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The morphology and adhesion mechanism of Octopus vulgaris suckers.

Tramacere F, Beccai L, Kuba M, Gozzi A, Bifone A, Mazzolai B - PLoS ONE (2013)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Center for Micro-BioRobotics, Istituto Italiano di Tecnologia, Pontedera, Italy. francesca.tramacere@iit.it

ABSTRACT
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.

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Schematic of the surfaces of action involved in adhesion.A) In Kier and Smith model [14], [15] the acetabular chamber is depicted as a hollow spherical cavity. Rin is the acetabular internal radius and h is the height of spherical cap that does not take part to suction. B) In the model proposed in this work the acetabular chamber presents a protuberance acting on the orifice and maintaining low pressure in the infundibular portion of the sucker. Ro is the radius of the orifice.
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pone-0065074-g008: Schematic of the surfaces of action involved in adhesion.A) In Kier and Smith model [14], [15] the acetabular chamber is depicted as a hollow spherical cavity. Rin is the acetabular internal radius and h is the height of spherical cap that does not take part to suction. B) In the model proposed in this work the acetabular chamber presents a protuberance acting on the orifice and maintaining low pressure in the infundibular portion of the sucker. Ro is the radius of the orifice.

Mentions: At the last stage of the adhesion process (Figure 7D), we suppose that the acetabular radial muscles stop contracting. We can thus argue that pressure in the acetabular compartment increases, but pressure in the infundibular compartment remains unchanged, since it is isolated from the acetabulum by means of orifice closure. In the light of this, the protuberance maintains contact with the upper part of the sidewalls of the orifice due to the cohesive force of water volume in the infundibular compartment. At this stage, no muscles are contracted. The passive elastic force of the acetabular tissues, which tend to return in rest configuration, counterbalances the above cohesive force. This phenomenon maintains suction at the water interface (Figure 7D). Thus, in our hypothesis the acetabular radial muscles are active at the beginning of the adhesion process, in order to remove the water from infundibular compartment and to initiate the contact between the acetabular protuberance and the upper part of the orifice sidewalls. Therefore, in our model the passive elastic restoring force of the acetabular protuberance performs sucker attachment over extended periods of time. Further support to our model is given by estimating the forces involved in the adhesion process. If we consider the acetabulum as a hollow spherical structure, the surface of action of the muscles responsible for generating the suction (acetabular radial muscles) is equal to 3πR2in, which results from 4πR2in–2πRinh (where Rin is the acetabular internal radius and h is the height of the spherical cap that does not take part in suction) and by approximating h to ½Rin, as shown in Figure 8A. Instead, in case of the observed O. vulgaris sucker morphology, the surface of action of the main element responsible for generating suction (acetabular protuberance) is the orifice opening, which is equal to πRo2, where Ro is the orifice radius (Figure 8B). Considering that the pressure is by definition a force per unit of area, if the surface of action decreases, the force needed to achieve the same suction pressure decreases as well. For example, by approximating Ro to ½Rin, in our model the force needed to generate suction would be reduced to 1/12 the force needed in case of hollow spherical acetabulum.


The morphology and adhesion mechanism of Octopus vulgaris suckers.

Tramacere F, Beccai L, Kuba M, Gozzi A, Bifone A, Mazzolai B - PLoS ONE (2013)

Schematic of the surfaces of action involved in adhesion.A) In Kier and Smith model [14], [15] the acetabular chamber is depicted as a hollow spherical cavity. Rin is the acetabular internal radius and h is the height of spherical cap that does not take part to suction. B) In the model proposed in this work the acetabular chamber presents a protuberance acting on the orifice and maintaining low pressure in the infundibular portion of the sucker. Ro is the radius of the orifice.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3672162&req=5

pone-0065074-g008: Schematic of the surfaces of action involved in adhesion.A) In Kier and Smith model [14], [15] the acetabular chamber is depicted as a hollow spherical cavity. Rin is the acetabular internal radius and h is the height of spherical cap that does not take part to suction. B) In the model proposed in this work the acetabular chamber presents a protuberance acting on the orifice and maintaining low pressure in the infundibular portion of the sucker. Ro is the radius of the orifice.
Mentions: At the last stage of the adhesion process (Figure 7D), we suppose that the acetabular radial muscles stop contracting. We can thus argue that pressure in the acetabular compartment increases, but pressure in the infundibular compartment remains unchanged, since it is isolated from the acetabulum by means of orifice closure. In the light of this, the protuberance maintains contact with the upper part of the sidewalls of the orifice due to the cohesive force of water volume in the infundibular compartment. At this stage, no muscles are contracted. The passive elastic force of the acetabular tissues, which tend to return in rest configuration, counterbalances the above cohesive force. This phenomenon maintains suction at the water interface (Figure 7D). Thus, in our hypothesis the acetabular radial muscles are active at the beginning of the adhesion process, in order to remove the water from infundibular compartment and to initiate the contact between the acetabular protuberance and the upper part of the orifice sidewalls. Therefore, in our model the passive elastic restoring force of the acetabular protuberance performs sucker attachment over extended periods of time. Further support to our model is given by estimating the forces involved in the adhesion process. If we consider the acetabulum as a hollow spherical structure, the surface of action of the muscles responsible for generating the suction (acetabular radial muscles) is equal to 3πR2in, which results from 4πR2in–2πRinh (where Rin is the acetabular internal radius and h is the height of the spherical cap that does not take part in suction) and by approximating h to ½Rin, as shown in Figure 8A. Instead, in case of the observed O. vulgaris sucker morphology, the surface of action of the main element responsible for generating suction (acetabular protuberance) is the orifice opening, which is equal to πRo2, where Ro is the orifice radius (Figure 8B). Considering that the pressure is by definition a force per unit of area, if the surface of action decreases, the force needed to achieve the same suction pressure decreases as well. For example, by approximating Ro to ½Rin, in our model the force needed to generate suction would be reduced to 1/12 the force needed in case of hollow spherical acetabulum.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Center for Micro-BioRobotics, Istituto Italiano di Tecnologia, Pontedera, Italy. francesca.tramacere@iit.it

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus