William M. Kier

Soft robotics: Biological inspiration, state of the art, and future research

Traditional robots have rigid underlying structures that limit their ability to interact with their environment. For example, conventional robot manipulators have rigid links and can manipulate objects using only their specialised end effectors. These robots often encounter difficulties operating in unstructured and highly congested environments. A variety of animals and plants exhibit complex movement with soft structures devoid of rigid components. Muscular hydrostats e.g. octopus arms and elephant trunks are almost entirely composed of muscle and connective tissue and plant cells can change shape when pressurised by osmosis. Researchers have been inspired by biology to design and build soft robots. With a soft structure and redundant degrees of freedom, these robots can be used for delicate tasks in cluttered and/or unstructured environments. This paper discusses the novel capabilities of soft robots, describes examples from nature that provide biological inspiration, surveys the state of the art and outlines existing challenges in soft robot design, modelling, fabrication and control.

The structure and adhesive mechanism of octopus suckers

Abstract Octopus suckers consist of a tightly packed three-dimensional array of muscle with three major muscle fiber orientations: 1) radial muscles that traverse the wall; 2) circular muscles arranged circumferentially around the sucker; and 3) meridional muscles oriented perpendicular to the circular and radial muscles. The sucker also includes inner and outer fibrous connective tissue layers and an array of crossed connective tissue fibers embedded in the musculature. Adhesion results from reducing the pressure inside the sucker cavity. This can be achieved by the three-dimensional array of muscle functioning as a muscular-hydrostat. Contraction of the radial muscles thins the wall, thereby increasing the enclosed volume of the sucker. If the sucker is sealed to a 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 attachment for extended periods. Measurements using miniature flush-mounted pressure transducers show that suckers can generate hydrostatic pressures below 0 kPa on wettable surfaces but cannot do so on non-wettable surfaces. Thus, cavitation, the failure of water in tension, may limit the attachment force of suckers. As depth increases, however, cavitation will cease to be limiting because ambient pressure increases with depth while the cavitation threshold is unchanged. Structural differences between suckers will then determine the attachment force.

The functional morphology of the musculature of squid (Loliginidae) arms and tentacles

The arms and tentacles of squid (Family Loliginidae: Sepioteuthis sepioidea (Blainville), Loligo pealei (LeSueur), Loligo plei (Blainville), Loliguncula brevis (Blainville)) do not possess the hardened skeletal elements or fluid‐filled cavities that typically provide skeletal support in other animals. Instead, these appendages are made up almost entirely of muscle. It is suggested here that the musculature serves as both the effector of movement and as the skeletal support system itself.

The morphology and mechanics of octopus suckers

The functional morphology of the suckers of several benthic octopus species was studied using histology and cinematography. The suckers consist of a tightly packed three-dimensional array of musculature. Three major muscle orientations are found in the wall of the sucker: (1) radial muscles that traverse the wall; (2) circular muscles that are oriented circumferentially around the sucker, including a major and minor sphincter muscle; and (3) meridional muscles that are oriented perpendicular to the circular and radial muscles. The connective tissue of the sucker includes inner and outer fibrous connective tissue layers and an array of crossed connective tissue fibers embedded in the musculature of the sucker. Attachment is achieved by reducing the pressure inside the sucker cavity. We propose the following mechanism to explain this pressure reduction. Contraction of the radial muscles thins the wall and thus increases the enclosed volume of the sucker. If the sucker is sealed to the substratum, however, the cohesiveness of water resists this expansion. Thus, contractile activity of the radial muscles reduces the pressure of the enclosed water. The radial muscles are antagonized by the circular and meridional muscles so that the three-dimensional array of muscle functions as a muscular-hydrostat. The crossed connective tissue fibers of the sucker may store elastic energy, providing a mechanism for maintaining attachment over extended periods.

