Cutaneous ulcerative lesions of unknown etiology affecting lionfish Pterois spp. in the Gulf of Mexico.

OBJECTIVE: Cutaneous ulcerative skin lesions in a complex of invasive Gulf of Mexico lionfish (Red Lionfish Pterois volitans, Devil Firefish P. miles, and the hybrid Red Lionfish × Devil Firefish) became epizootic beginning in mid-August 2017. Herein, we provide the first pathological descriptions of these lesions and summarize our analyses to elucidate the etiology of the disease. METHODS: We examined ulcerated and normal fish through gross pathology and histopathology, bacterial sampling, and unbiased metagenomic next-generation sequencing. We tracked prevalence of the disease, and we used biological health indicators (condition factor, splenosomatic and hepatosomatic index) to evaluate impacts to health, while considering sex and age as potential risk factors. RESULT: Typical ulcerative lesions were deep, exposing skeletal muscle, and were bordered by pale or reddened areas often with some degree of scale loss. Only incidental parasites were found in our examinations. Most fish (86%; n = 50) exhibited wound healing grossly and histologically, confirmed by the presence of granulation tissues. A primary bacterial pathogen was not evident through bacterial culture or histopathology. Metagenomic next-generation sequencing did not reveal a viral pathogen (DNA or RNA) but did provide information about the microbiome of some ulcerated specimens. Compared with clinically healthy fish, ulcerated fish had a significantly lower condition factor and a higher splenosomatic index. Disease prevalence at monitored sites through July 2021 indicated that ulcerated fish were still present but at substantially lower prevalence than observed in 2017. CONCLUSION: Although some common findings in a number of specimens suggest a potential role for opportunistic bacteria, collectively our suite of diagnostics and analyses did not reveal an intralesional infectious agent, and we must consider the possibility that there was no communicable pathogen.

Microbiota of wild-caught Red Snapper Lutjanus campechanus.

BACKGROUND: The microbiota plays an essential role in host health, particularly through competition with opportunistic pathogens. Changes in total bacterial load and microbiota structure can indicate early stages of disease, and information on the composition of bacterial communities is essential to understanding fish health. Although Red Snapper (Lutjanus campechanus) is an economically important species in recreational fisheries and a primary aquaculture candidate, no information is available on the microbial communities of this species. The aim of this study was to survey the microbiota of apparently healthy, wild-caught Red Snapper from the Gulf of Mexico. Sampled Red Snapper showed no physical signs of disease. Tissues that are either primary entry routes for pathogens (feces, gill) or essential to disease diagnosis (blood) were sampled. Bacteria were enumerated using culture-based techniques and characterized by pyrosequencing. RESULTS: Aerobic counts of feces and gill samples were 107 and 104 CFU g-1, respectively. All individuals had positive blood cultures with counts up to 23 CFU g-1. Gammaproteobacteria dominated the microbiota of all sample types, including the genera Pseudoalteromonas and Photobacterium in feces and Pseudomonas in blood and gill. Gill samples were also dominated by Vibrio while blood samples had high abundances of Nevskia. High variability in microbiota composition was observed between individuals, with percent differences in community composition ranging from 6 to 76 % in feces, 10 to 58 % in gill, and 52 to 64 % in blood. CONCLUSIONS: This study provides the first characterization of the microbiota of the economically significant Red Snapper via pyrosequencing. Its role in fish health highlights the importance of understanding microbiota composition for future work on disease prevention using microbial manipulation.

Eye lens-derived Δ14C signatures validate extreme longevity in the deepwater scorpaenid blackbelly rosefish (Helicolenus dactylopterus).

Many members of the scorpaenid subfamily: Sebastinae (rockfishes and their relatives) exhibit slow growth and extreme longevity (> 100 y), thus are estimated to be vulnerable to overfishing. Blackbelly rosefish (Helicolenus dactylopterus) is a deepwater sebastine whose longevity estimates range widely, possibly owing to different regional levels of fisheries exploitation across its Atlantic Ocean range. However, age estimation has not been validated for this species and ageing for sebastines in general is uncertain. We performed age validation of northern Gulf of Mexico blackbelly rosefish via an application of the bomb radiocarbon chronometer which utilized eye lens cores instead of more traditional otolith cores as the source of birth year Δ14C signatures. The correspondence of eye lens core Δ14C with a regional reference series was tested with a novel Bayesian spline analysis, which revealed otolith opaque zone counts provide accurate age estimates. Maximum observed longevity was 90 y, with 17.5% of individuals aged to be > 50 y. Bayesian growth analysis, with estimated length-at-birth included as a prior, revealed blackbelly rosefish exhibit extremely slow growth (k = 0.08 y-1). Study results have important implications for the management of blackbelly rosefish stocks, as extreme longevity and slow growth imply low resilience to fishing pressure.

