Hypoxia-acclimation adjusts skeletal muscle anaerobic metabolism and burst swim performance in a marine fish.

Red drum, Sciaenops ocellatus, are a marine teleost native to the Gulf of Mexico that routinely experiences periods of low oxygen (hypoxia). Recent work has demonstrated this species has the capacity to improve aerobic performance in hypoxia through respiratory acclimation. However, it remains unknown how hypoxia acclimation impacts anaerobic metabolism in red drum, and the consequences of exhaustive exercise and recovery. Juvenile fish were acclimated to normoxia (n = 15, DO 90.4 ± 6.42 %) or hypoxia (n = 15, DO 33.6 ± 7.2 %) for 8 days then sampled at three time points: at rest, after exercise, and after a 3 h recovery period. The resting time point was used to characterize the acclimated phenotype, while the remaining time points demonstrate how this phenotype responds to exhaustive exercise. Whole blood, red muscle, white muscle, and heart tissues were sampled for metabolites and enzyme activity. The resting phenotype was characterized by lower pHe and changes to skeletal muscle ATP. Exhaustive exercise increased muscle lactate, and decreased phosphocreatine and ATP with no effect of acclimation. Interestingly, hypoxia-acclimated fish had higher pHe and pHi than control in all exercise time points. Red muscle ATP was lower in hypoxia-acclimated fish versus control at each sample period. Moreover, acclimated fish increased lactate dehydrogenase activity in the red muscle. Hypoxia acclimation increased white muscle ATP and hexokinase activity, a glycolytic enzyme. In a gait-transition swim test, hypoxia-acclimated fish recruited anaerobic-powered burst swimming at lower speeds in normoxia compared to control fish. These data suggest that acclimation increases reliance on anaerobic metabolism, and does not benefit recovery from exhaustive exercise.

Early life-stage Deepwater Horizon crude oil exposure induces latent osmoregulatory defects in larval red drum (Sciaenops ocellatus).

Crude oil is known to induce developmental defects in teleost fish exposed during early-life stages (ELSs). A recent study has demonstrated that zebrafish (Danio rerio) larvae acutely exposed to Deepwater Horizon (DHW) crude oil showed transcriptional changes in key genes involved in early kidney (pronephros) development and function, which were coupled with pronephric morphological defects. Given the osmoregulatory importance of the kidney, it is unknown whether ELS effects arising from short-term crude exposures result in long-term osmoregulatory defects, particularly within estuarine fishes likely exposed to DWH oil following the spill. To address this knowledge gap, an acute 72 h exposure to red drum (Sciaenops ocellatus) larvae was performed using high-energy water-accommodated fractions (HEWAFs) of DWH weathered oil to analyze transcriptional changes in genes involved in pronephros development and function by quantitative PCR. To test the latent effects of oil exposure on osmoregulation ability, red drum larvae were first exposed to HEWAF for 24 h. Larvae were then reared in clean seawater for two weeks and a 96 h acute osmotic challenge test was performed by exposing the fish to waters with varying salinities. Latent effects of ELS crude oil exposure on osmoregulation were assessed by quantifying survival during the acute osmotic challenge test and analyzing transcriptional changes at 14 dpf. Results demonstrated that ELS crude oil exposure reduced survival of red drum larvae when challenged in hypoosmotic waters and that latent transcriptional changes in some target pronephric genes were evident, indicating that an affected kidney likely contributed to the increased mortality.

Exposure to Deepwater Horizon crude oil increases free cholesterol in larval red drum (Sciaenops ocellatus).

The 2010 Deepwater Horizon oil spill impacted over 2100 km of shoreline along the northern Gulf of Mexico, which coincided with the spawning season of many coastal species, including red drum (Sciaenops ocellatus). Red drum develop rapidly and are sensitive to crude oil exposure during the embryonic and larval periods. This study investigates the predictions from recent transcriptomic studies that cholesterol biosynthetic processes are impacted by oil exposure in fish early life stages. We found that red drum larvae exposed for 72 h to ΣPAH50 3.55-15.45 µg L-1 exhibited significantly increased pericardial area, a cardiotoxicity metric, but the expression of several genes targeted in the cholesterol synthesis pathway was not affected. However, whole-mount staining revealed significant increases in free cholesterol throughout the larval body (ΣPAH50 4.71-16.15 µg L-1), and total cholesterol followed an increasing trend (ΣPAH50 3.55-15.45 µg L-1). Cholesterol plays a critical role in fish embryo development and ion channel function. Therefore, the disruption of cholesterol homeostasis, as observed here, could play a role in the oil toxicity phenotype observed across many fish species.

