The Morphology and Adhesion Mechanism of Octopus vulgaris Suckers

The octopus sucker represents a fascinating natural system performing adhesion on different terrains and substrates. Octopuses use suckers to anchor the body to the substrate or to grasp, investigate and manipulate objects, just to mention a few of their functions. Our study focuses on the morphology and adhesion mechanism of suckers in Octopus vulgaris. We use three different techniques (MRI, ultrasonography, and histology) and a 3D reconstruction approach to contribute knowledge on both morphology and functionality of the sucker structure in O. vulgaris. The results of our investigation are two-fold. First, we observe some morphological differences with respect to the octopus species previously studied (i.e., Octopus joubini, Octopus maya, Octopus bimaculoides/bimaculatus and Eledone cirrosa). In particular, in O. vulgaris the acetabular chamber, that is a hollow spherical cavity in other octopuses, shows an ellipsoidal cavity which roof has an important protuberance with surface roughness. Second, based on our findings, we propose a hypothesis on the sucker adhesion mechanism in O. vulgaris. We hypothesize that the process of continuous adhesion is achieved by sealing the orifice between acetabulum and infundibulum portions via the acetabular protuberance. We suggest this to take place while the infundibular part achieves a completely flat shape; and, by sustaining adhesion through preservation of sucker configuration. In vivo ultrasonographic recordings support our proposed adhesion model by showing the sucker in action. Such an underlying physical mechanism offers innovative potential cues for developing bioinspired artificial adhesion systems. Furthermore, we think that it could possibly represent a useful approach in order to investigate any potential difference in the ecology and in the performance of adhesion by different species.     

Experimental Investigation on the Morphology and Adhesion Mechanism of Leech Posterior Suckers

The posterior sucker of a leech represents a fascinating natural system that allows the leech to adhere to different terrains and substrates. However, the mechanism of adhesion and desorption has not yet to be elucidated. In order to better understand how the adhesion is performed, we analyzed the surface structure, adsorption movements, the muscles’ distribution, physical characteristics, and the adsorption force of the leech posterior suckers by experimental investigation. Three conclusions can be drawn based on the obtained experimental results. First, the adhesion by the posterior sucker is wet adhesion, because the surface of the posterior sucker is smooth and the sealing can only be achieved on wet surfaces. Second, the deformation texture, consisting of soft collagen tissues and highly ductile epidermal tissues, plays a key role in adhering to rough surfaces. Finally, the adhesion and desorption is achieved by the synergetic operation of six muscle fibers working in different directions. Concrete saying, directional deformation of the collagen/epithermal interface driven by spatially-distributed muscle fibers facilitates the excretion of fluids in the sucker venter, thus allowing liquid sealing. Furthermore, we found that the adhesion strength is directly related to the size of the contact surface which is generated and affected by the sucker deformation. Such an underlying physical mechanism offers potential cues for developing innovative bio-inspired artificial adhesion systems.     

Development of Biomimetic Squid-Inspired Suckers

Biomechanical properties of squid suckers were studied to provide inspiration for the development of sucker artefacts for a robotic octopus.Mechanical support of the rings found inside squid suckers was studied by bending tests.Tensile tests were carried out to study the maximum possible sucking force produced by squid suckers based on the strength of sucker stalks,normalized by the sucking areas.The squid suckers were also directly tested to obtain sucking forces by a special testing arrangement.Inspired by the squid suckers,three types of sucker artefacts were developed for the arm skin of an octopus inspired robot.The first sucker artefact made of knitted nylon sheet reinforced silicone rubber has the same shape as the squid suckers.Like real squid suckers,this type of artefact also has a stalk that is connected to the arm skin and a ring to give radial support.The second design is a straight cylindrical structure with uniform wall thickness made of silicone rubber.One end of the cylinder is directly connected to the arm skin and the other end is open.The final design of the sucker has a cylindrical base and a concave meniscus top.The meniscus was formed naturally using the surface tension of silicone gel,which leads to a higher level of the liquid around the edge of a container.The wall thickness decreases towards the tip of the sucker opening.Sucking forces of all three types of sucker artefacts were measured.Advantages and disadvantages of each sucker type were discussed.The final design of suckers has been implemented to the arm skin prototypes.     

