Flow Physics Explains Morphological Diversity of Ciliated Organs.

Organs that pump fluids by the coordinated beat of motile cilia through the lumen are integral to animal physiology. Such organs include the human airways, brain ventricles, and reproductive tracts. Although cilia organization and duct morphology vary drastically in the animal kingdom, ducts are typically classified as either carpet or flame designs. The reason behind this dichotomy and how duct design relates to fluid pumping remain unclear. Here, we demonstrate that two structural parameters -- lumen diameter and cilia-to-lumen ratio -- organize the observed duct diversity into a continuous spectrum that connects carpets to flames across all animal phyla. Using a unified fluid model, we show that carpet and flame designs maximize flow rate and pressure generation, respectively. We propose that convergence of ciliated organ designs follows functional constraints rather than phylogenetic distance, along with universal design rules for ciliary pumps.

An in situ digital synthesis strategy for the discovery and description of ocean life.

Revolutionary advancements in underwater imaging, robotics, and genomic sequencing have reshaped marine exploration. We present and demonstrate an interdisciplinary approach that uses emerging quantitative imaging technologies, an innovative robotic encapsulation system with in situ RNA preservation and next-generation genomic sequencing to gain comprehensive biological, biophysical, and genomic data from deep-sea organisms. The synthesis of these data provides rich morphological and genetic information for species description, surpassing traditional passive observation methods and preserved specimens, particularly for gelatinous zooplankton. Our approach enhances our ability to study delicate mid-water animals, improving research in the world's oceans.

Nectophore coordination and kinematics by physonect siphonophores.

Siphonophores are ubiquitous and often highly abundant members of pelagic ecosystems throughout the open ocean. They are unique among animal taxa in that many species use multiple jets for propulsion. Little is known about the kinematics of the individual jets produced by nectophores (the swimming bells of siphonophores) or whether the jets are coordinated during normal swimming behavior. Using remotely operated vehicles and SCUBA, we video recorded the swimming behavior of several physonect species in their natural environment. The pulsed kinematics of the individual nectophores that comprise the siphonophore nectosome were quantified and, based on these kinematics, we examined the coordination of adjacent nectophores. We found that, for the five species considered, nectophores located along the same side of the nectosomal axis (i.e. axially aligned) were coordinated and their timing was offset such that they pulsed metachronally. However, this level of coordination did not extend across the nectosome and no coordination was evident between nectophores on opposite sides of the nectosomal axis. For most species, the metachronal contraction waves of nectophores were initiated by the apical nectophores and traveled dorsally. However, the metachronal wave of Apolemia rubriversa traveled in the opposite direction. Although nectophore groups on opposite sides of the nectosome were not coordinated, they pulsed with similar frequencies. This enabled siphonophores to maintain relatively linear trajectories during swimming. The timing and characteristics of the metachronal coordination of pulsed jets affects how the jet wakes interact and may provide important insight into how interacting jets may be optimized for efficient propulsion.

New Method for Rapid 3D Reconstruction of Semi-Transparent Underwater Animals and Structures.

Morphological features are the primary identifying properties of most animals and key to many comparative physiological studies, yet current techniques for preservation and documentation of soft-bodied marine animals are limited in terms of quality and accessibility. Digital records can complement physical specimens, with a wide array of applications ranging from species description to kinematics modeling, but options are lacking for creating models of soft-bodied semi-transparent underwater animals. We developed a lab-based technique that can live-scan semi-transparent, submerged animals, and objects within seconds. To demonstrate the method, we generated full three-dimensional reconstructions (3DRs) of an object of known dimensions for verification, as well as two live marine animals-a siphonophore and an amphipod-allowing detailed measurements on each. Techniques like these pave the way for faster data capture, integrative and comparative quantitative approaches, and more accessible collections of fragile and rare biological samples.

Autonomous agents for observing marine life.

Using artificial intelligence to facilitate autonomy in robotics will provide new insights into marine life.

Evolutionary traces of miniaturization in a giant-Comparative anatomy of brain and brain nerves in Bathochordaeus stygius (Tunicata, Appendicularia).

