Ecotoxicological Assessment of Microplastics and Cellulose Particles in the Galápagos Islands and Galápagos Penguin Food Web.

Microplastic pollution threatens some of the world's most iconic locations for marine biodiversity, including the remote Galápagos Islands, Ecuador. Using the Galápagos penguin (Spheniscus mendiculus) as a sentinel species, the present study assessed microplastics and suspected anthropogenic cellulose concentrations in surface seawater and zooplankton near Santa Cruz and Galápagos penguin colonies (Floreana, Isabela, Santiago), as well as in penguin potential prey (anchovies, mullets, milkfish) and penguin scat. On average, 0.40 ± 0.32 microplastics L-1 were found in surface seawater (<10 µm; n = 63 L), while 0.003, 0.27, and 5.12 microplastics individual-1 were found in zooplankton (n = 3372), anchovies (n = 11), and mullets (n = 6), respectively. The highest concentration (27 microplastics individual-1) was observed in a single milkfish. Calculations based on microplastics per gram of prey, in a potential diet composition scenario, suggest that the Galápagos penguin may consume 2881 to 9602 microplastics daily from prey. Despite this, no microplastics or cellulose were identified in 3.40 g of guano collected from two penguins. Our study confirms microplastic exposure in the pelagic food web and endangered penguin species within the UNESCO World Heritage site Galápagos Islands, which can be used to inform regional and international policies to mitigate plastic pollution and conserve biodiversity in the global ocean. Environ Toxicol Chem 2024;00:1-16. © 2024 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Data-driven determination of zooplankton bioregions and robustness analysis.

Identifying biogeographic regions through cluster analysis of species distribution data is a common method for partitioning ecosystems. Selecting the appropriate cluster analysis method requires a comparison of multiple algorithms. In this study, we demonstrate a data-driven process to select a method for bioregionalization based on community data and test its robustness to data variability following these steps: •We aggregated and curated zooplankton community observations from expeditions in the Northeast Pacific.•We determined the best bioregionalization approach by comparing nine cluster analysis methods using ten goodness of clustering indices.•We evaluated the robustness of the bioregionalization to different sources of sampling and taxonomic variability by comparing the bioregionalization of the overall dataset with bioregionalizations of subsets of the data. The K-means clustering of the log-chord transformed abundance was selected as the optimal method for bioregionalization of the zooplankton dataset. This clustering resulted in the emergence of four bioregions along the cross-shelf gradient: the Offshore, Deep Shelf, Nearshore, and Deep Fjord bioregions. The robustness analyses demonstrated that the bioregionalization was consistent despite variability in the spatial and temporal frequency of sampling, sampling methodology, and taxonomic coverage.

Distinct trophic ecologies of zooplankton size classes are maintained throughout the seasonal cycle.

Marine food webs are strongly size-structured and size-based analysis of communities is a useful approach to evaluate food webs in a way that can be compared across systems. Fatty acid analysis is commonly used to identify diet sources of species, offering a powerful complement to stable isotopes, but is rarely applied to size-structured communities. In this study, we used fatty acids and stable isotopes to characterize size-based variation in prey resources and trophic pathways over a nine-month temperate coastal ocean time series of seven plankton size classes, from > 0.7-µm particulate organic matter through > 2000-µm zooplankton. Zooplankton size classes were generally distinguishable by their dietary fatty acids, while stable isotopes revealed more seasonal variability. Fatty acids of zooplankton were correlated with those of their prey (particulate organic matter and smaller zooplankton) and identified trophic pathways, including widespread ties to the microbial food web. Diatom fatty acids also contributed to zooplankton but fall blooms were more important than spring. Concurrent isotope-based trophic position estimates and fatty acid markers of carnivory showed that some indicators (18:1ω9/18:1ω7) are not consistent across size classes, while others (DHA:EPA) are relatively reliable. Both analysis methods provided distinct information to build a more robust understanding of resource use. For example, fatty acid markers showed that trophic position was likely underestimated in 250-µm zooplankton, probably due to their consumption of protists with low isotopic fractionation factors. Applying fatty acid analysis to a size-structured framework provides more insight into trophic pathways than isotopes alone.

