Search

A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three-dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae, Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide-rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue.

The morphology of the musculature and connective tissues of the arms of Octopus bimaculoides was analyzed with light microscopy. We also studied O. briareus and O. digueti, which possess relatively more elongate and less elongate arms, respectively. The morphology of the arms was found to be remarkably uniform among species. The arms consist of a densely packed three-dimensional arrangement of muscle fibers and connective tissue fibers surrounding a central axial nerve cord. Three primary muscle fiber orientations were observed: 1) transverse muscle fibers oriented in planes perpendicular to the long axis of the arm; 2) longitudinal muscle fibers oriented parallel to the long axis; and 3) oblique muscle fibers arranged in helixes around the arm. The proportion of the arm cross section occupied by each of these muscle fiber groups (relative to the total cross sectional area of the musculature) remains constant along the length of the arm, even though the arm tapers from base to tip. A thin circular muscle layer wraps the arm musculature on the aboral side only. Much of this musculature has its origin and insertion on several robust connective tissue sheets including a layer surrounding the axial nerve cord and crossed-fiber connective tissue sheets located on the oral and the aboral sides of the arm. An additional thin layer of connective tissue wraps the arm musculature laterally and also serves as a site of origin and insertion of some of the muscle fibers. The fibers of the oral and aboral crossed-fiber connective tissue sheets are arranged oblique to the long axis of the arm with the same fiber angle as the oblique muscle layers that originate and insert on the sheets. The oblique muscle layers and the crossed-fiber connective tissue sheets thus form composite right- and left-handed helical fiber arrays. Analysis of arm morphology from the standpoint of biomechanics suggests that the transverse musculature is responsible for elongation of the arms, the longitudinal musculature is responsible for shortening, and the oblique muscle layers and associated connective tissues create torsion. Arm bending may involve unilateral contraction of longitudinal muscle bundles in combination with resistance to arm diameter increase due to contraction of the transverse musculature or passive stiffness of the arm tissues. The arms may also be bent by a combination of decrease in diameter due to contraction of the transverse musculature and maintenance of constant length on one side of the arm by unilateral activity of longitudinal muscle bundles. An increase in flexural stiffness of the arm may be achieved by cocontraction of the transverse and longitudinal muscle. Torsional stiffness may be increased by simultaneous contraction of both the right- and left-handed oblique muscle layers.

The arrangement of the musculature and connective tissues of the buccal mass of the coleoid cephalopods Octopus bimaculoides, Sepia officinalis, and Loliguncula brevis was examined using dissection and histology. Serial sections in three mutually perpendicular planes were used to identify the muscles and connective tissues responsible for beak movements and stability and to describe their morphology and fiber trajectories. Four major beak muscles were identified: the anterior, posterior, superior, and lateral mandibular muscles. The anterior, posterior, and superior mandibular muscles connect the upper beak and the lower beak. Although the lateral mandibular muscles originate on the upper beak, they do not connect to the lower beak and instead insert on a connective tissue sheath surrounding the buccal mass. Examination of the fibers of the lateral mandibular muscles reveals that they have the organization of a muscular hydrostat, with muscle fibers oriented in three mutually perpendicular orientations. Although the beaks are capable of complex opening, closing, and shearing movements, they do not contact one another and are instead connected only by the musculature of the buccal mass. Based on the morphological analysis and observations of freshly dissected beaks undergoing the stereotyped bite cycle, the functional role of the beak muscles is hypothesized. The anterior and superior mandibular muscles are likely responsible for beak closing and shearing movements. The posterior mandibular muscle is likely also involved in beak closing, but may act synergistically with the lateral mandibular muscles to open the beaks. The lateral mandibular muscles may use a muscular-hydrostatic mechanism to control the location of the pivot between the beaks and to generate the force required for beak opening. The lack of contact between the beaks and the morphology of the lateral mandibular muscles suggests that the buccal mass of coleoid cephalopods may represent a previously unexamined flexible joint mechanism. The term "muscle articulation" is proposed here to denote the importance of the musculature in the function of such a joint., (2005 Wiley-Liss, Inc.)

The renal organs of 32 species of cephalopods (renal appendage of all cephalopods, and renal and pancreatic appendages in decapods) were examined for parasite fauna and for histological comparison. Two phylogenetically distant organisms, dicyemid mesozoans and chromidinid ciliates, were found in 20 cephalopod species. Most benthic cephalopods (octopus and cuttlefish) were infected with dicyemids. Two pelagic cephalopod species, Sepioteuthis lessoniana and Todarodes pacificus, also harbored dicyemids. Chromidinid ciliates were found only in decapods (squid and cuttlefish). One dicyemid species was found in branchial heart appendages of Rossia pacifica. Dicyemids and chromidinids occasionally occurred simultaneously in Euprymna morsei, Sepia kobiensis, S. peterseni, and T. pacificus. The small-sized cephalopod species, Idiosepius paradoxus and Octopus parvus, harbored no parasites. Comparative histology revealed that the external surface of renal organs varies morphologically in various cephalopod species. The small-sized cephalopod species have a simple external surface. In contrast, the medium- to large-sized cephalopod species have a complex external surface. In the medium- to large-sized cephalopod species, their juveniles have a simple external surface of the renal organs. The external surface subsequently becomes complicated as they grow. Dicyemids and chromidinids attach their heads to epithelia or insert their heads into folds of renal appendages, pancreatic appendages, and branchial heart appendages. The rugged and convoluted external surface provides a foothold for dicyemids and chromidinids with a conical head. They apparently do not harm these tissues of their host cephalopods.

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 culticle, 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 run through the infundibular muscle and on to the ganglion of the sucker. The axons of the first cell-types terminated 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.