A review of the toxicology of oil in vertebrates: what we have learned following the Deepwater Horizon oil spill.

In the wake of the Deepwater Horizon (DWH) oil spill, a number of government agencies, academic institutions, consultants, and nonprofit organizations conducted lab- and field-based research to understand the toxic effects of the oil. Lab testing was performed with a variety of fish, birds, turtles, and vertebrate cell lines (as well as invertebrates); field biologists conducted observations on fish, birds, turtles, and marine mammals; and epidemiologists carried out observational studies in humans. Eight years after the spill, scientists and resource managers held a workshop to summarize the similarities and differences in the effects of DWH oil on vertebrate taxa and to identify remaining gaps in our understanding of oil toxicity in wildlife and humans, building upon the cross-taxonomic synthesis initiated during the Natural Resource Damage Assessment. Across the studies, consistency was found in the types of toxic response observed in the different organisms. Impairment of stress responses and adrenal gland function, cardiotoxicity, immune system dysfunction, disruption of blood cells and their function, effects on locomotion, and oxidative damage were observed across taxa. This consistency suggests conservation in the mechanisms of action and disease pathogenesis. From a toxicological perspective, a logical progression of impacts was noted: from molecular and cellular effects that manifest as organ dysfunction, to systemic effects that compromise fitness, growth, reproductive potential, and survival. From a clinical perspective, adverse health effects from DWH oil spill exposure formed a suite of signs/symptomatic responses that at the highest doses/concentrations resulted in multi-organ system failure.

Behavioral Changes in a Coastal Marine Fish Lead to Increased Predation Risk Following Oil Exposure.

Fishes exposed to crude oil have shown reduced sociability and poor habitat selection, which corresponded with increased predation risk. However, the contribution of oil-induced cardiorespiratory impairments to these findings is uncertain. This study explores the effect of oil exposure on predation risk in a model fish species, Sciaenops ocellatus, across a suite of physiological and behavioral end points to elucidate the mechanisms through which any observed effects are manifested. Using mesocosms to assess group predator avoidance, oil exposure to 36.3 µg l-1 ΣPAH reduced the time to 50% mortality from a mean time of 80.0 (74.1-86.0 95% confidence interval [CI]) min to 39.2 (35.6-42.8 95% CI) min. The influence of oil impaired cardiorespiratory and behavioral pathways on predation risk was assessed based on respiratory performance, swim performance, sociability, and routine activity. Swim trials demonstrated that cardiorespiratory and swim performance were unaffected by exposures to 26.6 or 100.8 µg l-1 ΣPAH. Interestingly, behavioral tests revealed that exposure to 26.6 µg l-1 ΣPAH increased distance moved, speed, acceleration, and burst activity. These data indicate that behavioral impairment is more sensitive than cardiorespiratory injury and may be a more important driver of downstream ecological risk following oil exposure in marine species.

Osmoregulatory plasticity during hypersaline acclimation in red drum, Sciaenops ocellatus.

Prolonged drought and freshwater diversion are making periods of hypersalinity more common in coastal ecosystems. This is especially true in the Laguna Madre system along the Texas coast where salinities can exceed 60 g/kg. As such, the ability to tolerate hypersalinity is critical to the success of endemic species, such as the commercially important red drum (Sciaenops ocellatus). This study evaluated acclimation of red drum to hypersalinity (60 g/kg) using a direct transfer protocol. Hypersalinity exposure resulted in significant impacts on plasma osmolality and muscle water in the first 24 h, but returned to control values coincident with a significant increase in intestinal water volume. Hypersalinity acclimation resulted in significant branchial and intestinal plasticity. The gill showed significant elevated nka α1a, nkcc1 and vha (B subunit) mRNA abundance, as well as NKA enzyme activity. The posterior intestine showed a stronger plasticity signal than the anterior intestine, which included a 12-fold increase in nkcc2 mRNA abundance and significant increases in NKA and VHA enzyme activity. These changes were corroborated by a significant threefold increase in bumetanide-sensitive absorptive short circuit current. These data suggest that the dynamic regulation of NKCC2-mediated intestinal water absorption is an important compliment to HCO3--mediated water absorption during hypersalinity exposure and acclimation.

The effects of temperature on oil-induced respiratory impairment in red drum (Sciaenops ocellatus).

