Measures and models of visual acuity in epipelagic and mesopelagic teleosts and elasmobranchs.

Eyes in low-light environments typically must balance sensitivity and spatial resolution. Vertebrate eyes with large "pixels" (e.g., retinal ganglion cells with inputs from many photoreceptors) will be sensitive but provide coarse vision. Small pixels can render finer detail, but each pixel will gather less light, and thus have poor signal relative-to-noise, leading to lower contrast sensitivity. This balance is particularly critical in oceanic species at mesopelagic depths (200-1000 m) because they experience low light and live in a medium that significantly attenuates contrast. Depending on the spatial frequency and inherent contrast of a pattern being viewed, the viewer's pupil size and temporal resolution, and the ambient light level and water clarity, a visual acuity exists that maximizes the distance at which the pattern can be discerned. We develop a model that predicts this acuity for common conditions in the open ocean, and compare it to visual acuity in marine teleost fishes and elasmobranchs found at various depths in productive and oligotrophic waters. Visual acuity in epipelagic and upper mesopelagic species aligned well with model predictions, but species at lower mesopelagic depths (> 600 m) had far higher measured acuities than predicted. This is consistent with the prediction that animals found at lower mesopelagic depths operate in a visual world consisting primarily of bioluminescent point sources, where high visual acuity helps localize targets of this kind. Overall, the results suggest that visual acuity in oceanic fish and elasmobranchs is under depth-dependent selection for detecting either extended patterns or point sources.

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.

Evidence that eye-facing photophores serve as a reference for counterillumination in an order of deep-sea fishes.

Counterillumination, the masking of an animal's silhouette with ventral photophores, is found in a number of mesopelagic taxa but is difficult to employ because it requires that the animal match the intensity of downwelling light without seeing its own ventral photophores. It has been proposed that the myctophid, Tarletonbeania crenularis, uses a photophore directed towards the eye, termed an eye-facing photophore, as a reference standard that it adjusts to match downwelling light. The potential use of this mechanism, however, has not been evaluated in other fishes. Here, we use micro-computed tomography, photography and dissection to evaluate the presence/absence of eye-facing photophores in three families of stomiiform fishes. We found that all sampled species with ventral photophores capable of counterillumination possess an eye-facing photophore that is pigmented on the anterior and lateral sides, thus preventing its use as a laterally directed signal, lure or searchlight. The two species that are incapable of counterillumination, Cyclothone obscura and Sigmops bathyphilus, lack an eye-facing photophore. After determining the phylogenetic distribution of eye-facing photophores, we used histology to examine the morphology of the cranial tissue in Argyropelecus aculeatus and determined that light from the eye-facing photophore passes through a transparent layer of tissue, then the lens, and finally strikes the accessory retina. Additionally, eight of the 14 species for which fresh specimens were available had an aphakic gap that aligned with the path of emitted light from the eye-facing photophore, while the remaining six had no aphakic gap. These findings, combined with records of eye-facing photophores from distantly related taxa, strongly suggest that eye-facing photophores serve as a reference for counterillumination in these fishes.

Variation in rod spectral sensitivity of fishes is best predicted by habitat and depth.

Rod spectral sensitivity data (λmax ), measured by microspectrophotometry, were compiled for 403 species of ray-finned fishes in order to examine four hypothesized predictors of rod spectral sensitivity (depth, habitat, diet and temperature). From this database, a subset of species that were known to be adults and available on a published phylogeny (n = 210) were included in analysis, indicating rod λmax values averaging 503 nm and ranging from 477 to 541 nm. Linear models that corrected for phylogenetic relatedness showed that variation in rod sensitivity was best predicted by habitat and depth, with shorter wavelength λmax values occurring in fishes found offshore or in the deep sea. Neither diet, nor the interaction of diet and habitat, had significant explanatory power. Although temperature significantly correlated with rod sensitivity, in that fishes in temperate latitudes had longer wavelength rod λmax values than those in tropical latitudes, sampling inequity and other confounds require the role of the temperature to be studied further. Together, these findings indicate that fish rod λmax is influenced by several ecological factors, suggesting that selection can act on even small differences in fish spectral sensitivity.