Morphological and ultrastructural aspects of Branchiobdella pentodonta Whit. (Annelida,oligochaeta) suckers

The muscular system in the posterior sucker of Branchiobdella pentodonta Whit. has circular, longitudinal and radial fibers. In the anterior sucker, which has circular and longitudinal fibers, the muscle system is scarce. Concentric fibers are found around the mouth. In both suckers the glandular elements form voluminous complexes secreting mucus for attachment to the substrate. Suckers show neuromuscular junctions and three distinct types of neuroglandular junctions: one with typical neurosecretory granules, one with larger neurosecretory granules produced by cells located at the origin of the segmental nerves, and one with presynaptic vesicles. The second type is peculiar to the posterior sucker. A comparison is made between suckers of Branchiobdella and those of leeches.     

The structure and adhesive mechanism of octopus suckers

Octopus suckers consist of a tightly packed three-dimensionalarray of muscle with three major muscle fiber orientations:1) radial muscles that traverse the wall; 2) circular musclesarranged circumferentially around the sucker; and 3) meridionalmuscles oriented perpendicular to the circular and radial muscles.The sucker also includes inner and outer fibrous connectivetissue layers and an array of crossed connective tissue fibersembedded in the musculature. Adhesion results from reducingthe pressure inside the sucker cavity. This can be achievedby the three-dimensional array of muscle functioning as a muscular-hydrostat.Contraction of the radial muscles thins the wall, thereby increasingthe enclosed volume of the sucker. If the sucker is sealed toa surface the cohesiveness of water resists this expansion.Thus, the pressure of the enclosed water decreases instead.The meridional and circular muscles antagonize the radial muscles.The crossed connective tissue fibers may store elastic energy,providing an economical mechanism for maintaining attachmentfor extended periods. Measurements using miniature flush-mountedpressure transducers show that suckers can generate hydrostaticpressures below 0 kPa on wettable surfaces but cannot do soon non-wettable surfaces. Thus, cavitation, the failure of waterin tension, may limit the attachment force of suckers. As depthincreases, however, cavitation will cease to be limiting becauseambient pressure increases with depth while the cavitation thresholdis unchanged. Structural differences between suckers will thendetermine the attachment force.     

Demonstration of primary and secondary muscle fiber architecture of the bovine tongue by diffusion tensor magnetic resonance imaging

The myoarchitecture of the tongue is comprised of a complex array of muscle fiber bundles, which form the structural basis for lingual deformations during speech and swallowing. We used magnetic resonance imaging of the water diffusion tensor to display the primary and secondary fiber architectural attributes of the excised bovine tongue. Fiber orientation mapping provides a subdivision of the tongue into its principal intrinsic and extrinsic muscular components. The anterior tongue consists of a central region of orthogonally oriented intrinsic fibers surrounded by an axially oriented muscular sheath. The posterior tongue consists principally of a central region of extrinsic fibers, originating at the inferior surface and projecting in a fan-like manner in the superior, lateral, and posterior directions, and lateral populations of extrinsic fibers directed posterior-inferior and posterior-superior. Analysis of cross-fiber anisotropy indicates a basic contrast of design between the extrinsic and the intrinsic fibers. Whereas the extrinsic muscles exhibit a uniaxial architecture typical of skeletal muscle, the intrinsic core muscles, comprised of the verticalis and the transversus muscles, show strong cross-fiber anisotropy. This pattern is consistent with the theory that the tongue's core functions as a muscular hydrostat in that conjoint contraction of the transverse and vertical fibers enable the tissue to expand at right angles to these fibers. These findings suggest that three-dimensional analysis of diffusion tensor magnetic resonance imaging provides a structural basis for understanding the micromechanics of the mammalian tongue.     