The 2010 Deepwater Horizon (DWH) crude oil spill, among the largest environmental disasters in U.S. history, affected numerous economically important fishes. Exposure to crude oil can lead to reduced cardiac function, limiting oxygen transport, ATP production, and aerobic performance. However, crude oil exposure is not the only stressor that affects aerobic performance, and increasing environmental temperatures are known to significantly increase metabolic demands in fishes. As the DWH spill was active during warm summer months in the Gulf of Mexico, it is important to understand the combined effects of oil and temperature on a suite of metabolic parameters. Therefore, we investigated the effects of 24h crude oil exposure on the aerobic metabolism and hypoxia tolerance of red drum (Sciaenops ocellatus) following 3 week chronic exposure to four ecologically relevant temperatures (18 °C, 22 °C, 25 °C, 28 °C). Our results show that individuals acclimated to higher temperatures had significantly higher standard metabolic rate than individuals at lower temperatures, which resulted in significantly decreased critical oxygen threshold and reduced recovery from exercise. As predicted, crude oil exposure resulted in lower maximum metabolic rates (MMR) across the temperature range, and a significantly reduced ability to recover from exercise. The lowest temperature acclimation showed the smallest effect of oil on MMR, while the highest temperature showed the smallest effect on exercise recovery. Reduced respiratory performance and hypoxia tolerance are likely to have meaningful impacts on the fitness of red drum, especially with climate-induced temperature increases and continued oil exploration in the Gulf of Mexico.

The effects of acute crude oil exposure on growth and competition in red drum, Sciaenops ocellatus.

Crude oil is a well-known toxicant that reduces cardiorespiratory performance in acutely exposed fishes. While toxic effects can manifest in death in severe cases, the ecological consequences of sub-lethal exposure remain uncertain. This study investigated the impact of crude oil exposure on long-term social competition, growth, and metabolic performance in a coastal species, the red drum (Sciaenops ocellatus). Fish were acutely exposed to either control or one of two environmentally relevant oil concentrations and reared together in groups of 15 (5 from each exposure concentration) for eight weeks under resource-rich or resource-limited scenarios. Relative to controls, a 41.3% and 45.9% reduction in the specific growth rate was-observed following exposure to 25.3 and 53.4 µg l-1 ΣPAH respectively under resource-limited conditions. These fish were subsequently sampled for metabolic performance and common indicators of social subordination including reduced glucocorticoid receptors in the gill and caudal fin damage. The reduction in specific growth rate coincided with a 15.1% and 17.3% reduction in standard metabolic rate; however, maximum metabolic rate and aerobic scope were unaffected. Additionally, measures of social subordination showed no differences between oil-exposed and control fish. These results reinforce the hypothesis that acute oil exposure can have prolonged sub-lethal effects that compromise the ability of exposed individuals to perform effectively in their environment, including gathering and/or metabolizing food. Furthermore, this work highlights the premise that oil spills can be more detrimental in already at-risk ecosystems.

The additive effects of oil exposure and hypoxia on aerobic performance in red drum (Sciaenops ocellatus).

Aerobic scope, the difference between standard metabolic requirements and maximum metabolic capacity, is considered a particularly important metric influencing ecological success in fishes. Crude oil exposure can impair cardiorespiratory function in fishes, which reduces maximum metabolic rate, aerobic scope, and may impair ecological performance. Oil exposure is not the only environmental stressor that can affect aerobic scope, especially in areas affected by crude oil spills. Hypoxia (low dissolved oxygen) is also known to constrain maximum metabolic rate, yet there has been little effort to explore how hypoxia may influence the magnitude of metabolic injury following oil exposure. Therefore, our goal was to investigate the effects of acute oil exposure and hypoxia on the metabolic performance of red drum (Sciaenops ocellatus), an economically important fish common in the Gulf of Mexico. Here, sub-adult red drum were exposed to crude oil for 24 h before being exposed to hypoxic conditions following exhaustive exercise. Our results show that hypoxia exposure combined with crude oil exposure results in significantly reduced aerobic scope, which was additive compared to the reductions caused by each stressor alone. We also quantified hypoxia tolerance among treatments following exposure, and our results showed no changes to hypoxia tolerance among individuals, regardless of exposure to hypoxia or oil. These data offer insight into the metabolic constraints facing fishes exposed to oil while concurrently subjected to hypoxia, a notable climate change stressor.

Mechanisms of acid-base regulation following respiratory alkalosis in red drum (Sciaenops ocellatus).