Future climate change-related decreases in food quality may affect juvenile Chinook salmon growth and survival.

Global climate change is projected to raise global temperatures by 3.3-5.7 °C by 2100, resulting in changes in species composition, abundance, and nutritional quality of organisms at the base of the marine food web. Predicted increases in prey availability and reductions in prey nutritional quality under climate warming in certain marine systems are expected to impact higher trophic levels, such as fish and humans. There is limited knowledge of the interplay between food quantity and quality under warming, specifically when food availability is high, but quality is low. Here, we conducted an experiment assessing the effects of food quality (fatty acid composition and ratios) on juvenile Chinook salmon's (Oncorhynchus tshawytscha) body and nutritional condition, specifically focusing on RNA:DNA ratio, Fulton's K, growth, mortality and their fatty acid composition. Experimental diets represented three different climate change scenarios with 1) a present-day diet (Euphausia pacifica), 2) a control diet (commercial aquaculture diet), and 3) a predicted Intergovernmental Panel on Climate Change (IPCC) worst-case scenario diet with low essential fatty acid concentrations (IPCC SSP5-8.5). We tested how growth rates, RNA:DNA ratio, Fulton's K index, fatty acid composition and mortality rates in juvenile Chinook salmon compared across diet treatments. Fatty acids were incorporated into the salmon muscle at varying rates but, on average, reflected dietary concentrations. High dietary concentrations of DHA, EPA and high DHA:EPA ratios, under the control and present-day diets, increased fish growth and condition. In contrast, low concentrations of DHA and EPA and low DHA:EPA ratios in the diets under climate change scenario were not compensated for by increased food quantity. This result highlights the importance of considering food quality when assessing fish response to changing ocean conditions.

Divergent RNA viruses infecting sea lice, major ectoparasites of fish.

Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order Mononegavirales, nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice (Lepeophtheirus salmonis, Caligus clemensi, and Caligus rogercresseyi) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in C. rogercresseyi. Our analyses showed that most of the viruses found in C. rogercresseyi occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms.

Seasonal variation in the lipid content of Fraser River Chinook Salmon (Oncorhynchus tshawytscha) and its implications for Southern Resident Killer Whale (Orcinus orca) prey quality.

In Southern British Columbia (BC), Canada, declines in southern resident killer whale (SRKW-Orcinus orca) populations have been linked to declines in numbers and average size of their preferred prey, Chinook salmon (Oncorhynchus tshawytscha). However, the life history diversity of Chinook suggests that there is a need to assess stock-specific differences in energy density to evaluate prey quality as a factor in SRKW declines. In this study, we calibrated a Distell fat meter to estimate Chinook whole-body lipid content, a proxy for energy density. The fat meter was deployed at the Fraser River, BC, Chinook test fishery during 2020, collecting lipid, weight, and length measurements from 1566 genetically stock identified individuals encompassing all major Fraser River Chinook population units (management units, MUs) at river entry. We found that MU-specific lipid content increased with distance and elevation to spawning grounds and was highest in the Spring-52 (12.8%) and Summer-52 (12.7%) MUs, intermediate in the Summer-41 MU (10.8%), and lowest in the Fall-41 MU (7.3%). Lipid content also decreased by up to 6 percentage points within MUs from the beginning to end of their migration period. Our data revealed SRKWs' most endangered prey sources, the Spring-52 and Summer-52 MUs, are also its most energy rich. It also indicated SRKWs have access to progressively lower energy density Chinook through the year, requiring up to ~ 30% more fish to meet energy demands in the fall than in the spring.

Air exposure moderates ocean acidification effects during embryonic development of intertidally spawning fish.