Fine-scale movement of northern Gulf of Mexico red snapper and gray triggerfish estimated with three-dimensional acoustic telemetry.

Red snapper and gray triggerfish are ecologically, economically, and culturally important reef fishes in the northern Gulf of Mexico (nGOM). Scientists and managers have sought to understand the effects of artificial reefs on reef fish ecology by focusing on fish residency and movement at artificial reefs with less attention paid to broader spatial and temporal patterns in reef fish movements among a seascape of artificial reefs and other natural habitats. We used novel large-scale (> 15 km2) geopositioning acoustic telemetry arrays to track the 3-dimensional movements of tagged red snapper (n = 59) and gray triggerfish (n = 15) among multiple nGOM artificial reefs up to 333 days. Tagged fish moved frequently among artificial reefs and had shorter residence times at the release reef (43 days for red snapper and 3 days for gray triggerfish) than reported in previous studies. Both species displayed high individual variability in movement dynamics, as well as seasonally variable diel patterns of habitat use, height above bottom, and distance to reefs, which may have been driven by dynamic influences of predation risk, physiological constraints, or foraging over time and space. The wider seascape view revealed in this study demonstrates the importance of including multiple artificial reefs over long timescales to capture individual, spatial, and temporal variability in reef fish movement.

Estimating reef fish size distributions with a mini remotely operated vehicle-integrated stereo camera system.

We tested the efficacy of a stereo camera (SC) system adapted for use with a remotely operated vehicle (ROV) to estimate fish length distributions at reef sites in the northern Gulf of Mexico. A pool experiment was conducted to test the effect of distance (1, 2, 3 or 5 m), angle of incidence (AOI; 0° to 40° at 5° increments), and SC baseline distance (BD; BD1 = 406, BD2 = 610, and BD3 = 762 mm camera separation) on the accuracy and precision of fish model length (288, 552, or 890 mm fork length) estimates compared to a red laser scaler (RLS). A field experiment was then conducted at 20 reef sites with SCs positioned at BD1 to compare fish length distribution estimates between the SC and RLS systems under in situ conditions. In the pool experiment, mean percent errors were consistently within the a priori selected threshold of ±5% at AOIs ≤10° at all distances with all four systems. However, SCs produced accurate estimates at AOIs up to 30° at all distances tested; 2-3 m was optimal. During reef site surveys, SCs collected 10.4 times as many length estimates from 4.3 times as many species compared to the RLS. Study results demonstrate that, compared to laser scalers, ROV-based SC systems can substantially increase the number of available fish length estimates by producing accurate length estimates at a wider range of target orientations while also enabling measurements from a greater portion of the cameras' field of view.

A mini ROV-based method for recovering marine instruments at depth.

Instruments are often deployed at depth for weeks to years for a variety of marine applications. In many cases, divers can be deployed to retrieve instruments, but divers are constrained by depth limitations and safety concerns. Acoustic release technology can also be employed but can add considerable expense and acoustic releases will at times fail. Here, we report a simple method that utilizes a commercially available mooring hook integrated with a mini remotely operated vehicle to attach lines to instruments deployed on the sea floor, which can then be winched to the surface. The mooring hook apparatus was tested in a pool setting and then used to retrieve acoustic telemetry receiver bases (50 kg) or fish traps (30-50 kg) from the northern Gulf of Mexico continental shelf at depths between 28 and 80 m. During 2013-2019, 539 retrievals (100% success rate) were made of receiver bases (n = 239) and traps (n = 300) on 30 sea days using this approach. This method could easily be applied to other types of instruments, or recovery and salvage of objects that are too deep for standard diving operations.

Life history of northern Gulf of Mexico Warsaw grouper Hyporthodus nigritus inferred from otolith radiocarbon analysis.