Respiratory acidosis and subsequent metabolic compensation are well-studied processes in fish exposed to elevated CO2 (hypercapnia). Yet, such exposures in the marine environment are invariably accompanied by a return of environmental CO2 to atmospheric baselines. This understudied phenomenon has the potential to cause a respiratory alkalosis that would necessitate base excretion. Here we sought to explore this question and the associated physiological mechanisms that may accompany base excretions using the red drum (Sciaenops ocellatus). As expected, when high pCO2 (15,000 µatm CO2) acclimated red drum were transferred to normal pCO2, their net H+ excretion shifted from positive (0.157 ± 0.044 µmol g-1 h-1) to negative (-0.606 ± 0.116 µmol g-1 h-1) in the 2 h post-transfer period. Net H+ excretion returned to control rates during the 3 to 24 h flux period. Gene expression and enzyme activity assays demonstrated that while the acidosis resulted in significant changes in several relevant transporters, no significant changes accompanied the alkalosis phase. Confocal microscopy was used to assess alkalosis-stimulated translocation of V-type H+ ATPase to the basolateral membrane previously seen in other marine species; however, no apparent translocation was observed. Overall, these data demonstrate that fluctuations in environmental CO2 result in both acidic and alkalotic respiratory disturbances; however, red drum maintain sufficient regulatory capacity to accommodate base excretion. Furthermore, this work does not support a role for basolateral VHA translocation in metabolic compensation from a systemic alkalosis in teleosts.

Oil exposure alters social group cohesion in fish.

Many animal taxa live in groups to increase foraging and reproductive success and aid in predator avoidance. For fish, a large proportion of species spend all or part of their lives in groups, with group coordination playing an important role in the emergent benefits of group-living. Group cohesion can be altered by an array of factors, including exposure to toxic environmental contaminants. Oil spills are one of the most serious forms of pollution in aquatic systems, and while a range of effects of acute oil exposure on animal physiology have been demonstrated, sub-lethal effects on animal behavior are relatively under-studied. Here we used an open-field behavioral assay to explore influence of acute oil exposure on social behavior in a gregarious fish native to the Gulf of Mexico, Atlantic croaker (Micropogonias undulatus). We used two oil concentrations (0.7% and 2% oil dilution, or 6.0 ± 0.9 and 32.9 ± 5.9 µg l-1 ΣPAH50 respectively) and assays were performed when all members of a group were exposed, when only one member was exposed, and when no individuals were exposed. Shoal cohesion, as assessed via mean neighbor distance, showed significant impairment following acute exposure to 2% oil. Fish in oil-exposed groups also showed reduced voluntary movement speed. Importantly, overall group cohesion was disrupted when even one fish within a shoal was exposed to 2% oil, and the behavior of unexposed in mixed groups, in terms of movement speed and proximity to the arena wall, was affected by the presence of these exposed fish. These results demonstrate that oil exposure can have adverse effects on fish behavior that may lead to reduced ecological success.

Impacts of deepwater horizon oil on fish.

An explosion on the Deepwater Horizon (DWH) oil rig in 2010 lead to the largest marine oil spill to occur in US history, resulting in significant impacts to the ecosystems and organisms in the Northern Gulf of Mexico (GoM). The present review sought to summarize and discuss findings from the 50+ peer-reviewed publications reporting effects of DWH oil exposure on teleost fish, and concludes that oil toxicity is a multi-target, multi-organ syndrome with substantial species-specific sensitivity differences. Of the 15 species tested with characterized exposures, 20% show effects at concentrations <1 µg l-1 while 50% display effects at <8.6 µg l-1 ΣPAH50, concentrations well within the range of reported environmental levels during the spill. Cardiotoxic effects are among the most frequently reported endpoints in DWH oil exposure studies and are thought to have significant downstream effects on fitness and survival. However, additional and possibly cardio-toxic independent impacts on sensory function and behavior are reported at very low exposure concentrations (< 1 µg l-1 ∑PAH50) and are clearly deserving of further study. Available information about modes of action leading to different categories of effects are summarized in the present review. An overview of the literature illustrates that early life stages (ELS) are approximately 1-order of magnitude more sensitive than corresponding later life stages, but also illustrates that adults can be impacted at concentrations as low as 4 µg l-1 ΣPAH50. The majority of studies exploring DWH oil toxicity in fish are performed using acute exposures (1-2 days), mid-range test temperatures (26-28 °C) and measure effects at the molecular to organismal levels, leaving a pressing need for more long-term exposures, exposures at the upper and lower levels of GoM relevant temperatures, and studies investigating population level impacts.