The function of the suckers of larval net-winged midges (Diptera: Blephariceridae)

1. Larval net-winged midges (Diptera: Blephariceridae) possess six ventral suckers that enable them to inhabit swift streams. Each sucker consists of a suction disc and a cavity with a piston. Large muscles are inserted within the piston, as well as at the base of the suction disc. This structure infers that both attachment and release of the sucker is achieved by vertical movements of the piston.
2. Live observations of blepharicerid larvae revealed that the sucker is indeed attached by an upward movement of the piston, but that the cavity is flooded when the sucker is released. The piston is lowered only at the end of a sucker 'step', expelling water from the cavity.
3. During foraging, the maxilla and the piston of the first sucker are moved synchronously, indicating that the first sucker functions as a holdfast thus facilitating grazing.
4. The adhesive forces, as well as the relative size of blepharicerid suckers, differ amongst species. They are highest in Hapalothrix lugubris and lowest in Liponeura cordata , which correlates with the hydraulic stress to which the larvae of these species are exposed in their preferred habitat. The balance between the efficiency of their retention structure and the hydraulic conditions of their preferred habitat defines a key dimension of their ecological niche.     

Sensory innervation in the rim of the octopus sucker

Anatomical components of afferent innervation in the rim of the octopus sucker are described. In the sensory epithelium under the smooth cuticle two associated ciliated receptor cell-types (presumably chemosensitive) occur in clusters. A third ciliated receptor cell-type under the toothed cuticle may be a mechanoreceptor. A non-ciliated receptor cell-type of unknown function, under the toothed cuticle, is characterized by a microvillus-lined apical canal containing dense granular material. The axons of the latter two receptors go directly into large nerve tracts which nm through the infundibular muscle and on to the ganglion of the sucker. The axons of the first cell-types terminate on interneurons either in the base of the epithelium or below the epithelium. All the interneurons of the basal region of the epithelium migrate centripetally and develop into encapsulated interneurons. Within the epithelium, fine fibers provide collateral contact among cluster receptors. Collateral interaction among basal and encapsulated interneurons occur in the infundibular plexus. The microanatomy of the rim of the sucker suggests that chemosensory cues are funneled into the interneurons where they are concentrated into integrated signals, while other sensory input is probably sent directly to the ganglia of the sucker and/or arm.     

Comparative morphology and osteology of pelvic fin‐derived midline suckers in lumpfishes,snailfishes and gobies

Some fishes use modified body structures – including pelvic fins – to produce suction to facilitate stability in turbulent environments. This study compares the morphology and osteology of the pelvic suckers of representative lumpfishes (Cyclopteridae), snailfishes (Liparidae) and gobies (Gobiidae). In all species studied the midline sucker (pelvic suctorial organ [PSO]) is formed from the pelvic girdle and fin rays I and 5 of the pelvic fins, comprised of similar osteological elements to those found in the pelvic girdle and pelvic fin rays although the morphology of the bony elements is species‐specific. Pelvic suctorial organs in those fishes that lack pelvic girdles are therefore homologous to pelvic girdles. The phenotypic diversity seen in so few species indicates that many sucker morphologies have arisen, origination depending on the concerted development of muscular, skeletal, nervous, and skin body tissues. The structure of the soft rays of the pelvic fins in the liparids and cyclopterids is unusual and indicative of unconventional developmental patterning of fin ray halves and of evolution in the underlying mechanisms responsible for the development of midline suckers.     

Morphological Studies on Holotrichous Ciliates of the Family Hysterocinetidae. II. Craticuloscuta escobari Gen. Nov., Sp. Nov., and Epicharocotyle kyburzi Gen. Nov., Sp. Nov.

