Dr. Allan Jones
University of Dundee
Table of Contents:Abstract & Introduction
Basic Overview of the Cephalopod
Basic Limb Terminology
The Use of Suckers
A Brief Description of Cavitation
Decapod Sucker Morphology
Octopod Sucker Morphology
Prehistoric Coleoids: Belemnoidea
The Case of Stauroteuthis syrtensis
The Case of the Vampyromorph
The Case of the Nautiluses
A Possible Evolutionary Theory
There have been plenty of studies on cephalopods (Phylum Mollusca), including their hard structures. Unfortunately this has hitherto been restricted mostly to the buccal mass and beak of animals such as squids (teuthids), octopuses and cuttlefishes (sepioids). There is relatively little literature on the subject of the sucker pads on the arms and tentacles of cephalopods. There is even less that displays the information in a comprehensive and focussed document, solely intended for that particular subject. Most of the information is spread across vast amounts of scientific papers and books, where any text on suckers is usually found to be at best fragmentary.
We are all familiar with cephalopods; their amazing abilities and behaviours. Their endeavours, such as the octopus' ability to squeeze through the smallest of gaps, and its ability to blend into the surrounding substrata almost instantaneously, or the cuttlefish's use of vivid colour changes to communicate its emotions and intentions, never fail to astound us. The class Cephalopoda has even captured the human race's imagination so much as to feature prolifically in our mythology and folklore, from the Norse Kraken to H. P. Lovecraft's Cthulhu, and other folktales. Despite this familiarity with them, we still know only a small portion of their form, their history and even their intellect, which renders an already alien animal even more bizarre and exotic. Another frequently omitted fact is that most of the cephalopods we see and know today, bar one genus, are only a portion of the class. These are the Coleoidea. The one extant genus that is not a coleoid is the Nautilus, from the subclass Nautiloidea.
During the early Devonian, the cephalopods radiated even further, creating new forms such as the early nautilda, and a new taxonomic group in the form of the ammonoids, of the subclass Ammonoidea. These were highly chambered, mostly with a spiral shell. These ammonoids survived for approximately three hundred and forty million years, until the end of the Cretaceous, when they became extinct. The Late Devonian also witnessed the emergence of the Coleoida as an offshoot of the ammonoids which comprise of all modern cephalopods except Nautilus, the sole the surviving remnant of the subclass Nautiloidea.
Method; the Alternatives to Literature Study
As well as searching for scientific papers, using journals such as the Journal of Experimental Biology, Integrated Comparative Biology, and Acta Plaeontologica Polonica, and books such as Kir Nesis' Cephalopods of the World, I had to supplement what I found with direct observation of specimens. I contacted the St. Andrews Aquarium (formerly Sea-life Centre), and acquired a well preserved specimen of Eledone cirrhosa Lamarck 1798; the Northern, or Curled, Octopus; a native of the British coast. This would be the specimen I would use as my typical model, since octopuses' suckers do not display much structural variation, and really only differ in their number and size across species.
Basic Overview of the Cephalopod
All Cephalopods are ocean-dwelling invertebrates of the phylum Mollusca. As stated previously, the majority are of the subclass Coleoidea, with the exception Nautilus, the one surviving member of the Nautiloidea. The Coleoidea are split into two subdivisions; the Neocoleoidea and the Belemnoidea, the prefix Neo- is used to describe the extant group of coleoids, the belemnoids being extinct. Modern coleoids consist of two superorders: the Decapodiformes and the Octopodiformes. These are distinguished by the number of arms they possess. In modern decapods, such as squids and cuttlefishes, two specialised arms have been developed for prey capture, as shown in fig 1b.
Decapods tend to live in the water column and have very active lifestyles. Virtually all cephalopods are short lived, with a high metabolism. Because of this they need to feed regularly. The best method of prey capture for a pelagic animal is to seize its prey, and decapods do this with specially designed arms called tentacles. These are the fourth arm pair on the animal (fig.1), and consist of an array of muscle called the "muscular hydrostat" (Kier & Van Leeuwen 1997), which allows the tentacles to be launched by elongation of this muscle. Once the prey is contacted the suckers adhere to the animal and it is dragged back to the mouth where the other arms manipulate that prey to be eaten. Some squids, however, use their tentacles more like a fishing line and just let them dangle in the water column, waiting for prey to pass by. This strategy is mostly employed by deep-sea squids (such as Chiroteuthis and Mastigoteuthis).
