Graeme Walla
4BSc Zoology
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
Functional Morphology
Structural Morphology
Octopod Sucker Morphology
Functional Morphology
Structural Morphology
Prehistoric Coleoids: Belemnoidea
Special Cases
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.

I chose to study the armature of cephalopods in order to perhaps shed some more light on such a little-documented topic. In order to do this I had to find scientific literature. Because there is scant recorded information, I also had to observe preserved specimens directly, of which I took photographs and detailed diagrams.

It was discovered that cephalopods exhibit a great deal of variation in the architecture of their armature. The chief structure investigated was the familiar sucker pad, but other structures, which could perhaps be called unique, are also discussed; such as the cirri in deep-sea cirrate octopods, the strange adhesive ridges in nautiluses, and the very basic, if impressive, hooks found on the arms of fossil belemnites. A brief but concise description of the functional morphology of the structures is also included.

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.

My focus is on the comparative morphology of the armatures of these cephalopods, which although would appear to be well known, is in fact rather poorly documented in the history of scientific literature, which is unfortunate as it proves to be a very deep and interesting subject, time and resources allowing. All known information on the subject is scattered across several pieces of literature, which for the most part are sketchy at best. True literature on the subject is indeed very difficult to come by as the morphology of suckers and the like have not been studied in any great detail. Also, half a year's study would not even scratch the surface of the subject owing to the diversity of the Class, and the probability that every paper on a new discovery would have to be studied in order to piece the facts together. As a result, I have had to come to several conclusions by looking at the evidence from what literature I have found, but also from direct observation of preserved specimens.

In order to give an idea of the immensity of the subject, with relation to just how long the cephalopods have been around, a brief history would seem appropriate.

The earliest cephalopods recorded have been described from Late Cambrian deposits from NE China. These primitive animals are typified by Plectronceras (such as P. cambria) and were very primitive, consisting of a small internally-chambered conical shell connected with a simple siphuncle. It is thought that they most probably lived a benthic lifestyle similar to marine gastropods.

It was not until the Ordovician that the cephalopods saw a huge evolutionary radiation resulting in the appearance of the orthoconic nautiloids. It is generally accepted that there were eight orders of orthocone, distinguished by the variations in the internal structure of their conical shells. These nautiloids enjoyed a long reign from the Ordovician to the Silurian almost unchallenged, filling many of the predatory niches that had been occupied by now long-extinct animals such as the Cambrian anomalocarids.

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.

It probably wasn't until after the Cretaceous extinction that the Coleoidea became more abundant and diverse; they were probably overshadowed by the ammonites until their disappearance, they were then able to diversify into some of the empty niches left by their externally shelled relatives.

The Carboniferous saw the beginnings of the diversifications amongst the Coleoida as well as the beginnings of a (coherent?) recognisably modern arm structure and the development of armature. Belemnoids showed a definite resemblance to modern squid, although from a different cohort, or group. They had ten arms displaying distinct armature, indicative of the basic coleoid plan, which would later be developed by the modern Decapodiformes.

It was at this time that what we recognise as modern coleoid cephalopods began to emerge, and diversify. Since belemnites are a separate branch on the taxonomic tree it is probable that suckers and hooks did not evolve linearly (one being the result of the other), as one might imagine, but very much at the same time. Because of the tiny amount of actual soft-bodied fossil evidence, owing to coleoid cephalopods being fragile creatures, it is very difficult to say for certain what happened. There are also questions raised such as those related to arm number, and the like.

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.

I also travelled to the National Museum of Scotland in Edinburgh, on the 5th December, 2005 to study several other specimens. The specimens were kept in a depot in West Granton Road where I spent the best part of a day studying specimens of Loligo forbesiiSteenstrup 1856 (veined squid), Todaropsis eblanae Ball 1841(lesser flying squid), Sepia officinalis Linnaeus 1758 (common cuttlefish) and Architeuthis dux Steenstrup 1857 (giant squid).

Several photographs were taken during the examination of the specimens, the best of which have been included for reference. Please note in that the photographs a degree of discolouration in the animal has occurred due to the use of Formalin as a fixing agent which coagulates the cells of the animal. The specimens were safe to handle as the formalin was bound to the cells and therefore not capable of any further fixing. The specimens from the Museum were kept in ethanol. I had to drain my acquired Eledone specimen and clean it of formalin before I was able to examine it.

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.

Neocoleoid cephalopods have suckers on their limbs. These are the main structures that allow the cephalopod to grab and hold onto things, and one of the main structures that distinguish them from other orders. The suckers are always situated along the oral surface of the limb (the ventral or "under-" side) and they aid in the passage of food to the mouth.


fig. 1: Display depicting arm arrangement and number. These numbers are actually used in describing the arm, and correspond to both left and right sides. Notice how the octopod has lost arm 2, but still retains the corresponding numbers!
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).

