The fluid dynamics of barnacle feeding.

Sessile barnacles feed by sweeping their basket-like cirral fan through the water, intercepting suspended prey. A primary component of the diet of adult barnacles is copepods that are sensitive to fluid disturbances and capable of escaping. How do barnacles manage to capture copepods despite the fluid disturbances they generate? We examined this question by describing the feeding current architecture of 1 cm sized Balanus crenatus using particle image velocimetry, and by studying the trajectories of captured copepods and the escapes of evading copepods. We found that barnacles produce a feeding current that arrives both from behind and the sides of the barnacle. The flow from the sides represents quiescent corridors of low fluid deformation and uninterrupted by the beating cirral fan. Potential prey arriving from behind are likely to encounter the cirral fan and, hence, capture here is highly unlikely. Accordingly, most captured copepods arrived through the quiet corridors, while most copepods arriving from behind managed to escape. Thus, it is the unique feeding flow architecture that allows feeding on evasive prey. We used the Landau-Squire jet as a simple model of the feeding current. For the Reynolds number of our experiments, the model reproduces the main features of the feeding current, including the lateral feeding corridors. Furthermore, the model suggests that smaller barnacle specimens, operating at lower Reynolds numbers, will produce a fore-aft symmetric feeding current without the lateral corridors. This suggests an ontogenetic diet shift from non-evasive prey to inclusion of evasive prey as the barnacle grows.

A Life Outside.

How do the morphologies of organisms affect their physical interactions with the environment and other organisms? My research in marine systems couples field studies of the physical habitats, life history strategies, and ecological interactions of organisms with laboratory analyses of their biomechanics. Here, I review how we pursued answers to three questions about marine organisms: (a) how benthic organisms withstand and utilize the water moving around them, (b) how the interaction between swimming and turbulent ambient water flow affects where small organisms go, and (c) how hairy appendages catch food and odors. I also discuss the importance of different types of mentors, the roadblocks for women in science when I started my career, the challenges and delights of interdisciplinary research, and my quest to understand how I see the world as a dyslexic.

Reconstructing the feeding ecology of Cambrian sponge reefs: the case for active suspension feeding in Archaeocyatha.

Sponge-grade Archaeocyatha were early Cambrian biomineralizing metazoans that constructed reefs globally. Despite decades of research, many facets of archaeocyath palaeobiology remain unclear, making it difficult to reconstruct the palaeoecology of Cambrian reef ecosystems. Of specific interest is how these organisms fed; previous experimental studies have suggested that archaeocyaths functioned as passive suspension feeders relying on ambient currents to transport nutrient-rich water into their central cavities. Here, we test this hypothesis using computational fluid dynamics (CFD) simulations of digital models of select archaeocyath species. Our results demonstrate that, given a range of plausible current velocities, there was very little fluid circulation through the skeleton, suggesting obligate passive suspension feeding was unlikely. Comparing our simulation data with exhalent velocities collected from extant sponges, we infer an active suspension feeding lifestyle for archaeocyaths. The combination of active suspension feeding and biomineralization in Archaeocyatha may have facilitated the creation of modern metazoan reef ecosystems.

Biomimetic models of fish gill rakers as lateral displacement arrays for particle separation.

Ram suspension-feeding fish, such as herring, use gill rakers to separate small food particles from large water volumes while swimming forward with an open mouth. The fish gill raker function was tested using 3D-printed conical models and computational fluid dynamics simulations over a range of slot aspect ratios. Our hypothesis predicting the exit of particles based on mass flow rates, dividing streamlines (i.e. stagnation streamlines) at the slots between gill rakers, and particle size was supported by the results of experiments with physical models in a recirculating flume. Particle movement in suspension-feeding fish gill raker models was consistent with the physical principles of lateral displacement arrays ('bump arrays') for microfluidic and mesofluidic separation of particles by size. Although the particles were smaller than the slots between the rakers, the particles skipped over the vortical region that was generated downstream from each raker. The particles 'bumped' on anterior raker surfaces during posterior transport. Experiments in a recirculating flume demonstrate that the shortest distance between the dividing streamline and the raker surface preceding the slot predicts the maximum radius of a particle that will exit the model by passing through the slot. This theoretical maximum radius is analogous to the critical separation radius identified with reference to the stagnation streamlines in microfluidic and mesofluidic devices that use deterministic lateral displacement and sieve-based lateral displacement. These conclusions provide new perspectives and metrics for analyzing cross-flow and cross-step filtration in fish with applications to filtration engineering.

