Environmental drivers of biogeography and community structure in a Mid-Atlantic estuary.

Estuaries include some of the most productive yet anthropogenically impacted marine ecosystems on the planet, and provide critical habitat to many ecologically and economically important marine species. In order to elucidate ecological function in estuaries, we must understand what factors drive community dynamics. Delaware Bay is the third largest estuary in the United States and hosts over 200 species of migrant and resident fishes and invertebrates. The Delaware Division of Fish and Wildlife has conducted two long-term trawl surveys at monthly intervals in Delaware Bay since 1966. The two surveys collect data on environmental conditions, species composition, and number of fishes and macroinvertebrates across different size classes and life histories. Using a suite of multivariate approaches including hierarchical cluster analysis, canonical correlation analysis, and permutational multivariate analysis of variance, we characterized the fish and macroinvertebrate community in Delaware Bay and found that community composition and environmental conditions varied across spatial and seasonal scales. We identified four distinct biogeographic regions, based on environmental conditions and community composition, which were consistent across surveys. We found that the community was driven primarily by gradients in temperature and salinity and that abundant, frequently occurring species in the Bay have well-defined environmental associations. Our work represents the first attempt to use an existing historical survey to better understand how environmental parameters influence diversity and distribution of macrofauna within Delaware Bay, providing insight into how abiotic variables, influenced by climate, may impact the Delaware Bay ecosystem and similar estuarine ecosystems worldwide.

An updated end-to-end ecosystem model of the Northern California Current reflecting ecosystem changes due to recent marine heatwaves.

The Northern California Current is a highly productive marine upwelling ecosystem that is economically and ecologically important. It is home to both commercially harvested species and those that are federally listed under the U.S. Endangered Species Act. Recently, there has been a global shift from single-species fisheries management to ecosystem-based fisheries management, which acknowledges that more complex dynamics can reverberate through a food web. Here, we have integrated new research into an end-to-end ecosystem model (i.e., physics to fisheries) using data from long-term ocean surveys, phytoplankton satellite imagery paired with a vertically generalized production model, a recently assembled diet database, fishery catch information, species distribution models, and existing literature. This spatially-explicit model includes 90 living and detrital functional groups ranging from phytoplankton, krill, and forage fish to salmon, seabirds, and marine mammals, and nine fisheries that occur off the coast of Washington, Oregon, and Northern California. This model was updated from previous regional models to account for more recent changes in the Northern California Current (e.g., increases in market squid and some gelatinous zooplankton such as pyrosomes and salps), to expand the previous domain to increase the spatial resolution, to include data from previously unincorporated surveys, and to add improved characterization of endangered species, such as Chinook salmon (Oncorhynchus tshawytscha) and southern resident killer whales (Orcinus orca). Our model is mass-balanced, ecologically plausible, without extinctions, and stable over 150-year simulations. Ammonium and nitrate availability, total primary production rates, and model-derived phytoplankton time series are within realistic ranges. As we move towards holistic ecosystem-based fisheries management, we must continue to openly and collaboratively integrate our disparate datasets and collective knowledge to solve the intricate problems we face. As a tool for future research, we provide the data and code to use our ecosystem model.

A multi-predator trophic database for the California Current Large Marine Ecosystem.

The California Current Trophic Database (CCTD) was developed at NOAA Southwest Fisheries Science Center in collaboration with numerous diet data contributors. We compiled the CCTD from twenty-four data sets, representing both systematic collections and directed trophic studies. Diet composition data, including stomach and scat samples, were obtained from 105,694 individual predators among 143 taxa collected throughout the California Current Large Marine Ecosystem (CCLME) from 1967-2019. Predator taxa consist of squids (n = 5), elasmobranchs (n = 13), bony fishes (n = 118), and marine mammals (n = 7). Extensive time series are available for some predators (e.g., California Sea Lion, Pacific Hake, Chinook Salmon). The CCTD represents the largest compilation of raw trophic data within the CCLME, allowing for more refined analyses and modeling studies within this region. Our intention is to further augment and periodically update the dataset as additional historical or contemporary data become available to increase its utility and impact.

Checklist of marine and estuarine fishes from the AlaskaYukon Border, Beaufort Sea, to Cabo San Lucas, Mexico.

This paper is a checklist of the fishes that have been documented, through both published and unpublished sources, in marine and estuarine waters, and out 200 miles, from the United States-Canadian border on the Beaufort Sea to Cabo San Lucas, Mexico. A minimum of 241 families and 1,644 species are known within this range, including both native and nonnative species. For each of these species, we include maximum size, geographic and depth ranges, whether it is native or nonnative, as well as a brief mention of any taxonomic issues.