SYNOPSIS. Two species of hysterocinetids occur in the alimentary tract of Drilocrius breymanni , an aquatic oligochaete collected in Departamento del Valle, Colombia. The suckers of both species are unusual for their complexity. In Craticuloscuta escobari gen. nov., sp. nov., the sucker is a shallow oval concavity with longitudinal and transverse supporting elements. About one-fifth of the area of the sucker, in its posterior portion, is ciliated, but argyrophilic punctations, which probably represent kinetosomes, are distributed in a regular pattern over most of its surface. In Epicharocotyle kyburzi gen. nov., sp. nov., the oval major portion of the sucker is deep, and continuous with a short trough which extends posteriorly and bends toward the left. Veil-like flanges, bordered by a fringe of thick, inactive cilia, arise from the margins of the sucker on either side. In the region of the trough, the flanges may overlap in such a way that the trough is almost completely covered. The trough and a small area of the major portion of the sucker anterior to it are ciliated. However, argyrophilic punctations which probably represent kinetosomes are distributed over most of the surface of the sucker. The pattern of longitudinal and transverse supporting elements found in the sucker itself extends into the flanges. In both Craticuloscuta and Epicharocotyle , the arrangement of the adoral and buccal ciliary organelles is essentially like that in Hysterocineta, Ptychostomum , and other ciliates of the family Hysterocinetidae.     

Biology of suckers: late-formed shoots in sugarcane

Suckers in sugarcane are tillers that form late in the growing season after the population of main stalks has been established. Their biology has rarely been studied, though unsubstantiated comments relating to their morphology, development and number are abundant. In this paper, the literature is reviewed and new experiments presented. Comparison of suckers, emerging plant and ratoon cane showed that suckers have a different leaf and stem morphology. Suckers have a greater diameter at their stem base and shorter and wider leaves than primary stalks of a similar age. In 1 ‐year‐old crops, suckers have been demonstrated to decrease the net sucrose concentration of harvested material by diluting sucrose in the main stalks. By comparing main stalks without suckers to those that have initiated suckers, evidence is presented that suckers may also be decreasing the sucrose content of the stalks from which they are growing. Genotypic and environmental factors influence sucker number. Several experiments were designed to identify environmental stimuli for suckering. Increased nitrogen, through application late in the growing season, was found to increase the numbers of suckers present. Manipulation of the light environment of main stalks showed that a change in light quality (but not necessarily quantity) stimulated suckering. Further work is underway to define how these environmental stimuli lead to sucker initiation and growth. Major scientific questions that should be addressed are: the identification of other potential environmental stimuli, how the signals are perceived and translated into sucker initiation, and why suckers have different morphology. The practical challenge is to combine the new information about sucker biology and develop from it strategies to alter agronomy and select new cultivars that results in decreased suckering.     

Potentially handicapped but otherwise functional: Malformations in prey capture tools show no impacts on octopus life

Larval mortality is a keystone ecological factor for many benthic octopus since it mostly occurs before their settlement in the sea bottom as benthic juveniles. The literature had revealed that records of adult animals with morphological abnormalities (teratologies) are fewer in species with complex life cycle than in those with direct development. This is a direct consequence of the morphological, physiological, and development challenges that the transition from the larval to the adult morphology represents. During a routine fishing sample, we found an immature female horned octopus with additional buccal structures in two suckers of its ventral arms, likely rendering these suckers as inefficient. Based on the literature about the natural history of octopus, we provide evidence that these abnormalities were present at the moment of hatch. We evaluated the impact of the teratologies by comparing the shape of the buccal beaks and the trophic niche of the individual with five normal conspecifics. Although the beaks showed a different shape than normal individuals, the trophic niche was similar. Surprisingly, the teratological condition of the individual likely had no severe impacts on its life, even though it likely represents a handicap for its survival during its planktonic life. We also comment on other previous records from the literature of teratological adult octopus to highlight the amazing adaptive capacity of octopus to deal with challenging morphologies.     