Pachyoliva columellaris G.B. Sowerby I, 1825 (Olividae, Caenogastropoda) in Peru: tidal migrations and population density

The gastropod Pachyoliva columellaris (formerly Olivella columellaris) is particularly common on many sandy beaches in North Peru. In the studied region north of Paita, Piura province, the species reaches densities of over 80,000 individuals per beach meter. The snails perform tidal migrations throughout the lunar cycle although tidal amplitudes differ four-fold between neap and spring tide. Not all animals complete their tidal migrations, and significant numbers remain above the water line at low tide. Throughout the tidal cycle, the proportion of small individuals is increased near the water line whereas large animals dominate in lower beach zones. I conclude that the sandy beaches north of Paita are well-suited for further studies of P. columellaris and the mechanisms underlying tidal migrations in invertebrates.

El gasterópodo Pachyoliva columellaris (antes Olivella columellaris) es particularmente común en las playas arenosas del norte de Perú. En la región estudiada al norte de Paita, provincia de Piura, la especie alcanza densidades de más de 80.000 individuos por metro de playa. Los caracoles realizan migraciones mareales durante todo el ciclo lunar, aunque las amplitudes de marea difieren cuatro veces entre la marea muerta y la marea viva. No todos los animales completan sus migraciones mareales y un número significativo permanece por encima del nivel del agua en marea baja. Durante todo el ciclo de marea, la proporción de individuos pequeños aumenta cerca del nivel del agua, mientras que los animales grandes dominan en las zonas bajas de la playa. Concluyo que las playas arenosas al norte de Paita son apropiadas para estudios adicionales de P. columellaris y los mecanismos de las migraciones de marea en invertebrados.

Hydrodynamic analysis of bioinspired vortical cross-step filtration by computational modelling.

Research on the suspension-feeding apparatus of fishes has led recently to the identification of novel filtration mechanisms involving vortices. Structures inside fish mouths form a series of 'backward-facing steps' by protruding medially into the mouth cavity. In paddlefish and basking shark mouths, porous gill rakers lie inside 'slots' between the protruding branchial arches. Vortical flows inside the slots of physical models have been shown to be important for the filtration process, but the complex flow patterns have not been visualised fully. Here we resolve the three-dimensional hydrodynamics by computational fluid dynamics simulation of a simplified mouth cavity including realistic flow dynamics at the porous layer. We developed and validated a modelling protocol in ANSYS Fluent software that combines a porous media model and permeability direction vector mapping. We found that vortex shape and confinement to the medial side of the gill rakers result from flow resistance by the porous gill raker surfaces. Anteriorly directed vortical flow shears the porous layer in the centre of slots. Flow patterns also indicate that slot entrances should remain unblocked, except for the posterior-most slot. This new modelling approach will enable future design exploration of fish-inspired filters.

Determining the Properties that Govern Selective Ingestion and Egestion of Microplastics by the Blue Mussel (Mytilus edulis) and Eastern Oyster (Crassostrea virginica).

Suspension feeding bivalve molluscs interact with different types of microplastics (MP) suspended in the water column. Most bivalves are selective suspension feeders and, thus, do not consume all particles to which they are exposed. Selection depends upon the physicochemical properties and size of the particle. Recent work has provided evidence that blue mussels, Mytilus edulis, and eastern oysters, Crassostrea virginica, ingest and egest microspheres (polystyrene) and microfibers (nylon) differently, but whether other factors, such as polymer type and shape, mediate selection have not been explored. To investigate these factors, mussels and oysters were offered similar sized nylon (Ny) and polyester (PES) microfibers or polyethylene (PE) and polystyrene (PS) microspheres, or different sized PES microfibers during a 2 h exposure. Feces and pseudofeces were collected separately and analyzed for MPs, and the data were used to develop a linear regression model for selection. Results demonstrated clear species-specific differences in the efficiency of particle selection. Both mussels and oysters, however, exhibited size-based rejection of PES microfibers, ingesting a higher proportion of shorter fibers than longer fibers. Polymer type did not impact selection of fibers or spheres. The relative size of particles (area and perimeter) was found to be the most important factor in predicting whether a MP will be rejected or ingested.