The diversity of hydrostatic skeletons

Summary A remarkably diverse group of organisms rely on a hydrostatic skeleton for support, movement, muscular antagonism and the amplification of the force and displacement of muscle contraction. In hydrostatic skeletons, force is transmitted not through rigid skeletal elements but instead by internal pressure. Functioning of these systems depends on the fact that they are essentially constant in volume as they consist of relatively incompressible fluids and tissue. Contraction of muscle and the resulting decrease in one of the dimensions thus results in an increase in another dimension. By actively (with muscle) or passively (with connective tissue) controlling the various dimensions, a wide array of deformations, movements and changes in stiffness can be created. An amazing range of animals and animal structures rely on this form of skeletal support, including anemones and other polyps, the extremely diverse wormlike invertebrates, the tube feet of echinoderms, mammalian and turtle penises, the feet of burrowing bivalves and snails, and the legs of spiders. In addition, there are structures such as the arms and tentacles of cephalopods, the tongue of mammals and the trunk of the elephant that also rely on hydrostatic skeletal support but lack the fluid-filled cavities that characterize this skeletal type. Although we normally consider arthropods to rely on a rigid exoskeleton, a hydrostatic skeleton provides skeletal support immediately following molting and also during the larval stage for many insects. Thus, the majority of animals on earth rely on hydrostatic skeletons.

The musculature of squid arms and tentacles: Ultrastructural evidence for functional differences

The transverse muscle mass of the arm and the transverse and circular muscle masses of the tentacle of squid (Loligo pealei and Illex illecebrosus) were examined by transmission electron microscopy. Previous work had indicated that although similar in gross arrangement, the transverse muscle mass of the tentacle creates rapid elongation during prey capture while the transverse muscle mass of the arm is involved in creating bending movements. The difference in function between the transverse muscle masses of the arms and tentacles is reflected in differences in ultrastructure. The transverse muscle mass of the arm is made up of regular, obliquely striated muscle fibers 1–6 μm in diameter. The transverse and associated circular muscle masses of the tentacle are made up of cross‐striated muscle fibers 1–3 μm in diameter. The cross‐striated muscle fibers have A bands approximately 0.5 μm (I. illecebrosus) and 0.9 μm (L. pealei) in length and a resting sarcomere length of 0.9 μm (I. illecebrosus) and 1.6 μm (L. pealei), suggesting a relatively high shortening speed for this muscle type. The cross‐striated cells are not divided up into myofibrils, and the sarcoplasmic reticulum is located beneath the sarcolemma. Vernier displacements of the sarcomeres were observed. The myofilaments of the obliquely striated muscle fibers of the arm surround a central core containing mitochondria and the cell nucleus. The sarcoplasmic reticulum of the obliquely striated cells is located beneath the sarcolemma, in the plane of the Z elements, and surrounding the mitochondrial core.

Ontogenetic changes in mantle kinematics during escape-jet locomotion in the oval squid, Sepioteuthis lessoniana Lesson, 1830

We investigated the kinematics of mantle movement during escape jet behavior in an ontogenetic series of Sepioteuthis lessoniana, the oval squid. Changes in mantle diameter during the jet were measured from digitized S-VHS video fields of tethered animals that ranged in age from hatchlings to 9 weeks. The amplitude of both mantle contraction and mantle hyperinflation (expressed as percent change from the resting mantle diameter) during an escape jet was significantly greater in hatchlings than in older, larger squid (P < 0.05). The maximum amplitude of mantle contraction during the escape jet decreased from an average of −40% in hatchlings to −30% in the largest animals studied. The maximum amplitude of mantle hyperinflation decreased from an average of 18% in hatchlings to 9% in the largest squid examined. In addition, the maximum rate of mantle contraction decreased significantly during ontogeny (P < 0.05), from a maximum of 8.6 mantle circumference lengths per second (L/s) in hatchlings to 3.8 L/s in the largest animals studied. The ontogenetic changes in the mantle kinematics of the escape jet occurred concomitantly with changes in the organization of collagenous connective tissue fiber networks in the mantle. The alteration in mantle kinematics during growth may result in proportionately greater mass flux during the escape jet in newly hatched squid than in larger animals.

