Burrowing dynamics and energy cost of transport in the soft-bodied marine invertebrates Polyphysia crassa and Priapulus caudatus

The dynamics and mechanical forces generated during burrowing in Polyphysia crassa (Annelida: Polychaeta) and Priapulus caudatus (Priapulida) were investigated. Both animals live in soft marine muds and burrow by utilizing a direct peristaltic wave alternating with a high internal pressure event which thrusts the anterior part of the body into the substratum. Forces generated during the various phases of a typical burrowing cycle were measured in animals moving beneath the natural substratum at 5±3 °C using electronic transducers and recorder. During 'head' advance Polyphysia generated 0.027 N, and during 'tail' advance 0.020 N, with peak internal pressures averaging 0.95 kPa (= 0.095 N/cm²). Force by Priapulus during head advance and tail advance was 0.081 N and 0.121 N, respectively, with peak internal pressures averaging 2.47 kPa (= 0.247 N/cm²). Polyphysia moves more slowly (0.24 cm/min) than does Priapulus (0.76 cm/min) and expends more energy on mass moved per unit distance. These force measurements during a burrowing cycle were used in place of respirometry as a basis for computation of net cost of transport (NCT) for each animal. NCT for Polyphysia was 635 J kg^-1 m^-1 and for Priapulus was 314Jkg^-1m^-l. Cost of transport for all burrowing animals thus far investigated is high compared to swimming, running and flying. For soft-bodied invertebrates that live an entirely buried existence this high cost must be interpreted in the broader context of the adaptive value of infaunal life, especially protection against predation, and not as simply a means of moving about.     

Burrowing of Priapulus caudatus (Vermes) and the significance of the direct peristaltic wave

Priapulus caudatus is an active predatory animal found burrowing in soft mud. It may employ relatively high body fluid pressures during escape reactions (up to 6 kPa recorded) but normal burrowing probably involves much lower pressures (< 2 kPa). Three points d'appui are formed during the burrowing cycle. A characteristic direct peristaltic wave (DPW) occurs at a low pressure stage in each cycle (<0–5 kPa). The DPW is regarded as an adaptation to burrowing in soft mud. Its function appears to be to transfer body wall anteriorily, providing "slack", which is used to allow the trunk to extend forward into the cavity vacated by retraction of the large praesoma at the end of each cycle. The circular and longitudinal muscles of the posterior trunk act synergically through most of the burrowing cycle.     

Burrowing,Locomotion and Other Movements of the Echiuran Ochetostoma caudex

Burrowing, iocomotory and other movements of the echiuran Ochetostoma caudex have been examined and discussed. A continuous body cavity enables the worm to undergo peristaltic waves to pump water through the burrow without causing locomotion. The animal is capable of both forward and backward locomotion in its burrow. During forward locomotion, retrograde peristaltic waves are utilized which advance the animal in a step-wise fashion. Pressure changes within the coelom during burrowing, locomotion and during irrigation movements have been measured with the use of electronic recording techniques and the results interpreted in relation to direct visual observation. The structural and functional specializations for burrowing are discussed and compared with the activities of Priapulus caudatus, Sipunculus nudus and Bonellia viridis.     

Machaeridian locomotion

The discovery that machaeridians (class Machaeridia Withers, 1926) are annelids allows their mode of locomotion to be interpreted in the context of the body plan of this phylum. The Plumulitidae were errant epibenthic forms, moving with parapodia. The body of Turrilepadidae and Lepidocoleidae, however, was enclosed largely within the mineralized plates that make up the skeleton. Articulated specimens indicate that these machaeridians were able to burrow like other annelids using peristaltic locomotion. A lepidocoleid specimen indicates that multiple waves of shortened and contracted regions moved over the body. This is in contrast to the mode of locomotion in earthworms and most polychaetes, but similar to peristaltic progression in Polyphysia (Scalibregmidae). Either the rugose sculpture (turrilepadids) and/or the margins of the overlapping shell plates functioned as a burrowing sculpture, allowing forward movement but preventing backwards slipping. A trace from the Devonian Hunsrück Slate associated with a lepidocoleid indicates that considerable flexing of the skeleton was possible, but this is an escape trace and does not represent normal locomotion. Features of the skeleton of machaeridians are convergent on those of molluscs where the shells likewise function in protection and burrowing.     