Na+ K+ ATPase isoform switching in zebrafish during transition to dilute freshwater habitats.

Na+ K+ ATPase (NKA) is crucial to branchial ion transport as it uses the energy from ATP to move Na+ against its electrochemical gradient. When fish encounter extremely dilute environments the energy available from ATP hydrolysis may not be sufficient to overcome thermodynamic constraints on ion transport. Yet many fish species-including zebrafish-are capable of surviving in dilute environments. Despite much study, the physiological mechanisms by which this occurs remain poorly understood. Here, we demonstrate that zebrafish acclimated to less than 10 µM Na+ water exhibit upregulation of a specific NKA α subunit ( zatp1a1a.5) that, unlike most NKA heterotrimers, would result in transfer of only a single Na+ and K+ per ATP hydrolysis reaction. Thermodynamic models demonstrate that this change is sufficient to reduce the activation energy of NKA, allowing it to overcome the adverse electrochemical gradient imposed by dilute freshwater. Importantly, upregulation of zatp1a1a.5 also coincides with the recovery of whole body Na+ post-transfer, which occurs within 24 h. While these structural modifications are crucial for allowing zebrafish to survive in ion-poor environments, phylogenetic and structural analysis of available α subunits from a range of teleosts suggests this adaptation is not widely distributed.

mRNA-miRNA-Seq Reveals Neuro-Cardio Mechanisms of Crude Oil Toxicity in Red Drum ( Sciaenops ocellatus).

Polycyclic aromatic hydrocarbons (PAHs) present in crude oil can cause global gene dysregulation and developmental impairment in fish. However, the mechanisms that alter gene regulation are not well understood. In this study, larval red drum ( Sciaenops ocellatus) were exposed to water accommodated fractions of source oil (6.8, 13.7, and 35.9 µg/L total PAHs) and weathered slick oil (4.7, 8.1, and 18.0 µg/L total PAHs) from the Deepwater Horizon (DWH) oil spill. The global mRNA-microRNA functional networks associated with the toxicity of DWH oil were explored by next-generation sequencing and in-depth bioinformatics analyses. Both source and slick oil significantly altered the expression of miR-18a, miR-27b, and miR-203a across all exposure concentrations. Consistent with the observed concentration-dependent morphological changes, the target mRNAs of these microRNAs were predominantly involved in neuro-cardio system development processes and associated key signaling pathways such as axonal guidance signaling, cAMP-response-element-binding protein signaling in neurons, calcium signaling, and nuclear-factor-of-activated T cells signaling in cardiac hypertrophy. The results indicated that the developmental toxicity of crude oil may result from the abnormal expression of microRNAs and associated target genes, especially for the nervous system. Moreover, we provide a case study for systematic toxicity evaluation leveraging mRNA-microRNA-seq data using nonmodel species.

Oil toxicity and implications for environmental tolerance in fish.

Crude oil and its constituent chemicals are common environmental toxicants in aquatic environments worldwide, and have been the subject of intense research for decades. Importantly, aquatic environments are also the sites of numerous other environmental disturbances that can impact the endemic fauna. While there have been a number of attempts to explore the potential additive and synergistic effects of oil exposure and environmental stressors, many of these efforts have focused on the cumulative effects on typical toxicological endpoints (e.g. survival, growth, reproduction and cellular damage). Fewer studies have investigated the impact that oil exposure may have on the ability of exposed animals to tolerate typically encountered environmental stressors, despite the fact that this is an important consideration when placing oil spills in an ecological context. Here we review the available data and highlight potentially understudied areas relating to how oil exposure may impair organismal responses to common environmental stressors in fishes. We focused on four common environmental stressors in aquatic environments - hypoxia, temperature, salinity and acid-base disturbances - while also considering social stress and impacts on the hypothalamus-pituitary-interrenal axis. Overall, we believe the evidence supports treating the impacts of oil exposure on environmental tolerance as an independent endpoint of toxicity in fishes.

Effects of Deepwater Horizon crude oil on ocular development in two estuarine fish species, red drum (Sciaenops ocellatus) and sheepshead minnow (Cyprinodon variegatus).