Are stable isotope ratios suitable for describing niche partitioning and individual specialization?

As concerns about anthropogenic and natural disturbance grow, understanding animal resource use patterns has been increasingly prioritized to predict how changes in environmental conditions, food web structure, and population dynamics will affect biological resilience. Among the tools used to assess resource use, stable isotope analysis has proliferated in ecological studies, particularly in relation to describing intra- and interspecific variation in trophic interactions. Despite a growing need to disseminate scientific information, the inherent limitations of stable isotope ratios and inappropriate synonymizing of distinct evolutionary and ecological processes may mislead ecological inferences in natural systems. This situation necessitates a re-evaluation of the utility of stable isotope ratios to address certain ecological questions. Here, we assess the efficacy of stable isotope ratios to describe two fundamental ecological processes, niche partitioning and individual specialization. Investigation of these processes has increased substantially in accordance with increased access to stable isotope data. This article discusses the circumstances and approaches that are necessary to evaluate niche partitioning and individual specialization, and outlines key considerations for the associated application of stable isotope ratios.

Trophic ecology of yellowtail rockfish (Sebastes flavidus) during a marine heat wave off central California, USA.

The yellowtail rockfish, Sebastes flavidus, is a widespread and abundant mesopredator in the California Current Large Marine Ecosystem. We utilized stomach content and stable isotope analyses to investigate the trophic ecology of this species at three sites off central California just before (August-October 2013) and during (August and October 2014) a marine heat wave. Sebastes flavidus largely consumed pelagic prey (zooplankton and micronekton). Diets were dominated by tunicates (salps and pyrosomes), pelagic crustaceans (euphausiids, hyperid amphipods, larval decapods), and fishes, with the relative contribution of these prey taxa varying spatially (sample location, longitude, depth) and temporally (year, month), based on complementary multivariate analyses. Prey-specific indices demonstrated that individual S. flavidus diet composition typically was dominated by one of these prey groups, and that prey switching occurred based on the relative availability of prey and their energetic importance. Stable isotope analysis of δ15N indicated that the S. flavidus populations sampled in 2014 had been feeding at an elevated trophic position and more variable prey spectrum relative to 2013, probably as a consequence of greater piscivory and the incorporation of temporal changes in diet composition. Because its opportunistic feeding behavior reflects the dynamism and heterogeneity of the pelagic forage preyscape, S. flavidus may be an important ecosystem indicator species. For example, the novel incorporation of pyrosomes as a large portion of the diet of S. flavidus during 2013-2014 directly related to the massive increase in pyrosome abundance in the California Current during the 2014 marine heat wave.

Evaluation of muscle tissue as a non-lethal proxy for liver and brain organic contaminant loads in an elasmobranch, the Bonnethead Shark (Sphyrna tiburo).

Elasmobranch ecotoxicological investigations are complicated because accessing organs that accumulate organic contaminants is usually lethal. Several metrics among liver, muscle, and brain were evaluated to determine their relative organic contaminant loads and the efficacy of using muscle as a non-lethal proxy for liver. Liver contained the highest concentrations (368-4020 ng/g wet weigth [ww]) and greatest estimated total load of contaminants. Brain had higher toxin concentrations than muscle (4.18-84.2 ng/g ww versus 0.94-4.73 ng/g ww). Liver and brain were similar to each other in terms of contaminant detection occurrence and signature overlap, whereas muscle poorly reflected those of liver and brain. However, the identity of contaminants detected in muscle constituted those that substantially contributed to summed liver and brain concentrations. Thus, studies utilizing muscle as a non-lethal liver alternative to study organic contaminant exposure in elasmobranchs should craft questions with care, considering its limited ability to serve as an accurate proxy.

Fisheries interactions and the challenges for target and nontargeted take on shark conservation in the Mexican Pacific.

