Brief Oil Exposure Reduces Fitness in Wild Gulf of Mexico Mahi-Mahi (Coryphaena hippurus).

The Deepwater Horizon (DWH) disaster released 3.19 million barrels of crude oil into the Gulf of Mexico (GOM) in 2010, overlapping the habitat of pelagic fish populations. Using mahi-mahi (Coryphaena hippurus)─a highly migratory marine teleost present in the GOM during the spill─as a model species, laboratory experiments demonstrate injuries to physiology and behavior following oil exposure. However, more than a decade postspill, impacts on wild populations remain unknown. To address this gap, we exposed wild mahi-mahi to crude oil or control conditions onboard a research vessel, collected fin clip samples, and tagged them with electronic tags prior to release into the GOM. We demonstrate profound effects on survival and reproduction in the wild. In addition to significant changes in gene expression profiles and predation mortality, we documented altered acceleration and habitat use in the first 8 days oil-exposed individuals were at liberty as well as a cessation of apparent spawning activity for at least 37 days. These data reveal that even a brief and low-dose exposure to crude oil impairs fitness in wild mahi-mahi. These findings offer new perspectives on the lasting impacts of the DWH blowout and provide insight about the impacts of future deep-sea oil spills.

Towards integrated modeling of the long-term impacts of oil spills.

Although great progress has been made to advance the scientific understanding of oil spills, tools for integrated assessment modeling of the long-term impacts on ecosystems, socioeconomics and human health are lacking. The objective of this study was to develop a conceptual framework that could be used to answer stakeholder questions about oil spill impacts and to identify knowledge gaps and future integration priorities. The framework was initially separated into four knowledge domains (ocean environment, biological ecosystems, socioeconomics, and human health) whose interactions were explored by gathering stakeholder questions through public engagement, assimilating expert input about existing models, and consolidating information through a system dynamics approach. This synthesis resulted in a causal loop diagram from which the interconnectivity of the system could be visualized. Results of this analysis indicate that the system naturally separates into two tiers, ocean environment and biological ecosystems versus socioeconomics and human health. As a result, ocean environment and ecosystem models could be used to provide input to explore human health and socioeconomic variables in hypothetical scenarios. At decadal-plus time scales, the analysis emphasized that human domains influence the natural domains through changes in oil-spill related laws and regulations. Although data gaps were identified in all four model domains, the socioeconomics and human health domains are the least established. Considerable future work is needed to address research gaps and to create fully coupled quantitative integrative assessment models that can be used in strategic decision-making that will optimize recoveries from future large oil spills.

Effects of Exposure to Low Concentrations of Oil on the Expression of Cytochrome P4501a and Routine Swimming Speed of Atlantic Haddock (Melanogrammus aeglefinus) Larvae In Situ.

Exposure to environmentally relevant concentrations of oil could impact survival of fish larvae in situ through subtle effects on larval behavior. During the larval period, Atlantic haddock (Melanogrammus aeglefinus) are transported toward nursery grounds by ocean currents and active swimming, which can modify their drift route. Haddock larvae are sensitive to dispersed oil; however, whether exposure to oil during development impacts the ability of haddock larvae to swim in situ is unknown. Here, we exposed Atlantic haddock embryos to 10 and 80 µg oil/L (0.1 and 0.8 µg ∑PAH/L) of crude oil for 8 days and used a novel approach to measure its effect on the larval swimming behavior in situ. We assessed the swimming behavior of 138 haddock larvae in situ, in the North Sea, using a transparent drifting chamber. Expression of cytochrome P4501a (cyp1a) was also measured. Exposure to 10 and 80 µg oil/L significantly reduced the average in situ routine swimming speed by 30-40% compared to the controls. Expression of cyp1a was significantly higher in both exposed groups. This study reports key information for improving oil spill risk assessment models and presents a novel approach to study sublethal effects of pollutants on fish larvae in situ.

Hydrodynamic and biological constraints on group cohesion in plankton.