Decapod suckers are commonly described as having a horny ring of chitin; although Nixon and Dilly (1977) claim that the structure does not contain chitin (referencing Rudall, 1955, as the source of this information). Nixon and Dilly fail to mention what the chemical composition of the ring is, in absence of chitin, and in light of many papers published after this one that refer to the ring as chitinous, it is safely assumed, for the purpose of this study at least, that the ring is made of chitin. Suckers are usually applied in two or four rows (also called series) along the arm and run pretty much along most of the length. The tentacle has suckers only on the club which is the large, spear or spoon-shaped part at the very end. These are arranged usually in four rows although as many as fifty rows of very tiny suckers have been documented (eg Sepiolidae, Nesis).

Minute suckers can be found on the carpus of the tentacle, and in several squids have unique structures. Suckers with smooth rings on one tentacle will have corresponding tubercles (or knobs) on the other. This allows the tentacles to be fastened together in a similar fashion to "popper" fasteners. It has been observed that squids do this while swimming rapidly which would suggest that it is employed as either a way to stop the tentacles from trailing behind or flailing about upon movement, or as a streamlining device. Since squids when swimming using water propulsion from the siphon are oriented mantle-first, and their arms to the rear, the former would seem the more plausible theory. This could also suggest that squids at least do not have as much motor control in their tentacles as they do with their arms, which would make sense as the tentacles are mainly used for prey capture only. Sepioids do not have these structures as they can fully retract their tentacles into pockets at either side of the head.

The main distinguishing feature of octopods is obviously the number of limbs. Essentially squids and cuttlefishes have eight arms as well; the retractile limbs usually being called tentacles, and have a different structure. The other difference with in the suckers of the animals being that octopuses also only have one or two rows, or series, of fleshy suckers running along their arms. Octopuses of the genus Eledone typically have only one row.

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 terminology of the tentacle is slightly more unique and specialised. The most proximal part of the club to the head is called the carpus. The carpus is the region just before the swelling of the club, and usually has a random number and distribution of suckers. The next region is called the manus and is essentially the bulk of the club. This is the widest region of the tentacular club, and houses the largest suckers. Sometimes variation among suckers is found such as the presence of hooks. The final region of the club is called the dactylus and is narrower than the manus.

fig. 2: the differences in the terminology.

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.

The differences between the limbs of the two superorders are not limited to their number, or indeed the presence/absence of chitinous rings. The morphology and structure are also completely different, and are described below. However, both types of suckers still face the problem of maintaining a pressure differential: that is, the difference between the pressures inside and outside the sucker when attached. Of course there is the potential danger of the pressure differential being too great, causing damage to, or even destruction of, the structure. In theory, too small a pressure could cause the sucker to collapse. However this may not be a problem, since the pressure differential is nearly always limited to a threshold determined by cavitation. Thus, the tenacity of the sucker (the measure of force per unit area) depends mostly upon the difference between the pressure inside and outside the sucker, which is in turn determined by depth.

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.

Typically, at sea level, the cavitation threshold limits a sucker to a pressure differential of between 100 and 200kPa. However, every 10m increase in depth allows an increase in pressure differential by about 100kPa, so at 10m the limit will be 200-300kPa, at 20m the limit would be 300-400kPa, and so on. With increasing depth, cavitation proves to be less of a problem.

The other factor that can determine the cavitation threshold is the area of the sucker. Smith (1995) proclaimed that an area of 7.5mm2 or greater showed had a "normal" pressure differential of 100kPa for both decapod and octopod when attached to a surface. However, an area less than 7.5mm2 showed a distinct increase in the ability to produce higher pressure differentials. How a smaller sucker achieves a greater pressure differential is unknown. It could be due to the small size being able to theoretically maintain a decent seal between the rim of the sucker and the surface. Smith also speculated that the smaller sized suckers behaved similarly to Laplace's law for pressurised containers, in that the stress observed in the wall of the container (in this case the sucker), while it maintains a reduced pressure, is proportional to the radius of the container. Admittedly, an area of 7.5mm2 does sound awfully small since this would mean a radius of about 2mm! Many cephalopods do have very small suckers, ranging in about this figure, but some of the larger squids may face problems with cavitation if they have a considerable amount of large suckers, at least at sea level.