Polycyclic aromatic hydrocarbons (PAHs) present in crude oil have been shown to cause the dysregulation of genes important in eye development and function, as well as morphological abnormalities of the eye. However, it is not currently understood how these changes in gene expression are manifested as deficits in visual function. Embryonic red drum (Sciaenops ocellatus) and sheepshead minnow (Cyprinodon variegatus) were exposed to water accommodated fractions (WAFs) of weathered crude oil and assessed for visual function using an optomotor response assay in early life-stage larvae, with subsequent samples taken for histological analysis of the eyes. Larvae of both species exposed to increasing concentrations of oil exhibited a reduced optomotor response. The mean diameters of retinal layers, which play an important role in visual function and image processing, were significantly reduced in oil-exposed sheepshead larvae, though not in red drum larvae. The present study provides evidence that weathered crude oil has a significant effect on visual function in early life-stage fishes.

Social competition in red drum (Sciaenops ocellatus) is influenced by crude oil exposure.

The present study examined impacts of crude oil exposure on dyad competition in juvenile red drum. Following the 2010 Deepwater Horizon oil spill, it has become well established that oil exposure can constrain maximum metabolic rate, reduce aerobic scope and exercise performance in marine fish. Aerobic scope is one of the physiological characteristics that is a known determinant of dominance in fish social hierarchy formation. As such, oil exposure may predispose individuals to subordinate social status, complete with the concomitant ecological costs. We tested this hypothesis on the gregarious Gulf of Mexico species, the red drum (Sciaenops ocellatus). Using a standard dyad, one-on-one, test design, we first assessed the parameters - including size and aerobic scope- that predict social dominance. Of the tested parameters, only aerobic scope was predictive of social dominance, with dominant individuals consistently having higher aerobic scopes than subordinates. Hierarchy formation between individuals exposed to one of two oil concentrations (5.7 ± 0.5 and 9.0 ± 0.2 µg l-1 ΣPAH50) and unexposed conspecifics were then investigated. As hypothesized, fish exposed to both oil concentrations were more likely to be subordinate than what would occur by random chance. These results demonstrate that the physiological constraints imposed by oil exposure can affect social status and behavior in fishes, which can have downstream consequences for ecological fitness.

The effects of oil induced respiratory impairment on two indices of hypoxia tolerance in Atlantic croaker (Micropogonias undulatus).

The Gulf of Mexico was home to the Deepwater Horizon oil spill, and is also known to exhibit seasonal declines in oxygen availability. Oil exposure in fish is known to impact oxygen uptake through cardiac impairment, which raises questions about the additive effects of these two stressors. Here we explore this question on the Atlantic croaker using two measures of hypoxia tolerance: critical oxygen threshold (Pcrit), and time to loss of equilibrium (LOE). We first demonstrated that 24 h exposure to 10.1 and 23.2 µg l-1 ΣPAH50 significantly impaired oxygen uptake. There was no effect of exposure on Pcrit or LOE. Exposure did result in significantly different repeatability between pre- and post-exposure Pcrit, suggesting that hypoxia tolerant individual may see greater impacts following exposure. These results suggest oil exposure does not have wide scale detrimental outcomes for hypoxia tolerance in fish, yet there may be fine scale impairments of ecological significance.

Publisher correction: Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments.

In the version of this Article originally published, a statistic relating to the northern Great Barrier Reef was attributed to the Great Barrier Reef as a whole. The sentence should have read 'In 2016 alone, more than 35% of corals on the northern Great Barrier Reef are estimated to have died following the worst bleaching event ever recorded'. This has been corrected in all versions of the Article.

Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments.

Global demand for energy and oil-based products is progressively introducing petrogenic polycyclic aromatic hydrocarbons (PAHs) into sensitive marine environments, primarily from fossil-fuel exploration, transport, and urban and industrial runoff. These toxic pollutants are found worldwide, yet the long-term ecological effects on coral reef ecosystems are unknown. Here, we demonstrate that oil exposure spanning PAH concentrations that are environmentally relevant for many coastal marine ecosystems (≤5.7 µg l-1), including parts of the Great Barrier Reef, Red Sea, Asia and the Caribbean, causes elevated mortality and stunted growth rates in six species of pre-settlement coral reef fishes, spanning two evolutionarily distinct families (Pomacentridae and Lethrinidae). Furthermore, oil exposure alters habitat settlement and antipredator behaviours, causing reduced sheltering, shoaling and increased risk taking, all of which exacerbate predator-induced mortality during recruitment. These results suggest a previously unknown path, whereby oil and PAH exposure impair higher-order cognitive processing and behaviours necessary for the successful settlement and survival of larval fishes. This emphasizes the risks associated with industrial activities within at-risk ecosystems.