Basic Limb Terminology
The arms of cephalopods, as shown in fig. 2, have pretty uniform terms describing the regions. The base (or basal end) of the arm is that part which is closest to the main body, usually the widest part of the arm and proximal to the mouthparts. The median is the middle of the arm and the furthest part of the arm, and the tip, is the distal end.
The use of Suckers
The function in suckers, as adhesive structures, is to create an area of pressure inside the cavity of the sucker that is lower than that of the surrounding ambient pressure. This essentially "sucks" the object, or substratum, towards the sucker, creating a seal where the rim contacts the substratum. This rim is integral to keeping the reduced pressure inside constant. A breach in the seal will mean failure of adhesion, which is obviously not what the cephalopod wants, be it a decapod or an octopod.
A brief description of Cavitation
Cavitiation is the formation of bubbles of gas in a fluid when subject to a reduced pressure (Smith 1995). It actually causes failure of suction-based adhesive structures that are experiencing cavitation. This is important to cephalopods since they employ the use of suckers to adhere to surfaces, be it a prey item or a piece of substratum. So the cavitation threshold is essentially the highest amount of pressure a cephalopod sucker can attain before failure of adhesion, breaking the cephalopod's hold of the object. This limit is not set, however, and there are factors that can change the pressure differential such as depth and area of the sucker. Depth has an effect because of the relationship between depth and ambient pressure.
DECAPOD SUCKER MORPHOLOGY
The specimen of Sepia officinalis displayed relatively large suckers on their tentacle clubs in the second outermost row. The diameter is 4mm, so the area will be about 12.6 mm2 which is quite considerable for a coastal animal! According to Smith, the highest pressure differential the cuttlefish could achieve would be 100kPa.
Another structural pattern in the sucker ring is that of a crenellate shape; being square, like that of a castle or tower rampart. In fact, it very much resembles this defensive structure, although the function is completely different. An interesting structural form is that of a completely smooth ring surrounding the edge of the sucker, which is found in the family Onychoteuthidae (Nesis, 1982). These muscular squids display the smooth ring in both rows along their arms. The tentacles of the family are markedly different from the arms, in terms of the armature, due to the presence of hooks running in two rows. Onychoteuthidae typically only have two rows on their clubs from the manus to the dactylus, with a circle of the inter-locking "popper" suckers on the carpus, as described above.
The cuttlefish, of the order Sepiida, displayed slightly different superficial sucker architecture. Although the suckers were obviously virtually identical in their functional morphology, the sepioid sucker did look a little different. For one thing, in the typical teuthid sucker, at least from the research and observations conducted for this paper, the rim of the sucker cavity (and the ring) was similar to the area of largest diameter on the sucker body, which gave the structure a defined bulb-like appearance, whereas the cuttlefish sucker appeared more "enclosed" in that the rim of the sucker cavity looked as if it melded with the rest of the structure behind it. This can be seen by comparing figs. 5 and 6.
OCTOPOD SUCKER MORPHOLOGY
The principles of octopod suckers are similar to that of decapods: in order for the structure to adhere to an object, the aim is to generate a reduced pressure. While squids and cuttlefish employ the use of a muscular piston, octopus suckers use two cavities. A seal is formed between the object and the sucker, by the fleshy rim. The radial muscles in the acetabular wall and roof contract so that the acetabulum increases in size. This is because the radial wall and roof become thinner and longer making the acetabulum wider and taller. If this were to happen in the water column then water would just rush in to fill the larger area. However, the sucker is pressed against an object, prey item or piece of substratum, so no excess water can enter. The water inside the sucker resists expansion and so there is a decrease in pressure. This water essentially begins to act like a solid whilst under pressure, allowing adherence to the surface. In the acetabular wall, the circular muscle bundles are the antagonists of the radial muscle, and reduce the circumference and height of the acetabulum upon contraction, which in turn releases the sucker.
The suckers can also rotate, and move quite freely (as demonstrated by the example of it folding), which is how the octopus is able to manipulate prey and move it towards the mouth.