The dynamics of plankton in the ocean are determined by biophysical interactions. Although physics and biotic behaviors are known to influence the observed patchiness of planktonic populations, it is still unclear how much, and if, group behavior contributes to this biophysical interaction. Here, we demonstrate how simple rules of behavior can enhance or inhibit active group cohesion in plankton in a turbulent environment. In this study, we used coral-reef fish larvae as a model to investigate the interaction between microscale turbulence and planktonic organisms. We synthesized available information on the swimming speeds and sizes of reef fish larvae, and developed a set of equations to investigate the effects of viscosity and turbulence on larvae dispersion. We then calculated the critical dispersion rates for three different swimming strategies - cruise, random-walk, and pause-travel - to determine which strategies could facilitate group cohesion during dispersal. Our results indicate that swimming strategies and migration to low-turbulence regions are the key to maintaining group cohesion, suggesting that many reef fish species have the potential to remain together, from hatching to settlement. In addition, larvae might change their swimming strategies to maintain group cohesion, depending on environmental conditions and/or their ontogenic stage. This study provides a better understanding of the hydrodynamic and biological constraints on group formation and cohesion in planktonic organisms, and reveals a wide range of conditions under which group formation may occur.

Auto-correlated directional swimming can enhance settlement success and connectivity in fish larvae.

Larvae of coastal-marine fishes have been shown repeatedly to swim directionally in the pelagic environment. Yet, biophysical models of larval dispersal typically impose a Simple Random Walk (SRW) algorithm to simulate non-directional movement in the open ocean. Here we investigate the use of a Correlated Random Walk (CRW) algorithm; imposing auto-correlated directional swimming onto simulated larvae within a high-resolution 3D biophysical model of the Gulf of Aqaba, the Red Sea. Our findings demonstrate that implementation of auto-correlated directional swimming can result in an increase of up to ×2.7 in the estimated success rate of larval-settlement, as well as an increase in the extent of connectivity. With accumulating empirical support for the capacity for directional-swimming during the pelagic phase, we propose that CRW should be applied in biophysical models of dispersal by coastal marine fish-larvae.

Uniting paradigms of connectivity in marine ecology.

The connectivity of marine organisms among habitat patches has been dominated by two independent paradigms with distinct conservation strategies. One paradigm is the dispersal of larvae on ocean currents, which suggests networks of marine reserves. The other is the demersal migration of animals from nursery to adult habitats, requiring the conservation of connected ecosystem corridors. Here, we suggest that a common driver, wave exposure, links larval and demersal connectivity across the seascape. To study the effect of linked connectivities on fish abundance at reefs, we parameterize a demographic model for The Bahamas seascape using maps of habitats, empirically forced models of wave exposure and spatially realistic three-dimensional hydrological models of larval dispersal. The integrated empirical-modeling approach enabled us to study linked connectivity on a scale not currently possible by purely empirical studies. We find sheltered environments not only provide greater nursery habitat for juvenile fish but larvae spawned on adjacent reefs have higher retention, thereby creating a synergistic increase in fish abundance. Uniting connectivity paradigms to consider all life stages simultaneously can help explain the evolution of nursery habitat use and simplifies conservation advice: Reserves in sheltered environments have desirable characteristics for biodiversity conservation and can support local fisheries through adult spillover.

How much do marine connectivity fluctuations matter?

There is growing awareness that fluctuations in larval flux (connectivity) depress the long-run growth of marine metapopulations, but by how much is unclear. Here, we explore how reproductive schedule and larval behavior affect how much connectivity fluctuations depress growth. We combine larval dispersal simulations from the Florida Keys with theoretical results to calculate the effect of fluctuations on bicolor damselfish (Stegastes partitus). We find that fluctuations depress growth only slightly (∼2%), but the effect would be much stronger for an organism that spawned only part of the year. Larval behavior can also matter, as vertical migration allows larvae to become entrained in eddies. Eddies synchronize connectivity fluctuations, further decreasing growth. However, here, they also divide the Keys into largely independently fluctuating regions, mitigating the effects of local synchrony. Therefore, in situations where connectivity fluctuations matter, the presence of independently fluctuating regions due to larval behavior may be important.

First evidence of fish larvae producing sounds.