Relating divergence in polychaete musculature to different burrowing behaviors: A study using opheliidae (Annelida)

Divergent morphologies among related species are often correlated with distinct behaviors and habitat uses. Considerable morphological and behavioral differences are found between two major clades within the polychaete family Opheliidae. For instance, Thoracophelia mucronata burrows by peristalsis, whereas Armandia brevis exhibits undulatory burrowing. We investigate the anatomical differences that allow for these distinct burrowing behaviors, then interpret these differences in an evolutionary context using broader phylogenetic (DNA‐based) and morphological analyses of Opheliidae and taxa, such as Scalibregmatidae and Polygordiidae. Histological three‐dimensional‐reconstruction of A. brevis reveals bilateral longitudinal muscle bands as the prominent musculature of the body. Circular muscles are absent; instead oblique muscles act with unilateral contraction of longitudinal muscles to bend the body during undulation. The angle of helical fibers in the cuticle is consistent with the fibers supporting turgidity of the body rather than resisting radial expansion from longitudinal muscle contraction. Circular muscles are present in the anterior of T. mucronata, and they branch away from the body wall to form oblique muscles. Helical fibers in the cuticle are more axially oriented than those in undulatory burrowers, facilitating radial expansion during peristalsis. A transition in musculature accompanies the change in external morphology from the thorax to the abdomen, which has oblique muscles similar to A. brevis. Muscles in the muscular septum, which extends posteriorly to form the injector organ, act in synchrony with the body wall musculature during peristalsis: they contract to push fluid anteriorly and expand the head region following a direct peristaltic wave of the body wall muscles. The septum of A. brevis is much thinner and is presumably used for eversion of a nonmuscular pharynx. Mapping of morphological characters onto the molecular‐based phylogeny shows close links between musculature and behavior, but less correlation with habitat. J. Morphol. 275:548–571, 2014. © 2014 Wiley Periodicals, Inc.     

The hydraulic system in a burrowing worm, Priapulus caudatus

The function of the coelom as a locomotory hydraulic system in Priapulus caudatus has been examined and discussed. Pressure changes within the coelom during burrowing have been measured and used to monitor the activities of the muscular system.     

Onset of heartbeat revealed by successive structural changes in the developing single embryonic heart of the waterstrider (Gerris paludum insularis)

Videofilm images of the heartbeat in the living embryos of the waterstrider, Gerris paludum insularis, were analyzed to demonstrate successive changes in the width of the contractile heart at the different developmental stages. This information is graphically represented and termed structural cardiogram. Onset of the embryonic heartbeat characterized by anteriorly spreading peristaltic movement of the heart wall occurs at about 55% HL (percent heart length) as early as at about 81 h after katatrepsis (K+81 h embryo). This peristaltic wave occurs almost always following swinging movement of abdominal tip observed exclusively at this stage. Similar peristaltic wave of the heart wall may also be observed at later stages, exclusively in the anterior two-fifth of the heart. Conduction velocity of the peristaltic wave estimated from structural cardiogram of K+81 h embryo was approximately 0.57 mm/s; it was approximately 1.33 mm/s in the K+102 h embryos. In the posterior three-fifth of the heart, however, rhythmic movement was not peristaltic. Development of heartbeat generator in the specific region of the heart was discussed in relation to the onset of embryonic heartbeat.     

