Model-assisted measurements of suspension-feeding flow velocities.

Benthic marine suspension feeders provide an important link between benthic and pelagic ecosystems. The strength of this link is determined by suspension-feeding rates. Many studies have measured suspension-feeding rates using indirect clearance-rate methods, which are based on the depletion of suspended particles. Direct methods that measure the flow of water itself are less common, but they can be more broadly applied because, unlike indirect methods, direct methods are not affected by properties of the cleared particles. We present pumping rates for three species of suspension feeders, the clams Mya arenaria and Mercenaria mercenaria and the tunicate Ciona intestinalis, measured using a direct method based on particle image velocimetry (PIV). Past uses of PIV in suspension-feeding studies have been limited by strong laser reflections that interfere with velocity measurements proximate to the siphon. We used a new approach based on fitting PIV-based velocity profile measurements to theoretical profiles from computational fluid dynamic (CFD) models, which allowed us to calculate inhalant siphon Reynolds numbers (Re). We used these inhalant Re and measurements of siphon diameters to calculate exhalant Re, pumping rates, and mean inlet and outlet velocities. For the three species studied, inhalant Re ranged from 8 to 520, and exhalant Re ranged from 15 to 1073. Volumetric pumping rates ranged from 1.7 to 7.4 l h-1 for M. arenaria, 0.3 to 3.6 l h-1 for M. mercenaria and 0.07 to 0.97 l h-1 for C. intestinalis We also used CFD models based on measured pumping rates to calculate capture regions, which reveal the spatial extent of pumped water. Combining PIV data with CFD models may be a valuable approach for future suspension-feeding studies.

Diet of worms emended: an update of polychaete feeding guilds.

Polychaetes are common in most marine habitats and dominate many infaunal communities. Functional guild classification based on taxonomic identity and morphology has linked community structure to ecological function. The functional guilds now include osmotrophic siboglinids as well as sipunculans, echiurans, and myzostomes, which molecular genetic analyses have placed within Annelida. Advances in understanding of encounter mechanisms explicitly relate motility to feeding mode. New analyses of burrowing mechanics explain the prevalence of bilateral symmetry and blur the boundary between surface and subsurface feeding. The dichotomy between microphagous deposit and suspension feeders and macrophagous carnivores, herbivores, and omnivores is further supported by divergent digestive strategies. Deposit feeding appears to be limited largely to worms longer than 1 cm, with juveniles and small worms in general restricted to ingesting highly digestible organic material and larger, rich food items, blurring the macrophage-microphage dichotomy that applies well to larger worms.

Burrowing in marine muds by crack propagation: kinematics and forces.

The polychaete Nereis virens burrows through muddy sediments by exerting dorsoventral forces against the walls of its tongue-depressor-shaped burrow to extend an oblate hemispheroidal crack. Stress is concentrated at the crack tip, which extends when the stress intensity factor (KI) exceeds the critical stress intensity factor (KIc). Relevant forces were measured in gelatin, an analog for elastic muds, by photoelastic stress analysis, and were 0.015+/-0.001 N (mean +/- s.d.; N=5). Measured elastic moduli (E) for gelatin and sediment were used in finite element models to convert the forces in gelatin to those required in muds to maintain the same body shapes observed in gelatin. The force increases directly with increasing sediment stiffness, and is 0.16 N for measured sediment stiffness of E=2.7 x 10(4) Pa. This measurement of forces exerted by burrowers is the first that explicitly considers the mechanical behavior of the sediment. Calculated stress intensity factors fall within the range of critical values for gelatin and exceed those for sediment, showing that crack propagation is a mechanically feasible mechanism of burrowing. The pharynx extends anteriorly as it everts, extending the crack tip only as far as the anterior of the worm, consistent with wedge-driven fracture and drawing obvious parallels between soft-bodied burrowers and more rigid, wedge-shaped burrowers (i.e. clams). Our results raise questions about the reputed high energetic cost of burrowing and emphasize the need for better understanding of sediment mechanics to quantify external energy expenditure during burrowing.

