Kelly M. Dorgan

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

SUMMARY 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=2.7×104 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.

Worms as wedges: Effects of sediment mechanics on burrowing behavior

Recent studies document linear elastic response of muddy marine sediments to load and deformation on temporal and spatial scales relevant to animal movement, with burrowers making openings for movement in such sediments by fracture. Cracks propagate through linear elastic solids in mode I (opening-mode crack growth) when the stress intensity factor (KI) at the crack tip exceeds the material’s fracture toughness (KIc). Fracture mechanics depend on material stiffness as well as fracture toughness, and we prepared a range of transparent gels that varied in stiffness and fracture toughness to assess the dependence of burrowing behavior on these material properties. When the polychaete Nereis virens elongated its burrow, it altered its body shape and behavior across these gels in a manner consistent with fracture mechanics theory. We modeled burrow elongation as stable, wedge-driven crack growth, and calculated that KI values at the tips of the burrows reached KIc values of most gels without pharynx eversion and exceeded KIc when the pharynx was everted. In materials with higher fracture toughnesses, worms everted their pharynges to become thicker and blunter wedges, as predicted from simple wedge theory. In stiff materials with low toughness, worms moved their heads from side-to-side to extend crack edges laterally, relieving elastic forces compressing them and allowing them to maintain body shape more easily. This solution extends the crack in small increments that each require relatively little force. We introduce a dimensionless “wedge” number to characterize the relative importance of work to fracture the material and extend the burrow and work to maintain body shape against the elastic restoring force of the material. The mechanism of burrowing by crack propagation is utilized across a range of material properties found in natural muds, and variation in these properties strongly influences burrowing behaviors. These results demonstrate how quantifying the mechanical properties of muds can improve our understanding of bioturbation. On spatial and temporal scales relevant to burrower activity, variations in these properties may impact particle mixing by influencing burrower behavior.

The biomechanics of burrowing and boring.

Burrowers and borers are ecosystem engineers that alter their physical environments through bioturbation, bioirrigation and bioerosion. The mechanisms of moving through solid substrata by burrowing or boring depend on the mechanical properties of the medium and the size and morphology of the organism. For burrowing animals, mud differs mechanically from sand; in mud, sediment grains are suspended in an organic matrix that fails by fracture. Macrofauna extend burrows through this elastic mud by fracture. Sand is granular and non-cohesive, enabling grains to more easily move relative to each other, and macrofaunal burrowers use fluidization or plastic rearrangement of grains. In both sand and mud, peristaltic movements apply normal forces and reduce shear. Excavation and localized grain compaction are mechanisms that plastically deform sediments and are effective in both mud and sand, with bulk excavation being used by larger organisms and localized compaction by smaller organisms. Mechanical boring of hard substrata is an extreme form of excavation in which no compaction of burrow walls occurs and grains are abraded with rigid, hard structures. Chemical boring involves secretion to dissolve or soften generally carbonate substrata. Despite substantial differences in the mechanics of the media, similar burrowing behaviors are effective in mud and sand.

It's tough to be small: dependence of burrowing kinematics on body size

SUMMARY Burrowing marine infauna are morphologically diverse and range in size over several orders of magnitude. Whilst effects of ontogenetic and morphological differences on running, flying and swimming are relatively well understood, similar analyses of burrowing mechanics and kinematics are lacking. The polychaete Nereis virens Sars extends its burrow by fracture, using an eversible pharynx to exert force on the walls of the burrow. The resulting stress is amplified at the anterior tip of the burrow, which extends when the stress exceeds the fracture toughness of the material. Here we show that the polychaete Cirriformia moorei extends its burrow by a similar mechanism, but by using its hydrostatic skeleton rather than an eversible pharynx. Based on the dimensionless wedge number, which relates work of fracture to work to maintain body shape against the elasticity of sediment, we predicted that smaller worms would exhibit behaviors characteristic of tougher sediments and that scaling of kinematics would reflect decreasing difficulty in fracturing sediment with increasing body size. We found that smaller worms were relatively blunter and thicker, and had a greater variation of thickness than larger worms as they burrowed. Although these kinematic differences increase the stress amplification at the crack tip, smaller worms still generate lower stress intensity factors. The greater relative body thickness and shape changes of smaller worms are consistent with ontogenetic changes in forces exerted by earthworms, and are likely driven by the challenge of exerting enough stress to extend a crack with a small body size.

Meandering worms: mechanics of undulatory burrowing in muds

Recent work has shown that muddy sediments are elastic solids through which animals extend burrows by fracture, whereas non-cohesive granular sands fluidize around some burrowers. These different mechanical responses are reflected in the morphologies and behaviours of their respective inhabitants. However, Armandia brevis, a mud-burrowing opheliid polychaete, lacks an expansible anterior consistent with fracturing mud, and instead uses undulatory movements similar to those of sandfish lizards that fluidize desert sands. Here, we show that A. brevis neither fractures nor fluidizes sediments, but instead uses a third mechanism, plastically rearranging sediment grains to create a burrow. The curvature of the undulating body fits meander geometry used to describe rivers, and changes in curvature driven by muscle contraction are similar for swimming and burrowing worms, indicating that the same gait is used in both sediments and water. Large calculated friction forces for undulatory burrowers suggest that sediment mechanics affect undulatory and peristaltic burrowers differently; undulatory burrowing may be more effective for small worms that live in sediments not compacted or cohesive enough to extend burrows by fracture.

