Robert K. Cowen’s research while affiliated with Oregon State University and other places
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Doliolids have a unique ability to impact the marine microbial community through bloom events and filter feeding. Their predation on large eukaryotic microorganisms is established and evidence of predation on smaller prokaryotic microorganisms is beginning to emerge. We studied the association between microorganisms and wild‐caught doliolids in the Northern California Current system. Doliolids were collected during bloom events identified at three different shelf locations with variable upwelling intensity. We discovered doliolids were associated with a range of prokaryotic microbial functional groups, which included free‐living pelagic Archaea, SAR11, and picocyanobacteria. The results suggest the possibility that doliolids could feed on the smallest members of the microbial community, expanding our understanding of doliolid feeding and microbial mortality. Given the ability of doliolids to clear large portions of seawater by filtration and their high abundance in this system, we suggest that doliolids could be an important player in shaping the microbial community structure of the Northern California Current system.
Eastern Boundary Systems support major fisheries whose early life stages depend on upwelling production. Upwelling can be highly variable at the regional scale, with substantial repercussions for new productivity and microbial loop activity. Studies that integrate the classic trophic web based on new production with the microbial loop are rare due to the range in body forms and sizes of the taxa. Underwater imaging can overcome this limitation, and with machine learning, enables fine resolution studies spanning large spatial scales. We used the In-situ Ichthyoplankton Imaging System (ISIIS) to investigate the drivers of plankton community structure in the northern California Current, sampled along the Newport Hydrographic (NH) and Trinidad Head (TR) lines, in OR and CA, respectively. The non-invasive imaging of particles and plankton over 1644km in the winters and summers of 2018 and 2019 yielded 1.194 billion classified plankton images. Combining nutrient analysis, flow cytometry, and 16S rRNA gene sequencing of the microbial community with mesoplankton underwater imaging enabled us to study taxa from 0.2µm to 15cm, including prokaryotes, copepods, ichthyoplankton, and gelatinous forms. To assess community structure, >2000 single-taxon distribution profiles were analyzed using high resolution spatial correlations. Co-occurrences on the NH line were consistently significantly higher off-shelf while those at TR were highest on-shelf. Random Forests models identified the concentrations of microbial loop associated taxa such as protists, Oithona copepods, and appendicularians as important drivers of co-occurrences at NH line, while at TR, cumulative upwelling and chlorophyll a were of the highest importance. Our results indicate that the microbial loop is driving plankton community structure in intermittent upwelling systems such as the NH line and supports temporal stability, and further, that taxa such as protists, Oithona copepods, and appendicularians connect a diverse and functionally redundant microbial community to stable plankton community structure. Where upwelling is more continuous such as at TR, primary production may dominate patterns of community structure, obscuring the underlying role of the microbial loop. Future changes in upwelling strength are likely to disproportionately affect plankton community structure in continuous upwelling regions, while high microbial loop activity enhances community structure resilience.
The small sizes of most marine plankton necessitate that plankton sampling occur on fine spatial scales, yet our questions often span large spatial areas. Underwater imaging can provide a solution to this sampling conundrum but collects large quantities of data that require an automated approach to image analysis. Machine learning for plankton classification, and high-performance computing (HPC) infrastructure, are critical to rapid image processing; however, these assets, especially HPC infrastructure, are only available post-cruise leading to an ‘after-the-fact’ view of plankton community structure. To be responsive to the often-ephemeral nature of oceanographic features and species assemblages in highly dynamic current systems, real-time data are key for adaptive oceanographic sampling. Here we used the new In-situ Ichthyoplankton Imaging System-3 (ISIIS-3) in the Northern California Current (NCC) in conjunction with an edge server to classify imaged plankton in real-time into 170 classes. This capability together with data visualization in a heavy.ai dashboard makes adaptive real-time decision-making and sampling at sea possible. Dual ISIIS-Deep-focus Particle Imager (DPI) cameras sample 180 L s⁻¹, leading to >10 GB of video per min. Imaged organisms are in the size range of 250 µm to 15 cm and include abundant crustaceans, fragile taxa (e.g., hydromedusae, salps), faster swimmers (e.g., krill), and rarer taxa (e.g., larval fishes). A deep learning pipeline deployed on the edge server used multithreaded CPU-based segmentation and GPU-based classification to process the imagery. AVI videos contain 50 sec of data and can contain between 23,000 - 225,000 particle and plankton segments. Processing one AVI through segmentation and classification takes on average 3.75 mins, depending on biological productivity. A heavyDB database monitors for newly processed data and is linked to a heavy.ai dashboard for interactive data visualization. We describe several examples where imaging, AI, and data visualization enable adaptive sampling that can have a transformative effect on oceanography. We envision AI-enabled adaptive sampling to have a high impact on our ability to resolve biological responses to important oceanographic features in the NCC, such as oxygen minimum zones, or harmful algal bloom thin layers, which affect the health of the ecosystem, fisheries, and local communities.