Muscle development in squid: Ultrastructural differentiation of a specialized muscle fiber type

The ultrastructural differentiation of two muscle fiber types of the squid Sepioteuthis lessoniana was correlated with development of prey‐capture behavior. Transmission electron microscopy was used to document the differentiation of the fast‐contracting cross‐striated muscle cells of the tentacles and the obliquely striated muscle cells of the arms of specimens sampled at one week intervals from hatching to 5 weeks. By using high‐speed video recordings, the ultrastructural differentiation was correlated with changes in prey‐capture behavior that occur during development and growth. The ultrastructural analysis focused on the muscle cells of the transverse muscle of the tentacles and the transverse muscle of the arms. For the first 2 weeks after hatching, the tentacle transverse muscle fibers do not show the adult ultrastructure and are indistinguishable from the obliquely striated fibers of the transverse muscle of the arms. Transverse striation of the tentacle muscle cells appears at approximately three weeks and adult ultrastructure is present by 4–5 weeks after hatching. The high‐speed video recordings show correlated behavioral changes. During the first 2–3 weeks after hatching, the animals use a different prey‐capture mode from the adults; they jet forward and capture the prey with splayed arms and tentacles rather than employing the rapid tentacular strike.

Ontogenetic Changes in Fibrous Connective Tissue Organization in the Oval Squid, Sepioteuthis lessoniana Lesson, 1830

Ontogenetic changes in the organization and volume fraction of collagenous connective tissues were examined in the mantle of Sepioteuthis lessoniana, the oval squid. Outer tunic fiber angle (the angle of a tunic collagen fiber relative to the long axis of the squid) decreased from 33.5° in newly hatched animals to 17.7° in the largest animals studied. The arrangement of intramuscular collagen fiber systems 1 (IM-1) and 2 (IM-2) also changed significantly during ontogeny. Because of the oblique trajectory of the IM-1 collagen fibers, two fiber angles were needed to describe their organization: (1) IM-1SAG, the angle of an IM-1 collagen fiber relative to the squid’s long axis when viewed from a sagittal plane and (2) IM-1TAN, the angle of an IM-1 collagen fiber relative to the squid’s long axis when viewed from a plane tangential to the outer curvature of the mantle. The sagittal component (IM-1SAG) of the IM-1 collagen fiber angle was lowest in hatchling squid (32.7°) and increased exponentially during growth to 43° in squid with a dorsal mantle length (DML) of 15 mm. In squid larger than 15 mm DML, IM-1SAG fiber angle did not change. The tangential component (IM-1TAN) of IM-1 collagen fiber angle was highest in hatchling squid (39°) and decreased to 32° in the largest squid examined. IM-2 collagen fiber angle (the angle of an IM-2 collagen fiber relative to the outer surface of the mantle) was lowest in hatchling squid (34.6°) and increased exponentially to about 50° in 15-mm DML animals. In squid larger than 15 mm DML, IM-2 fiber angle increased slightly with size. The volume fraction of collagen in IM-1 and IM-2 increased 68 and 36 times, respectively, during growth. The ontogenetic changes in the organization of collagen fibers in the outer tunic, IM-1, and IM-2 may lead to ontogenetic differences in the kinematics of mantle movement and in elastic energy storage during jet locomotion.

Venom kinematics during prey capture in Conus: the biomechanics of a rapid injection system.

SUMMARY Cone snails use an extensile, tubular proboscis as a conduit to deliver a potent cocktail of bioactive venom peptides into their prey. Previous studies have focused mainly on understanding the venoms role in prey capture but successful prey capture requires both rapid physiological and biomechanical mechanisms. Conus catus, a fish-hunting species, uses a high-speed hydraulic mechanism to inject its hollow, spear-like radular tooth into prey. We take an integrated approach to investigating the biomechanics of this process by coupling kinematic studies with morphological analyses. Taking advantage of the opaque venom and translucent proboscis of a mollusc-hunting juvenile cone snail, Conus pennaceus, we have determined that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey. Two morphological structures were found to play crucial roles in this process. A constriction of the lumen near the tip of the proboscis, composed of tall epithelial cells densely packed with microfilaments, impedes forward movement of the radular tooth prior to its propulsion. Proximal to the constriction, a muscular sphincter was found to regulate venom flow and pressurization in the proboscis. In C. pennaceus, the rapid appearance and flushing of venom within the proboscis during prey capture suggests a mechanism involving the delivery of a discrete quantity of venom. The interplay between these elements provides a unique and effective biomechanical injection system for the fast-acting cone snail venom peptides.