Spectral sensitivity in ray-finned fishes: diversity, ecology and shared descent.

A major goal of sensory ecology is to identify factors that underlie sensory-trait variation. One open question centers on why fishes show the greatest diversity among vertebrates in their capacity to detect color (i.e. spectral sensitivity). Over the past several decades, λmax values (photoreceptor class peak sensitivity) and chromacy (photoreceptor class number) have been cataloged for hundreds of fish species, yet the ecological basis of this diversity and the functional significance of high chromacy levels (e.g. tetra- and pentachromacy) remain unclear. In this study, we examined phylogenetic, physiological and ecological patterns of spectral sensitivity of ray-finned fishes (Actinoptergyii) via a meta-analysis of data compiled from 213 species. Across the fishes sampled, our results indicate that trichromacy is most common, ultraviolet λmax values are not found in monochromatic or dichromatic species, and increasing chromacy, including from tetra- to pentachromacy, significantly increases spectral sensitivity range. In an ecological analysis, multivariate phylogenetic latent liability modeling was performed to analyze correlations between chromacy and five hypothesized predictors (depth, habitat, diet, body coloration, body size). In a model not accounting for phylogenetic relatedness, each predictor with the exception of habitat significantly correlated with chromacy: a positive relationship in body color and negative relationships with body size, diet and depth. However, after phylogenetic correction, the only remaining correlated predictor was depth. The findings of this study indicate that phyletic heritage and depth are important factors in fish spectral sensitivity and impart caution about excluding phylogenetic comparative methods in studies of sensory trait variation.

Decadal Assessment of Polycyclic Aromatic Hydrocarbons in Mesopelagic Fishes from the Gulf of Mexico Reveals Exposure to Oil-Derived Sources.

This study characterizes a decadal assessment of polycyclic aromatic hydrocarbons (PAHs) in the muscle tissues of mesopelagic fish species as indicators of the environmental health of the Gulf of Mexico (GoM) deep-pelagic ecosystem. Mesopelagic fishes were collected prior to the Deepwater Horizon (DWH) oil spill (2007), immediately post-spill (2010), 1 year after the spill (2011), and 5-6 years post-spill (2015-2016) to assess if the mesopelagic ecosystem was exposed to, and retained, PAH compounds from the DWH spill. Results indicated that a 7- to 10-fold increase in PAHs in fish muscle tissues occurred in 2010-2011 (4972 ± 1477 ng/g) compared to 2007 (630 ± 236 ng/g). In 2015-2016, PAH concentrations decreased close to the levels measured in 2007 samples (827 ± 138 ng/g); however, the composition of PAHs still resembles a petrogenic source similar to samples collected in 2010-2011. PAH composition in muscle samples indicated that natural sources (e.g., Mississippi River and natural seeps) or spatial variability within the GoM do not explain the temporal variability of PAHs observed from 2007 to 2016. Furthermore, analysis of different fish tissues indicated the dietary intake and maternal transfer of PAHs as the primary mechanisms for bioaccumulation in 2015-2016, explaining the elevated levels and composition of PAHs in ovarian eggs.

Visual acuity in ray-finned fishes correlates with eye size and habitat.

Visual acuity (the ability to resolve spatial detail) is highly variable across fishes. However, little is known about the evolutionary pressures underlying this variation. We reviewed published literature to create an acuity database for 159 species of ray-finned fishes (Actinopterygii). Within a subset of those species for which we had phylogenetic information and anatomically measured acuity data (n=81), we examined relationships between acuity and both morphological (eye size and body size) and ecological (light level, water turbidity, habitat spatial complexity and diet) variables. Acuity was significantly correlated with eye size (P<0.001); a weaker correlation with body size occurred via a correlation between eye and body size (P<0.001). Acuity decreased as light level decreased and turbidity increased; however, these decreases resulted from fishes in dark or murky environments having smaller eyes and bodies than those in bright or clear environments. We also found significantly lower acuity in horizon-dominated habitats than in featureless or complex habitats. Higher acuity in featureless habitats is likely due to species having absolutely larger eyes and bodies in that environment, though eye size relative to body size is not significantly different from that in complex environments. Controlling for relative eye size, we found that species in complex environments have even higher acuity than predicted. We found no relationship between visual acuity and diet. Our results show that eye size is a primary factor underlying variation in fish acuity. We additionally show that habitat type is an important ecological factor that correlates with acuity in certain species.