Eastern Boundary Systems support major fisheries whose early life stages depend on upwelling production. Upwelling can be highly variable at the regional scale, with substantial repercussions for new productivity and microbial loop activity. A holistic assessment of plankton community structure is challenging due to the range in body forms and sizes of the taxa. Thus, studies that integrate the classic trophic web based on new production with the microbial loop are rare. Underwater imaging can overcome this limitation, and together with machine learning, enables fine resolution studies spanning large spatial scales. We used the In-situ Ichthyoplankton Imaging System (ISIIS) to investigate the drivers of plankton community structure in the northern California Current, sampled along the Newport Hydrographic (NH) and Trinidad Head (TR) lines, in OR and CA, respectively. The non-invasive imaging of particles and plankton (250μm - 15cm) over 1644km (30 transects) in the winters and summers of 2018 and 2019 yielded 1.194 billion classified plankton images. The imaged plankton community ranged from protists, crustaceans, and gelatinous taxa to larval fishes. To assess community structure, >2000 single-taxon distribution profiles were analyzed using high resolution spatial correlations. Co-occurrences on the NH line were consistently significantly higher off-shelf while those at TR tended to be highest on-shelf. Taxa co-occurrences at TR increased significantly with upwelling strength and in 2019 TR summer co-occurrences were similar to those on the NH line. Random Forests models identified the concentrations of microbial loop taxa such as protists, Oithona copepods, and appendicularians as important drivers of co-occurrences at NH line, while at TR, cumulative upwelling and chlorophyll a were of the highest importance. Our results indicate that the microbial loop is actively driving plankton community structure in intermittent upwelling systems such as the NH line and may induce temporal stability. Where upwelling is more continuous such as at TR, primary production may dominate patterns of community structure, obscuring the underlying role of the microbial loop. Future changes in upwelling strength are likely to disproportionately affect plankton community structure in continuous upwelling regions, while high microbial loop activity enhances community structure resilience.
Eastern boundary systems support major fisheries of species whose early stages depend on upwelling production. However, upwelling can be highly variable at the regional scale, leading to complex patterns of feeding, growth, and survival for taxa that are broadly distributed in space and time. The northern California Current (NCC) is characterized by latitudinal variability in the seasonality and intensity of coastal upwelling. We examined the diet and larval growth of a dominant myctophid (Stenobrachius leucopsarus) in the context of their prey and predators in distinct NCC upwelling regimes. Larvae exhibited significant differences in diet and growth, with greater seasonal than latitudinal variability. In winter, during reduced upwelling, growth was substantially slower, guts less full, and diets dominated by copepod nauplii. During summer upwelling, faster-growing larvae had guts that were more full from feeding on calanoid copepods and relying less heavily on lower trophic level prey. Yet, our findings revealed a dome-shaped relationship with the fastest growth occurring at moderate upwelling intensity. High zooplanktivorous predation pressure led to above average growth, which may indicate the selective loss of slower-growing larvae. Our results suggest that species whose spatio-temporal distributions encompass multiple regional upwelling regimes experience unique feeding and predation environments throughout their range with implications for larval survivorship.