Functional Morphology
The suckers of decapods display a great deal of structural variation in the form of the chitinous rings, but the basic morphology is similar. Decapods have suckers located on stalks. The sucker is essentially a rigid cylinder with a muscular piston housed within it (the acetabulum). This is all connected to the tentacle by a stalk. The chitinous ring is housed at the rim of the sucker (the infundibulum). Upon examining the preserved specimens I noticed that the suckers could be pivoted and manipulated using forceps, albeit in a fairly limited arc of movement. They could be twisted slightly and "wiggled" which seemed to suggest that decapod suckers are far from sessile, and can be moved and rotated.

To generate a low pressure of the water inside the sucker, the muscular piston is pulled away from the cavity, towards the arm. Smith (1996) discovered that pulling on the stalk in turn pulled the piston, which reduced the pressure of the water in the sucker. Presumably, therefore, the squid can engage the suckers by pulling the muscular pistons and disengage by relaxing them.

As was described, cephalopods are limited to a pressure differential of 100-200kPa at sea level, but the threshold increases with depth, as well as increasing inversely with a reduction in sucker area.

What is interesting about decapod suckers is that with this decrease in area, it is not a slight increase in pressure differential that is observed, but an exponentially large increase anywhere up to 800kPa!

Structural Morphology:

It must be made clear that decapod suckers are employed for prey capture only, except in some special cases where sexual dimorphism occurs. Sexual dimorphism is a term used to describe traits that distinguish the male and female of the species. In this case, a prime example would be the Grimaldi scaled squid Lepidoteuthis grimaldii Joubin 1895, which displays a grossly enlarged sucker and hook, found only in the males (Jackson and O'Shea, 2003), which would suggest a reproductive function as opposed to a feeding one.

Most squids and cuttlefish that have a neritic (coastal) lifestyle, or at least stay close to surface waters, tend to appear to have slightly smaller suckers. Cuttlefish are generally associated with neritic zones or benthic upper-slopes as opposed to pelagic zones.

The larger squids, including the giant squid, Architeuthis dux (fig.3) have very large suckers, as would be expected, reaching a diameter of nearly 20mm. Since cavitation is not so much a problem at depth, and indeed giant squid are reported live only at extreme depths, it can afford to have large suckers, although quite why it would need to have such large armature is mysterious. The only reason that springs to mind would be predation on large prey or as protection against predation itself. Since most of the giant squid's diet consists (at least in part) of prey items not considered to be overly large (eg. E. cirrhosa, and Norway Lobster Nephrops norvegicus, although the Atlantic Horse Mackerel Trachurus trachurus can achieve a considerable 70cm total length!), it seems odd that they display suckers of such size. Bolstad and O'Shea (2004) discovered in the gut of an individual the remains of another giant squid, which would suggest at least cannibalism in the species. They also proposed that Architeuthis dux is in fact a pelagic animal rather than bentho-pelagic. This would suggest that the giant squid would probably live at much lesser depths than is commonly believed, since most trawled specimens were found at a depth of between 400 and 600m. Still, the reason for such a large diameter (the area would be roughly 314mm2!) is still a conundrum, unless the squid relies more upon the huge horny rings around the rim of the sucker.

fig. 3: Suckers on the tentacle of Architeuthis dux. Note the clearly visible piston musculature at the base of the sucker cavity. Inset: side view of the chitinous ring.

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.

What distinguishes the decapods, though, is the variation in the formations surrounding the edge of the sucker cavity. Surrounding the cavity of the sucker pad is a horny ring. This ring typically consists of chitin, a polysaccharide. It is usually circular, and quite often has structures that protrude from its base. These denticles, or teeth, display a large variation across species, even families, of squids and cuttlefish; the most variation evident in squids. In coastal families such as the Loliginidae, and in most sepioid cuttlefish, circularis muscles surround the base of this chitinous ring, although information on the function of this muscle was unobtainable. Presumably it is just to hold the ring in place, or may facilitate some movement. The ring surrounding the sucker has many proposed functions; the most obvious being to aid the sucker in prey capture. Of course, the sucker is the primary weapon for seizing prey, but the horny ring would aid in latching onto the prey item initially in he strike.

In the Loliginidae, the teeth are relatively small and can be described as acuminate (Nesis); the term used to describe claw-like or conical teeth. Another feature in the rings of Loliginid squids is the tendency for larger and smaller teeth to alternate round the circumference. Indeed, the Loligo forbesii specimen I examined showed this characteristic, although the size difference was little in the alternating denticles there was still variation. The arms of the specimen showed two rows of suckers, the diameters being relatively similar until quite far along the distal part of the arm. The tentacles were fairly typical in that there were four distinct rows, with the largest suckers present on the Manus; the middle section of the club (fig.4).

fig. 4: a shows the club, with diameter of the largest sucker, as well as a sucker of similar diameter to those on the medial part of the arms. Notice the dark brown ring; this is the chitin! B is a line drawing of the sucker. The ring is slightly exaggerated to show its formation.