HYDRAULIC BURROWING IN THE BIVALVE MYA ARENARIA LINNAEUS (MYOIDEA) AND ASSOCIATED LIGAMENTAL ADAPTATIONS

The burrowing behaviour of the bivalve Mya arenaria from tidalflats of the Dutch Wadden Sea has been observed and recorded.Compared to other bivalves, M. arenaria is a very slow burrower,its burrowing behaviour being unique among bivalves since itis based essentially on the ejection of water through the pedalgape, with little assistance by the foot, which performs onlyan anchoring function. Water ejection is specially powerfuland individual jets may last several seconds, thus constitutingan effective means of removing sand from below the animal duringdigging. This hydraulic burrowing is more effective in loosesandy than in cohesive muddy substrates. Water ejection is providedby the ability of the bivalve to rock its valves across a dorsoventralaxis. This rocking motion implies special modifications of theligamental area. The ligament is conical in appearance and runsdorso-ventrally between the two chondrophores which are placedin two planes parallel to the cardinal axis. During rockingthe whole ligament acts in torsion and the lamellar layer ofthe ligament opposes closing of the anterior part of the valves.During normal adduction of the valves the ligament acts in bending,the axis of motion being placed internally with respect to thecardinal axis. This leads to approaching of the umbones withcomplete adduction and to resorption of the left umbo. Fromthe adaptive point of view, the slow hydraulic mode of burrowingis sufficient to cope with the slow sedimentation and erosionrates of the tidal flats in which M. arenaria lives. This burrowingmode implies the existence of a tiny foot, which leaves roomfor other organs within the mantle cavity. This, together withanterior divarication of the valves permits a large volume ofwater to be ejected from the mantle cavity, but, in the caseof M. arenaria, also the existence of an enormous stomach, possiblyas an adaptation for food processing. (Received 12 April 1996; accepted 2 October 1996)     

Strategies of burrowing in soft muddy sediments by diverse polychaetes

Muddy sediments are elastic solids through which morphologically diverse animals extend burrows by fracture. Muddy sediments inhabited by burrowing infauna vary considerably in mechanical properties, however, and at high enough porosities, muds can be fluidized. In this study, we examined burrowing behaviors and mechanisms of burrow extension for three morphologically diverse polychaete species inhabiting soft muddy sediments. Worms burrowed in gelatin, a transparent analog for muddy sediments, and in natural sediments in a novel viewing box enabling visualization of behaviors and sediment responses. Individuals of Scalibregma inflatum and Sternaspis scutata can extend burrows by fracture, but both also extended burrows by plastic deformation and by combinations of fracture and plastic deformation. Mechanical responses of sediments corresponded to different burrowing behaviors in Scalibregma; direct peristalsis was used to extend burrows by fracture or a combination of plastic deformation and fracture, whereas a retrograde expansive peristaltic wave extended burrows by plastic deformation. Burrowing speeds differed between behaviors and sediment mechanical responses, with slower burrowing associated with plastic deformation. Sternaspis exhibited less variability in behavior and burrowing speed but did extend burrows by different mechanisms consistent with observations of Scalibregma. Individuals of Ophelina acuminata did not extend burrows by fracture; rather individuals plastically deformed sediments similarly to individuals of the related Armandia brevis. Our results extend the range of natural sediments in which burrowing by fracture has been observed, but the dependence of burrow extension mechanism on species, burrowing behavior, and burrowing speed highlights the need for better understanding of mechanical responses of sediments to burrowers.     

Amoebocytes in the Lining of the Body Cavity and Mesenteries of Priapulus caudatus (Priapulida)

Nuclei associated with membranes lining the body cavity in Priapulus caudatus are shown by electron microscopy to be the nuclei of amoebocytes. The membranes themselves are not cellular and do not constitute a peritoneum. Mesenteries, present in the body cavity, also are not cellular; amoebocytes occasionally are found within them. These findings weaken the idea that priapulids are coelomates, although unequivocal proof that priapulids are pseudocoelomates would require a fine structural study of the early developmental stages.     

Burrowing with a kinetic snout in a snake (Elapidae: Aspidelaps scutatus)

Of the few elongate, fossorial vertebrates that have been examined for their burrowing mechanics, all were found to use an akinetic, reinforced skull to push into the soil, powered mostly by trunk muscles. Reinforced skulls were considered essential for head‐first burrowing. In contrast, I found that the skull of the fossorial shield‐nosed cobra (Aspidelaps scutatus ) is not reinforced and retains the kinetic potential typical of many non‐fossorial snakes. Aspidelaps scutatus burrows using a greatly enlarged rostral scale that is attached to a kinetic snout that is independently mobile with respect to the rest of the skull. Two mechanisms of burrowing are used: (1) anteriorly directed head thrusts from a loosely bent body that is anchored against the walls of the tunnel by friction, and (2) side‐to‐side shovelling using the head and rostral scale. The premaxilla, to which the rostral scale is attached, lacks any direct muscle attachments. Rostral scale movements are powered by, first, retractions of the palato‐pterygoid bar, mediated by a ligament that connects the anterior end of the palatine to the transverse process of the premaxilla and, second, by contraction of a previously undescribed muscle slip of the m. retractor pterygoidei that inserts on the skin at the edge of the rostral scale. In derived snakes, palatomaxillary movements are highly conserved and power prey capture and transport behaviors. Aspidelaps scutatus has co‐opted those mechanisms for the unrelated function of burrowing without compromising the original feeding functions, showing the potential for evolution of functional innovations in highly conserved systems.     