Tegumental ultrastructure of adult Gynaecotyla squatarolae (Digenea: Microphallidae)

Gynaecotyla squatarolae (Digenea: Microphallidae) adult flukes were recovered from experimental chicks at day 4-6 post-infection and their tegumental ultrastructure was observed with a scanning electron microscopy. They were pyriform in shape, and their anterior halves were concaved ventrally. The whole body surface was covered with tegumental spines, which were wide and 16-17 digitated between oral and ventral suckers. The density of spines and number of digits decreased posteriorly. The oral sucker was subterminal and the excretory pore was at the posterior end of the worm. Two ventral suckers were similar in appearance and protruded near midline of the worm. The genital atrium was dextral to the small ventral sucker. The dorsal surface was covered with tegumental spines, but the spines were sparser than on the ventral surface. On the middle portion of the dorsal surface, a small opening presumed to be the Laurer's canal was seen. From these findings, it has been confirmed that the adult G. squatarolae has unique characteristics in the surface ultrastructure.     

A finite element simulation scheme for biological muscular hydrostats

An explicit finite element scheme is developed for biological muscular hydrostats such as squid tentacles, octopus arms and elephant trunks. The scheme is implemented by embedding muscle fibers in finite elements. In any given element, the fiber orientation can be assigned arbitrarily and multiple muscle directions can be simulated. The mechanical stress in each muscle fiber is the sum of active and passive parts. The active stress is taken to be a function of activation state, muscle fiber shortening velocity and fiber strain; while the passive stress depends only on the strain. This scheme is tested by simulating extension of a squid tentacle during prey capture; our numerical predictions are in close correspondence with existing experimental results. It is shown that the present finite element scheme can successfully simulate more complex behaviors such as torsion of a squid tentacle and the bending behavior of octopus arms or elephant trunks.     

Tegumental ultrastructure of juvenile and adult Echinostoma cinetorchis]

The tegumental ultrastructure of juvenile and adult Echinostoma cinetorchis (Trematoda: Echinostomatidae) was observed by scanning electron microscopy. Three-day (juvenile) and 16-day (adult) worms were harvested from rats (Sprague-Dawley) experimentally fed the metacercariae from the laboratory-infected fresh water snail, Hippeutis cantori. The worms were fixed with 2.5% glutaraldehyde, processed routinely, and observed by an ISI Korea DS-130 scanning electron microscope. The 3-day old juvenile worms were elongated and ventrally curved, with their ventral sucker near the anterior two-fifths of the body. The head crown was bearing 37-38 collar spines arranged in a zigzag pattern. The lips of the oral and ventral suckers had 8 and 5 type II sensory papillae respectively, and between the spines, a few type III papillae were observed. Tongue or spade-shape spines were distributed anteriorly to the ventral sucker, whereas peg-like spines were distributed posteriorly and became sparse toward the posterior body. The spines of the dorsal surface were similar to those of the ventral surface. The 16-day old adults were leaf-like, and their oral and ventral suckers were located very closely. Aspinous head crown, oral and ventral suckers had type II and type III sensory papillae, and numerous type I papillae were distributed on the tegument anterior to the ventral sucker. Scale-like spines, with broad base and round tip, were distributed densely on the tegument anterior to the ventral sucker but they became sparse posteriorly. At the dorsal surface, spines were observed at times only at the anterior body. The results showed that the tegument of E. cinetorchis is similar to that of other echinostomes, but differs in the number and arrangement of collar spines, shape and distribution of tegumenal spines, and type and distribution of sensory papillae.     