Many populations rely on dispersal as a critical life history event, from seed dispersal in plants to migration behaviors in birds, insects, and fishes. Species traits alter dispersal propensity and distance, and these in turn influence fitness. Vertical distribution behaviors, as have been observed in many taxa of fish larvae, are assumed to influence planktonic transport. Particular attention has been paid to the potential adaptive benefit of increased retention near the parental population due to ontogenetic vertical migration (OVM), in which larvae move deeper with age. By combining a large observational dataset with individual-based modeling, we investigated the prevalence of OVM compared to other behaviors, and the effects of different vertical behaviors on dispersal and connectivity. We analyzed two years of monthly field observations of larval vertical distribution behaviors for 23 taxa of coral reef fish, with resolution across larval ontogeny. We found a diversity of behaviors both within and among coral reef fish families, with three prevalent patterns: surface dwelling, ontogenetic vertical migration (OVM), and wide vertical spread. Using generalized versions of these three behaviors, we modeled larval dispersal throughout the Caribbean Sea over 5 years, for two pelagic larval durations (PLDs) that are typical of coral reef fishes. Models of surface-dwelling behavior generally led to more long-distance dispersal, lower local retention, and higher population connectivity than the uniformly-distributed and OVM behaviors. These latter two behaviors with deeper distributions during all or part of the larval stage had similar outcomes for dispersal, connectivity, and local retention. Similar impacts of behavior on dispersal, connectivity, and retention were observed under both short and long PLD. We also found that the effects of vertical behavior on larval dispersal were stronger than the effects of seasonal or interannual variation in currents. Our results suggest that there are other advantages beyond higher local retention that contribute to the selection of a complex behavior such as OVM—these may include predator avoidance, temperature-driven metabolic changes, and directional swimming.
Doliolids are common gelatinous grazers in marine ecosystems around the world and likely influence carbon cycling due to their large population sizes with high growth and excretion rates. Aggregations or blooms of these organisms occur frequently, but they are difficult to measure or predict because doliolids are fragile, under sampled with conventional plankton nets, and can aggregate on fine spatial scales (1–10 m). Moreover, ecological studies typically target a single region or site that does not encompass the range of possible habitats favoring doliolid proliferation. To address these limitations, we combined in situ imaging data from six coastal ecosystems, including the Oregon shelf, northern California, southern California Bight, northern Gulf of Mexico, Straits of Florida, and Mediterranean Sea, to resolve and compare doliolid habitat associations during warm months when environmental gradients are strong and doliolid blooms are frequently documented. Higher ocean temperature was the strongest predictor of elevated doliolid abundances across ecosystems, with additional variance explained by chlorophyll a fluorescence and dissolved oxygen. For marginal seas with a wide range of productivity regimes, the nurse stage tended to comprise a higher proportion of the doliolids when total abundance was low. However, this pattern did not hold in ecosystems with persistent coastal upwelling. The doliolids tended to be most aggregated in oligotrophic systems (Mediterranea and southern California), suggesting that microhabitats within the water column favor proliferation on fine spatial scales. Similar comparative approaches can resolve the realized niche of fast‐reproducing marine animals, thus improving predictions for population‐level responses to changing oceanographic conditions.
Doliolids are common gelatinous grazers in marine ecosystems around the world and likely influence carbon cycling due to their large population sizes and high growth and excretion rates. Aggregations or blooms of these organisms occur frequently, but they are difficult to measure or predict because doliolids are fragile, under sampled with conventional plankton nets, and can aggregate on fine spatial scales (1-10 m). Moreover, ecological studies typically target particular regions that do not encompass the range of possible habitats favoring doliolid proliferation. To address these limitations, we combined in situ imaging data from six coastal ecosystems, including the Oregon shelf, northern California, southern California Bight, northern Gulf of Mexico, Straits of Florida, and Mediterranean Sea, to resolve and compare doliolid habitat associations during warm months when environmental gradients are strong and doliolid blooms are frequently documented. Higher ocean temperature was the strongest predictor of elevated doliolid abundances across ecosystems, with additional variance explained by chlorophyll-a fluorescence and oxygen. The relative abundance of the nurse stage tended to increase when total doliolid abundance was low, but this pattern did not hold in upwelling ecosystems, indicating that nurses occupy less favorable habitats in established populations with wider shelf habitats. The doliolids tended to be most aggregated in oligotrophic systems (Mediterranean and southern California), suggesting that microhabitats within the water column favor proliferation on fine spatial scales. Similar comparative approaches can resolve the realized niche of fast-reproducing marine animals, thus improving predictions of population changes in response to oceanographic conditions.
