed the highest δ15N signatures, implying an elevated trophic position above the underlying microzooplankton baseline. Ontogenetic dietary shifts were observed in the BFT larvae from the GOM and MED which indicates early life trophodynamics differences between these spawning habitats. Significant trophic differences between the GOM and MED larvae were observed in relation to δ15N signatures in favour of the MED larvae, which may have important implications in their growth during their early life stages.These low δ15N levels in the zooplankton from the GOM may be an indication of a shifting isotopic baseline in pelagic food webs due to diatrophic inputs by cyanobacteria. Lack of enrichment for δ15N in BFT larvae compared to zooplankton implies an alternative grazing pathway from the traditional food chain of phytoplankton-zooplankton-larval fish. Results provide insight for a comparative characterization of the trophic pathways variability of the two main spawning grounds for BFT larvae.