Appendicularia comprises 70 marine, invertebrate, chordate species. Appendicularians play important ecological and evolutionary roles, yet their morphological disparity remains understudied. Most appendicularians are small, develop rapidly, and with a stereotyped cell lineage, leading to the hypothesis that Appendicularia derived progenetically from an ascidian-like ancestor. Here, we describe the detailed anatomy of the central nervous system of Bathochordaeus stygius, a giant appendicularian from the mesopelagic. We show that the brain consists of a forebrain with on average smaller and more uniform cells and a hindbrain, in which cell shapes and sizes vary to a greater extent. Cell count for the brain was 102. We demonstrate the presence of three paired brain nerves. Brain nerve 1 traces into the epidermis of the upper lip region and consists of several fibers with some supportive bulb cells in its course. Brain nerve 2 innervates oral sensory organs and brain nerve 3 innervates the ciliary ring of the gill slits and lateral epidermis. Brain nerve 3 is asymmetric, with the right nerve consisting of two neurites originating posterior to the left one that contains three neurites. Similarities and differences to the anatomy of the brain of the model species Oikopleura dioica are discussed. We interpret the small number of cells in the brain of B. stygius as an evolutionary trace of miniaturization and conclude that giant appendicularians evolved from a small, progenetic ancestor that secondarily increased in size within Appendicularia.

FathomNet: A global image database for enabling artificial intelligence in the ocean.

The ocean is experiencing unprecedented rapid change, and visually monitoring marine biota at the spatiotemporal scales needed for responsible stewardship is a formidable task. As baselines are sought by the research community, the volume and rate of this required data collection rapidly outpaces our abilities to process and analyze them. Recent advances in machine learning enables fast, sophisticated analysis of visual data, but have had limited success in the ocean due to lack of data standardization, insufficient formatting, and demand for large, labeled datasets. To address this need, we built FathomNet, an open-source image database that standardizes and aggregates expertly curated labeled data. FathomNet has been seeded with existing iconic and non-iconic imagery of marine animals, underwater equipment, debris, and other concepts, and allows for future contributions from distributed data sources. We demonstrate how FathomNet data can be used to train and deploy models on other institutional video to reduce annotation effort, and enable automated tracking of underwater concepts when integrated with robotic vehicles. As FathomNet continues to grow and incorporate more labeled data from the community, we can accelerate the processing of visual data to achieve a healthy and sustainable global ocean.

Muscular adaptations in swimming scale worms (Polynoidae, Annelida).

Annelids are predominantly found along with the seafloor, but over time have colonized a vast diversity of habitats, such as the water column, where different modes of locomotion are necessary. Yet, little is known about their potential muscular adaptation to the continuous swimming behaviour required in the water column. The musculature and motility were examined for five scale worm species of Polynoidae (Aphroditiformia, Annelida) found in shallow waters, deep sea or caves and which exhibit crawling, occasional swimming or continuous swimming, respectively. Their parapodial musculature was reconstructed using microCT and computational three-dimensional analyses, and the muscular functions were interpreted from video recordings of their locomotion. Since most benthic scale worms are able to swim for short distances using body and parapodial muscle movements, suitable musculature for swimming is already present. Our results indicate that rather than rearrangements or addition of muscles, a shift to a pelagic lifestyle is mainly accompanied by structural loss of muscle bundles and density, as well as elongation of extrinsic dorsal and ventral parapodial muscles. Our study documents clear differences in locomotion and musculature among closely related annelids with different lifestyles as well as points to myoanatomical adaptations for accessing the water column.

A hybrid underwater robot for multidisciplinary investigation of the ocean twilight zone.

Mesobot, an autonomous underwater vehicle, addresses specific unmet needs for observing and sampling a variety of phenomena in the ocean's midwaters. The midwater hosts a vast biomass, has a role in regulating climate, and may soon be exploited commercially, yet our scientific understanding of it is incomplete. Mesobot has the ability to survey and track slow-moving animals and to correlate the animals' movements with critical environmental measurements. Mesobot will complement existing oceanographic assets such as towed, remotely operated, and autonomous vehicles; shipboard acoustic sensors; and net tows. Its potential to perform behavioral studies unobtrusively over long periods with substantial autonomy provides a capability that is not presently available to midwater researchers. The 250-kilogram marine robot can be teleoperated through a lightweight fiber optic tether and can also operate untethered with full autonomy while minimizing environmental disturbance. We present recent results illustrating the vehicle's ability to automatically track free-swimming hydromedusae (Solmissus sp.) and larvaceans (Bathochordaeus stygius) at depths of 200 meters in Monterey Bay, USA. In addition to these tracking missions, the vehicle can execute preprogrammed missions collecting image and sensor data while also carrying substantial auxiliary payloads such as cameras, sonars, and samplers.