Suspension feeders: diversity, principles of particle separation and biomimetic potential.

Suspension feeders (SFs) evolved a high diversity of mechanisms, sometimes with remarkably convergent morphologies, to retain plankton, detritus and man-made particles with particle sizes ranging from less than 1 µm to several centimetres. Based on an extensive literature review, also including the physical and technical principles of solid-liquid separation, we developed a set of 18 ecological and technical parameters to review 35 taxa of suspension-feeding Metazoa covering the diversity of morphological and functional principles. This includes passive SFs, such as gorgonians or crinoids that use the ambient flow to encounter particles, and sponges, bivalves or baleen whales, which actively create a feeding current. Separation media can be flat or funnel-shaped, built externally such as the filter houses in larvaceans, or internally, like the pleated gills in bivalves. Most SFs feed in the intermediate flow region of Reynolds number 1-50 and have cleaning mechanisms that allow for continuous feeding. Comparison of structure-function patterns in SFs to current filtration technologies highlights potential solutions to common technical design challenges, such as mucus nets which increase particle adhesion in ascidians, vanes which reduce pressure losses in whale sharks and changing mesh sizes in the flamingo beak which allow quick adaptation to particle sizes.

Ultrastructure of the gill ciliary epithelium of Limnoperna fortunei (Dunker 1857), the invasive golden mussel.

BACKGROUND: Limnoperna fortunei is a freshwater bivalve mollusc originally from southern Asia that invaded South America in the 1990's. Due to its highly efficient water pumping and filtering, and its capacity to form strong adhesions to a variety of substrates by byssus thread, this invasive species has been able to adapt to several environments across South America, causing significant ecological and economic damages. By gaining a deeper understanding of the biological and ecological aspects of L. fortunei we will be able to establish more effective strategies to manage its invasion. The gills of the mollusc are key structures responsible for several biological functions, including respiration and feeding. In this work, we characterized the ultrastructure of L. fortunei gills and its ciliary epithelium using light microscopy, transmission and scanning electron microscopies. This is the first report of the morphology of the epithelial cells and cilia of the gill of L. fortunei visualized in high resolution. RESULTS: The analysis showed highly organized and abundant ciliary structures (lateral cilia, laterofrontal cirri and frontal cilia) on the entire length of the branchial epithelium. Mitochondria, smooth endoplasmic reticulum and glycogen granules were abundantly found in the epithelial cells of the gills, demonstrating the energy-demanding function of these structures. Neutral mucopolysaccharides (low viscosity mucus) were observed on the frontal surface of the gill filaments and acid mucopolysaccharides (high viscosity mucus) were observed to be spread out, mainly on the lateral tract. Spherical vesicles, possibly containing mucus, could also be observed in these cells. These findings demonstrate the importance of the mucociliary processes in particle capture and selection. CONCLUSIONS: Our data suggest that the mechanism used by this mollusc for particle capture and selection could contribute to a better understanding of key aspects of invasion and also in the establishment of more efficient and economically viable strategies of population control.

Larval morphology of three syntopic species of emKaloula/em Gray (Anura: Microhylidae) from Vietnam.

The external larval morphology of three species of the microhylid genus Kaloula (K. indochinensis, K. mediolineata, and K. pulchra) inhabiting the southern and central regions of Vietnam is studied. The similarities and the distinctive features of their morphometric characters, the structure of their mouthparts and spiracle, and their coloration are analysed with consideration of the geographic variability. A description of the tadpole of K. indochinensis is provided for the first time. The interspecific comparison revealed the shape of the mouthparts and the spiracle as the most reliable diagnostic characters for the field identification of the coexistent Kaloula tadpoles. The first description of the larval chondrocranium and hyobranchial apparatus of K. indochinensis demonstrates a set of morphological traits characteristic of suspension-feeding microhylids. Some developmental parameters (egg number and size, duration of embryonic and larval development, larvae size and stage at hatching) are provided for K. indochinensis and K. pulchra.

