Peter A. Jumars

Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals

Abstract A new extension of digestion theory and re-interpretation of published empirical evidence suggest that the principal pathway of dissolved organic carbon (DOC) from phytoplankton to bacteria is through the byproducts of animal ingestion and digestion rather than via excretion of DOC directly from intact phytoplankton. Simple model calculations reveal that for a substance with diffusion coefficient equalling 10−5 cm2 s−1, excess (over ambient) concentrations of solute in a fecal pellet of typical size (diam. ⩽ 1 mm) are lost rapidly; ⩾ 50% of any excess is diffused out of the pellet within 5 min—even in a stagnant water column and without particle sinking. Reasons for rapid loss and its insensitivity to fluid dynamic conditions are small size of the pelletal reservoir and the sharp concentration gradient between pelletal and ambient concentrations upon pellet release. As a consequence, most solutes initially contained in fecal pellets of zooplankton generally will remain in the 10–100 m thick water layer within which the pellets initially are deposited. Focus on animal-caused organic release over these very short time scales may help to resolve some of the growing paradoxes of DOC standing stocks and fluxes in the upper ocean.

Abyssal community analysis from replicate ☐ cores in the central North Pacific

Abstract A 0·25 m 2 United States Naval Electronics Laboratory ☐ corer was used to take replicate samples from an oligotrophic bottom under the North Pacific Central Water Mass (∼ 28°N, 155°W). The bottom is a red clay with manganese nodules at a depth of 5500–5800 m. Macrofaunal density ranges from 84 to 160 individuals per m 2 and is therefore much the same as in Northwest Atlantic Gyre waters. Of the macrofaunal taxa, polychaetes dominate (55%), followed by tanaids (18%), bivalves (7%), and isopods (6%). Meiofaunal taxa were only partially retained by the 297 μm screen used in washing. Even then, they are 1·5–3·9 times as abundant as the macrofaunal taxa, with nematodes being numerically dominant by far. Foraminifera seem to comprise an important portion of the community, but could not be assessed accurately because of the inability to discriminate living and dead tests. Remains of what are probably xenophyophoridans are also very important, but offer the same problem. Faunal diversity is extremely high, with deposit feeders comprising the overwhelming majority. Most species are rare, being encountered only once. The distributions of only three species show any significant deviation from randomness. The polychaete fauna from ☐ cores collected from 90 miles to the north was not significantly different from that of the principal study locality. Concordance appeared at several taxonomic levels, from species through macrofaunal/meiofaunal relationships. As a result, the variation in total animal abundance shows aggregation among cores. We discuss Sokolovas concept of a deep-sea oligotrophic zone dominated by suspension feeders, and reconcile it with our present findings. The high diversity of the fauna combined with the low food level contradict theories that relate diversity directly with productivity.

Modeling Animal Guts as Chemical Reactors

Chemical-reactor theory recognizes three ideal reactor types: batch reactors, which are filled with reactants, continuously stirred during the reaction, and then emptied of products after a given reaction period; plug-flow reactors (PFRs), in which reactants continuously enter and products continuously exit with no mixing along the flow path; and continuous-flow, stirred-tank reactors (CSTRs), in which reactants continuously enter and products continuously leave a stirred vessel. Performance equations for these reactors, together with kinetic models for simple enzymatic catalysis and microbially mediated (autocatalytic) digestive fermentation, reveal necessary functional relationships among initial concentrations of the limiting food component, gut volume, throughput time or gut holding time, and digestive reaction kinetics. We use these models to suggest optimization constraints for digestion, analogous to those of optimal foraging theory. Two general predictions are possible. To sustain the greatest digestive production rate in minima of throughput time and gut volume, an animal dependent on its own digestive enzymes should function as a PFR. Animals fermenting refractory materials should combine a CSTR and a PFR in series at all but the slowest throughput rates, when a PFR will suffice. We make specific predictions for deposit feeders because they digest little of the ingested volume, greatly simplifying digestive performance equations and making them ideal subjects for initial tests of our models. The majority conform to the prediction of PFR guts, but some deposit feeders apparently use CSTR-PFR series (terebellimorph polychaetes) and batch processing (asteroids and ophiuroids). We suggest that terebellimorph polychaetes may use the CSTR to overcome digestive-rate constraints imposed by diffusion limitations; asteroids and ophiuroids may use a variety of foraging modes to obtain the highest-quality foods available. We also apply reactor theory to mammalian fermenters because empirical feeding information is extensive. Specifically, we compare the dynamics of foregut versus hindgut fermentation. Foregut fermenters should optimize fermentation with respect to ingested foods and optimize subsequent catalytic digestion with respect to fermentation products. In contrast, hindgut fermenters should optimize foregut catalytic digestion and then optimize fermentation of the residue. According to the principles of dynamic programming, the first digestive stage in each case sets the pace of digesta throughput: slower in foregut fermenters than in hindgut fermenters of similar size. Hindgut fermentation is seen to be competitive, especially for small animals, when food quality is high or variable or when body size is large and throughput rate set in the foregut is slow enough for hindgut fermentation to yield high conversion. Coprophagy and caecotrophy, tactics used by small hindgut fermenters to increase throughput time and utilization of fermentation digesta, are easily understood in terms of industrial recycle-reactor equivalents. A great advantage in deriving models of digestion from reactor theory is that many foreseeable modifications (e.g., explicit incorporation of volume changes during digestion or of coprophagy) to ideal models have analogues in diverse industrial reactor configurations already modeled and tested.