Depth as a driver of evolution in the deep sea: Insights from grenadiers (Gadiformes: Macrouridae) of the genus Coryphaenoides.

Here we consider the role of depth as a driver of evolution in a genus of deep-sea fishes. We provide a phylogeny for the genus Coryphaenoides (Gadiformes: Macrouridae) that represents the breadth of habitat use and distributions for these species. In our consensus phylogeny species found at abyssal depths (>4000m) form a well-supported lineage, which interestingly also includes two non-abyssal species, C. striaturus and C. murrayi, diverging from the basal node of that lineage. Biogeographic analyses suggest the genus may have originated in the Southern and Pacific Oceans where contemporary species diversity is highest. The abyssal lineage seems to have arisen secondarily and likely originated in the Southern/Pacific Oceans but diversification of this lineage occurred in the Northern Atlantic Ocean. All abyssal species are found in the North Atlantic with the exception of C. yaquinae in the North Pacific and C. filicauda in the Southern Ocean. Abyssal species tend to have broad depth ranges and wide distributions, indicating that the stability of the deep oceans and the ability to live across wide depths may promote population connectivity and facilitate large ranges. We also confirm that morphologically defined subgenera do not agree with our phylogeny and that the Giant grenadier (formerly Albatrossia pectoralis) belongs to Coryphaenoides, indicating that a taxonomic revision of the genus is needed. We discuss the implications of our findings for understanding the radiation and diversification of this genus, and the likely role of adaptation to the abyss.

Deep-pelagic fishes: Demographic instability in a stable environment.

Demographic histories are frequently a product of the environment, as populations expand or contract in response to major environmental changes, often driven by changes in climate. Meso- and bathy-pelagic fishes inhabit some of the most temporally and spatially stable habitats on the planet. The stability of the deep-pelagic could make deep-pelagic fishes resistant to the demographic instability commonly reported in fish species inhabiting other marine habitats, however the demographic histories of deep-pelagic fishes are unknown. We reconstructed the historical demography of 11 species of deep-pelagic fishes using mitochondrial and nuclear DNA sequence data. We uncovered widespread evidence of population expansions in our study species, a counterintuitive result based on the nature of deep-pelagic ecosystems. Frequency-based methods detected potential demographic changes in nine species of fishes, while extended Bayesian skyline plots identified population expansions in four species. These results suggest that despite the relatively stable nature of the deep-pelagic environment, the fishes that reside here have likely been impacted by past changes in climate. Further investigation is necessary to better understand how deep-pelagic fishes, by far Earth's most abundant vertebrates, will respond to future climatic changes.

An Investigation into the Mechanism Mediating Counterillumination in Myctophid Fishes (Myctophidae).

AbstractCounterillumination is a camouflage strategy employed primarily by mesopelagic fishes, sharks, crustaceans, and squid, which use ventral bioluminescence to obscure their silhouettes when viewed from below. Although certain counterilluminating species have been shown to control the intensity of their ventral emissions to match the background downwelling light, the feedback mechanism mediating this ability is poorly understood. One proposed mechanism involves the presence and use of eye-facing photophores that would allow simultaneous detection and comparison of photophore emissions and downwelling solar light. Eye-facing photophores have been found in at least 34 species of counterilluminating stomiiform fishes and the myctophid Tarletonbeania crenularis. Here, we examined nine phylogenetically spaced myctophid species for eye-facing photophores to assess whether this mechanism is as prevalent in this group as it is in the Stomiiformes. First, microcomputed tomography imaging data were collected for each species, and three-dimensional reconstructions of the fishes were developed to identify potential eye-facing photophores. The fishes were then dissected under a stereomicroscope to confirm the presence of all identified photophores, probe for any photophores missed in the reconstruction analysis, and determine the orientation of the photophores' emissions. Although photophores were identified near the orbits of all species examined, none of the fishes' photophores directed light into their orbits, suggesting that myctophids may regulate bioluminescence through an alternative mechanism.