The biological plastic pump: Evidence from a local case study using blue mussel and infaunal benthic communities.

The distinct spatial variability in microplastic concentrations between marine regions and habitats calls for a better understanding about the transport pathways of this omnipresent pollutant in the marine environment. This study provides empirical evidence that a sessile filter feeder, the Blue mussel M. edulis, accelerates microplastic deposition by aggregating them into sinking particulate faeces and pseudofaeces. After settling to the seafloor, the bioturbation of benthic fauna quickly buries these microplastics. Collectively, these results suggest that if such biologically-mediated benthic-pelagic coupling would be integrated into hydrodynamic transport models, the spatial variability and source-sink dynamics of microplastics would be better understood. It is proposed that microplastic pollution is monitored through sampling that takes into account faeces and pseudofaeces underneath filter feeders. The implications of this detrital pathway for microplastic transfer to the seafloor, and the role of shellfish mariculture in this process, are discussed. Studies that consider filter feeders and benthic communities from other regions, and during different seasons, are needed to validate the proposed biological pump mechanism across space and time.

Ancient life and moving fluids.

Over 3.7 billion years of Earth history, life has evolved complex adaptations to help navigate and interact with the fluid environment. Consequently, fluid dynamics has become a powerful tool for studying ancient fossils, providing insights into the palaeobiology and palaeoecology of extinct organisms from across the tree of life. In recent years, this approach has been extended to the Ediacara biota, an enigmatic assemblage of Neoproterozoic soft-bodied organisms that represent the first major radiation of macroscopic eukaryotes. Reconstructing the ways in which Ediacaran organisms interacted with the fluids provides new insights into how these organisms fed, moved, and interacted within communities. Here, we provide an in-depth review of fluid physics aimed at palaeobiologists, in which we dispel misconceptions related to the Reynolds number and associated flow conditions, and specify the governing equations of fluid dynamics. We then review recent advances in Ediacaran palaeobiology resulting from the application of computational fluid dynamics (CFD). We provide a worked example and account of best practice in CFD analyses of fossils, including the first large eddy simulation (LES) experiment performed on extinct organisms. Lastly, we identify key questions, barriers, and emerging techniques in fluid dynamics, which will not only allow us to understand the earliest animal ecosystems better, but will also help to develop new palaeobiological tools for studying ancient life.

Selective factors in the evolution of multicellularity in choanoflagellates.

Choanoflagellates, unicellular eukaryotes that can form multicellular colonies by cell division and that share a common ancestor with animals, are used as a model system to study functional consequences of being unicellular versus colonial. This review examines performance differences between unicellular and multicellular choanoflagellates in swimming, feeding, and avoiding predation, to provide insights about possible selective advantages of being multicellular for the protozoan ancestors of animals. Each choanoflagellate cell propels water by beating a single flagellum and captures bacterial prey on a collar of microvilli around the flagellum. Formation of multicellular colonies does not improve the swimming performance, but the flux of prey-bearing water to the collars of some of the cells in colonies of certain configurations can be greater than for single cells. Colony geometry appears to affect whether cells in colonies catch more prey per cell per time than do unicellular choanoflagellates. Although multicellular choanoflagellates show chemokinetic behavior in response to oxygen, only the unicellular dispersal stage (fast swimmers without collars) use pH signals to aggregate in locations where bacterial prey might be abundant. Colonies produce larger hydrodynamic signals than do single cells, and raptorial protozoan predators capture colonies while ignoring single cells. In contrast, ciliate predators entrain both single cells and colonies in their feeding currents, but reject larger colonies, whereas passive heliozoan predators show no preference. Thus, the ability of choanoflagellate cells to differentiate into different morphotypes, including multicellular forms, in response to variable aquatic environments might have provided a selective advantage to the ancestors of animals.

A deposit-feeder sea cucumber also ingests suspended particles through the mouth.