Effects of biological activity on the entrainment of marine sediments

Nowell, A.R.M., Jumars, P.A. and Eckman, J.E., 1981. Effects of biological activity on the entrainment of marine sediments. Mar. Geol., 42: 133-153. The effects of animal tracks and fecal pellet production on the critical entrainment velocity of marine sediments were examined experimentally. Laboratory measurements in a free-surface, seawater flume were made using three sediment sizes. Effects of three species of polychaetes and two species of bivalves were tested. Boundary shear velocity was calculated from the mean velocity profile in the logarithmic region of the boundary layer. Measurements were made with a hot film anemometer. Tracking doubled the boundary roughness and decreased the critical entrainment velocity by 20%. Ambient or “free” sediments were more easily entrained than fecal mounds, which were restrained from movement by mucous adhesion between the fecal coils. Isolated pellets, such as those egested by Amphicteis scaphobranchiata, transported readily as bedload over a cohesive sediment surface.

Deep-sea deposit-feeding strategies suggested by environmental and feeding constraints

The principle of lost opportunity from optimal foraging theory, coupled with recent information about fluxes in the deep sea, allows prediction of feeding behaviours potentially specific to deep-sea deposit feeders. One possible strategy, thus far documented only indirectly, is to ‘ squirrel ’ away rich food from the seasonal or episodic pulses that recently have been shown to fuel meiofaunal growth. Echiurans and sipunculids show morphological and faecal handling patterns consonant with this suggestion. Where it is prevalent, this foraging strategy can have profound effects on stratigraphy. Autocoprophagy is another expected behaviour across a wider taxonomic spectrum, but one that is especially difficult to document. The principle of lost opportunity also predicts highly selective ingestion, not necessarily accomplished by the assessment of individual particles but possibly through pit building in areas where fluids move near-bed material. Under many depositions regimes, small but abundant feeding depressions may be the primary sites where deposition occurs. Conversely, digestive utilization of heterogeneous refractory substrates like humic acids seems as unlikely as an effective municipal waste recycling system that starts with mixed garbage. High gut: body volume ratios in deep-sea deposit feeders, rather than representing an adaptation to use this heterogeneous and refractory end of the food spectrum, instead may allow (through greater residence time of ingested material) greater conversion and absorption of the labile fraction of sediments as it becomes scarcer. Intense natural selection for particle selection ability in fact is one possible reason for the prevalence of meiofauna in the deep sea, and for the diminutive size of macrofaunal taxa there. This selective pressure probably imposes a very restrictive bottleneck on the initial developmental stages of deposit feeders.

Bubble growth and rise in soft sediments

The mechanics of uncemented soft sediments during bubble growth are not widely understood and no rheological model has found wide acceptance. We offer definitive evidence on the mode of bubble formation in the form of X-ray computed tomographic images and comparison with theory. Natural and injected bubbles in muddy cohesive sediments are shown to be highly eccentric oblate spheroids (disks) that grow either by fracturing the sediment or by reopening preexisting fractures. In contrast, bubbles in soft sandy sediment tend to be spherical, suggesting that sand acts fluidly or plastically in response to growth stresses. We also present bubble-rise results from gelatin, a mechanically similar but transparent medium, that suggest that initial rise is also accomplished by fracture. Given that muddy sediments are elastic and yield by fracture, it becomes much easier to explain physically related phenomena such as seafloor pockmark formation, animal burrowing, and gas buildup during methane hydrate melting.