Energetics of burrowing by the cirratulid polychaete Cirriformia moorei

SUMMARY Burrowing through marine sediments has been considered to be much more energetically expensive than other forms of locomotion, but previous studies were based solely on external work calculations and lacked an understanding of the mechanical responses of sediments to forces applied by burrowers. Muddy sediments are elastic solids through which worms extend crack-shaped burrows by fracture. Here we present data on energetics of burrowing by Cirriformia moorei. We calculated the external energy per distance traveled from the sum of the work to extend the burrow by fracture and the elastic work done to displace sediment as a worm moves into the newly formed burrow to be 9.7 J kg–1 m–1 in gelatin and 64 J kg–1 m–1 in sediment, much higher than for running or walking. However, because burrowing worms travel at slow speeds, the increase in metabolic rate due to burrowing is predicted to be small. We tested this prediction by measuring aerobic metabolism (oxygen consumption rates) and anaerobic metabolism (concentrations of the anaerobic metabolite tauropine and the energy-storage molecule phosphocreatine) of C. moorei. None of these components was significantly different between burrowing and resting worms, and the low increases in oxygen consumption rates or tauropine concentrations predicted from external work calculations were within the variability observed across individuals. This result suggests that the energy to burrow, which could come from aerobic or anaerobic sources, is not a substantial component of the total metabolic energy of a worm. Burrowing incurs a low cost per unit of time.

Burrow extension with a proboscis: mechanics of burrowing by the glycerid Hemipodus simplex

Burrowing marine infauna are morphologically diverse and ecologically important as ecosystem engineers. The polychaetes Nereis virens and Cirriformia moorei extend their burrows by crack propagation. Nereis virens does so by everting its pharynx and C. moorei, lacking an eversible pharynx or proboscis, uses its hydrostatic skeleton to expand its anterior. Both behaviors apply stress to the burrow wall that is amplified at the tip of the crack, which extends by fracture. That two species with such distinct morphologies and life histories both burrow by fracturing sediment suggests that this mechanism may be widespread among burrowers. We tested this hypothesis with the glycerid polychaete Hemipodus simplex, which has an eversible proboscis that is much longer and everts more rapidly than the pharynx of N. virens. When the proboscis is fully everted, the tip flares out wider than the rest of the proboscis, creating a shape and applying a stress distribution similar to that of N. virens and resulting in relatively large forces near the tip of the crack. These forces are larger than necessary to extend the crack by fracture and are surprisingly uncorrelated with the resulting stress amplification at the crack tip, which is also larger than necessary to extend the burrow by fracture. These large forces may plastically deform the mud, allowing the worm to build a semi-permanent burrow. Our results illustrate that similar mechanisms of burrowing are used by morphologically different burrowers.

Anchor Ice and Benthic Disturbance in Shallow Antarctic Waters: Interspecific Variation in Initiation and Propagation of Ice Crystals

Sea ice typically forms at the ocean’s surface, but given a source of supercooled water, an unusual form of ice—anchor ice—can grow on objects in the water column or at the seafloor. For several decades, ecologists have considered anchor ice to be an important agent of disturbance in the shallow-water benthic communities of McMurdo Sound, Antarctica, and potentially elsewhere in polar seas. Divers have documented anchor ice in the McMurdo communities, and its presence coincides with reduced abundance of the sponge Homaxinella balfourensis, which provides habitat for a diverse assemblage of benthic organisms. However, the mechanism of this disturbance has not been explored. Here we show interspecific differences in anchor-ice formation and propagation characteristics for Antarctic benthic organisms. The sponges H. balfourensis and Suberites caminatus show increased incidence of formation and accelerated spread of ice crystals compared to urchins and sea stars. Anchor ice also forms readily on sediments, from which it can grow and adhere to organisms. Our results are consistent with, and provide a potential first step toward, an explanation for disturbance patterns observed in shallow polar benthic communities. Interspecific differences in ice formation raise questions about how surface tissue characteristics such as surface area, rugosity, and mucus coating affect ice formation on invertebrates.

Burrowing Behavior in Mud and Sand of Morphologically Divergent Polychaete Species (Annelida: Orbiniidae)

Muddy and sandy sediments have different physical properties. Muds are cohesive elastic solids, whereas granular beach sands are non-cohesive porous media. Infaunal organisms such as worms that burrow through sediments therefore face different mechanical challenges that potentially lead to a variety of burrowing strategies and morphologies. In this study we compared three morphologically distinct polychaete species representing different clades in the family Orbiniidae and related differences in their burrowing behaviors and morphologies to their natural environments (mud or sand). Worms burrowed in transparent analogs for muds and sands, and kinematic analysis showed differences both among species and between materials. Leitoscoloplos pugettensis lives in mud and burrows by fracture, using its pointed head to concentrate stress at the tip of the burrow. Naineris dendritica lives in sand and uses its broader head that fluctuates in width over a burrowing cycle to decrease backward slipping in sand, potentially preventing burrow collapse. Orbinia johnsoni lives in sand and uses internal body expansions to pack sand grains, another mechanism to prevent burrow collapse. By combining data from species and materials to obtain a broad range of burrowing velocities, we show that burrowing worms control their velocity by increasing or decreasing their burrowing frequency rather than by altering cycle distance as shown previously for crawling earthworms. This study demonstrates how fairly small evolutionary divergences in morphologies and behaviors facilitate locomotion in environments with different physical constraints.