Sharks have been of great cultural and socioeconomic importance in Mexico since the late 19th century, when the first fisheries were prosecuted in the Gulf of California to export fins to China. Mexican shark and ray fisheries are classified mainly by the size of the fishing vessel and include small- (7.5-10m), medium- (10-27m), and large-sized (>27m) fisheries. All are multispecies fisheries that use longline or gillnet gear, with their relative productivity varying over time. Off the Pacific coast, early shark small size vessel fisheries in the Gulf of California were driven by the need for vitamin A from livers, especially during World War II. As this fishery declined, new shark fishing opportunities arose because of government support and the development of the medium-sized fishery, which was capable of farther offshore excursions. Shark meat became an important part of the diets of poor and impoverished citizens during the 1950s and 1960s. The establishment of a Mexican Exclusive Economic Zone in 1976 pushed foreign vessels from Asia out of Mexican waters and led to the development of the large-sized vessel fishery to exploit pelagic sharks in offshore waters. By the early 1980s, Mexico shark fisheries were among the most productive in the world; however, a national economic crisis reduced effort and landings until the late 1980s, when several new fisheries emerged. Landings from Pacific states fluctuated between ~13,000 and 24,000t (dressed weight) during 1987-2012 but expanded steadily thereafter because of government support and offshore fleet expansion. Shark fisheries landings from the Mexican Pacific are currently at their highest recorded levels, exceeding 31,000t; however, a lack of species-specific landings and life history information has precluded population assessments of targeted stocks. In addition, though several recent management measures have been enacted to protect Mexican shark and ray fishery resources, the enforcement of these regulations is severely lacking. Therefore, the long-term sustainability of current fishing levels is unknown but should engender concern based on anecdotal evidence of serial depletion among historical elasmobranch targets in the Mexican Pacific.

Co-aligned chondrocytes: Zonal morphological variation and structured arrangement of cell lacunae in tessellated cartilage.

In most vertebrates the embryonic cartilaginous skeleton is replaced by bone during development. During this process, cartilage cells (chondrocytes) mineralize the extracellular matrix and undergo apoptosis, giving way to bone cells (osteocytes). In contrast, sharks and rays (elasmobranchs) have cartilaginous skeletons throughout life, where only the surface mineralizes, forming a layer of tiles (tesserae). Elasmobranch chondrocytes, unlike those of other vertebrates, survive cartilage mineralization and are maintained alive in spaces (lacunae) within tesserae. However, the functions of the chondrocytes in the mineralized tissue remain unknown. Applying a custom analysis workflow to high-resolution synchrotron microCT scans of tesserae, we characterize the morphologies and arrangements of stingray chondrocyte lacunae, using lacunar morphology as a proxy for chondrocyte morphology. We show that the cell density is comparable in unmineralized and mineralized tissue and that cells maintain similar volume even when they have been incorporated into tesserae. Our findings support previous hypotheses that elasmobranch chondrocytes, unlike those of other taxa, do not proliferate, hypertrophy or undergo apoptosis during mineralization. Tessera lacunae show zonal variation in their shapes, being flatter further from and more spherical closer to the unmineralized cartilage matrix, and larger in the center of tesserae. The lacunae show pronounced organization into parallel layers and strong orientation toward neighboring tesserae. Tesserae also exhibit local variation in lacunar density, with the density considerably higher near pores passing through the tesseral layer, suggesting pores and cells interact, and that pores may contain a nutrient source. We propose that the different lacunar types reflect the stages of the tesserae formation process, while also representing local variation in tissue architecture and cell function. Lacunae are linked by small passages (canaliculi) in the matrix to form elongated series at the tesseral periphery and tight clusters in the center of tesserae, creating a rich connectivity among cells. The network arrangement and the shape variation of chondrocytes in tesserae indicate that cells may interact within and between tesserae and manage mineralization differently from chondrocytes in other vertebrates, perhaps performing analogous roles to osteocytes in bone.

Mechanical properties of stingray tesserae: High-resolution correlative analysis of mineral density and indentation moduli in tessellated cartilage.