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.

It is generally accepted that the coastal Myopsid squids (the suborder that comprises the Loliginidae and the Australiteuthidae) have simple ring structures. These structures do vary in the manner described, from pointed to square, alternate to all the same size to even slightly uneven rings.

The Oegopsid squids, including the onychoteuthidae already mentioned, are a large suborder that contains the most dominant squids in the pelagic regions. These squids are very much oceanic, which is reflected by a variety of structural differences to the myopsids. One difference is that they lack the circularis muscle found in most loliginids. The other, and perhaps the most obvious, is the presence of actual tentacle hooks, found commonly in the oegopsids.

The hooks are formed by specialisation of the chitin ring, usually housed in distinguishably larger suckers. It would seem (Nesis 1982, Engeser & Clarke 1988) that the hooks develop during the growth of the young animal, and are not present at birth. Thus hooks, or more specifically a full quota, can be associated with a fully mature animal. The denticles (Engeser & Clarke) on the ring of such a sucker are lost save for the central, most distal, one. The distal end with the one remaining denticle then begins to extend, which draws the sucker edges together. The edges then fuse, which causes the proximal edge of the ring to form basal lobes. Usually a sheath accompanies the hook, which may play a protective role, either for the hook itself or to minimise the risk of the squid impaling itself!

The presence of a hook reduces the sucker to virtually nothing, except maybe a small opening in the structure. Although there are many squids that employ both hooks and suckers, as in the case of L. grimaldii which has, for the majority, suckers, there are many squids that employ the use of hooks only, at least on the tentacles of the onychoteuthidae. Because of this, it is safe to assume that these squids are not relying on negative pressure to adhere to a prey item, but impaling the prey in order to catch it. It was suggested above that the hooks in L. grimaldii were not to aid in predation, but in reproduction. The main apparent reason for this is that the hooks are not located on the tentacles, the primary hunting tool, but on the second arms. They also occur only in the males. According to photographs taken by Jackson and O'Shea, sucker ring is still very much present, and the huge hook resembles a very pronounced single denticle, albeit looking particularly like a miniature claymore or broadsword! It was proposed that the hooks were embedded directly into the female's skin or lock into her scales (dermal cushions that give the species its name). It is also possible that the hooks are employed in male-male agonistic mating displays. The scaled squid does not have a hectocotylised arm, and instead has a relatively long penis (or terminal organ), which probably means that it implants the spermatophores directly into the female's mantle cavity, which would mean that hooks which allow purchase of the female's body during this mode of reproduction would indeed be favoured. In this case, reproduction would probably take place "head to feet" as it were, with the partners facing opposite directions. Technically this means that a female with damage to either her mantle or the scales would indicate the probable use of the hooks, where a male has held the female during reproduction.

The formation of the ring in the lesser flying squid is rather notable in that the denticles appear to protrude from fleshy ridges, which resembled sockets, the denticles, or at least what was visible of them, were very small, and slightly rounded (fig.5).

fig. 5: a, clockwise from left: the full club, one of the larger suckers on the manus, the dactylus. Part b shows the tentacle- It looks like only 1 series of suckers, but it is in fact 2. Part c is a line drawing showing the folds with the small, rounded denticles.

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.

The common cuttlefish specimen exhibited denticles that resembled tiny, curved claws. The actual ring itself was hidden in the rim of the sucker. This order also has the circularis muscles that the loliginids possess. The suckers did not appear to be located on stalks, but they did move quite freely upon gentle manipulation with a pair of forceps, which would suggest the presence of a stalk. The outside of the sucker was very broad giving an upturned bowl shape, which is what probably rendered the stalk invisible.

fig. 6: a, left: the tentacle club of S. officinalis and right: the triangular arm, b; schematic of the large (4mm) tentacular sucker.

This appears to be fairly typical of sepioid cuttlefish suckers. The suckers on the arm were in four tightly packed rows. The arms themselves were interesting in that they were actually short and stumpy, tapering sharply to form almost triangular arms. The presence of the fully retractable tentacles means that the cuttlefish doesn't always have to employ them to hunt. Cuttlefish are mostly neritic animals living near the sea bed, and the common cuttlefish is a model of this. It seems that when hunting benthic animals the cuttlefish merely hangs above its prey and lunges at it using the eight arms, and not the tentacles (Nixon & Dilly). The tentacles therefore, are probably reserved for fast swimming, pelagic animals like prawns or fish, as opposed to crabs. All of these comprise part of the common cuttlefish's diet, and probably that of other species, since most live in coastal waters.]
Original publish date
Jul 22, 2007