PREHISTORIC COLEOIDS: BELEMNOIDEA
Belemnoids are prehistoric coleoids that were most abundant during the Mesozoic era, and became extinct at the end of the Cretaceous. They came from the same ancestral stock as the neocoleoids, and lived alongside them from the early Carboniferous right up until their demise at the KT boundary.
The hook itself is split up into several sections, each with its own distinct nomenclature as shown in fig.13. The presence of this small hairline groove known as the orbicular scar indicates that the hook was probably not exposed, and was housed within a sheath of soft tissue. Because the tissue attachment point is quite far up the shaft, only the uncinus would be visible, or at least naked. Engeser and Clarke proposed that the hook was stalked, and that it was attached by muscles that could have allowed lateral movement. Since the belemnoid did not have an extensile pair of limbs, like the tentacles of squids and cuttlefish, or the flexible, muscular sucker discs like octopuses, it would have had to manipulate the prey for eating by using its whole arm. If the hooks were sessile, bearing in mind that it may have had up to fifty, then the belemnoid would be severely limited in its arms' movement. Having hooks that could be moved, even slightly, would allow the animal more movement. The manner in which the hooks were positioned, recurved, would have also helped, in that the trapped prey, which was obviously caught by being impaled, could only move in one direction in order to free itself from the hook: towards the mouth. According to Engeser and Clarke, there are three groups of belemnoids that display arm hooks, and one that does not. The Phragmoteuthids are reported as far back as the late Permian and are described as having more slender, slighter hooks than what is described as the "normal" or archetypal hook (fig.13) although variations including enlarged bases and more curved uncini are reported in species. The Belemnoteuthids have more typical hooks, although Chondroteuthis wunnenbergi Bode 1933, exhibited prominent spurs on the proximal lower third. The Belemnitids, most well known as the belemnites, also display a deal of variation. Acrocoelites (Toaricibelus) raui Werner 1912 appears to have two different types of hook, differentiating from the typical hook to those with an internal spur towards the distal end of the arm. Two fossil specimens of Passaloteuthis paxillosa Schlotheim 1820 showed the same structural oddities of having no hooks whatsoever towards the distal parts of the arms. This suggests that this species may well have lacked hooks at the ends of their arms. Unfortunately no other specimens were described or even mentioned, so a conclusion can only be drawn from these two fossils alone.
Ideally a more thorough investigation into prehistoric cephalopod arm structure would have been desirable, but there is so little fossil evidence of cephalopods, being a soft-bodied animal naturally, that such a task is nigh on impossible at present. Most of the neocoleoid fossils are little more than faint outlines with maybe the presence of one or two organs, or surfaces, but this can be sketchy at best, since the fossils are interpreted differently. For this reason, only belemnoids have been included as a representative of prehistoric cephalopods since the available information on fossil cephalopods with regard to armature is pretty much restricted to the belemnoids. It is curious just how well these animals have preserved compared to the other prehistoric cephalopods, given that this class has been in the world's oceans since the Late Cambrian.
The case of Stauroteuthis syrtensis:
Another predator-avoidance strategy is the use of photophores in the skin, combined with ejection of mucous containing bubbles of bioluminescent light. Once a string has been completed the squid halts operation of its photophores and slips of, leaving the bioluminescent mucous thread decoy with the predator.
The case of the Nautiluses:
Similarities and Differences:
A possible Evolutionary Theory:
For sake of completeness, further development into the octopods sucker, lacking a ring, is included. If this were to happen, then because octopods did not branch off of decapods, and both more or less diverged in the same manner as with the belemnoids, theoretically the first octopods would have had some hard structures until these vanished. Of course the internal morphology would have to change again, but slight modification of the infundibulum and acetabulum, and the development of the piston into the acetabular roof could facilitate this. This is highly speculative as there is not a lot of evidence of fossil neocoleoids, but I'd like to hope that it fits together as a sound theory. One interesting fact is that the "paper nautilus" Argonaut argo, an incirrate octopus that secretes a very thin shell, appears to have hooks between the rim of the sicker and infundibulum (Nixon & Dilly); could this be a throwback to a day when all coleoid cephalopods had hard armature?
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Tree of Life web project: www.tolweb.org/tree
Waikiki Aquarium website: www.waquarium.org
The Cephalopod Page: www.thecephalopodpage.org
All sites are operational as of July 2007.
Comparative Morphology of Cephalopod Armature
A study by Graeme Walla, 2007