Expanding our view of the cold-water coral niche and accounting of the ecosystem services of the reef habitat.

Coral reefs are iconic ecosystems that support diverse, productive communities in both shallow and deep waters. However, our incomplete knowledge of cold-water coral (CWC) niche space limits our understanding of their distribution and precludes a complete accounting of the ecosystem services they provide. Here, we present the results of recent surveys of the CWC mound province on the Blake Plateau off the U.S. east coast, an area of intense human activity including fisheries and naval operations, and potentially energy and mineral extraction. At one site, CWC mounds are arranged in lines that total over 150 km in length, making this one of the largest reef complexes discovered in the deep ocean. This site experiences rapid and extreme shifts in temperature between 4.3 and 10.7 °C, and currents approaching 1 m s-1. Carbon is transported to depth by mesopelagic micronekton and nutrient cycling on the reef results in some of the highest nitrate concentrations recorded in the region. Predictive models reveal expanded areas of highly suitable habitat that currently remain unexplored. Multidisciplinary exploration of this new site has expanded understanding of the cold-water coral niche, improved our accounting of the ecosystem services of the reef habitat, and emphasizes the importance of properly managing these systems.

MesopTroph, a database of trophic parameters to study interactions in mesopelagic food webs.

Mesopelagic organisms play a crucial role in marine food webs, channelling energy across the predator-prey network and connecting depth strata through their diel vertical migrations. The information available to assess mesopelagic feeding interactions and energy transfer has increased substantially in recent years, owing to the growing interest and research activity in the mesopelagic realm. However, such data have not been systematically collated and are difficult to access, hampering estimation of the contribution of mesopelagic organisms to marine ecosystems. Here we present MesopTroph, a georeferenced database of diet, trophic markers, and energy content of mesopelagic and other marine taxa compiled from 203 published and non-published sources. MesopTroph currently includes data on stomach contents, carbon and nitrogen stable isotopes, major and trace elements, energy density, fatty acids, trophic positions, and diet proportion estimates for 498 species/genera. MesopTroph will be expanded with new data emerging from ongoing studies. MesopTroph provides a unique tool to investigate trophic interactions and energy flow mediated by mesopelagic organisms, and to evaluate the ecosystem services of this community.

Discovering marine biodiversity in the 21st century.

We review the current knowledge of the biodiversity of the ocean as well as the levels of decline and threat for species and habitats. The lack of understanding of the distribution of life in the ocean is identified as a significant barrier to restoring its biodiversity and health. We explore why the science of taxonomy has failed to deliver knowledge of what species are present in the ocean, how they are distributed and how they are responding to global and regional to local anthropogenic pressures. This failure prevents nations from meeting their international commitments to conserve marine biodiversity with the results that investment in taxonomy has declined in many countries. We explore a range of new technologies and approaches for discovery of marine species and their detection and monitoring. These include: imaging methods, molecular approaches, active and passive acoustics, the use of interconnected databases and citizen science. Whilst no one method is suitable for discovering or detecting all groups of organisms many are complementary and have been combined to give a more complete picture of biodiversity in marine ecosystems. We conclude that integrated approaches represent the best way forwards for accelerating species discovery, description and biodiversity assessment. Examples of integrated taxonomic approaches are identified from terrestrial ecosystems. Such integrated taxonomic approaches require the adoption of cybertaxonomy approaches and will be boosted by new autonomous sampling platforms and development of machine-speed exchange of digital information between databases.

Global phylogeography suggests extensive eucosmopolitanism in Mesopelagic Fishes (Maurolicus: Sternoptychidae).

