Metachronal Wave Research Articles

Physical constrints on the evolution of ctenophore size and shape

Cilia bundled into combs or ctenes are an evolutionary innovation that allow comb jellies (animals in the phylum Ctenophora) to swim faster and grow to sizes at least two orders of magnitude larger than animals that propel themselves by beating single cilia. Ctenophore size, shape and swimming behaviors, however, may be constrained by the mechanisms that coordinate comb plate oscillations. Oscillations of comb plates onPleurobrachia bachei (a cydippid comb jelly), are coupled by fluid interactions between combs. Ctenes beat metachronously (in sequence) and the flows generated byP. bachei are retarded by the amount of time it takes a wave to pass down a group of ctenes. Our model predicts thatP. bachei size is constrained by the maximum thrust that can be produced by ctenes that beat in sequence and our flow visualization studies suggest that swimming via metachronous comb oscillations may constrainP. bachei to spherical shapes. In contrast, comb plate oscillations onMnemiopsis leidyi, a lobate comb jelly, are neurally coordinated and groups of ctenes beat in synchrony. As a result, fluid flows generated byM. leidyi are not retarded by the passage of metachronal waves down each comb row.M. leidyi reach sizes 15 times larger, but swim relatively slower (body lengths per second) thanP. bachei. We propose that propulsion via metachronous or synchronous comb plate oscillations has played an important role in the evolution of ctenophore shape and size and may have divided comb jellies into two evolutionary lineages.

A simple model of light transmission through metachronally moving cilia

A ‘‘matchbox’’ model of a ciliary field under the influence of metachronal waves is analyzed. The optical absorption response of an optical absorbing system is calculated. Results show a characteristic double-peaked wave train.

On metachronism in ciliary systems: A model describing the dependence of the metachronal wave properties on the intrinsic ciliary parameters

A mathematical model is proposed to explain the dependence of the direction and the length of the metachronal wave on parameters that characterize the ciliary beat, the dimensions of the cilia, and the geometry of their arrangement on the ciliated surface. The metachronal wave is decomposed into two mutually perpendicular components, which are chosen in such a way that the direction of one of them is in the direction of the effective stroke. The magnitudes of the two components are determined by using the concept of the time of delay between adjacent cilia. The properties of the metachronal wave are then calculated as a function of the ciliary parameters. The results obtained with the present model predict that the direction of the wave propagation is strongly dependent on the type of metachronism in the direction of the effective stoke and the polarization in time and in space of the ciliary beat. The metachronal wavelength is found to depend on four parameters: the ciliary length, the angle of the arc projected on the cell surface by the ciliary tip during the recovery stroke, the degree of asymmetry of ciliary beat, and the portion of the cycle occupied by the pause. The metachronal wavelength is also found to be only weakly dependent on the ciliary frequency. At this stage there exists relatively little experimental information with which to characterize fully the metachronal properties of ciliary systems. Even when only partial information exists, the model allows prediction, to within a certain range, of the direction of the wave propagation. It also suggests a possible mechanism for the influence of changes in environmental conditions on wave direction and wavelength. In several cases in which full information does exist, good agreement between the experimental findings and the predictions of the model is found. According to this model it will be worthwhile to invest more effort in measuring the time and space polarization of ciliary beating and times of delay between cilia.

Characterization of metachronal wave in beating cilia: distribution of phases in space.

We have examined phase differences between beating cilia measured in different directions on the surface. The measurements were performed on tissue cultures taken from frog palate epithelium. This experiment was based on a method developed earlier, which measures simultaneously scattered light from two different and relatively small areas. Moreover, the distance between the two small areas can be accurately defined and varied. Rotating the stage around the optical axis permits us to repat these measurements at different space angles. It was found that: a) the phase gradient is a periodic function of the angle of rotation; b) the periodicity can be described quantitatively by a cosine function; c) good agreement exists between Machemer's findings in protozoa and our results, despite the differences between the two systems and techniques used.