Metachronal Motion across Scales: Current Challenges and Future Directions.

Metachronal motion is used across a wide range of organisms for a diverse set of functions. However, despite its ubiquity, analysis of this behavior has been difficult to generalize across systems. Here we provide an overview of known commonalities and differences between systems that use metachrony to generate fluid flow. We also discuss strategies for standardizing terminology and defining future investigative directions that are analogous to other established subfields of biomechanics. Finally, we outline key challenges that are common to many metachronal systems, opportunities that have arisen due to the advent of new technology (both experimental and computational), and next steps for community development and collaboration across the nascent network of metachronal researchers.

Metachronal Swimming with Flexible Legs: A Kinematics Analysis of the Midwater Polychaete Tomopteris.

Aquatic animals have developed a wide array of adaptations specific to life underwater, many of which are related to moving in the water column. Different swimming methods have emerged, such as lift-based flapping, drag-based body undulations, and paddling. Patterns occur across scales and taxa, where animals with analogous body features use similar locomotory methods. Metachronal paddling is one such wide-spread propulsion mechanism, occurring in taxa as diverse as ctenophores, crustaceans, and polychaetes. Sequential movement of multiple, near identical appendages, allows for steady swimming through phase-offsets between adjacent propulsors. The soft-bodied, holopelagic polychaete Tomopteris has two rows of segmental appendages (parapodia) positioned on opposite sides along its flexible body that move in a metachronal pattern. The outer one-third of their elongate parapodia consist of two paddle-like pinnules that can be spread or, when contracted, fold together to change the effective width of the appendage. Along with metachronal paddling, tomopterid bodies undulate laterally, and by using high speed video and numerical modeling, we seek to understand how these two behaviors combine to generate effective swimming. We collected animals using deep-diving remotely operated vehicles, and recorded video data in shore- and ship-based imaging laboratories. Kinematics were analyzed using landmark tracking of features in the video data. We determined that parapodia are actively moved to generate thrust and pinnules are actively spread and contracted to create differences in drag between power and recovery strokes. At the same time, the body wave increases the parapodium stroke angle and extends the parapodia into undisturbed water adjacent to the body, enhancing thrust. Based on kinematics measurements used as input to a 1D numerical model of drag-based swimming, we found that spreading of the pinnules during the power stroke provides a significant contribution to propulsion, similar to the contribution provided by the body wave. We conclude that tomopterids combine two different propulsive modes, which are enabled by their flexible body plan. This makes their anatomy and kinematics of interest not only for biologists, but also for soft materials and robotics engineers.

Revealing enigmatic mucus structures in the deep sea using DeepPIV.

Many animals build complex structures to aid in their survival, but very few are built exclusively from materials that animals create 1,2. In the midwaters of the ocean, mucoid structures are readily secreted by numerous animals, and serve many vital functions3,4. However, little is known about these mucoid structures owing to the challenges of observing them in the deep sea. Among these mucoid forms, the 'houses' of larvaceans are marvels of nature5, and in the ocean twilight zone giant larvaceans secrete and build mucus filtering structures that can reach diameters of more than 1 m6. Here we describe in situ laser-imaging technology7 that reconstructs three-dimensional models of mucus forms. The models provide high-resolution views of giant larvacean houses and elucidate the role that house structure has in food capture and predator avoidance. Now that tools exist to study mucus structures found throughout the ocean, we can shed light on some of nature's most complex forms.

Author Correction: The vertical distribution and biological transport of marine microplastics across the epipelagic and mesopelagic water column.

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

Quantifying the swimming gaits of veined squid (Loligo forbesii) using bio-logging tags.