Burrowing mechanics: burrow extension by crack propagation.

Until now, the analysis of burrowing mechanics has neglected the mechanical properties of impeding, muddy, cohesive sediments, which behave like elastic solids. Here we show that burrowers can progress through such sediments by using a mechanically efficient, previously unsuspected mechanism--crack propagation--in which an alternating 'anchor' system of burrowing serves as a wedge to extend the crack-shaped burrow. The force required to propagate cracks through sediment in this way is relatively small: we find that the force exerted by the annelid worm Nereis virens in making and moving into such a burrow amounts to less than one-tenth of the force it needs to use against rigid aquarium walls.

Inhibition of digestive enzyme activities by copper in the guts of various marine benthic invertebrates.

Digestive systems of deposit and suspension feeders can be exposed to high concentrations of copper (Cu) by ingestion of contaminated sediments. We assessed a potential impact of this Cu exposure on digestive enzyme activities in a wide range of benthic organisms by monitoring enzyme activities in their gut fluids during in vitro titrations with dissolved Cu, which mimics Cu solubilization from sediments. Increasing Cu inhibited digestive protease activities at threshold values, which varied widely among organisms, from 8 microM for an echinoderm to 0.4 M for an echiuran. More Cu was required to inhibit proteases in guts containing higher amino acid concentrations because strong Cu-binding sites on amino acids prevent Cu interaction with the enzymatically active sites. Threshold Cu concentrations were similar for proteases, esterases, lipases, and alpha- and beta-glucosidases, suggesting the same inhibition mechanism. Copper was less effective at inhibiting enzymes at lower pH, suggesting that protons can compete with Cu ion for binding to enzymatically active sites or that enzyme conformation is less vulnerable to Cu inhibition at lower pH. These results lead to the counterintuitive conclusion that deposit feeders with low enzyme activity, low amino acid concentration, and high pH values are most vulnerable to harm from sedimentary Cu by this mechanism, although they solubilize less sedimentary Cu than their counterparts with high enzyme activity, high amino acid concentrations, and low gut pH. In general, digestive systems of echinoderms may therefore be more susceptible to Cu contamination than those of polychaetes, with various other phyla showing intermediate susceptibilities. If threshold Cu values are converted to solid-phase sedimentary Cu concentrations, the thresholds are at least consistent with Cu loadings that have been observed to lead to biological impacts in the field.

Animal Guts as Ideal Chemical Reactors: Maximizing Absorption Rates.

I solved equations that describe coupled hydrolysis in and absorption from a continuously stirred tank reactor (CSTR), a plug flow reactor (PFR), and a batch reactor (BR) for the rate of ingestion and/or the throughput time that maximizes the rate of absorption (=gross rate of gain from digestion). Predictions are that foods requiring a single hydrolytic step (e.g., disaccharides) yield ingestion rates that vary inversely with the concentration of food substrate ingested, whereas foods that require multiple hydrolytic and absorptive reactions proceeding in parallel (e.g., proteins) yield maximal ingestion rates at intermediate substrate concentrations. Counterintuitively, then, animals acting to maximize their absorption rates should show compensatory ingestion (more rapid feeding on food of lower concentration), except for the lower range of diet quality for complex diets and except for animals that show purely linear (passive) uptake. At their respective maxima in absorption rates, the PFR and BR yield only modestly higher rates of gain than the CSTR but do so at substantially lower rates of ingestion. All three ideal reactors show milder than linear reduction in rate of absorption when throughput or holding time in the gut is increased (e.g., by scarcity or predation hazard); higher efficiency of hydrolysis and extraction offset lower intake. Hence adding feeding costs and hazards of predation is likely to slow ingestion rates and raise absorption efficiencies substantially over the cost-free optima found here.

Animal Guts as Nonideal Chemical Reactors: Partial Mixing and Axial Variation in Absorption Kinetics.