Skeletal tissues are built and shaped through complex, interacting active and passive processes. These spatial and temporal variabilities make interpreting growth mechanisms from morphology difficult, particularly in bone, where the remodeling process erases and rewrites local structural records of growth throughout life. In contrast to the majority of bony vertebrates, the elasmobranch fishes (sharks, rays, and their relatives) have skeletons made of cartilage, reinforced by an outer layer of mineralized tiles (tesserae), which are believed to grow only by deposition, without remodeling. We exploit this structural permanence, performing the first fine-scale correlation of structure and material properties in an elasmobranch skeleton. Our characterization across an age series of stingray tesserae allows unique insight into the growth processes and mechanical influences shaping the skeleton. Correlated quantitative backscattered electron imaging (qBEI) and nanoindentation measurements show a positive relationship between mineral density and tissue stiffness/hardness. Although tessellated cartilage as a whole (tesserae plus unmineralized cartilage) is considerably less dense than bone, we demonstrate that tesserae have exceptional local material properties, exceeding those of (mammal) bone and calcified cartilage. We show that the finescale ultrastructures recently described in tesserae have characteristic material properties suggesting distinct mechanical roles and that regions of high mineral density/stiffness in tesserae are confined predominantly to regions expected to bear high loads. In particular, tesseral spokes (laminated structures flanking joints) exhibit particularly high mineral densities and tissue material properties, more akin to teeth than bone or calcified cartilage. We conclude that these spokes toughen tesserae and reinforce points of contact between them. These toughening and reinforcing functions are supported by finite element simulations incorporating our material data. The high stresses predicted for spokes, and evidence we provide that new spoke laminae are deposited according to their local mechanical environment, suggest tessellated cartilage is both mutable and responsive, despite lacking remodeling capability. STATEMENT OF SIGNIFICANCE: The study of vertebrate skeletal materials is heavily biased toward mammal bone, despite evidence that bone and cartilage are extremely diverse. We broaden the perspective on vertebrate skeleton materials and evolution in an investigation of stingray tessellated cartilage, a curious type of unmineralized cartilage with a shell of mineralized tiles (tesserae). Combining high-resolution imaging and material testing, we demonstrate that tesserae have impressive local material properties for a vertebrate skeletal tissue, arguing for unique tissue organization relative to mammalian calcified cartilage and bone. Incorporating our materials data into mechanical models, we show that finescale material arrangements allow this cartilage to act as a functional and responsive alternative to bone, despite lacking bone's ability to remodel. These results are relevant to a diversity of researchers, from skeletal, developmental, and evolutionary biologists, to materials scientists interested in high-performance, low-density composites.

Large batoid fishes frequently consume stingrays despite skeletal damage.

The shapes of vertebrate teeth are often used as hallmarks of diet. Here, however, we demonstrate evidence of frequent piscivory by cartilaginous fishes with pebble-like teeth that are typically associated with durophagy, the eating of hard-shelled prey. High-resolution micro-computed tomography observation of a jaw specimen from one batoid species and visual investigation of those of two additional species reveal large numbers of embedded stingray spines, arguing that stingray predation of a scale rivalling that of the largest carnivorous sharks may not be uncommon for large, predatory batoids with rounded, non-cutting dentition. Our observations demonstrate that tooth morphology is not always a reliable indicator of diet and that stingray spines are not as potent a deterrent to predation as normally believed. In addition, we show that several spines in close contact with the jaw skeleton of a wedgefish (Rhynchobatus) have become encased in a disorganized mineralized tissue with a distinctive ultrastructure, the first natural and unequivocal evidence of a callus-building response in the tessellated cartilage unique to elasmobranch skeletons. Our findings reveal sampling and analysis biases in vertebrate ecology, especially with regard to the role of large, predatory species, while also illustrating that large body size may provide an escape from anatomical constraints on diet (e.g. gape size, specialist dentition). Our observations inform our concepts of skeletal biology and evolution in showing that tessellated cartilage-an ancient alternative to bone-is incapable of foreign tissue resorption or of restoring damaged skeletal tissue to its original state, and attest to the value of museum and skeletal specimens as records of important aspects of animal life history.

Diet Composition and Trophic Ecology of Northeast Pacific Ocean Sharks.

Although there is a general perception of sharks as large pelagic, apex predators, most sharks are smaller, meso- and upper-trophic level predators that are associated with the seafloor. Among 73 shark species documented in the eastern North Pacific (ENP), less than half reach maximum lengths >200cm, and 78% occur in demersal or benthic regions of the continental shelf or slope. Most small (≤200cm) species (e.g., houndsharks) and demersal, nearshore juveniles of larger species (e.g., requiem sharks) consume small teleosts and decapod crustaceans, whereas large species in pelagic coastal and oceanic environments feed on large teleosts and squids. Several large, pelagic apex predator species occur in the ENP, but the largest species (i.e., Basking Shark, Whale Shark) consume zooplankton or small nekton. Size-based dietary variability is substantial for many species, and segregation of juvenile and adult foraging habitats also is common (e.g., Horn Shark, Shortfin Mako). Temporal dietary differences are most pronounced for temperate, nearshore species with wide size ranges, and least pronounced for smaller species in extreme latitudes and deep-water regions. Sympatric sharks often occupy various trophic positions, with resource overlap differing by space and time and some sharks serving as prey to other species. Most coastal species remain in the same general region over time and feed opportunistically on variable prey inputs (e.g., season migrations, spawning, or recruitment events), whereas pelagic, oceanic species actively seek hot spots of prey abundance that are spatiotemporally variable. The influence of sharks on ecosystem structure and regulation has been downplayed compared to that of large teleosts species with higher per capita consumption rates (e.g., tunas, billfishes). However, sharks also exert indirect influences on prey populations by causing behavioural changes that may result in restricted ranges and reduced fitness. Except for food web modelling efforts in Alaskan waters, the trophic impacts of sharks are poorly incorporated into current ecosystem approaches to fisheries management in the NEP.