Ocean acidification can negatively impact the early life-stages of marine fish, due to energetic costs incurred by the maintenance of acid-base homeostasis, leaving less energy available for growth and development. The embryos of intertidally spawning fishes, such as Pacific herring, are often air exposed for hours. We hypothesized that air exposure would be beneficial to the developing embryo due to a higher oxygen availability (and thus reduced metabolic costs to secure adequate oxygen) and permitting excess CO2 associated with ocean acidification to be off-gassed during emersion. To investigate this, we reared Pacific herring (Clupea pallasii) embryos under three tidal regimes (subtidal: fully immersed, low intertidal: 2 × 2 h air exposure, and high intertidal: 5 + 9 h air exposure) fully crossed with three aquatic CO2 levels (400, 1500 and 3200 µatm) at a water temperature of 9.5 °C and naturally fluctuating air temperature during air exposure. We measured the effects on embryonic development and hatch, as well as carry-over effects on larval development and survival. Air exposure during embryonic development had significant positive effects on growth, condition and survival in larval Pacific herring, with some interactive effects with CO2. Interestingly, CO2 by itself in the fully immersed treatment had no effect, but had significant interactions with air exposure. Our research suggests that air exposure during low tide can be highly beneficial to intertidally spawning fishes and needs to be taken into account in climate change studies and modeling.

Differential response of distinct copepod life history types to spring environmental forcing in Rivers Inlet, British Columbia, Canada.

The temporal dynamics of five copepod species common to coastal waters of the Pacific Northwest were examined in relation to variability in spring temperature and phytoplankton dynamics in 2008, 2009, and 2010 in Rivers Inlet, British Columbia, Canada. The five species were differentiated by life history strategies. Acartia longiremis, Metridia pacifica, and Paraeuchaeta elongata remained active over most of the year. By contrast, the reproductive effort of Eucalanus bungii and Calanus marshallae was concentrated over the spring period and they spent most of the year in diapause as C5 copepodites. A delay in the timing of the spring bloom was associated with a shift in the phenology of all species. However, following the delay in spring bloom timing, recruitment to the G1 cohort was reduced only for E. bungii and C. marshallae. Recruitment successes of E. bungii and C. marshallae was also drastically reduced in 2010, an El Niño year, when spring temperatures were highest. Reasons for the observed differential response to spring environmental forcing, and its effect on upper trophic levels, are discussed.

Experimentally derived trophic enrichment and discrimination factors for Chinook salmon, Oncorhynchus tshawytscha.

RATIONALE: Stable isotope analysis (SIA) can provide important insights into food web structure and is a widely used tool in ecological conservation and management. It has recently been augmented by compound-specific stable isotope analysis of amino acids (CSIA-AA), an innovation that can provide greater precision when analyzing trophic level and food web connectivity. The utility of SIA rests on confidence in its constituent parameters such as the trophic enrichment factor (TEF). There is increasing emphasis on the need to experimentally derive species and tissue specific TEFs for studies utilizing SIA. Chinook salmon, Oncorhynchus tshawytscha, is a species with high potential for study using SIA due to the difficulty in observing its ecology during its marine phase and the significance of the conservation consequences of recent population declines. METHODS: Bulk and amino acid-specific TEFs were determined for juvenile and adult Chinook salmon fed specific diets. Three controlled feeding studies were performed: adult salmon were fed a biofeed, juvenile salmon were fed a biofeed, and juvenile salmon were fed krill. Bulk and compound-specific stable isotope data were collected from diet samples and from salmon muscle tissue after a minimum of 8 weeks of controlled feeding. Bulk isotope signatures were measured using EA-IRMS and CSIA-AA signatures using GC/C-IRMS, allowing the TEFs to be calculated. RESULTS: The bulk isotope TEFs were higher than those predicted for similar marine organisms and averaged 3.5‰ for ∆15 N and 1.3‰ for ∆13 C. The TEFs derived for nitrogen isotopes of amino acids were in line with expectations for this approach: the mean value for ∆15 NGlu - ∆15 NPhe was 7.06‰ and, using a multi-AA approach, the value for ∆15 NTrophic - ∆15 NSource was 6.67‰. For carbon isotopes of amino acids, the derived TEFs of Iso, Leu and Phe were near 0‰, as was that of Met, supporting their use of as source amino acids in future CSIA studies. CONCLUSIONS: This study presents Chinook salmon-specific TEFs for bulk and amino acid SIA. It supports the application of future research applying SIA to the study of Chinook salmon and validates previous research on species-specific TEFs.