The organization of the muscle system of the causative agent of dicrocoeliosis,Dicrocoelium dendriticum

The musculature of parasitic flatworms plays a central role in locomotory movement, attachment to the host, and in the function of the digestive, reproductive, and excretory systems. We examine for the first time the muscle system of the flatworm Dicrocoelium dendriticum, a causative agent of the parasitic disease dicrocoeliosis, by use of fluorescently labeled phalloidin and confocal laser scanning microscopy. Somatic musculature of D. dendriticum consists of the circular, longitudinal, and diagonal muscles. The distribution of the muscle fibers in the body wall differed among the anterior, middle, and posterior body regions of the worm. The musculature of the attachment organs, the oral and ventral suckers, includes several types of muscles: the external equatorial and meridional muscles, internal circular and semicircular muscles, and radial muscles. Inside of the ventral sucker the diagonally located muscles were revealed and the supplementary u-shaped muscles were found adjoined to the base of the sucker from outside. The musculature of the internal organs composed of the excretory, reproductive, and digestive systems were characterized. Our results increase our knowledge of the morphology of trematodes and the arrangement of their muscle system.     

Spatial arrangement of white muscle fibers and myoseptal tendons in fishes

We describe the arrangement of white muscle fibers and tendinous myoseptal structures and the relation of these structures to each other in order to provide an anatomical framework for discussions and experimental research on fish swimming mechanics. For the three major craniate groups, the petromyzontids, myxinids and gnathostomes, we identify three conditions that differ remarkably. Myxinids are characterized by asymmetrical myosepta with long cones. Within a single myoseptum these are connected by collagenous fibers that are almost oriented longitudinally. Distinct tendons are absent in myxinid myosepta. Petromyzontid myosepta lack cones and distinct myoseptal tendons, whereas gnathostomes bear cones and distinct tendinous structures: the lateral band, epineural (epipleural) tendon and myhabdoid tendon. Myoseptal fibers of petromyzontids and myoseptal tendons of gnathostome myosepta are firmly anchored in the skin. Myxinids lack firm myoseptal-skin-connections. Their muscular arrangement is neither comparable to that of petromyzontids nor to that of gnathostomes. The latter two bear archlike arrangements of muscle fibers spanning several segments that are hypothesized to play a role during bending. In gnathostomes, archlike helical muscle fiber arrangements (HMFAs) are present that span the length of several body segments and are multiply intersected by myosepta. Hence, a series of tendinous lateral bands of myosepta is embedded in HMFAs. The posterodorsally oriented HMFAs are underlain by posteroventrally oriented crossing muscle fibers (CMFs). Bending may be generated by contraction of the muscle fibers belonging to an HMFA and the simultaneous counteraction of CMFs. Moving caudally, this anterior muscle fiber arrangement gradually changes, eventually becoming the posterior muscle fiber arrangement. This pattern suggests that the function of the myomeres will also change. Three additional putative roles of myoseptal tendons can be deduced from their relations to white muscle fibers in gnathostomes (and in part in petromyzontids): (1) Posterior transmission of anteriorly generated muscular forces via lateral bands and/or myorhabdoid tendons. These tendons are more robust posteriorly. Anterior and posterior cones appear to play an important role in force transmission. (2) Pulling on collagen fibers of the skin via lateral bands and myorhabdoid tendons, suggesting a transmission of muscular forces that puts the skin into tension. (3) Resisting radial expansion of contracting muscle fibers by epineural (epipleural) tendons. By the latter two mechanisms modulation of body stiffness is likely to be achieved.     

Biological resorption of fibers from chitosan in endomysium and perimysium of muscular tissue

The resorption of fibers from chitosan implanted into emdomysium and perimysium of the rat’s broadest muscle of the back is comparatively studied in vivo by the scanning electron microscopy and histologic analysis methods. It is shown that the mechanism and rate of resorption of the fibers from chitosan depend on the fiber localization in the muscular tissue. Implantation of chitosan fibers into endomysium, where they have been in direct contact with muscle fibers, results in 14 days in the formation of transverse cracks, fiber fragmentation, and their partial resorption. Complete resorption of fibers in endomysium is observed in 30 days. Fibers implanted into perimysium maintain integrity in 7 days of the experiment, and a fibrous tissue is formed around the fibers. There is no destruction of chitosan fibers in 45 days of the exposition. The biocompatibility of the chitosan fibers is confirmed by the effective adhesion and proliferation mesenchyme stem cells on their surface.