Squid are mobile, diverse, ecologically important marine organisms whose behavior and habitat use can have substantial impacts on ecosystems and fisheries. However, as a consequence in part of the inherent challenges of monitoring squid in their natural marine environment, fine-scale behavioral observations of these free-swimming, soft-bodied animals are rare. Bio-logging tags provide an emerging way to remotely study squid behavior in their natural environments. Here, we applied a novel, high-resolution bio-logging tag (ITAG) to seven veined squid, Loligo forbesii, in a controlled experimental environment to quantify their short-term (24 h) behavioral patterns. Tag accelerometer, magnetometer and pressure data were used to develop automated gait classification algorithms based on overall dynamic body acceleration, and a subset of the events were assessed and confirmed using concurrently collected video data. Finning, flapping and jetting gaits were observed, with the low-acceleration finning gaits detected most often. The animals routinely used a finning gait to ascend (climb) and then glide during descent with fins extended in the tank's water column, a possible strategy to improve swimming efficiency for these negatively buoyant animals. Arms- and mantle-first directional swimming were observed in approximately equal proportions, and the squid were slightly but significantly more active at night. These tag-based observations are novel for squid and indicate a more efficient mode of movement than suggested by some previous observations. The combination of sensing, classification and estimation developed and applied here will enable the quantification of squid activity patterns in the wild to provide new biological information, such as in situ identification of behavioral states, temporal patterns, habitat requirements, energy expenditure and interactions of squid through space-time in the wild.

Augmenting biologging with supervised machine learning to study in situ behavior of the medusa Chrysaora fuscescens.

Zooplankton play critical roles in marine ecosystems, yet their fine-scale behavior remains poorly understood because of the difficulty in studying individuals in situ Here, we combine biologging with supervised machine learning (ML) to propose a pipeline for studying in situ behavior of larger zooplankton such as jellyfish. We deployed the ITAG, a biologging package with high-resolution motion sensors designed for soft-bodied invertebrates, on eight Chrysaora fuscescens in Monterey Bay, using the tether method for retrieval. By analyzing simultaneous video footage of the tagged jellyfish, we developed ML methods to: (1) identify periods of tag data corrupted by the tether method, which may have compromised prior research findings, and (2) classify jellyfish behaviors. Our tools yield characterizations of fine-scale jellyfish activity and orientation over long durations, and we conclude that it is essential to develop behavioral classifiers on in situ rather than laboratory data.

The vertical distribution and biological transport of marine microplastics across the epipelagic and mesopelagic water column.

Plastic waste has been documented in nearly all types of marine environments and has been found in species spanning all levels of marine food webs. Within these marine environments, deep pelagic waters encompass the largest ecosystems on Earth. We lack a comprehensive understanding of the concentrations, cycling, and fate of plastic waste in sub-surface waters, constraining our ability to implement effective, large-scale policy and conservation strategies. We used remotely operated vehicles and engineered purpose-built samplers to collect and examine the distribution of microplastics in the Monterey Bay pelagic ecosystem at water column depths ranging from 5 to 1000 m. Laser Raman spectroscopy was used to identify microplastic particles collected from throughout the deep pelagic water column, with the highest concentrations present at depths between 200 and 600 m. Examination of two abundant particle feeders in this ecosystem, pelagic red crabs (Pleuroncodes planipes) and giant larvaceans (Bathochordaeus stygius), showed that microplastic particles readily flow from the environment into coupled water column and seafloor food webs. Our findings suggest that one of the largest and currently underappreciated reservoirs of marine microplastics may be contained within the water column and animal communities of the deep sea.

From the surface to the seafloor: How giant larvaceans transport microplastics into the deep sea.

Plastic waste is a pervasive feature of marine environments, yet little is empirically known about the biological and physical processes that transport plastics through marine ecosystems. To address this need, we conducted in situ feeding studies of microplastic particles (10 to 600 µm in diameter) with the giant larvacean Bathochordaeus stygius. Larvaceans are abundant components of global zooplankton assemblages, regularly build mucus "houses" to filter particulate matter from the surrounding water, and later abandon these structures when clogged. By conducting in situ feeding experiments with remotely operated vehicles, we show that giant larvaceans are able to filter a range of microplastic particles from the water column, ingest, and then package microplastics into their fecal pellets. Microplastics also readily affix to their houses, which have been shown to sink quickly to the seafloor and deliver pulses of carbon to benthic ecosystems. Thus, giant larvaceans can contribute to the vertical flux of microplastics through the rapid sinking of fecal pellets and discarded houses. Larvaceans, and potentially other abundant pelagic filter feeders, may thus comprise a novel biological transport mechanism delivering microplastics from surface waters, through the water column, and to the seafloor. Our findings necessitate the development of tools and sampling methodologies to quantify concentrations and identify environmental microplastics throughout the water column.