Distribution,substratum preference and burrowing behaviour of Lovenia elongata (Gray) (Echinoidea: Spatangoida) in the Gulf of Elat ('Aqaba), Red Sea

Lovenia elongata (Gray), the Indo-West Pacific spatangoid, was studied in the Gulf of Elat ('Aqaba) at the northern end of the Red Sea. The occurrence and local distribution of this macrobenthic burrowing species was determined and related to the particle size distribution of the substrata in which it was found. Its habitat preference is for clean, grassless, sandy bottoms in intertidal areas (beaches and sandbars), and on sublittoral level bottoms of protected bays and lagoons sheltered from heavy wave action. The preferred sediments were found to range from medium to fine sand. The population density, size frequency distribution, growth, reproduction, recruitment, and mortality of a sublittoral population of L. elongata (at Wadi Taba, Sinai) were studied.The mode of life of this burrowing heart urchin was observed in situ and in aquaria. Its burrowing and emergence behaviour are described. Experiments were carried out on the effect of particle size on burrowing behaviour. There are significant differences in the ability of L. elongata to manipulate substrata of varying grain size. The burrowing process was found to be most rapid in natural sand of medium-fine composition, corresponding to the normal sediment of the urchin's habitat. Such sediments were also found to be suitable for successful larval settlement; juveniles did not survive in coarser sand.Differences in population density and spatial distribution between various size groups are attributed to differences in their ability to manipulate the substratum. L. elongata is found to be morphologically suited to sand, particularly medium-fine sand; however, it is restricted by its morphology to shallow burrowing, since it lacks specialized mechanisms for deeper burrowing and funnel building.     

Vascular physiology of the ascidian Pyura praeputialis

Blood pressure was measured at both ends of the heart of Pyura praeputialis (Heller) after removing the tunic.
For posterior anterior heart waves average upstream pressures were 23–25 mm H₂O (positive): corresponding downstream pressures averaged 8 mm H₂O (negative). For anterior posterior waves average upstream pressures were 17–18 mm H₂O (+) and downstream values were 7–8 mm H₂O (-). Maximum pulse amplitudes recorded were about 30 mm H₂O (upstream).
Speed of the peristaltic wave was 25-31 mm/s. In one experiment the speed was demonstrably different over the two halves of the heart (48 mm/s over the rear half and 29 mm/s over the front half).
Number of peristaltic waves per series (i.e. between successive reversals) varied from 20 to 178. Duration of each series varied from 120 s to 690 s. Wave frequency ranged from 8 to 21 per min. Reversal frequency ranged from 5 to 30 reversals per hour.
Most preparations showed periods of reduced heart activity ("rest periods") during the the 2 4 h of the experiment. All showed spasmodic contractions of the mantle muscles which caused pressure "surges" in the vascular system.
It is shown that, in both directions of beat, most or all of the pressure wave is contributed by the front half of the heart (half towards which peristaltic wave is travelling). This can be related to the "reversed spiral" structure of the heart: each "half" of the heart (i.e. each spiral) serves primarily as the pump for one direction.     

Ultrastructure of erythrocytes and leucocytes of Priapulus caudatus (de Lamarck) (Priapulida)

The marine priapulid Priapulus caudatus has a voluminous body cavity filled with a blood-like fluid containing erythrocytes and leucocytes (amoebocytes). The hematocrit of animals weighing 0.5–14 gm was 2–10%. The erythrocytes contain a hemerythrin blood pigment. The structure of the coelomocytes was studied by light and electron microscopy. The erythrocytes are nucleated and contain marginal bands, vacuoles and occasionally crystals. The cytoplasm has few organelles. The leucocytes are amoeboid motile cells, the cytoplasm of which contains numerous organelles. The most conspicuous of these are oval particles, probably representing developmental stages of lysosomes. Most of these organelles contain tubules stretching from one pole to another. In the hind part of the animal, certain tissues, primarily the posterior warts contain large numbers of coelomocytes. The histological picture is complicated, showing some resemblance to the lymphoepithelial tissues of vertebrates.     