The acoustic ecology of marine fishes has traditionally focused on adults, while overlooking the early life-history stages. Here, we document the first acoustic recordings of pre-settlement stage grey snapper larvae (Lutjanus griseus). Through a combination of in situ and unprovoked laboratory recordings, we found that L. griseus larvae are acoustically active during the night, producing 'knock' and 'growl' sounds that are spectrally and temporally similar to those of adults. While the exact function and physiological mechanisms of sound production in fish larvae are unknown, we suggest that these sounds may enable snapper larvae to maintain group cohesion at night when visual cues are reduced.

Does fish larval dispersal differ between high and low latitudes?

Several factors lead to expectations that the scale of larval dispersal and population connectivity of marine animals differs with latitude. We examine this expectation for demersal shorefishes, including relevant mechanisms, assumptions and evidence. We explore latitudinal differences in (i) biological (e.g. species composition, spawning mode, pelagic larval duration, PLD), (ii) physical (e.g. water movement, habitat fragmentation), and (iii) biophysical factors (primarily temperature, which could strongly affect development, swimming ability or feeding). Latitudinal differences exist in taxonomic composition, habitat fragmentation, temperature and larval swimming, and each difference could influence larval dispersal. Nevertheless, clear evidence for latitudinal differences in larval dispersal at the level of broad faunas is lacking. For example, PLD is strongly influenced by taxon, habitat and geographical region, but no independent latitudinal trend is present in published PLD values. Any trends in larval dispersal may be obscured by a lack of appropriate information, or use of 'off the shelf' information that is biased with regard to the species assemblages in areas of concern. Biases may also be introduced from latitudinal differences in taxa or spawning modes as well as limited latitudinal sampling. We suggest research to make progress on the question of latitudinal trends in larval dispersal.

Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow.

Understanding patterns of connectivity among populations of marine organisms is essential for the development of realistic, spatially explicit models of population dynamics. Two approaches, empirical genetic patterns and oceanographic dispersal modelling, have been used to estimate levels of evolutionary connectivity among marine populations but rarely have their potentially complementary insights been combined. Here, a spatially realistic Lagrangian model of larval dispersal and a theoretical genetic model are integrated with the most extensive study of gene flow in a Caribbean marine organism. The 871 genets collected from 26 sites spread over the wider Caribbean subsampled 45.8% of the 1900 potential unique genets in the model. At a coarse scale, significant consensus between modelled estimates of genetic structure and empirical genetic data for populations of the reef-building coral Montastraea annularis is observed. However, modelled and empirical data differ in their estimates of connectivity among northern Mesoamerican reefs indicating that processes other than dispersal may dominate here. Further, the geographic location and porosity of the previously described east-west barrier to gene flow in the Caribbean is refined. A multi-prong approach, integrating genetic data and spatially realistic models of larval dispersal and genetic projection, provides complementary insights into the processes underpinning population connectivity in marine invertebrates on evolutionary timescales.

Orientation behavior in fish larvae: a missing piece to Hjort's critical period hypothesis.

Larval reef fish possess considerable swimming and sensory abilities, which could enable navigation towards settlement habitat from the open ocean. Due to their small size and relatively low survival, tagging individual larvae is not a viable option, but numerical modeling studies have proven useful for understanding the role of orientation throughout ontogeny. Here we combined the theoretical framework of the biased correlated random walk model with a very high resolution three-dimensional coupled biophysical model to investigate the role of orientation behavior in fish larvae. Virtual larvae of the bicolor damselfish (Stegastes partitus) were released daily during their peak spawning period from two locations in the Florida Keys Reef Tract, a region of complex eddy fields bounded by the strong Florida Current. The larvae began orientation behavior either before or during flexion, and only larvae that were within a given maximum detection distance from the reef were allowed to orient. They were subjected to ontogenetic vertical migration, increased their swimming speed during ontogeny, and settled on reefs within a flexible window of 24 to 32 days of pelagic duration. Early orientation, as well as a large maximum detection distance, increased settlement, implying that the early use of large-scale cues increases survival. Orientation behavior also increased the number of larvae that settled near their home reef, providing evidence that orientation is a mechanism driving self-recruitment. This study demonstrates that despite the low swimming abilities of the earliest larval stages, orientation during this "critical period" would have remarkable demographic consequences.

Evolution of the Macondo well blowout: simulating the effects of the circulation and synthetic dispersants on the subsea oil transport.