Although the sea cucumber Apostichopus japonicus has been characterised as a deposit feeder, nutrients sourced from the water column have been recorded in the intestines of this species. However, the mechanisms whereby nutrients in the water enter the intestinal tract of A. japonicus, and whether other suspended particles can be ingested via the mouth of A. japonicus adults, remain unknown. Here, we reveal how A. japonicus ingests suspended particles through the mouth. We used synthetic particles and video recording to confirm the suspension uptake by the sea cucumber. Apostichopus japonicus continued to ingest suspended particles (if present) over time, and the particle ingestion rate was positively correlated with the concentration of suspended particles (Pearson correlation: r=0.808). Additionally, clearance rates of the suspended particles ranged from 0.3 to 0.9 l h-1 The findings of this study thus provide evidence of a previously undescribed particle uptake mechanism in a commercially important species.

Was the Devonian placoderm Titanichthys a suspension feeder?

Large nektonic suspension feeders have evolved multiple times. The apparent trend among apex predators for some evolving into feeding on small zooplankton is of interest for understanding the associated shifts in anatomy and behaviour, while the spatial and temporal distribution gives clues to an inherent relationship with ocean primary productivity and how past and future perturbations to these may impact on the different tiers of the food web. The evolution of large nektonic suspension feeders-'gentle giants'-occurred four times among chondrichthyan fishes (e.g. whale sharks, basking sharks and manta rays), as well as in baleen whales (mysticetes), the Mesozoic pachycormid fishes and at least twice in radiodontan stem group arthropods (Anomalocaridids) during the Cambrian explosion. The Late Devonian placoderm Titanichthys has tentatively been considered to have been a megaplanktivore, primarily due to its gigantic size and narrow, edentulous jaws while no suspension-feeding apparatus have ever been reported. Here, the potential for microphagy and other feeding behaviours in Titanichthys is assessed via a comparative study of jaw mechanics in Titanichthys and other placoderms with presumably differing feeding habits (macrophagy and durophagy). Finite-element models of the lower jaws of Titanichthys termieri in comparison to Dunkleosteus terrelli and Tafilalichthys lavocati reveal considerably less resistance to von Mises stress in this taxon. Comparisons with a selection of large-bodied extant taxa of similar ecological diversity reveal similar disparities in jaw stress resistance. Our results, therefore, conform to the hypothesis that Titanichthys was a suspension feeder with jaws ill-suited for biting and crushing but well suited for gaping ram feeding.

A possible case of inverted lifestyle in a new bivalved arthropod from the Burgess Shale.

The origin of the arthropod carapace, an enlargement of cephalic tergites, can be traced back to the Cambrian period. However, its disparity and evolution are still not fully understood. Here, we describe a new 'bivalved' arthropod, Fibulacaris nereidis gen. et sp. nov., based on 102 specimens from the middle Cambrian (Wuliuan Stage) Burgess Shale, Marble Canyon area in British Columbia's Kootenay National Park, Canada. The laterally compressed carapace covers most of the body. It is fused dorsally and merges anteriorly into a conspicuous postero-ventrally recurved rostrum as long as the carapace and positioned between a pair of backwards-facing pedunculate eyes. The body is homonomous, with approximately 40 weakly sclerotized segments bearing biramous legs with elongate endopods, and ends in a pair of small flap-like caudal rami. Fibulacaris nereidis is interpreted as a suspension feeder possibly swimming inverted, in a potential case of convergence with some branchiopods. A Bayesian phylogenetic analysis places it within a group closely related to the extinct Hymenocarina. Fibulacaris nereidis is unique in its carapace morphology and overall widens the ecological disparity of Cambrian arthropods and suggests that the evolution of a 'bivalved' carapace and an upside-down lifestyle may have occurred early in stem-group crustaceans.

Filter-feeding in Colonial Protists.

Many protists form cell colonies. Among them several are filter-feeders depending on suspended food particles such as bacteria. It has been suggested that the formation of colonies enhances feeding efficiency and implied that - in the case of colonial choanoflagellates - it was an adaptive trait that led to the evolution of metazoans. Here it is shown experimentally - for a colonial peritrich ciliate and for a choanoflagellate - that colony-formation does not enhance the efficiency of filter-feeding relative to solitary cells and that the adaptive significance of cell colony-formation must have some other explanation.

Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates.

Choanoflagellates, eukaryotes that are important predators on bacteria in aquatic ecosystems, are closely related to animals and are used as a model system to study the evolution of animals from protozoan ancestors. The choanoflagellate Salpingoeca rosetta has a complex life cycle with different morphotypes, some unicellular and some multicellular. Here we use computational fluid dynamics to study the hydrodynamics of swimming and feeding by different unicellular stages of S. rosetta: a swimming cell with a collar of prey-capturing microvilli surrounding a single flagellum, a thecate cell attached to a surface and a dispersal-stage cell with a slender body, long flagellum and short collar. We show that a longer flagellum increases swimming speed, longer microvilli reduce speed and cell shape only affects speed when the collar is very short. The flux of prey-carrying water into the collar capture zone is greater for swimming than sessile cells, but this advantage decreases with collar size. Stalk length has little effect on flux for sessile cells. We show that ignoring the collar, as earlier models have done, overestimates flux and greatly overestimates the benefit to feeding performance of swimming versus being attached, and of a longer stalk for attached cells.

First large-scale ecological impact study of desalination outfall reveals trade-offs in effects of hypersalinity and hydrodynamics.

Desalination is an increasingly common method of meeting potable water demands, but the associated ecological risks are not well understood. Seawater desalination plants discharge large volumes of hypersaline brine directly into the ocean, raising concerns about potential impacts to marine life. In order to reduce impacts of brine, newer desalination outfalls are often fitted with high-pressure diffusers that discharge brine at high velocity into the water column, increasing the mixing and dilution of brine with ocean water. However, there are few published studies of marine impacts of desalination brine, and no well replicated before-after designs. Here we report a six-year study testing for impacts and subsequent recovery of sessile marine invertebrate recruitment near a desalination outfall with high-pressure diffusers. We used a Multiple Before-After-Control-Impact (MBACI) design to test for impacts and recovery at two distances (30 m and 100 m) from a 250 ML/day plant outfall, as well as a gradient design to test the strength of impacts relative to distance from the outfall. The diffusers achieved the target of less than 1 psµ salinity difference to surrounding ambient waters within 100 m of the discharge outfall, but sessile invertebrates were nonetheless impacted. Polychaetes, bryozoans and sponges reduced in cover as far as 100 m from the outfall, while barnacles showed the opposite pattern and were more abundant near the discharging outfall. Ecological impacts were disproportionate to the relatively minor change in salinity (∼1 psµ), suggesting a mechanism other than salinity. We propose that impacts were primarily driven by changes in hydrodynamics caused by the diffusers, such as higher near-bed flow away from the outfall. This is consistent with flow preferences of various taxonomic groups, which differ due to differences in settlement and feeding abilities. High-pressure diffusers designed to reduce impacts of hypersalinity may inadvertently cause impacts through hydrodynamics, leading to a trade-off in minimizing combined salinity and hydrodynamic stress. This study provides the first before-after test of ecological impacts of desalination brine on sessile marine communities, and rare insight into mechanisms behind impacts of a growing form of human disturbance.

Effects of concentration and size of suspended particles on the ingestion, reproduction and mortality rates of the copepod, Acartia tonsa.

Suspended sediments are a common occurrence in the marine environment. They can be generated by natural causes, including waves and currents, or brought about by anthropogenic activities such as reclamation and dredging. High sediment concentrations are known to have negative consequences on copepods; however, the impact of sediment size has largely been overlooked. Here we examine the effects of sediment size and concentration in combination with varying algae concentrations on the ingestion rate, egg production, hatching success and survivorship of the copepod species, Acartia tonsa. High concentration of 'small' sediments at 'low' food availability had the greatest negative impact on all parameters except hatching success. Greater food concentration was able to mitigate some of these effects. High concentrations of 'large' sediments also reduced egg production rates, possibly due to A. tonsa avoiding falling particles. We conclude that it is important to examine the particle size distribution when evaluating the impacts of suspended sediments on copepods.