Warsaw grouper, Hyporthodus nigritus, is a western Atlantic Ocean species typically found at depths between 55 and 525 m. It is listed as a species of concern by the U.S. National Marine Fisheries Service and as near threatened by the International Union for the Conservation of Nature. However, little information exists on the species' life history in the northern Gulf of Mexico (nGOM) and its stock status in that region is currently unknown. Age of nGOM Warsaw grouper was investigated via opaque zone counts in otolith thin sections (max age = 61 y), and then the bomb 14C chronometer was employed to validate the accuracy of age estimates. Otolith cores (n = 14) were analyzed with accelerator mass spectrometry and resulting Δ14C values overlain on a loess regression computed for a regional coral and known-age red snapper Δ14C time series. Residual analysis between predicted Δ14C values from the loess regression versus Warsaw grouper otolith core Δ14C values indicated no significant difference in the two data series. Therefore, the accuracy of otolith-based aging was validated, which enabled growth and longevity estimates to be made for nGOM Warsaw grouper. Dissolved inorganic carbon (DIC) Δ14C values collected from the nGOM support the inference that juvenile Warsaw grouper occur in shelf waters (<200 m) since DIC Δ14C values in this depth range are enriched in 14C and similar to the Δ14C values from otolith cores. A Bayesian model was fit to fishery-dependent age composition data and produced von Bertalanffy growth function parameters of L∞ = 1,533 mm, k = 0.14 y-1, and t0 = 1.82 y. Fishing mortality also was estimated in the model, which resulted in a ratio of fishing to natural mortality of 5.1:1. Overall, study results indicate Warsaw grouper is a long-lived species that is estimated to have experienced significant overfishing in the nGOM, with the age of most landed fish being <10 y.

Changes in Reef Fish Community Structure Following the Deepwater Horizon Oil Spill.

Large-scale anthropogenic disturbances can have direct and indirect effects on marine communities, with direct effects often taking the form of widespread injury or mortality and indirect effects manifesting as changes in food web structure. Here, we report a time series that captures both direct and indirect effects of the Deepwater Horizon Oil Spill (DWH) on northern Gulf of Mexico (nGoM) reef fish communities. We observed significant changes in community structure immediately following the DWH, with a 38% decline in species richness and 26% decline in Shannon-Weiner diversity. Initial shifts were driven by widespread declines across a range of trophic guilds, with subsequent recovery unevenly distributed among guilds and taxa. For example, densities of small demersal invertivores, small demersal browsers, generalist carnivores, and piscivores remained persistently low with little indication of recovery seven years after the DWH. Initial declines among these guilds occurred prior to the arrival of the now-widespread, invasive lionfish (Pterois spp.), but their lack of recovery suggests lionfish predation may be affecting recovery. Factors affecting persistently low densities of generalist carnivores and piscivores are not well understood but warrant further study given the myriad ecosystem services provided by nGoM reef fishes.

Author Correction: Changes in Reef Fish Community Structure Following the Deepwater Horizon Oil Spill.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Precipitous Declines in Northern Gulf of Mexico Invasive Lionfish Populations Following the Emergence of an Ulcerative Skin Disease.

Invasive Indo-Pacific lionfish Pterois volitans/miles have become well-established in many western Atlantic marine habitats and regions. However, high densities and low genetic diversity could make their populations susceptible to disease. We examined changes in northern Gulf of Mexico (nGOM) lionfish populations following the emergence of an ulcerative skin disease in August 2017, when estimated disease prevalence was as high as 40%. Ulcerated female lionfish had 9% lower relative condition compared to non-ulcerated females. Changes in lionfish size composition indicated a potential recruitment failure in early summer 2018, when the proportion of new recruits declined by >80%. Remotely operated vehicle surveys during 2016-2018 indicated lionfish population density declined in 2018 by 75% on natural reefs. The strongest declines (77-79%) in lionfish density were on high-density (>25 lionfish per 100 m2) artificial reefs, which declined to similar levels as low-density (<15 lionfish per 100 m2) artificial reefs that had prior lionfish removals. Fisheries-dependent sampling indicated lionfish commercial spearfishing landings, commercial catch per unit effort (CPUE), and lionfish tournament CPUE also declined approximately 50% in 2018. Collectively, these results provide correlative evidence for density-dependent epizootic population control, have implications for managing lionfish and impacted native species, and improve our understanding of biological invasions.

Impacts of the Deepwater Horizon oil spill evaluated using an end-to-end ecosystem model.

We use a spatially explicit biogeochemical end-to-end ecosystem model, Atlantis, to simulate impacts from the Deepwater Horizon oil spill and subsequent recovery of fish guilds. Dose-response relationships with expected oil concentrations were utilized to estimate the impact on fish growth and mortality rates. We also examine the effects of fisheries closures and impacts on recruitment. We validate predictions of the model by comparing population trends and age structure before and after the oil spill with fisheries independent data. The model suggests that recruitment effects and fishery closures had little influence on biomass dynamics. However, at the assumed level of oil concentrations and toxicity, impacts on fish mortality and growth rates were large and commensurate with observations. Sensitivity analysis suggests the biomass of large reef fish decreased by 25% to 50% in areas most affected by the spill, and biomass of large demersal fish decreased even more, by 40% to 70%. Impacts on reef and demersal forage caused starvation mortality in predators and increased reliance on pelagic forage. Impacts on the food web translated effects of the spill far away from the oiled area. Effects on age structure suggest possible delayed impacts on fishery yields. Recovery of high-turnover populations generally is predicted to occur within 10 years, but some slower-growing populations may take 30+ years to fully recover.