During the Deepwater Horizon incident, crude oil flowed into the Gulf of Mexico from 1522 m underwater. In an effort to prevent the oil from rising to the surface, synthetic dispersants were applied at the wellhead. However, uncertainties in the formation of oil droplets and difficulties in measuring their size in the water column, complicated further assessment of the potential effect of the dispersant on the subsea-to-surface oil partition. We adapted a coupled hydrodynamic and stochastic buoyant particle-tracking model to the transport and fate of hydrocarbon fractions and simulated the far-field transport of the oil from the intrusion depth. The evaluated model represented a baseline for numerical experiments where we varied the distributions of particle sizes and thus oil mass. The experiments allowed to quantify the relative effects of chemical dispersion, vertical currents, and inertial buoyancy motion on oil rise velocities. We present a plausible model scenario, where some oil is trapped at depth through shear emulsification due to the particular conditions of the Macondo blowout. Assuming effective mixing of the synthetic dispersants at the wellhead, the model indicates that the submerged oil mass is shifted deeper, decreasing only marginally the amount of oil surfacing. In this scenario, the oil rises slowly to the surface or stays immersed. This suggests that other mechanisms may have contributed to the rapid surfacing of oil-gas mixture observed initially. The study also reveals local topographic and hydrodynamic processes that influence the oil transport in eddies and multiple layers. This numerical approach provides novel insights on oil transport mechanisms from deep blowouts and on gauging the subsea use of synthetic dispersant in mitigating coastal damage.

Surface evolution of the deepwater horizon oil spill patch: combined effects of circulation and wind-induced drift.

Following the Deepwater Horizon blowout, major concerns were raised about the probability that the Loop Current would entrain oil at the surface of the Gulf of Mexico toward South Florida. However, such a scenario did not materialize. Results from a modeling approach suggest that the prevailing winds, through the drift they induced at the ocean surface, played a major role in pushing the oil toward the coasts along the northern Gulf, and, in synergy with the Loop Current evolution, prevented the oil from reaching the Florida Straits. This implies that both oceanic currents and surface wind-induced drift must be taken into account for the successful forecasting of the trajectories and landfall of oil particles, even in energetic environments such as the Gulf of Mexico. Consequently, the time range of these predictions is limited to the weather forecasting range, in addition to the range set up by ocean forecasting capabilities.

PAH depletion in weathered oil slicks estimated from modeled age-at-sea during the Deepwater Horizon oil spill.

During time-periods oil slicks are in the marine environment (age-at-sea), weathering causes significant changes in composition and mass loss (depletion) of oil spill chemicals including the more toxic polycyclic aromatic hydrocarbons (PAHs). The goal of this study was to estimate the age-at-sea of weathered oil slicks using the oil spill module of the Connectivity Modeling System and to use this age to interpret PAH concentration measurements. Percent depletion (PD) for each measurement was computed as the percentage difference between the original and measured PAH concentration in the crude oil and weathered oil slicks, normalized upon the mass losses relative to hopane. Mean PD increased with estimated age-at-sea for all PAHs. Less PD was observed for alkylated than for parent PAHs, likely due to decreasing vapor pressure with increasing degree of alkylation. We conclude that estimated age-at-sea can be used to explain PAH depletion in weathered oil slicks. We propose PAH vapor pressure can be coupled with the model to expand capacity for predicting concentration distributions of individual parent and alkylated PAHs in weathered oil along the coastline. This new module will advance the science supporting oil spill response by providing more certain estimates of health risks from oil spills.

Evidence for a consistent use of external cues by marine fish larvae for orientation.

The larval stage is the main dispersive process of most marine teleost species. The degree to which larval behavior controls dispersal has been a subject of debate. Here, we apply a cross-species meta-analysis, focusing on the fundamental question of whether larval fish use external cues for directional movement (i.e., directed movement). Under the assumption that directed movement results in straighter paths (i.e., higher mean vector lengths) compared to undirected, we compare observed patterns to those expected under undirected pattern of Correlated Random Walk (CRW). We find that the bulk of larvae exhibit higher mean vector lengths than those expected under CRW, suggesting the use of external cues for directional movement. We discuss special cases which diverge from our assumptions. Our results highlight the potential contribution of orientation to larval dispersal outcomes. This finding can improve the accuracy of larval dispersal models, and promote a sustainable management of marine resources.