As the basis of oceanic food webs and a key component of the biological carbon pump, planktonic organisms play major roles in the oceans. Their study benefited from the development of in situ imaging instruments, which provide higher spatio-temporal resolution than previous tools. But these instruments collect huge quantities of images, the vast majority of which are of marine snow particles or imaging artifacts. Among them, the In Situ Ichthyoplankton Imaging System (ISIIS) samples the largest water volumes (> 100 L s⁻¹) and thus produces particularly large datasets. To extract manageable amounts of ecological information from in situ images, we propose to focus on planktonic organisms early in the data processing pipeline: at the segmentation stage. We compared three segmentation methods, particularly for smaller targets, in which plankton represents less than 1% of the objects: (i) a traditional thresholding over the background, (ii) an object detector based on maximally stable extremal regions (MSER), and (iii) a content-aware object detector, based on a Convolutional Neural Network (CNN). These methods were assessed on a subset of ISIIS data collected in the Mediterranean Sea, from which a ground truth dataset of > 3,000 manually delineated organisms is extracted. The naive thresholding method captured 97.3% of those but produced ~340,000 segments, 99.1% of which were therefore not plankton (i.e. recall = 97.3%, precision = 0.9%). Combining thresholding with a CNN missed a few more planktonic organisms (recall = 91.8%) but the number of segments decreased 18-fold (precision increased to 16.3%). The MSER detector produced four times fewer segments than thresholding (precision = 3.5%), missed more organisms (recall = 85.4%), but was considerably faster. Because naive thresholding produces ~525,000 objects from 1 minute of ISIIS deployment, the more advanced segmentation methods significantly improve ISIIS data handling and ease the subsequent taxonomic classification of segmented objects. The cost in terms of recall is limited, particularly for the CNN object detector. These approaches are now standard in computer vision and could be applicable to other plankton imaging devices, the majority of which pose a data management problem.
Blooms of the colonial pelagic tunicate Pyrosoma atlanticum in 2014–2018 followed a marine heatwave in the eastern Pacific Ocean. Pyrosome blooms could alter pelagic food webs of the northern California Current (NCC) by accelerating the biological pump via active transport, fecal pellet production and mortality events. Although aggregations of P. atlanticum have the potential to shape marine trophic dynamics via carbon export, little is known about pyrosome vertical distribution patterns. In this study, we estimated the distribution of P. atlanticum in the NCC along transects off of Oregon (45°N and 124°W) and northern California (41°N and 124°W), USA during February and July 2018. Depth-stratified plankton tows provided volume-normalized pyrosome abundance and biovolume estimates that complemented fine-scale counts by a vertically deployed camera system. Pyrosomes were numerous offshore during February, especially off Oregon. Colonies were distributed non-uniformly in the water column with peak numbers associated with vertical gradients in environmental parameters, notably density and chl-a. Vertical distributions shifted over the 24-h period, indicative of diel vertical migration. Understanding the vertical distribution of these gelatinous grazers in the NCC gives insight to their behavior and ecological role in biologically productive temperate ecosystems as conditions become more favorable for recurring blooms.
... Other environmental factors such as salinity, current patterns, and wind patterns can also interact with SST and Chl-a, forming more complex conditions for aquatic ecosystems. The interaction between salinity and currents, for example, can affect plankton distribution and fish migration, while seasonally varying wind patterns can trigger large-scale changes in upwelling processes and nutrient distribution (Schmid et al., 2023). Therefore, further studies that include these variables will provide a more holistic picture of the factors controlling the distribution and productivity of mackerel in Banten Bay. ...