Using stable isotopes to infer stock-specific high-seas distribution of maturing sockeye salmon in the North Pacific.

The stock-specific distribution of maturing salmon in the North Pacific has been a persistent information gap that has prevented us from determining the ocean conditions experienced by individual stocks. This continues to impede understanding of the role of ocean conditions in stock-specific population dynamics. We assessed scale archives for 17 sockeye salmon (Oncorhynchus nerka) stocks covering the entire North Pacific, from the Columbia River (Washington State and British Columbia) to Kamchatka Peninsula (Russia), to infer salmon locations during their last growing season before returning to their spawning grounds. The approach used, first pioneered in salmon stocks in the Atlantic, relies on the relationship between temporal changes in δ13C in salmon scales and sea surface temperature to estimate salmon distribution based on correlation strength. An advantage of this approach is that it does not require fish sampling at sea, but relies on existing fishery agency collections of salmon scales. Significant correlations were found for 7 of the stocks allowing us to propose plausible feeding grounds. Complementary information from δ15N, historical tagging studies, and connectivity analysis were used to further refine distribution estimates. This study is a first step toward estimating stock-specific distributions of salmon in the North Pacific and provides a basis for the application of the approach to other salmon scale archives. This information has the potential to improve our ability to relate stock dynamics to ocean conditions, ultimately enabling improved stock management. For example, our estimated distributions of Bristol Bay and NE Pacific stocks demonstrated that they occupy different areas with a number of the former being distributed in the high productivity shelf waters of the Aleutian Islands and Bering Sea. This may explain why these stocks seem to have responded differently to changes in ocean conditions, and the long-term trend of increased productivity of Bristol Bay sockeye.

A salmon diet database for the North Pacific Ocean.

The North Pacific Marine Salmon Diet Database is an open-access relational database built to centralize and make accessible salmon diet data through a standardized database structure. The initial data contribution contains 21,862 observations of salmon diet, and associated salmon biological parameters, prey biological parameters, and environmental data from the North Pacific Ocean. The data come from 907 unique spatial areas and mostly fall within two time periods, 1959-1969 and 1987-1997, during which there are more data available compared to other time periods. Data were extracted from 62 sources identified through a systematic literature review, targeting peer-reviewed and gray literature. The purpose of this database is to consolidate data into a common format to address gaps in our ecological understanding of the North Pacific Ocean, particularly with respect to salmon. This database can be used to address a variety of questions regarding salmon foraging, productivity, and marine survival. The North Pacific Marine Salmon Diet Database will continue to grow in the future as more data are digitized and become available.

Integrating fish scale and bone isotopic compositions for 'deep time' retrospective studies.

Isotopic studies of archived fish scales have tremendous potential to develop long-term retrospectives that provide important insights into how humans have altered aquatic ecosystems. However, fish specimens in museum archives and other repositories typically date to time periods when the impacts of industrial societies may have already caused profound environmental changes. Archaeological fish bones offer an opportunity to bridge this key temporal gap by providing samples spanning from the recent past to as far back as the Pleistocene. Collagen is the primary protein component of both fish scale and bone, but the comparability of isotopic compositions from these tissues has not been established experimentally. To lay the framework for integrating isotopic datasets from these tissues, we compare δ13C and δ15N of bone and scale collagen, as well as other tissues, from fish with life-time controlled diets. Results show that while there is no difference in δ13C between scale and bone collagen, there may be a very slight but meaningful inter-tissue offset in δ15N (<0.3‰). We discuss potential sources of δ15N variation in scale and bone collagen measurements. Because there is no difference in scale and bone δ13C, and the observed offset in δ15N is very small (less than analytical uncertainty in many studies), our findings demonstrate that collagen isotopic compositions from these tissues should be directly comparable when integrating datasets from modern and ancient samples to build more powerful, millennium-scale isotopic times series. In linking isotopic compositions of collagen from modern, historical (scales), and archaeological (bones) fish, our findings open the way for more nuanced contextualization of how ecosystems functioned prior to large-scale exploitation and how they have responded to mounting anthropogenic pressures in the intervening centuries.