Relative contributions of "pressure pump" and "peristaltic pump" to gastric emptying

The relative contributions to gastric emptying from common cavity antroduodenal pressure difference ("pressure pump") vs. propagating high-pressure waves in the distal antrum ("peristaltic pump") were analyzed in humans by high-resolution manometry concurrently with time-resolved three-dimensional magnetic resonance imaging during intraduodenal nutrient infusion at 2 kcal/min. Gastric volume, space-time pressure, and contraction wave histories in the antropyloroduodenal region were measured in seven healthy subjects. The subjects fell into two distinct groups with an order of magnitude difference in levels of antral pressure activity. However, there was no significant difference in average rate of gastric emptying between the two groups. Antral pressure history was separated into "propagating high-pressure events" (HPE), "nonpropagating HPEs," and "quiescent periods." Quiescent periods dominated, and average pressure during quiescent periods remained unchanged with decreasing gastric volume, suggesting that common cavity pressure levels were maintained by increasing wall muscle tone with decreasing volume. When propagating HPEs moved to within 2-3 cm of the pylorus, pyloric resistance was found statistically to increase with decreasing distance between peristaltic waves and the pylorus. We conclude that transpyloric flow tends to be blocked when antral contraction waves are within a "zone of influence" proximal to the pylorus, suggesting physiological coordination between pyloric and antral contractile activity. We further conclude that gastric emptying of nutrient liquids is primarily through the "pressure pump" mechanism controlled by pyloric opening during periods of relative quiescence in antral contractile wave activity.     

Gastric flow and mixing studied using computer simulation

The fed human stomach displays regular peristaltic contraction waves that originate in the proximal antrum and propagate to the pylorus. High-resolution concurrent manometry and magnetic resonance imaging (MRI) studies of the stomach suggest a primary function of antral contraction wave (ACW) activity unrelated to gastric emptying. Detailed evaluation is difficult, however, in vivo. Here we analyse the role of ACW activity on intragastric fluid motions, pressure, and mixing with computer simulation. A two-dimensional computer model of the stomach was developed with the 'lattice-Boltzmann' numerical method from the laws of physics, and stomach geometry modelled from MRI. Time changes in gastric volume were specified to match global physiological rates of nutrient liquid emptying. The simulations predicted two basic fluid motions: retrograde 'jets' through ACWs, and circulatory flow between ACWs, both of which contribute to mixing. A well-defined 'zone of mixing', confined to the antrum, was created by the ACWs, with mixing motions enhanced by multiple and narrower ACWs. The simulations also predicted contraction-induced peristaltic pressure waves in the distal antrum consistent with manometric measurements, but with a much lower pressure amplitude than manometric data, indicating that manometric pressure amplitudes reflect direct contact of the catheter with the gastric wall. We conclude that the ACWs are central to gastric mixing, and may also play an indirect role in gastric emptying through local alterations in common cavity pressure.     

Zur feinstruktur integumentaler bildungen bei priapuliden (Halicryptus spinulosus und Priapulus caudatus)

Zusammentassung Die Integumente der Priapuliden Halicryptus spinulosus und Priapulus caudatus sind ähnlich aufgebaut. Die miteinander verzahnten und über lange septierte Desmosomen verbundenen Epithelzellen tragen apikal eine amorphe, in Abhgngigkeit von der Häutungsphase± geschichtete Kutikula. Ähnliche Kutikulastrukturen finden sich bei Nematoden. Der Panzer der Halicryptus-Larve ist in seiner Ultrastruktur deutlich verschieden von der Kutikula adulter Tiere and zeigt auch keine Übereinstimmung mit dem Panzer der Kinorhynchen.Die epithelialen Stacheln der Art Halicryptus spinulosus enthalten mehrere Sekretzelltypen. Die epithelialen Differenzierungen am Rumpfende von Priapulus caudatus sind durch ihre Ultrastruktur ebenfalls als sezernierende Zellkomplexe gekennzeichnet.Der Feinbau des distalen Anhangsorganes von Priapulus caudatus entspricht der Ultrastruktur von Zellen mit aktivem Ionentransport. AuBerdem ist dieses Organ Träger von Mechanorezeptoren.