New technology reveals the role of giant larvaceans in oceanic carbon cycling.

To accurately assess the impacts of climate change on our planet, modeling of oceanic systems and understanding how atmospheric carbon is transported from surface waters to the deep benthos are required. The biological pump drives the transport of carbon through the ocean's depths, and the rates at which carbon is removed and sequestered are often dependent on the grazing abilities of surface and midwater organisms. Some of the most effective and abundant midwater grazers are filter-feeding invertebrates. Although the impact of smaller, near-surface filter feeders is generally known, efforts to quantify the impact of deeper filter feeders, such as giant larvaceans, have been unsuccessful. Giant larvaceans occupy the upper 400 m of the water column, where they build complex mucus filtering structures that reach diameters greater than 1 m. Because of the fragility of these structures, direct measurements of filtration rates require in situ methods. Hence, we developed DeepPIV, an instrument deployed from a remotely operated vehicle that enables the direct measurement of in situ filtration rates. The rates measured for giant larvaceans exceed those of any other zooplankton filter feeder. Given these filtration rates and abundance data from a 22-year time series, the grazing impact of giant larvaceans far exceeds previous estimates, with the potential for processing their 200-m principal depth range in Monterey Bay in as little as 13 days. Technologies such as DeepPIV will enable more accurate assessments of the long-term removal of atmospheric carbon by deep-water biota.

Morphology Alters Fluid Transport and the Ability of Organisms to Mix Oceanic Waters.

Mixing in the ocean is opposed by the stratification of fluid, such that density of seawater increases with greater depth. The mechanisms by which mixing occurs have been attributed largely to physical processes that include atmospheric forcing, tides, and internal waves. Biogenic mixing, another potential source of mixing in the ocean, may generate significant transport of fluid during diel vertical migrations of organisms. Biogenic mixing is not limited to the near-surface or to regions of rough bottom topography, as are other physical mixing processes, and may contribute significantly to the energy budget of mixing in mid-ocean. "Fluid drift", a mechanism first described by Charles Galton Darwin, has been identified as a mechanism that allows for long-distance, vertical transport of fluid by the smallest of swimming organisms. However, little is known about how fluid drift varies with morphology and behavior of swimming organisms. We conducted numerical simulations of theoretical and experimentally measured flows of swimming medusae (Phyllorhiza sp.), and compared the volume of the drift induced by these flows. Our numerical simulations of fluid drift showed that morphology coupled with swimming behavior alters the transport of fluid both spatially and temporally. Given empirical velocity field data, the methods presented here allow us to systematically compare fluid transport across taxa, and enable us to deduce the potential of swimming organisms to influence fluid transport.

Ontogenetic propulsive transitions by Sarsia tubulosa medusae.

While swimming in their natural environment, marine organisms must successfully forage, escape from predation, and search for mates to reproduce. In the process, planktonic organisms interact with their fluid environment, generating fluid signatures around their body and in their downstream wake through ontogeny. In the early stages of their life cycle, marine organisms operate in environments where viscous effects dominate and govern physical processes. Ontogenetic propulsive transitions in swimming organisms often involve dramatic changes in morphology and swimming behavior. However, for organisms that do not undergo significant changes in morphology, swimming behavior or propulsive mode, how is their swimming performance affected? We investigated the ontogenetic propulsive transitions of the hydromedusa Sarsia tubulosa, which utilizes jet propulsion and possesses a similar bell morphology throughout its life cycle. We used digital particle image velocimetry and high-speed imaging to measure the body kinematics, velocity fields and wake structures induced by swimming S. tubulosa with bell exit diameters from 1 to 10 mm. Our experimental observations revealed three distinct classes of hydrodynamic wakes: elongated vortex rings for 1030 (larger than 2 mm bell exit diameter) and elliptical vortex rings (or leading vortex rings) followed by trailing jets for most instances where Re>100 (larger than 4 or 5 mm bell exit diameter). The relative travel distance and propulsive efficiency remained unchanged throughout ontogeny, and the swimming proficiency and hydrodynamic cost of transport decreased non-linearly.