Physiological resilience of pink salmon to naturally occurring ocean acidification.

Pacific salmon stocks are in decline with climate change named as a contributing factor. The North Pacific coast of British Columbia is characterized by strong temporal and spatial heterogeneity in ocean conditions with upwelling events elevating CO2 levels up to 10-fold those of pre-industrial global averages. Early life stages of pink salmon have been shown to be affected by these CO2 levels, and juveniles naturally migrate through regions of high CO2 during the energetically costly phase of smoltification. To investigate the physiological response of out-migrating wild juvenile pink salmon to these naturally occurring elevated CO2 levels, we captured fish in Georgia Strait, British Columbia and transported them to a marine lab (Hakai Institute, Quadra Island) where fish were exposed to one of three CO2 levels (850, 1500 and 2000 µatm CO2) for 2 weeks. At ½, 1 and 2 weeks of exposure, we measured their weight and length to calculate condition factor (Fulton's K), as well as haematocrit and plasma [Cl-]. At each of these times, two additional stressors were imposed (hypoxia and temperature) to provide further insight into their physiological condition. Juvenile pink salmon were largely robust to elevated CO2 concentrations up to 2000 µatm CO2, with no mortality or change in condition factor over the 2-week exposure duration. After 1 week of exposure, temperature and hypoxia tolerance were significantly reduced in high CO2, an effect that did not persist to 2 weeks of exposure. Haematocrit was increased by 20% after 2 weeks in the CO2 treatments relative to the initial measurements, while plasma [Cl-] was not significantly different. Taken together, these data indicate that juvenile pink salmon are quite resilient to naturally occurring high CO2 levels during their ocean outmigration.

Seasonal and spatial dynamics of the planktonic trophic biomarkers in the Strait of Georgia (northeast Pacific) and implications for fish.

Fish growth and survival are largely determined by the nutritional quality of their food, and the fish that grow quickly during early life stages are more likely to reproduce. To adequately estimate the quality of the prey for fish, it is necessary to understand the trophic links at the base of the food-web. Trophic biomarkers (e.g., stable isotopes and fatty acids) are particularly useful to discriminate and quantify food-web relationships. We explored the connections between plankton food-web components, and the seasonal and spatial dynamics of the trophic biomarkers and how this determines the availability of high-quality prey for juvenile Pacific salmon and Pacific herring in the Strait of Georgia, Canada. We demonstrate that the plankton food-web in the region is largely supported by diatom and flagellate production. We also show that spatial differences in terms of energy transfer efficiency exist in the region. Further, we found that the fatty acid composition of the zooplankton varied seasonally, matching a shift from diatom dominated production in the spring to flagellate dominated production in the summer. This seasonal shift conferred a higher nutritional value to zooplankton in the summer, indicating better quality prey for juvenile salmon and herring during this period.

Differentiating salmonid migratory ecotypes through stable isotope analysis of collagen: Archaeological and ecological applications.

The ability to distinguish between different migratory behaviours (e.g., anadromy and potamodromy) in fish can provide important insights into the ecology, evolution, and conservation of many aquatic species. We present a simple stable carbon isotope (δ13C) approach for distinguishing between sockeye (anadromous ocean migrants) and kokanee (potamodromous freshwater residents), two migratory ecotypes of Oncorhynchus nerka (Salmonidae) that is applicable throughout most of their range across coastal regions of the North Pacific Ocean. Analyses of kokanee (n = 239) and sockeye (n = 417) from 87 sites spanning the North Pacific (Russia to California) show that anadromous and potamodromous ecotypes are broadly distinguishable on the basis of the δ13C values of their scale and bone collagen. We present three case studies demonstrating how this approach can address questions in archaeology, archival, and conservation research. Relative to conventional methods for determining migratory status, which typically apply chemical analyses to otoliths or involve genetic analyses of tissues, the δ13C approach outlined here has the benefit of being non-lethal (when applied to scales), cost-effective, widely available commercially, and should be much more broadly accessible for addressing archaeological questions since the recovery of otoliths at archaeological sites is rare.