... A major advantage of automated imaging instruments is their ability to provide rapid and unbiased data that can be stored digitally and quickly made available for use (Giering et al., 2022), and without the need for preservatives, since samples can be analysed live. As access to high processing power is becoming more affordable, real-time imaging, including classification and visualisation, is also becoming a real possibility with Edge computing (Schmid et al., 2023). Because imaging instruments enumerate delicate or gelatinous organisms which may be damaged or under-represented in nets, they allow powerful and complementary insights into pelagic food web structure (Lombard et al., 2019), and crucially, if multiple instruments are used they can bridge the size span between large protists and small metazoa that gets missed in the gap between bottle and net sampling (Atkinson et al., 2021). ...
... Use of ISIIS and now ISIIS-3 creates a big data challenge. The combination of high-resolution imagery and the need to image a large volume of water results in extremely high numbers of imaged plankton individuals (0.1 to > 1 billion per study; Schmid et al., 2020;Robinson et al., 2021;Schmid et al., 2021;Schmid et al., 2023b). The two line scan cameras of the ISIIS-3 gather 10 GB of data per min, and >35 TB for a typical two-week research cruise (160 h of imagery). ...
... Sponaugle et al., 2009;Swieca et al., 2023). Prey abundance, a critical determinant of food availability, is closely aligned with the longitudinal gradients of water temperature and nutrient concentration downstream. ...
... Velocity fields are interpolated in time and space with a fourth order Runge-Kutta scheme, and the random-walk scheme can be scaled by turbulent diffusion obtained from regional oceanography observations. CMS represents biological traits of adults and early life stages organisms, including spawning seasons and frequencies, mortality, ontogenetic vertical migration (OVM) which is the trend in vertical larval distributions with age (Irisson et al., 2010;Hernández et al., 2023), variable competency period, and pelagic larval duration. The habitat, including spawning and settlement sites, is represented by 3D spatial polygons. ...
... Doliolid distribution and abundance Doliolids were identified using ISIIS images and confirmed by visual inspection of muscle banding and gut morphology (Fig. 2a), as described in detail previously (Greer et al. 2022;Schmid et al. 2023a). On the NH line, doliolids were absent from the majority of the transect except for one bloom, defined as > 25 zooids per m 3 (Walters et al. 2019), which extended from the surface down to 40 m, at the off-shelf (NH5) location. ...
... Shadowgraph imagers have also been integrated into slow-moving (15 cm s À1 ) autonomous systems, such as the Zooglider , which have sampling trajectories similar to the towed vehicles (moving vertically through the water column while traveling horizontally). The typical requirement of large vehicles for shadowgraph systems contrasts with smaller volume imaging systems, which have become increasingly compact and deployable on a wide variety of sampling platforms, including CTD rosettes (e.g., Drago et al. 2022;Panaïotis et al. 2022) and vertical profilers (Campbell et al. 2020) that integrate into station-based sampling procedures. ...
... They are also functionally diverse, serving various trophic roles as grazers, predators (Hays et al. 2018;Décima et al. 2019), and prey for higher trophic level species (Cardona et al. 2012;Hoving and Haddock 2017). Some gelatinous zooplankton (e.g., pelagic tunicates) undergo blooms, which can drastically alter community composition, biomass, and food web structure (Brodeur et al. 2019;Lyle et al. 2022). Identifying trophic relationships among gelatinous zooplankton is, therefore, essential for understanding how energy flows through ecosystems and ...
... Expanding the classifier to cover more taxonomic groups is possible, and recently, the research community has been able to access enormous plankton imagery thanks to the advent of highresolution in situ automatic acquisition technologies (e.g. Sosik and Olson, 2007;Robinson et al., 2021). Nevertheless, acquiring unbiased annotations is time-and resource consuming, and in situ datasets are often severely imbalanced (Johnson and Khoshgoftaar, 2019), with many images available for the most common species and few images available for multiple rarer species. ...
... Although diatoms generally are considered to be adversely affected by increasing stratification, they also commonly are found in these thin layers. For example, McManus et al. (2021) found that Pseudo-nitzschia spp. was the most abundant phytoplankton in the thin layer in Monterey Bay. Studies have shown that there is a close relationship between water column stratification and an increase in cell abundance of HAB species such as dinoflagellate Karlodinium veneficum and Penicillium verruculosa (Dai et al. 2014;Mardones et al. 2021). ...