The Tentacle Cilia of Aglantha digitale (Hydrozoa: Trachylina) and their Control

AbstractThe tentacles of Aglantha have ciliary bands along the sides. Metachronal waves pass along these bands. The strong ciliary currents produced propel water past the tentacles, increasing the probability of prey capture. The ciliated cells are unusual in having many (up to about 500) cilia per cell, where most cnidarian ciliated cells have only one. The cells are also peculiar in containing numerous axonemes without membrane coverings, lying loose in the cytoplasm.Tentacles show independent, rhythmic, slow flexions in the oral direction and groups of tentacles show coordinated, slow flexions as part of a regularly repeated fishing cycle. In both cases, these slow, graded movements are mediated by a slowly conducting system, probably the network of small neurons present in the ectoderm, and are accompanied by ciliary arrests. Much faster, more powerful, coordinated contractions of the tentacles occur in the context of escape behaviour; these are mediated by giant axons which run down the tentacles and are also accompanied by ciliary arrest. Ciliary and muscle effectors evidently share a common motor innervation. Electron microscopy shows that the giant and non‐giant nerves both synapse with muscle cells. The latter are joined to the ciliated cells by gap junctions, and it is suggested that whenever the muscles are excited depolarizations spread to the ciliated cells through the gap junctions and cause ciliary arrests. Neuronal control of ciliary activity has not previously been reported in the Hydrozoa.

Intensification of ciliary motility by extracellular ATP.

Ciliary metachronism and motility were examined optically in tissue cultures from frog palate epithelium as a function of extracellular ATP concentration in the range of 10(-7)-10(-3) M. The main findings were: a) upon addition of ATP the metachronal wavelength increased by a factor of up to 2. b) the velocity of the metachronal wave increased by a factor of up to 5. c) the frequency of ciliary beating increased by a factor of up to 2-3, the increase being temperature insensitive in the range of 15 degrees C-25 degrees C. d) the area under the 1-second FFT spectrum decreased by a factor of up to 2.5. e) the energy of the metachronal wave is increased by a factor of up to 9.5. f) all the spectrum parameters are subject to influence by ATP, as also by ADP and AMP. However, there are pronounced differences in the various responses to them. Based on these findings, physical aspects of the rate increase of particle transport caused by addition of extracellular ATP are explained. A plausible overall chemical mechanism causing pronounced changes in ciliary motility is discussed.

Structure and function of the metachronal wave in Tubifex tubifex spermatozeugmata (Annelida, Oligochaeta)

The spermatozeugmata of Tubifex tubifex are bundles of spermatozoa, stored in the spermathecae and composed of two types of sperm cells. The eupyrene, fertilizing, spermatozoa are stored parallel to the central axial cylinder, whereas the oligopyrene spermatozoa are helically arranged in the cortex. The main portions of their tails are connected by a junctional complex. When placed in Ringer solution the free extremities of the oligopyrene sperm tails start beating with metachronal waves, forming a series of wave fronts that are helically arranged around the spermatozeugma. The wavelength is 2.76 μm and the beat frequently is around 10 Hz. Besides the functions already suggested for the spermatozeugmata (holding together fertilizing spermatozoa; selecting nutrients from the lumen of the spermatheca) another function is proposed: the oligopyrene sperm tails, which form the helical metachronal wave, may help the transport of the spermatozeugma from the spermatheca to the opening of the spermathecal duct.

Ultrastructure and motion analysis of permeabilized Paramecium capable of motility and regulation of motility.

Structural and behavioral features of intact and permeabilized Paramecium tetraurelia have been defined as a basis for study of Ca2+ control of ciliary reversal. Motion analysis of living paramecia shows that all the cells in a population swim forward with gently curving spirals at speeds averaging 369 +/- 19 microns/second. Ciliary reversal occurs in 10% of the cell population per second. Living paramecia, quick-fixed for scanning electron microscopy (SEM), show metachronal waves and an effective stroke obliquely toward the posterior end of the cell. Upon treatment with Triton X-100, swimming ceases and both scanning and transmission electron microscopy reveal cilia that uniformly project perpendicularly from the cell surface. Thin sections of these cells indicate that the ciliary, cell, and outer alveolar membranes are greatly disrupted or entirely missing and that the cytoplasm is also disrupted. These permeabilized paramecia can be reactivated and are capable of motility and regulation of motility. Motion analysis of cells reactivated with Mg2+ and ATP in low Ca2+ buffer (pCa greater than 7) shows that 71% swim forward in straight or curved paths at speeds averaging 221 +/- 20 microns/second. When these cells are quick-fixed for SEM the metachronal wave patterns of living, forward swimming cells reappear. Motion analysis of permeabilized cells reactivated in high Ca2+ buffers (pCa 5.5) shows that 94% swim backward in tight spirals at a velocity averaging 156 +/- 7 microns/second. SEM reveals a metachronal wave pattern with an effective stroke toward the anterior region. Although the permeabilized cells do not reverse spontaneously, the pCa response is preserved and the Ca2+ switch remains intact. The ciliary axonemes are largely exposed to the external environment. Therefore, the behavioral responses of these permeabilized cells depend on interaction of Ca2+ with molecules that remain bound to the axonemes throughout the extraction and reactivation procedures.