Fishes in the mesopelagic zone (200-1000 m) have recently been highlighted for potential exploitation. Here we assess global phylogeography in Maurolicus, the Pearlsides, an ecologically important group. We obtained new sequences from mitochondrial COI and nuclear ITS-2 from multiple locations worldwide, representing 10 described species plus an unknown central South Pacific taxon. Phylogenetic analyses identified five geographically distinct groupings, three of which comprise multiple described species. Species delimitation analyses suggest these may represent four species. Maurolicus muelleri and M. australis are potentially a single species, although as no shared haplotypes are found between the two disjunct groups, we suggest maintenance of these as two species. Maurolicus australis is a predominantly southern hemisphere species found in the Pacific, Indian and southern South Atlantic Oceans, comprising five previously allopatric species. M. muelleri (previously two species) is distributed in the North Atlantic and Mediterranean Sea. Maurolicus weitzmani (previously two species) inhabits the eastern equatorial Atlantic, Gulf of Mexico and western North and South Atlantic. Maurolicus mucronatus is restricted to the Red Sea. No Maurolicus have previously been reported in the central South Pacific but we have identified a distinct lineage from this region, which forms a sister group to Maurolicus from the Red Sea.

Assessing Deep-Pelagic Shrimp Biomass to 3000 m in The Atlantic Ocean and Ramifications of Upscaled Global Biomass.

We assess the biomass of deep-pelagic shrimps in the Atlantic Ocean using data collected between 40°N and 40°S. Forty-eight stations were sampled in discrete-depth fashion, including epi- (0-200 m), meso- (200-800/1000 m), upper bathy- (800/1000-1500 m), and lower bathypelagic (1500-3000 m) strata. We compared samples collected from the same area on the same night using obliquely towed trawls and large vertically towed nets and found that shrimp catches from the latter were significantly higher. This suggests that vertical nets are more efficient for biomass assessments, and we report these values here. We further compared day and night samples from the same site and found that biomass estimates differed only in the epi- and mesopelagic strata, while estimates from the bathypelagic strata and the total water column were independent of time of day. Maximal shrimp standing stocks occurred in the upper bathypelagic (52-54% of total biomass) and in the mesopelagic (42-43%). We assessed shrimp biomass in three major regions of the Atlantic between 40°N and 40°S, and the first-order extrapolation of these data suggests that the global low-latitude deep-pelagic shrimp biomass (1700 million tons) may lie within the range reported for mesopelagic fishes (estimations between 1000 and 15000 million tons). These data, along with previous fish-biomass estimates, call for the reassessment of the quantity and distribution of nektonic carbon in the deep ocean.

Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment.

Deep-sea anglerfishes are relatively abundant and diverse, but their luminescent bacterial symbionts remain enigmatic. The genomes of two symbiont species have qualities common to vertically transmitted, host-dependent bacteria. However, a number of traits suggest that these symbionts may be environmentally acquired. To determine how anglerfish symbionts are transmitted, we analyzed bacteria-host codivergence across six diverse anglerfish genera. Most of the anglerfish species surveyed shared a common species of symbiont. Only one other symbiont species was found, which had a specific relationship with one anglerfish species, Cryptopsaras couesii. Host and symbiont phylogenies lacked congruence, and there was no statistical support for codivergence broadly. We also recovered symbiont-specific gene sequences from water collected near hosts, suggesting environmental persistence of symbionts. Based on these results we conclude that diverse anglerfishes share symbionts that are acquired from the environment, and that these bacteria have undergone extreme genome reduction although they are not vertically transmitted.

Characterization of the microbiome and bioluminescent symbionts across life stages of Ceratioid Anglerfishes of the Gulf of Mexico.