Anthropogenic disturbance homogenizes seagrass fish communities.

Anthropogenic activities have led to the biotic homogenization of many ecological communities, yet in coastal systems this phenomenon remains understudied. In particular, activities that locally affect marine habitat-forming foundation species may perturb habitat and promote species with generalist, opportunistic traits, in turn affecting spatial patterns of biodiversity. Here, we quantified fish diversity in seagrass communities across 89 sites spanning 6° latitude along the Pacific coast of Canada, to test the hypothesis that anthropogenic disturbances homogenize (i.e., lower beta-diversity) assemblages within coastal ecosystems. We test for patterns of biotic homogenization at sites within different anthropogenic disturbance categories (low, medium, and high) at two spatial scales (within and across regions) using both abundance- and incidence-based beta-diversity metrics. Our models provide clear evidence that fish communities in high anthropogenic disturbance seagrass areas are homogenized relative to those in low disturbance areas. These results were consistent across within-region comparisons using abundance- and incidence-based measures of beta-diversity, and in across-region comparisons using incidence-based measures. Physical and biotic characteristics of seagrass meadows also influenced fish beta-diversity. Biotic habitat characteristics including seagrass biomass and shoot density were more differentiated among high disturbance sites, potentially indicative of a perturbed environment. Indicator species and trait analyses revealed fishes associated with low disturbance sites had characteristics including stenotopy, lower swimming ability, and egg guarding behavior. Our study is the first to show biotic homogenization of fishes across seagrass meadows within areas of relatively high human impact. These results support the importance of targeting conservation efforts in low anthropogenic disturbance areas across land- and seascapes, as well as managing anthropogenic impacts in high activity areas.

The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill.

A dominant Antarctic ecological paradigm suggests that winter sea ice is generally the main feeding ground for krill larvae. Observations from our winter cruise to the southwest Atlantic sector of the Southern Ocean contradict this view and present the first evidence that the pack-ice zone is a food-poor habitat for larval development. In contrast, the more open marginal ice zone provides a more favourable food environment for high larval krill growth rates. We found that complex under-ice habitats are, however, vital for larval krill when water column productivity is limited by light, by providing structures that offer protection from predators and to collect organic material released from the ice. The larvae feed on this sparse ice-associated food during the day. After sunset, they migrate into the water below the ice (upper 20 m) and drift away from the ice areas where they have previously fed. Model analyses indicate that this behaviour increases both food uptake in a patchy food environment and the likelihood of overwinter transport to areas where feeding conditions are more favourable in spring.

Nutrients and Other Environmental Factors Influence Virus Abundances across Oxic and Hypoxic Marine Environments.

Virus particles are highly abundant in seawater and, on average, outnumber microbial cells approximately 10-fold at the surface and 16-fold in deeper waters; yet, this relationship varies across environments. Here, we examine the influence of a suite of environmental variables, including nutrient concentrations, salinity and temperature, on the relationship between the abundances of viruses and prokaryotes over a broad range of spatial and temporal scales, including along a track from the Northwest Atlantic to the Northeast Pacific via the Arctic Ocean, and in the coastal waters of British Columbia, Canada. Models of varying complexity were tested and compared for best fit with the Akaike Information Criterion, and revealed that nitrogen and phosphorus concentrations, as well as prokaryote abundances, either individually or combined, had significant effects on viral abundances in all but hypoxic environments, which were only explained by a combination of physical and chemical factors. Nonetheless, multivariate models of environmental variables showed high explanatory power, matching or surpassing that of prokaryote abundance alone. Incorporating both environmental variables and prokaryote abundances into multivariate models significantly improved the explanatory power of the models, except in hypoxic environments. These findings demonstrate that environmental factors could be as important as, or even more important than, prokaryote abundance in describing viral abundance across wide-ranging marine environments.