Mucus transport in the lung

In this paper, the mucus transport in the lung due to metachronal wave motion of the cilia and longitudinal wave motion of the epithelium caused by coughing is studied by taking into account the effect of shear force at the mucus air interface. It is shown that as the parameters characterising these factors increase, the mucus flow rate increases. By taking into account the variation of viscosity across the mucus layer (two layer model), it is also pointed out that the flow rate decreases as the viscosity of mucus layer in contact with the air mucus interface increases.

Direct measurement of the velocity of the metachronal wave in beating cilia.

Recently a computerized electro-optical method was developed which enables one to simultaneously measure the frequency and the wavelength of the metachronal waves in beating cilia. The method is based on measurement of scattered light from two areas at a given distance apart. The distance between measured areas can be varied from zero to hundreds of microns. The relative ease of the measurement and data analysis of this method enable one to create large statistical ensembles in order to obtain reliable averages. In this work we show that in addition to the previously mentioned parameters this system can measure directly the velocity of the metachronal wave. It was found that the average velocity in the tissue culture from frog's palate epithelium at room temperature is approximately 270 micron/sec, about twice the average particle velocity at the frog's palate.

Characterization of metachronal wave of beating cilia on frog's palate epithelium in tissue culture.

1. A method is suggested to measure phase versus distance between beating cilia by means of a photoelectric device. A statistical method interpreting the results thus obtained is discussed. 2. It was found that: (a) an average phase exists between beating cilia, (b) despite strong fluctuations in phase on a short time scale, the average phase was kept constant over periods of 8 h, (c) the ciliary frequency and the length of the metachronal wave can be measured simultaneously. 3. The average phase differences are linearly dependent on distance. 4. The effective range of synchronization between cilia is of the order of 10 micron indicating that it occurs within one cell. 5. During the cycle of ciliary beating there are periods where coupling is stronger.

MORPHOLOGICAL ADAPTATIONS TO BURROWING INCHIRIDOTEA COECA(CRUSTACEA, ISOPODA)

The burrowing isopod Chiridotea coeca lives in medium to coarse sand. It preferentially burrows into sands of particle size ranges which most closely resemble its native substrate (particles sizes 250-1000 µm), and burrowing is fastest in these substrates. Pereiopods and pleopods are fouled in substrates with particles smaller than 100 µm.Locomotory rhythms above and below the substrate are similar. Phase differences between adjacent legs are 30% with metachronal waves moving forward. Power stroke for all pereiopods is by extension at the coxo-basal and basi-ischial articulations. Directions of leg thrust vary from almost perpendicular to the longitudinal body axis for gnathopods, to directly posterior for the last ambulatory leg.The body is dorso-ventrally flattened. Power and recovery stroke occur in very nearly the same plane and limb planes approach vertical posteriorly. Pereiopods lack the ventrally directed carpo-propodal flexure found in most free living isopods. Setae provide a conspicuous morphological adaptation to burrowing. Stout, posteriorly directed serrulate setae on the pereiopods increase the area of contact with sand grains, and provide an expanded tip around the dactyl. On the second and third gnathopods and all locomotory legs, a fringe of posteriorly directed plumose setae provides a shelter into which the leg behind can swing during recovery stroke. These setae increase in length and number with body size but the intersetal distance remains sufficiently close to exclude virtually all of the native sand grains from the spaces between the legs. Other morphological adaptations are discussed and the species is compared with other burrowing Peracarida.