---

Fine structure of integumental features in priapulids (Halicryptus spinulosus and Priapulus caudatus)

Summary The integuments of the priapulids Halicryptus spinulosus and Priapulus caudatus exhibit a similar ultrastructure. The epithelial cells, the neighbouring lateral plasma membranes of which are frequently highly interdigitated, are connected by long septate desmosomes and are apically covered by an amorphous cuticle. The latter shows a stratification, the pattern of which is dependent on the moulting phase. Similar cuticular structures are to be found in nematodes. The cuticle of the larvae of Halicryptus differs markedly from that of the adult animals and also does not show agreements with the armour of kinorhynchs. It is threelaminated and contains in the middle layer canalicular structures. The epithelial spines of Halicryptus spinulosus contain various types of secretory cells. The epithelial differentiations at the end of the body of Priapulus caudatus also represent, according to their ultrastructure, secretory cells. The fine structure of the appendicular organs of Priapulus caudatus corresponds to that of cells engaged in ion transport. In addition this organ possesses mechanoreceptors. Both priapulids carry, on the integumental papillae and within the epithelium of the body and pharynx, characteristically constructed receptors with an apical cilium surrounded by seven microvilli. They are interpreted to represent mechanoreceptors.

---

---

Für die Überlassung eines Arbeitsplatzes im Institut far Pharmakognosie Kiel danke ich Herrn Prof. Dr. D. Frohne. Alit dankenswerter Unterstützung durch die Deutsche Forschungsgemeinschaft.     

Burrowing behaviour in the European lugworm Arenicola marina (Polychaeta: Arenicolidae)

A detailed analysis is presented of the mechanism of burrowing in Arenicola marina (L.). The following were recorded electronically, using further developments of the techniques introduced by Trueman: movement into the sand, internal pressure at various points in the body, external pressure in the surrounding sand. The results are interpreted in relation to direct visual observation of the burrowing process. The structural and functional specializations of the lugworm for burrowing and the factors concerned in the release and control of burrowing activity, are discussed.     

Burrowing of the lingulid brachiopod Glottidia pyramidata: its ecologic and paleoecologic significance

Contrary to popular assumption, the pedicle of Glottidia is not its principal burrowing organ. The brachiopod props itself up with the pedicle and enters the sediment with the valves leading, anterior end first. The pedicle trails behind. Burrowing is accomplished by cyclical valve motions: rotary, sliding, and gaping movements are used. Rapid valve closure ejects water from the mantle cavity to loosen the sediment. The lateral setae convey mucus-bound sand posteriorly (upwards). X-radiography shows that the burrows are U-shaped: in a few hours, the animal reappears in feeding position with the anterior end pointing out of the sediment and the pedicle extending down into the burrow. This burrowing process explains the substrate preferences of lingulids. The thick. closely spaced setae are adapted for burrowing. The spacing between individuals is increased, suggesting competition for food.     

A scanning electron microscope study of the developing embryo of Manduca sexta (L.) (Lepidoptera : Sphingidae)

Scanning electron microscopy of the developing Manduca sexta (Lepidoptera : Sphingidae) embryo reveals that the body wall of the insect undergoes considerable morphogenesis beginning at 20 hr post-oviposition. The elongated 19 hr embryo contracts in length, which gives rise to the formation of rudimentary segments. By 33 hr, many of the appendage anlagen are visible, the presumptive spiracles appear as bifurcate pits and the proctodeum begins invagination. During this same period, prior to katatrepsis, the body walls become established, and the segments and appendages develop. Between 50 and 60 hr post-oviposition, involution of the oral cavity and reorientation of the associated gnathal appendages occurs. During this same period, katatrepsis and provisional dorsal closure take place. Developmental polarity is evident as a distinctive wave of specialization proceeding posterior to anterior in the thorax/abdomen, and anterior to posterior in the head. Configuration of the oral cavity is strikingly prognathous until just prior to eclosion. Two embryonic molts are apparent, as determined by the remnants of ecdysed “embryonic cuticles”.