Animal guts have been idealized as axially uniform plug-flow reactors (PFRs) without significant axial mixing or as combinations in series of such PFRs with other reactor types. To relax these often unrealistic assumptions and to provide a means for relaxing others, I approximated an animal gut as a series of n continuously stirred tank reactors (CSTRs) and examined its performance as a function of n. For the digestion problem of hydrolysis and absorption in series, I suggest as a first approximation that a tubular gut of length L and diameter D comprises [Formula: see text] tanks in series. For [Formula: see text], there is little difference between performance of the nCSTR model and an ideal PFR in the coupled tasks of hydrolysis and absorption. Relatively thinner and longer guts, characteristic of animals feeding on poorer forage, prove more efficient in both conversion and absorption by restricting axial mixing. In the same total volume, they also give a higher rate of absorption. I then asked how a fixed number of absorptive sites should be distributed among the n compartments. Absorption rate generally is maximized when absorbers are concentrated in the hindmost few compartments, but high food quality or suboptimal ingestion rates decrease the advantage of highly concentrated absorbers. This modeling approach connects gut function and structure at multiple scales and can be extended to include other nonideal reactor behaviors observed in real animals.

Gut architecture, digestive constraints and feeding ecology of deposit-feeding and carnivorous polychaetes.

We analyze gut architectures of 42 species of marine polychaetes in terms of their anatomically distinct compartments, and quantify differences among guts in terms of ratios of body volume to gut volume, relative compartmental volumes, total gut aspect ratios and compartmental aspect ratios. We use multivariate techniques to classify these polychaetes into 4 groups: carnivores with tubular guts; deposit feeders with tubular guts; deposit feeders with 3 gut compartments; and deposit feeders with 4 or 5 gut compartments. Tubular guts, morphological expressions of plug flow, are common among deposit feeders and may allow relatively rapid ingestion rates and short throughput times. Median gut volume per unit of body volume in deposit feeders (31%) is twice that of carnivores (15%) and ranges up to 83% in one deep-sea species. Deep-sea deposit feeders tend to have relatively larger and longer guts than closely-related nearshore and shelf species. Guts of a number of deep-sea deposit feeders and nearshore and shelf deposit feeders from muddy environments are relatively longer and narrower as body size increases, suggesting that digestive diffusion limitations may be important. Gut volume scales as (body volume)1 while ingestion rate scales as (body volume)0.7. If diet and the chemical kinetics of digestion do not change appreciably, throughput time and thus the extent of digestion of given dietary components therefore must increase as a deposit feeder grows. Digestive processing constrainst may be most important in juveniles of species (especially those species with plug-flow guts) that are deposit feeders as adults.

Competition among the pioneers in a seasonal soft-bottom benthic succession: field experiments and analysis of the Gilpin-Ayala competition model.

Controlled experiments, designed to assess the effects of pioneers on succession on an intertidal sandflat, provided evidence for interspecific competition between juvenile Hobsonia florida (Polychaeta, Ampharetidae) and oligochaetes. The field data were fitted to both the linear Volterra and non-linear Gilpin-Ayala competition equations. With its greater number of parameters, the Gilpin-Ayala model must provide a better fit to observed population abundances. The Gilpin-Ayala model is flawed as an explanation of the population trajectories of the H. florida and oligochaetes, because its non-linearity parameter affects only intraspecific competion. With either model our field data demonstrate a solution to Hutchinson's paradox. With competition coefficients near unity and similar carrying capacities, the predicted population trajectories are heavily dependent on initial conditions. The predicted times to competitive exclusion are long and can easily exceed the typical period of environmental constancy. Our study offers evidence for Neill's competitive bottleneck: competition acts primarily on the developmental stages of one of a pair of competing species. The permanent meiofauna may act as a competitive bottleneck for the population growth of benthic macrofauna. The mechanism of this competitive interaction probably involves exploitative interspecific competition for benthic diatoms.