Functional morphology and feeding behavior of Paraprionospio pinnata (Polychaeta: Spionidae)

The functional morphology and feeding behavior of Paraprionospio pinnata (Ehlers) were studied. The tentacular feeding palps of P. pinnata possess four groups of cilia: laterals, latero-frontal cirri, frontals and basal transverse rows. The lateral cilia beat in metachronal waves creating in current that flows toward the frontal surface of the palp. The latero-frontal cirri deflect suspended particles onto the frontal surface and potentially resuspend deposited particles. The frontal cilia line the groove of the palp and transport particles to the ciliated pharynx. The basal transverse cilia also beat in metachronal waves and together with the frontal cilia of the branchiae produce a “U”-shaped current that removes particles rejected by the pharynx from the burrow. The significance of particle selection at the site of the pharynx in spionid polychaetes is hypothesized to be constrained by the interaction of specific morphologies and behaviors that reduce the effects of epifaunal predation and browsing. The relationship between sediment permeability and type of respiratory or ventilation current is hypothesized to be a potentially important factor in understanding the distribution of spionid polychaetes.

中耳及び耳管の形態学的研究 第二報 実験的耳管狭さくによる耳管粘膜及び中耳粘膜の走査電子顕微鏡的観察

Ten adult dogs were used in this study. The pharyngeal orifice of the Eustachian tube was obstructed by laminaria or electrocoagulation. The epithelium of the Eustachian tube was observed 1, 3 and 5 weeks after surgery by light microscope and scanning electronmicroscope. One week after obstruction effusion was noted in the middle ear cavity and the cilia of the Eustachian tube lost their metachronal wave. Three weeks later, there were numerous holes in the mucous membrane of the Eustachian tube. At the bottom of the holes, one could see the surface of goblet cells surrounded by adhesive cilia with mucus. At 5 weeks the effusion had progressed and the metachronal wave of the cilia had disappeared completely. Some of the cilia had disappeared and others were deformed.

INACTIVATION OF CELL MOVEMENT FOLLOWING SEXUAL CELL RECOGNITION INPARAMECIUM CAUDATUM

A positive correlation between sexual cell recognition and decrease in swimming velocity was studied in the ciliated protozoan, Paramecium caudatum. Ciliary membrane vesicles with conjugation-inducing activity rapidly decreased swimming velocity of living cells of the opposite mating type. Immobilization of the ventral cilia and perturbation of metachronal waves in the dorsal cilia were observed upon application of the membrane vesicles. Anterior shift of the beating direction and decrease in the beating angle or amplitude were also observed in the cells reacting to the vesicles. A similar change of swimming behavior and ciliary inactivation was seen in the chemical induction of conjugation. A possible regulatory mechanism of ciliary movement is discussed.

An Analysis of Waving Behaviour: an Alternative Motor Programme for the Thoracic Appendages of Decapod Crustacea

ABSTRACT Decapod Crustacea display a slow metachronal rhythm of the third maxillipeds and pereiopod pairs one to four when undisturbed in the natural habitat. The dactyl tips are lifted off the substrate, and the unweighted limbs promote and remote at a slow frequency (range for all species 9–30min− 1). Movement is limited to the T-C joint. This behaviour, called waving, has been observed in many macrurans and an analogous activity, limited to the third maxillipeds, has been seen in several brachyurans. Analysis of EMGs shows: (a) the promotor activity increases in strength during a burst due to facilitation and motoneurone recruitment; (b) the rhythm period is stable throughout long waving sessions; (c) the promotor and remotor strokes are of equal duration and co-vary with period. Ipsilateral coupling is strong, with equal phases between adjacent limbs of 0· 05. The metachronal wave can pass anteriorly or posteriorly along an ipsilateral row. Bilateral coupling is weak. The two sides maintain equal frequency, and antiphasic coordination between the two ipsilateral sets of limbs is favoured. Possible functions for waving include gill grooming and supplementary gill ventilation. Comparisons between waving and other rhythmical motor programmes are discussed. Waving is an alternative programme for the walking legs, and is expressed when proprioceptive feedback is reduced.