A multi-year study of hepatic biomarkers in coastal fishes from the Gulf of Mexico after the Deepwater Horizon Oil Spill.

Following the 2010 Gulf of Mexico oil spill, concerns were raised regarding exposure of fish to crude oil components, particularly polycyclic aromatic hydrocarbons (PAHs). This three year study examined hepatic enzymes in post-mitochondrial supernatant fractions from red snapper (Lutjanus campechanus) and gray triggerfish (Balistes capriscus) collected in the north central Gulf of Mexico between 2011 and 2014. Biomarker activities evaluated included benzo(a)pyrene hydroxylase (AHH), ethoxyresorufin O-deethylase (EROD), glutathione transferase (GST), and glutathione peroxidase (GPx). Mean EROD activity was higher in gray triggerfish (12.97 ± 7.15 pmol/min/mg protein [mean ± SD], n = 115) than red snapper (2.75 ± 1.92 pmol/min/mg protein, n = 194), p < 0.0001. In both species, EROD declined over time between 2011 and 2014. Declines in GST and GPx activities were also noted over this time period for both species. Gray triggerfish liver was fatty, and heptane extracts of the liver fat contained fluorescent substances with properties similar to known PAHs, however the origin of these PAHs is unknown.

Habitat-specific density and diet of rapidly expanding invasive red lionfish, Pterois volitans, populations in the northern Gulf of Mexico.

Invasive Indo-Pacific red lionfish, Pterois volitans, were first reported in the northern Gulf of Mexico (nGOM) in summer 2010. To examine potential impacts on native reef fish communities, lionfish density and size distributions were estimated from fall 2010 to fall 2013 with a remotely operated vehicle at natural (n = 16) and artificial (n = 22) reef sites. Lionfish (n = 934) also were sampled via spearfishing to examine effects of habitat type, season, and fish size on their diet and trophic ecology. There was an exponential increase in lionfish density at both natural and artificial reefs over the study period. By fall 2013, mean lionfish density at artificial reefs (14.7 fish 100 m(-2)) was two orders of magnitude higher than at natural reefs (0.49 fish 100 m(-2)), and already was among the highest reported in the western Atlantic. Lionfish diet was significantly different among habitats, seasons, and size classes, with smaller (<250 mm total length) fish consuming more benthic invertebrates and the diet of lionfish sampled from artificial reefs being composed predominantly of non-reef associated prey. The ontogenetic shift in lionfish feeding ecology was consistent with δ15N values of white muscle tissue that were positively related to total length. Overall, diet results indicate lionfish are generalist mesopredators in the nGOM that become more piscivorous at larger size. However, lionfish diet was much more varied at artificial reef sites where they clearly were foraging on open substrates away from reef structure. These results have important implications for tracking the lionfish invasion in the nGOM, as well as estimating potential direct and indirect impacts on native reef fish communities in this region.

Age and growth of endangered smalltooth sawfish (Pristis pectinata) verified with LA-ICP-MS analysis of vertebrae.

Endangered smalltooth sawfish (Pristis pectinata) were opportunistically sampled in south Florida and aged by counting opaque bands in sectioned vertebrae (n=15). Small sample size precluded traditional age verification, but fish collected in spring and summer had translucent vertebrae margins, while fish collected in winter had opaque margins. Trends in Sr:Ca measured across vertebrae with laser ablation-inductively coupled plasma-mass spectrometry corresponded well to annual salinity trends observed in sawfish estuarine nursery habitats in south Florida, thus serve as a chemical marker verifying annual formation of opaque bands. Based on that finding and assumptions about mean birth date and timing of opaque band formation, estimated age ranged from 0.4 y for a 0.60 m total length (TL) male to 14.0 y for a 4.35 m TL female. Von Bertalanffy growth parameters computed from size at age data were 4.48 m for L(∞), 0.219 y(-1)for k, and -0.81 y for t(0). Results of this study have important implications for sawfish conservation as well as for inferring habitat residency of euryhaline elasmobranchs via chemical analysis of vertebrae.