Reserve design for uncertain responses of coral reefs to climate change.

Rising sea temperatures cause mass coral bleaching and threaten reefs worldwide. We show how maps of variations in thermal stress can be used to help manage reefs for climate change. We map proxies of chronic and acute thermal stress and develop evidence-based hypotheses for the future response of corals to each stress regime. We then incorporate spatially realistic predictions of larval connectivity among reefs of the Bahamas and apply novel reserve design algorithms to create reserve networks for a changing climate. We show that scales of larval dispersal are large enough to connect reefs from desirable thermal stress regimes into a reserve network. Critically, we find that reserve designs differ according to the anticipated scope for phenotypic and genetic adaptation in corals, which remains uncertain. Attempts to provide a complete reserve design that hedged against different evolutionary outcomes achieved limited success, which emphasises the importance of considering the scope for adaptation explicitly. Nonetheless, 15% of reserve locations were selected under all evolutionary scenarios, making them a high priority for early designation. Our approach allows new insights into coral holobiont adaptation to be integrated directly into an adaptive approach to management.

The choice of droplet size probability distribution function for oil spill modeling is not trivial.

The droplet size distribution (DSD) formed by gas-saturated oil jets is one of the most important characteristics of the flow to understand and model the fate of uncontrolled deep-sea oil spills. The shape of the DSD, generally modeled as a theoretical lognormal, Rosin-Rammler or non-fundamental distribution function, defines the size and the mass volume range of the droplets. Yet, the fundamental DSD shape has received much less attention than the volume median size (d50) and range of the DSD during ten years of research following the Deepwater Horizon (DWH) blowout. To better understand the importance of the distribution function of the droplet size we compare the oil rising time, surface oil mass, and sedimented and beached masses for different DSDs derived from the DWH literature in idealized and applied conditions, while keeping d50 constant. We highlight substantial differences, showing that the probability distribution function of the DSD for far-field modeling is, regardless of the d50, consequential for oil spill response.

An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish.

The dispersal of marine larvae determines the level of connectivity among populations, influences population dynamics, and affects evolutionary processes. Patterns of dispersal are influenced by both ocean currents and larval behavior, yet the role of behavior remains poorly understood. Here we report the first integrated study of the ontogeny of multiple sensory systems and orientation behavior throughout the larval phase of a coral reef fish-the neon goby, Elacatinus lori. We document the developmental morphology of all major sensory organs (lateral line, visual, auditory, olfactory, gustatory) together with the development of larval swimming and orientation behaviors observed in a circular arena set adrift at sea. We show that all sensory organs are present at hatch and increase in size (or number) and complexity throughout the larval phase. Further, we demonstrate that most larvae can orient as early as 2 days post-hatch, and they swim faster and straighter as they develop. We conclude that sensory organs and swimming abilities are sufficiently developed to allow E. lori larvae to orient soon after hatch, suggesting that early orientation behavior may be common among coral reef fishes. Finally, we provide a framework for testing alternative hypotheses for the orientation strategies used by fish larvae, laying a foundation for a deeper understanding of the role of behavior in shaping dispersal patterns in the sea.

Invisible oil beyond the Deepwater Horizon satellite footprint.

Major oil spills are catastrophic events that immensely affect the environment and society, yet determining their spatial extent is a highly complex task. During the Deepwater Horizon (DWH) blowout, ~149,000 km2 of the Gulf of Mexico (GoM) was covered by oil slicks and vast areas of the Gulf were closed for fishing. Yet, the satellite footprint does not necessarily capture the entire oil spill extent. Here, we use in situ observations and oil spill transport modeling to examine the full extent of the DWH spill, focusing on toxic-to-biota (i.e., marine organisms) oil concentration ranges. We demonstrate that large areas of the GoM were exposed to invisible and toxic oil that extended beyond the boundaries of the satellite footprint and the fishery closures. With a global increase in petroleum production-related activities, a careful assessment of oil spills' full extent is necessary to maximize environmental and public safety.