The interdependence of diverse organisms through symbiosis reaches even the deepest parts of the oceans. As part of the DEEPEND project (deependconsortium.org) research on deep Gulf of Mexico biodiversity, we profiled the bacterial communities ('microbiomes') and luminous symbionts of 36 specimens of adult and larval deep-sea anglerfishes of the suborder Ceratioidei using 16S rDNA. Transmission electron microscopy was used to characterize the location of symbionts in adult light organs (esca). Whole larval microbiomes, and adult skin and gut microbiomes, were dominated by bacteria in the genera Moritella and Pseudoalteromonas. 16S rDNA sequencing results from adult fishes corroborate the previously published identity of ceratioid bioluminescent symbionts and support the findings that these symbionts do not consistently exhibit host specificity at the host family level. Bioluminescent symbiont amplicon sequence variants were absent from larval ceratioid samples, but were found at all depths in the seawater, with a highest abundance found at mesopelagic depths. As adults spend the majority of their lives in the meso- and bathypelagic zones, the trend in symbiont abundance is consistent with their life history. These findings support the hypothesis that bioluminescent symbionts are not present throughout host development, and that ceratioids acquire their bioluminescent symbionts from the environment.

Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes.

Diverse marine fish and squid form symbiotic associations with extracellular bioluminescent bacteria. These symbionts are typically free-living bacteria with large genomes, but one known lineage of symbionts has undergone genomic reduction and evolution of host dependence. It is not known why distinct evolutionary trajectories have occurred among different luminous symbionts, and not all known lineages previously had genome sequences available. In order to better understand patterns of evolution across diverse bioluminescent symbionts, we de novo sequenced the genomes of bacteria from a poorly studied interaction, the extracellular symbionts from the "lures" of deep-sea ceratioid anglerfishes. Deep-sea anglerfish symbiont genomes are reduced in size by about 50% compared to free-living relatives. They show a striking convergence of genome reduction and loss of metabolic capabilities with a distinct lineage of obligately host-dependent luminous symbionts. These losses include reductions in amino acid synthesis pathways and abilities to utilize diverse sugars. However, the symbiont genomes have retained a number of categories of genes predicted to be useful only outside the host, such as those involved in chemotaxis and motility, suggesting that they may persist in the environment. These genomes contain very high numbers of pseudogenes and show massive expansions of transposable elements, with transposases accounting for 28 and 31% of coding sequences in the symbiont genomes. Transposon expansions appear to have occurred at different times in each symbiont lineage, indicating either independent evolutions of reduction or symbiont replacement. These results suggest ongoing genomic reduction in extracellular luminous symbionts that is facilitated by transposon proliferations.IMPORTANCE Many female deep-sea anglerfishes possess a "lure" containing luminous bacterial symbionts. Here we show that unlike most luminous symbionts, these bacteria are undergoing an evolutionary transition toward small genomes with limited metabolic capabilities. Comparative analyses of the symbiont genomes indicate that this transition is ongoing and facilitated by transposon expansions. This transition may have occurred independently in different symbiont lineages, although it is unclear why. Genomic reduction is common in bacteria that only live within host cells but less common in bacteria that, like anglerfish symbionts, live outside host cells. Since multiple evolutions of genomic reduction have occurred convergently in luminous bacteria, they make a useful system with which to understand patterns of genome evolution in extracellular symbionts. This work demonstrates that ecological factors other than an intracellular lifestyle can lead to dramatic gene loss and evolutionary changes and that transposon expansions may play important roles in this process.

Dining in the Deep: The Feeding Ecology of Deep-Sea Fishes.

Deep-sea fishes inhabit ∼75% of the biosphere and are a critical part of deep-sea food webs. Diet analysis and more recent trophic biomarker approaches, such as stable isotopes and fatty-acid profiles, have enabled the description of feeding guilds and an increased recognition of the vertical connectivity in food webs in a whole-water-column sense, including benthic-pelagic coupling. Ecosystem modeling requires data on feeding rates; the available estimates indicate that deep-sea fishes have lower per-individual feeding rates than coastal and epipelagic fishes, but the overall predation impact may be high. A limited number of studies have measured the vertical flux of carbon by mesopelagic fishes, which appears to be substantial. Anthropogenic activities are altering deep-sea ecosystems and their services, which are mediated by trophic interactions. We also summarize outstanding data gaps.