Cinefilms of particle capture by an induced local change of beat of lateral cilia of a bryozoan

A local disruption of the metachronal wave always accompanies capture of algal cells by tentacles of Flustrellidra hispida (Fabricius). Beat changes for ≈0.2 s over ≈100μm of the ciliated band during capture of a 10-μm particle. The halted parcel of water is therefore larger than the particle of food but much smaller than the flow that continues past the tentacles elsewhere. These events are consistent with the hypothesis that an induced local reversal of beat concentrates particles for those suspension feeders that retain particles upstream from a band of simple cilia (adults or larvae of bryozoans, brachiopods, phoronids, hemichordates, and echinoderms). These events are not explained by other hypotheses that have been advanced for concentration of particles by these suspension feeders. Aerosol filtration models of direct interception are not applicable to this type of ciliary suspension feeder because retention depends on the magnitude of a stimulus and response to it. The stimulus will not be the same function of diameter of the food particle, and response is unlikely below a threshold stimulus.

Two sperm types in the spermatozeugmata of Tubifex tubifex (annelida, oligochaeta).

The spermatozeugmata (sperm bundles lacking a distinct wall) from the spermathecae of Tubifex tubifex are composed of two different zones: an internal axial cylinder containing conventional spermatozoa and an external cortex composed of modified spermatozoa, tightly packed together. The conventional spermatozoa conform to the classical clitellate scheme: very long and thin with a complex acrosome, a filiform nucleus, small mitochondria, and a flagellum with Y links and β glycogen granules as accessory structures. The modified spermatozoa show "empty" acrosomes, degenerating nuclei, and tails which contain γ glycogen granules. The tails are helically wound around the spermatozeugma and are connected to each other by junctional complexes. The tips of the cortical tails are free and move with a metachronal wave. The presence of two sperm types in tubificids is discussed and a protective function for the modified cortical spermatozoa is proposed.

Ciliary activity of cultured rabbit tracheal epithelium: beat pattern and metachrony.

The beat pattern of rabbit tracheal cilia has been investigated using high-speed cine photography and scanning electron microscopy, on cultured epithelia of known orientation. The cilia normally rest in the position reached at the end of the effective stroke, the ciliary tips pointing towards the oropharynx. Each beat begins with a recovery (or preparative) stroke in which a bend is propagated up the cilium causing the cilium to rotate backwards in a clockwise sweep, as viewed from above. At the end of its recovery stroke the cilium progresses immediately into the effective (or power) stroke, which is almost planar and in a cephalad direction. The active cilium describes an arc of almost 110 degrees before reaching the rest stage. This beat pattern is not significantly altered over an increase in frequency from 13-29 Hz; the relative duration of the 2 active phases of the beat remain similar over this range. Metachronal waves exist in the form of short erratic areas of coordinated beating which travel only short distances. Within each area, the non-planar recovery strokes initiate an antilaeoplectic wave of activity which recruits inactive cilia to extent the wave. As cilia perform their effective strokes, adjacent cilia in the plane of beating move in an antiplectic sequence. This pattern of coordination is related to the pattern of beat of the cilia and their distribution on the epithelium.

Changes in salinity and the endogenous release of neurotransmitters in the mussel, Mytilus Edulis

1. Metachronal wave activity was studied on a nerve-gill preparation of Mytilus edulis. This is an indicator of lateral ciliary activity on the gill. 2. Nerve stimulation with 10 or 50 hz produced an accelerated or decreased the average rate in metachronal lateral wave activity respectively. 3. The low or high frequency electrical stimulation response could be significantly modified in the presence of decreasing salinities (36, 27, 18 and 9%) and EGTA (calcium chelator). 4. After prolonged electrical stimulation at the low and high electrical delivery, the cilio-excitatory and cilio-inhibitory response was gradually modified in the presence of changing salinities (36-6%) and EGTA plus lanthanum chloride (LaCl 3). The latter chemical agents in concert significantly altered the cilio-excitatory (low frequency electrical) to one of cilio-inhibition. 5. The normal increase of basal lateral metachronal wave activity to a gradual increase in salinity (6–36%) was significantly altered upon perfusion with EGTA and EGTA plus LaCl 3. 6. The increase in lateral metachronal wave activity produced by perfusion with serotonin (5-HT) was not significantly changed in the presence of decreasing salinities. However, the endogenous release of this cilio-excitatory neurotransmitter was significantly effected by decreasing the salinity in the surrounding medium. 7. It is probable that decreasing salinity in the bathing medium (and in effect reducing calcium) plays a critical role in the endogenous release of 5-HT from the presynaptic nerve terminals in the gill.