Spatial segregation in eastern North Pacific skate assemblages.

Skates (Rajiformes: Rajoidei) are common mesopredators in marine benthic communities. The spatial associations of individual species and the structure of assemblages are of considerable importance for effective monitoring and management of exploited skate populations. This study investigated the spatial associations of eastern North Pacific (ENP) skates in continental shelf and upper continental slope waters of two regions: central California and the western Gulf of Alaska. Long-term survey data were analyzed using GIS/spatial analysis techniques and regression models to determine distribution (by depth, temperature, and latitude/longitude) and relative abundance of the dominant species in each region. Submersible video data were incorporated for California to facilitate habitat association analysis. We addressed three main questions: 1) Are there regions of differential importance to skates?, 2) Are ENP skate assemblages spatially segregated?, and 3) When skates co-occur, do they differ in size? Skate populations were highly clustered in both regions, on scales of 10s of kilometers; however, high-density regions (i.e., hot spots) were segregated among species. Skate densities and frequencies of occurrence were substantially lower in Alaska as compared to California. Although skates are generally found on soft sediment habitats, Raja rhina exhibited the strongest association with mixed substrates, and R. stellulata catches were greatest on rocky reefs. Size segregation was evident in regions where species overlapped substantially in geographic and depth distribution (e.g., R. rhina and Bathyraja kincaidii off California; B. aleutica and B. interrupta in the Gulf of Alaska). Spatial niche differentiation in skates appears to be more pronounced than previously reported.

Bottles as models: predicting the effects of varying swimming speed and morphology on size selectivity and filtering efficiency in fishes.

We created physical models based on the morphology of ram suspension-feeding fishes to better understand the roles morphology and swimming speed play in particle retention, size selectivity and filtration efficiency during feeding events. We varied the buccal length, flow speed and architecture of the gills slits, including the number, size, orientation and pore size/permeability, in our models. Models were placed in a recirculating flow tank with slightly negatively buoyant plankton-like particles (~20-2000 µm) collected at the simulated esophagus and gill rakers to locate the highest density of particle accumulation. Particles were captured through sieve filtration, direct interception and inertial impaction. Changing the number of gill slits resulted in a change in the filtration mechanism of particles from a bimodal filter, with very small (≤ 50 µm) and very large (>1000 µm) particles collected, to a filter that captured medium-sized particles (101-1000 µm). The number of particles collected on the gill rakers increased with flow speed and skewed the size distribution towards smaller particles (51-500 µm). Small pore sizes (105 and 200 µm mesh size) had the highest filtration efficiencies, presumably because sieve filtration played a significant role. We used our model to make predictions about the filtering capacity and efficiency of neonatal whale sharks. These results suggest that the filtration mechanics of suspension feeding are closely linked to an animal's swimming speed and the structural design of the buccal cavity and gill slits.

The evolution of cranial design, diet, and feeding mechanisms in batoid fishes.

The batoid fishes (electric rays, sawfishes, skates, guitarfishes, and stingrays) are a trophically and morphologically diverse clade in which the observed range of diets is a product of a feeding mechanism with few parts and therefore a limited number of functional interactions. This system allows an intriguing comparison to the complex network of associations in the feeding apparatus of bony fishes and an anatomically simple framework for investigations of the mechanisms underlying the evolution of functional and phenotypic diversity. We quantified morphology from reconstructed CT scans of 40 batoid species, representing more than half of the extant genera. We used pairwise comparisons to evaluate the extent of coevolution among components of the feeding apparatus and among morphologies and diets. These relationships were then used to predict diets in poorly studied taxa and in a reconstruction of the batoid ancestor. Although functionally there are fewer examples of convergence in the batoid feeding mechanism than in bony fishes, our data show multiple evolutions of similar dietary compositions underlain by a broad morphological diversity. Elements of the feeding apparatus evolved independently of one another, suggesting that decoupling components of the head skeleton created separate but interacting evolutionary modules that allowed trophic diversification. Our data imply that food habits exhibit strong independent and convergent evolution and that suites of morphologies are associated with certain diets; however, lack of behavioral data for this clade, and one example of divergent diets underlain by convergent morphology, caution against the assumption of simplistic relationships between form and function. We therefore urge future work to ground truth our study by testing the functional, dietary and evolutionary hypotheses suggested by our data.