FACILITATION OF SOFT-BOTTOM BENTHIC SUCCESSION BY TUBE BUILDERS'

2School of Oceanography, University of Washington,Seattle, Washington 98195 USAAbstract. Controlled field experiments were used to test the effects of surface-deposit feederson succession at the Skagit flats, an intertidal sandflat in northern Puget Sound . The tube buildersHobsonio florida (Polychaeta, Ampharetidae), Pseudopolydora kempi japonica (Polychaeta, Spioni-dae), and Tanais sp. (Crustacea, Peracarida) facilitate the recruitment of other taxa to 10-cm 2 azoicpatches. Simulated animal tubes facilitated the immigration of Tanais sp. and oligochaetes. Macomabalthica, a tellinid bivalve, facilitated the immigration of H. Florida, while inhibiting that of Tanaissp. These experiments clearly documented that facilitation rather than inhibition is the dominantprocess governing succession in the Skagit community. The facilitation model of succession offers aviable alternate explanation for many soft-bottom benthic processes previously explained by theinhibition model.Key words: community structure; controlled manipulations; facilitation; infauna; polychaetes;succession; tube builders.

A Predictive Model of Bacterial Foraging by Means of Freely Released Extracellular Enzymes

A bstractExtracellular enzymes are important agents for microbial foraging and material cycling in diverse natural and man-made systems. Their abundance and effects are analyzed empirically on scales much larger than the forager. Here, we use a modelling approach to analyze the potential costs and benefits, to an individual immobile microbe, of freely releasing extracellular enzymes into a fluid-bathed, stable matrix of both inert and food-containing particles. The target environments are marine aggregates and sediments, but the results extend to biofilms, bioreactors, soils, stored foods, teeth, gut contents, and even soft tissues attacked by disease organisms. Model predictions, consistent with macroscopic observations of enzyme activity in laboratory and environmental samples, include: support of significant bacterial growth by cell-free enzymes; preponderance of particle-attached, as opposed to dissolved, cell-free enzymes; solubilization of particulate substrates in excess of resident microbe growth requirements; and constitutive, abundant enzyme release in some environments. Feeding with cell-free enzymes appears to be limited to substrates within a well-defined distance of the enzyme source. Fluxes of dissolved organic material out of pelagic oceanic aggregates and marine sediments, and difficulty detecting dissolved enzymes in such environments, may reflect characteristics of cell-free enzyme foraging and properties of the enzymes. Our calculations further suggest that cell-free enzymes may often be used by microorganisms as the fastest means to search for food.

Induction of suspension feeding in spionid polychaetes by high particulate fluxes

The feeding behavior of three species of spionid polychaetes varied with water velocity. At moderate flows the worms ceased deposit feeding, formed their feeding tentacles into helices, and lifted them into the water column to capture material in suspension. This behavior was apparently a response to increased flux of suspended matter at high flows rather than to flow velocity alone. Organisms capable of switching their feeding behavior may be common in dynamically variable benthic environments.

Digestive environments of benthic macroinvertebrate guts: Enzymes, surfactants and dissolved organic matter

Hydrolytic enzyme activity, surfactancy, and dissolved organic matter in the digestive lumens of 19 benthic echinoderm and polychaete species were examined, using consistent and quantifiable methods. Enzyme activities were compared with those of extracellular enzymes from ambient sediments. Enzyme activities ranged over five orders of magnitude, with averages decreasing in the order polychaetes > echinoderms > sediment. Highest activities in animals were usually associated with the fluid phase in midgut sections, with posteriorward decreases indicating little export to the external environment. At some phyletic levels, activity correlated inversely with animal size. Hydrolase patterns reflected food type; for example, high 1ipase:protease ratios in carnivores reflected esterified lipids in their diets. High surfactant activity was found in gut sections having high enzyme activity. Deposit feeders had the most intense surfactancy, including evidence for micelles. While enzymes reflected the biochemical nature of the digestible food substrate regardless of feeding mode (e.g., deposit vs. suspension feeder), surfactants reflected dilution of this digestible substrate with mineral grains. Dissolved organic matter levels were high, with amino acids reaching levels > 1 M and lipids commonly 1 g L-r. Among polychaete deposit-feeders, low molecular weight amino acids reflected the composition of the food substrate, but were present at much higher concentrations than could be explained by sediment present in the gut-suggesting longer residence times for fluid than for transiting sediment particles. Deposit feeder digestive fluids are better able to solubilize sedimentary food substrates than are sedimentary extracellular enzymes, owing to either more powerful solubilizing agents or to their deployment in freely diffusing, dissolved form. Gut environments may lead to chemical condensation as well as solubilization reactions.